Bennett & Brachman's Hospital Infections, 5th Edition

23

Dialysis-Associated Complications and Their Control*

Matthew J. Arduino

Introduction

The number of patients who have end stage renal disease (ESRD) has increased dramatically in the past 40 years. ESRD patients are treated by three major forms of renal replacement therapy: hemodialysis applications (conventional dialysis, hemofiltration, or hemodiafiltration), peritoneal dialysis (continuous ambulatory peritoneal dialysis, intermittent peritoneal dialysis, or automated peritoneal dialysis), or kidney transplant. Data from the U.S. Renal Data System (USRDS) suggests that by 2003 there were approximately 453,000 patients with ESRD. In the United States, the predominant form of renal replacement therapy (for approximately 298,000) is maintenance hemodialysis. Only about 6–7% of all patients receiving dialysis therapies are treated by one form of peritoneal dialysis [1].

In 1967, approximately 1,000 patients were undergoing maintenance or chronic hemodialysis. In 1973, when full Medicare coverage was extended to ESRD patients, approximately 11,000 patients were undergoing dialysis in independent or hospital-based centers and in homes in the United States. At the end of 2002, approximately 264,000 patients were undergoing maintenance hemodialysis at 4,035 dialysis centers with 58,000 staff members throughout the United States [2]. The ESRD program is administered by the Center for Medicare and Medicaid Services (CMS) of the Department of Health and Human Services. It is the only Medicare entitlement that is based on the diagnosis of a medical condition.

The technology for performing dialysis as well as the potential for complications has changed significantly over the years. In the early 1960s, hemodialysis was used almost exclusively for the treatment of acute renal failure. Subsequently, the development of the arteriovenous shunt and certain other ancillary technologic advances in dialysis equipment expanded the use of hemodialysis to maintenance therapy for ESRD. In the 1970s, the primary mode for dialysis treatment was hemodialysis performed with various types of artificial kidney machines. Subsequently, the use of peritoneal dialysis, accomplished by automated machines or by intermittent cycling, increased. By the end of 2003, only 25,825 (approximately 8%) patients were being treated by peritoneal dialysis applications. Continuous ambulatory peritoneal dialysis (CAPD), automated peritoneal dialysis (APD), or intermittent peritoneal dialysis (IPD) modality is more popular among pediatric nephrology programs (approximately 40% of all pediatric dialysis patients) [1]. One must also recognize that patients may change modality due to vascular access failure, peritonitis, peritoneal transport issues, and so on.

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All patients with chronic kidney disease, including dialysis patients, have a compromised immune system and other co-morbidities that place them at increased risk for infectious diseases. This chapter describes the major infectious diseases and several toxic complications due to chemical contamination that can be acquired in the dialysis center setting, the important epidemiologic and environmental microbiologic considerations, and infection control strategies.

The Centers for Disease Control and Prevention (CDC) compiled date from two sources. The first includes outbreak investigations in dialysis settings conducted by CDC and National Surveillance studies. During the past 33 years, the CDC investigated 36 outbreaks in the dialysis setting; 17 involved bacterial infections or pyrogenic reactions, 10 viral infections, 8 toxic chemical complications, and 1 allergic complication of dialysis. In addition, the CDC performed national surveys of Hepatitis B virus (HBV) incidence and prevalence in the early 1970s. These national surveys subsequently evolved into the National Surveillance of Dialysis-Associated Diseases in the United States performed by CDC in collaboration with CMS in 1976, 1980, 1982–1997, and 1999–2002 [2,3,4,5,6,7,8,9,10,11,12,13,14,15]. The data collected includes hemodialysis practices, infection control precautions, and the occurrence of certain hemodialysis-associated diseases.

Bacterial and Chemical Contaminants in Hemodialysis Systems

A typical hemodialysis system consists of a water supply, a system for mixing water and dialysis fluid concentrates, and a machine to pump the dialysis fluid through the artificial kidney (commonly referred to as the hemodialyzer or dialyzer). The dialyzer is connected to the patient's circulatory system and pumps blood through it to accomplish dialysis through a membrane to remove waste products from the patient's blood by both diffusion and convection.

Microbial Contamination of Water

Technical development and clinical use of hemodialysis delivery systems improved dramatically in the late 1960s and early 1970s. However, a number of microbiologic parameters were not accounted for in the design of many hemodialysis machines and their respective water supply systems. In many situations, certain types of gram-negative water bacteria can persist and actively multiply in aqueous environments associated with hemodialysis equipment. This can result in the production of massive levels of gram-negative bacteria, which can directly or indirectly cause septicemia or endotoxemia in patients [16,17,18,19].

A number of factors can influence microbial contamination of fluids associated with hemodialysis systems (Table 23-1). The gram-negative water bacteria can be significant contaminants in hemodialysis systems (Table 23-2), and virtually all disinfection strategies for fluid water distribution lines and dialysis machines are targeted to this group of bacteria. Gram-negative water bacteria are capable of multiplying rapidly in all types of waters, even those containing relatively small amounts of organic matter, such as water treated by distillation, softening, deionization, or reverse osmosis. These organisms can attain levels ranging from 105 to 107 per milliliter of water and, under certain circumstances, can be a health hazard for patients undergoing dialysis; they constitute a direct threat of bacteremia, and they contain bacterial endotoxin (lipopolysaccharide) that can cause pyrogenic reactions [17,18,19,20,21]. It should be emphasized that virtually any gram-negative water bacterium that can grow in water systems represents a potential problem in a hemodialysis unit. These bacteria adhere to surfaces and can form biofilms (glycocalyxes) that can make them virtually impossible to eradicate [18,22,23,24]. In fact, control strategies are designed to reduce levels of microbial contamination in water and dialysis fluid to relatively low levels but not to completely eradicate them.

Gram-negative water bacteria can grow even more rapidly in treated water mixed with dialysate concentrate. This mixture results in dialysis fluid that is a balanced salt solution and growth medium that is almost as rich in nutrients as conventional nutrient broth [19,25,26]. Gram-negative water bacteria growing in distilled, deionized, or reverse osmosis treated water can reach levels of 105–107 organisms per milliliter, but these cell populations are not visibly turbid. On the other hand, these same bacteria growing in dialysis fluids can achieve levels of 108–109 organisms per milliliter and often are associated with noticeable turbidity [25].

Nontuberculous mycobacteria also can multiply in water (Table 23-2). Although they do not contain bacterial endotoxin, they are comparatively resistant to chemical germicides and, as will be discussed later, have been responsible for patient infections due to inadequately disinfected dialyzers that are reprocessed and inadequately disinfected peritoneal dialysis machines [27,28,29,30].

The strategy for controlling massive accumulations of gram-negative water bacteria or nontuberculous mycobacteria in dialysis systems primarily involves preventing their growth. This can be accomplished by proper disinfection of water treatment system and hemodialysis machines. Gram-negative water bacteria and their associated lipopolysaccharides (bacterial endotoxins) and nontuberculous mycobacteria ultimately come from the community water supply, and levels of these bacteria can be amplified depending on the water treatment systems, dialysate distribution systems, type of dialysis machine, and method of disinfection [17,27,28,31,32] (see Table 23-1). Each of these components is discussed separately in some detail.

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TABLE 23-1
FACTORS INFLUENCING MICROBIAL CONTAMINATION IN HEMODIALYSIS SYSTEMS

Factors

Comments

Water supply

Source of community water

Groundwater

Contains endotoxin and bacteria

Surface water

Contains high levels of endotoxin and bacteria

Water treatment at dialysis center

None

Not recommended

Filtration

Prefilter

Uses particulate filter to protect equipment; does not remove microorganisms

Absolute filter (depth or membrane)

Removes bacteria but, unless changed frequently or disinfected, bacteria will accumulate and grow through filter; acts as significant reservoir of bacteria and endotoxin

Activated carbon filter

Removes organics and available chlorine or chloramine; significant reservoir of water bacteria and endotoxin

Water treatment devices

Ion-exchange softener

Both softeners and de-ionizers are significant reservoirs of bacteria and do not remove endotoxin

Deionization

Reverse osmosis

Removes bacteria and endotoxin but must be disinfected; operates at high water pressure

Ultraviolet light

Kills some bacteria, but there is no residual, and ultraviolet-resistant bacteria can develop

Ultrafilter

Removes bacteria and endotoxin; operates on normal line pressure; can be positioned distal to de-ionizer; must be disinfected

Water and dialysate distribution system

Distribution pipes

Size

Oversized diameter and length decrease fluid flow and increase bacteria reservoir for both treated water and centrally prepared dialysate

Construction

Can act as bacterial reservoirs because of rough joints, dead ends, and unused branches

Elevation

Outlet taps should be located at highest elevation to prevent loss of disinfectant

Storage tanks

Is undesirable because they act as reservoir of water bacteria; if present, must be designed properly, and routinely scrubbed and disinfected

Dialysis machines

Single pass

Disinfectant should have contact with all parts of machine that are exposed to water or dialysis fluid

Recirculating single pass or overnight recirculating (batch)

Recirculating pumps and machine design allow for massive contamination levels if not properly disinfected. Chemical germicide treatment recommended

Water Supply

Dialysis centers use water from a public supply that may be derived from surface, ground, or blends of surface and ground waters. The source of the water may be important in terms of chemical, bacterial, and endotoxin content. Surface waters frequently contain endotoxin from gram-negative water bacteria and from certain types of blue-green algae (Cyanobacteria). Endotoxin levels are not substantially reduced by conventional municipal water treatment processes and can be high enough to cause pyrogenic reactions in patients undergoing dialysis [33].

Essentially all public water supplies are contaminated with water bacteria; consequently, a dialysis center's water treatment and distribution systems and dialysis machines are challenged repeatedly with continuous inoculation of these ubiquitous bacteria. Even adequately chlorinated water supplies commonly contain low levels of these microorganisms. Whereas chlorine and other disinfectants added to the city water may prevent high levels of contamination, the presence of these chemicals in dialysis fluids is undesirable because of adverse effects on patients undergoing dialysis [34,35,36,37,38]. Furthermore, the dialysis water treatment systems described in the following section

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effectively remove chlorine, allowing for the unrestricted growth of water microorganisms.

TABLE 23-2
TYPES OF WATER MICROORGANISMS THAT HAVE BEEN FOUND IN DIALYSIS SYSTEMS

Gram-Negative Water Bacteria
Pseudomonas spp.
Flavobacterium spp.
Enterobacter cloacae
Klebsiella pneumoniae
Burkholderia cepacia complex
Pseudomonas aeruginosa
Ralstonia pickettii
Serratia liquefaciens
S. marcescens
Stenotrophomonas maltophilia

Nontuberculous mycobacteria
Mycobacterium chelonae
M. abscessus
M. mucogenicum
M. fortuitum
M. gordonae
M. scrofulaceum

Fungi
Candida parapsilosis
C. albicans
Phialemonium curvatum

Water Treatment Systems

Water used to produce dialysis fluid must be treated to remove chemical contaminants. The Association for the Advancement of Medical Instrumentation (AAMI) has published guidelines for the chemical and bacteriologic quality of water used to prepare dialysis fluid [39,40]. Since 1997, most maintenance dialysis facilities (at least 97%) use water treatment that includes reverse osmosis either alone or in combination with deionization [13]. Water systems are divided into three types of components: pretreatment, treatment, and posttreatment. Some components may vary based on the area of the United States and local water quality. A variety of different water treatment system components is used, but most of them are associated with amplification of water bacteria (Table 23-1). The most common treatment component is ion exchange using water softeners (pretreatment) and deionizers (treatment or posttreatment polisher). However, neither of these components removes endotoxins or bacteria, and both provide sites of significant bacterial multiplication [41]. An effective means of treating water for dialysis is reverse osmosis. Reverse osmosis or deionization water treatment systems are used in 99% of U.S. dialysis centers [13]. Reverse osmosis possesses the singular advantage of being able to remove both bacterial endotoxins and bacteria from supply water. However, low numbers of gram-negative or nontuberculous mycobacteria water bacteria can either penetrate this barrier, or by other means colonize the downstream portion of the reverse osmosis unit. Consequently, reverse osmosis systems must be disinfected routinely.

Various filters are marketed to control bacterial contamination in water and dialysis fluids. Most of these are inadequate, especially if they are not routinely disinfected or changed frequently. Particulate filters, commonly called prefilters, operate by depth filtration and do not remove bacteria or bacterial endotoxins. These filters can become colonized with gram-negative water bacteria, resulting in amplification of the levels of both bacteria and endotoxin in the filter effluent. Absolute filters, including the membrane types, temporarily remove bacteria from passing water. However, some of these filters tend to clog, and gram-negative water bacteria can “grow through” the filter matrix and colonize the downstream surface of the filters within a couple of days. Furthermore, absolute filters do not reduce levels of endotoxin in the effluent water. These types of filters should be changed regularly in accordance with the manufacturer's directions and disinfected in the same manner and at the same time as the dialysis system.

Activated carbon filters/tanks remove certain organic chemicals and available chlorine (free and combined chlorine) from water by adsorption, but the filters also significantly increase the level of water bacteria and do not remove bacterial endotoxins.

Germicidal ultraviolet irradiation (GUI) lamps are sometimes used to reduce bacterial contamination in water. These lamps should operate at a wavelength of 254 nm and provide a dose of radiant energy of 30 milliwatt-sec/cm2. Several studies have demonstrated that a dose of 30 milliwatt-sec/cm2 will kill more than 99.99% of a variety of bacteria, including Pseudomonas species, in a flow-through device [42,43]. However, certain gram-negative water bacteria appear to be more resistant to GUI than others, and using sublethal doses of GUI or exposing water for an insufficient contact time may lead to proliferation of these resistant bacteria in the water system [19,44]. This problem may be accentuated in recirculating dialysis systems in which repeated exposures to sublethal doses of GUI are used to ensure adequate disinfection. The multiplication of those microorganisms surviving initial exposure enhanced resistance to GUI. In addition, bacterial endotoxins are not affected by GUI.

As mentioned, an effective means of treating water for dialysis is the correct use of a reverse osmosis unit. This author recommends using a water treatment system that produces chemically adequate water without massive levels of microbial contamination. Such a system is well suited for hard water and involves the following procedure [45]: community-supplied water is passed through a pretreatment chain consisting of prefilters, softener, carbon adsorption media (filters or tanks), and a particulate filter and then is passed through the treatment components, a reverse osmosis unit, and finally

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a deionization unit. Through these phases, the water becomes progressively more pure chemically, but the level of bacterial contamination increases. To compensate, an ultrafilter can be included in the final step of the system to remove bacteria and bacterial endotoxins. The ultrafilter consists of similar types of membranes as in a reverse osmosis unit or a polysulfone membrane, but it can be operated at ordinary water line pressure. This entire system can be augmented with other source-water treatment devices, depending on the chemical quality of the water in question. If this system is adequately disinfected, the microbial content of water should be well within the recommended guidelines discussed Microbiologic Monitoring of Water and Dialysis Fluid.

Distribution Systems

Dialysis centers use one of two general systems for delivering dialysis fluids to individual dialysis machines. The first type treats the incoming supply water and distributes it to individual free-standing dialysis stations either in a direct feed system or an indirect feed system (recirculating system). At each station, the water is mixed with a dialysate concentrate according to automatic proportioning by the dialysis machine. A second type of system, usually found in large dialysis centers, involves the automatic mixing of treated water and dialysate concentrate at a central location followed by distribution of the warmed dialysis fluid through pipes to individual dialysis stations. In both designs, the distribution system consists of plastic pipes (usually polyvinyl chloride) and appurtenances.

These distribution systems can contribute to microbial contamination in two ways. First, they frequently use pipes that are larger in diameter and longer than necessary to handle the required fluid flow. This slows the fluid velocity and increases both the total fluid volume and the wetted surface area of the system. Gram-negative bacteria in fluids remaining in pipes may multiply rapidly and colonize the wetted surfaces of the pipes, producing bacterial populations and endotoxin quantities in proportion to the volume and surface area. Such colonization results in bacterial formation of protective biofilm, which is difficult to remove and protects the bacteria from disinfection [46].

Because pipes can constitute a source of water bacteria in a distribution system, routine disinfection should be performed at least weekly. To ensure that the disinfectant cannot drain from pipes by gravity before contact time is adequate, distribution systems should be designed with all outlet taps at equal elevation and at the highest point of the system. Furthermore, the system should be free of rough joints, dead-end pipes, and unused branches and taps. Fluid trapped in such stagnant areas can serve as reservoirs of bacteria capable of continuously inoculating the entire volume of the system [21].

Incorporation of a storage tank in a distribution system greatly increases the volume of fluid and surface area available to act as reservoirs for the multiplication of water bacteria. Storage tanks should not be used in dialysis systems unless they are properly designed, frequently drained, and adequately disinfected, including scrubbing the sides of the tank to remove bacterial biofilm. It is also recommended that an ultrafilter be used distal to the storage tank [47,48].

Hemolysis Machines

Currently in the United States, virtually all centers use single-pass hemodialysis machines. In the 1970s, most machines were of the recirculating or recirculating single-pass type. The nature of their design contributed to a relatively high level of gram-negative bacterial contamination in dialysis fluid. Single-pass dialysis machines tend to respond to adequate cleaning and disinfection procedures and, in general, have lower levels of bacterial contamination in their dialysis fluid than do recirculating machines. Levels of contamination in single-pass machines depend primarily on the bacteriologic quality of the incoming water and on the method of machine disinfection [17,18,19].

A frequent error in disinfecting single-pass systems occurs when the disinfectant is introduced in the same manner and through the same port as the dialysate concentrate. By so doing, the pipes and tubing of the incoming water are not exposed to a disinfectant; thus, the environment is such that bacteria can readily colonize and proliferate, acting as a constant reservoir of contamination. To adequately disinfect a single-pass system, the disinfectant must reach all parts of the system's fluid pathways.

Dialyzers

The dialyzer (artificial kidney) usually does not contribute significantly to bacterial contamination of the dialysate. Most dialysis centers use hollow-fiber dialyzers [5,7,8], which tend not to amplify bacterial contamination in the dialysis systems. The percentage of centers that reported reuse of disposable dialyzers on the same patient increased from 18–82% during the period from 1976 to 1997 but declined slightly over the next 5 years to 63% in 2002 [2]. Improper reprocessing techniques have been associated with outbreaks of bacteremia and pyrogenic reactions in dialysis patients (Table 23-3).

Disinfection of Hemodialysis Systems

The objective of a dialysis system disinfection procedure is to primarily inactivate bacteria and fungi in the fluid pathways associated with the dialysis system and to prevent these organisms from growing to significant levels once the system is in operation. Routine disinfection of isolated components of a dialysis system frequently produces inadequate results in which the hazard to the

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patient persists. Consequently, the total dialysis system (water treatment system, distribution system, and dialysis machine) needs to be considered when selecting and applying disinfection procedures.

TABLE 23-3
OUTBREAKS ASSOCIATED WITH DIALYZER REUSE

Description

Cause(s) of Outbreak

Corrective Measure(s) Recommended

Reference

Mycobacterial infections in 27 patients

Inadequate concentration of dialyzer disinfectant

Increase formaldehyde concentration used to disinfect dialyzers to 4%

[27]

Mycobacterial infections in 5 high-flux dialysis patients; 2 deaths

Inadequate concentration of dialyzer disinfectant and inadequate disinfection of water treatment system

Use higher concentration of Peracetic acid for reprocessing dialyzers and follow manufacturers labeled recommendations; increase frequency of disinfecting the water treatment system

[29]

Bacteremia in 6 patients

Inadequate concentration of dialyzer disinfectant; water used to reprocess dialyzers did not meet AAMI standards

Use AAMI quality water; ensure proper germicide concentration in the dialyzer

[CDC unpublished data]

Bacteremia and pyrogenic reactions in 6 patients

Dialyzer disinfectant diluted to improper concentration

Use disinfectant at the manufacturers recommended dilution and verify concentration

[49]

Bacteremia and pyrogenic reactions in 6 patients

Inadequate mixing of dialyzer disinfectant

Thoroughly mix disinfectant and verify proper concentration

[50]

Bacteremia in 33 patients at 2 dialysis centers

Dialyzer disinfectant created holes in the dialyzer membrane

Change disinfectant (product was withdrawn from the marketplace by the manufacturer)

[51]

Bacteremia in 6 patients; all blood isolates had similar plasmid profiles

Dialyzers were contaminated during removal and cleaning of headers with gauze; staff was not routinely changing gloves; dialyzers not reprocessed for several hours after disassembly and cleaning

Do not use gauze or similar material to remove clots from header; change gloves frequently; process dialyzers after rinsing and cleaning

[52]

Pyrogenic reactions in 3 high-flux dialysis patients

Dialyzer reprocessed with 2 disinfectants; water for reuse did not meet AAMI standards

Do not disinfect dialyzers with multiple germicides; more frequent disinfection of water treatment system and conduct routine environmental monitoring of water for reuse

[53]

Pyrogenic reactions during high-flux dialysis

Dialyzers rinsed with city (tap) water containing high levels of endotoxin; water used to reprocess dialyzers did not meet AAMI standards

Do not rinse or reprocess dialyzers with tap water; use AAMI quality water for rinsing and preparing dialyzer disinfectant

[CDC unpublished data]

Pyrogenic reactions in 18 patients

Dialyzers rinsed with city (tap) water containing high levels of endotoxin; water used to reprocess dialyzers did not meet AAMI standards

Do not rinse or reprocess dialyzers with tap water; use AAMI quality water for rinsing and preparing dialyzer disinfectant

[54]

Pyrogenic reactions in 22 patients

Water for reuse did not meet AAMI standards; improper microbiological technique was used on samples collected for monthly monitoring

Use the recommended assay procedure for water analysis of water and dialysate; disinfect water distribution system

[55]

Bacteremia and Candidemia among patients in 7 dialysis units (Minnesota and California)

Dialyzers were not reprocessed in a timely manner; some dialyzer refrigerated for extended periods of time before reprocessing; company recently made changes to header cleaning protocol

Reprocess dialyzers as soon as possible; follow joint CDC and dialyzer reprocessing equipment and disinfectant manufacturer guidance for cleaning and disinfecting headers of dialyzer

[CDC unpublished data]

Chlorine-based disinfectants (e.g., sodium hypochlorite solutions) are convenient and effective in most parts of the dialysis system when used at the manufacturer's recommended concentration. Also, the test for residual available chlorine to confirm adequate rinsing is simple and sensitive. However, because of the corrosive nature of chlorine, the disinfectant normally is rinsed from the system after a short (20–30 minute) exposure time. This

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practice commonly negates the disinfection procedure because the rinse water is not sterile and invariably contains waterborne microorganisms that immediately resume multiplication. If permitted to stand overnight, the water may contain significant microbial contamination levels. Therefore, chlorine disinfectants are most effective when applied just before the start-up of the dialysis system rather than at the end of the daily operation. In some large centers with multiple shifts, it may be reasonable to use sodium hypochlorite disinfection between shifts (this may not be necessary with some single-pass machines if the levels of bacterial contamination are below AAMI action limits [40]) and formaldehyde, peracetic acid, hydrogen peroxide, ozone, and hot water disinfection at the end of the day.

Aqueous formaldehyde, hydrogen peroxide, and peracetic acid solutions can produce good disinfection results. They are not as corrosive as hypochlorite solutions and can be allowed to remain in the dialysis system for long periods when it is not operational, thereby preventing the growth of bacteria in the system. Formaldehyde has good penetrating characteristics but is considered an environmental hazard and potential carcinogen and is associated with irritating qualities that are objectionable to staff members. Commercial tests (e.g., Formalert, Organon Teknika, Durham, NC) are available that are sensitive for testing for formaldehyde in water at concentrations as low as 1 part per million (ppm). (Use of trade name and commercial products is for identification purposes only and does not imply endorsement by the Centers for Disease Control and Prevention of the U.S. Public Health Service.) When used according to the manufacturers' recommendations, commercially available peracetic acid disinfectants for dialysis systems are not corrosive to machines and are good germicides [56].

Some dialysis systems use hot-water disinfection (pasteurization) to control microbial contamination. In this type of system, water heated to >80°C (176°F) is passed through all proportioning, distribution, and patient-monitoring devices before use. This system is excellent for controlling bacterial contamination [47,57]. Use of ozone also has been increasing as a means of sanitizing water treatment distribution loops and central bicarbonate delivery systems [47,57,58,59].

Monitoring Water and Dialysis Fluid

Bacteriologic assays of water and dialysis fluids should be performed at least once a month. Chemical analysis of water used for dialysis should be done before the system is designed and then at least seasonally (since feed water quality changes) to ensure that the water is of sufficient quality for hemodialysis applications [39,40]. The recommended levels of microbial contamination in water used to prepare dialysis fluid should not exceed 200 colony forming units per ml (CFU/ml) and contamination levels should not exceed 2000 CFU/ml in dialysis fluids [60,61]. These particular numbers are based on bacteriologic assays during epidemiologic investigations. However, an increasing body of evidence indicates that dialysate may be responsible in part for the chronic inflammatory state in dialysis patients [62,63,64,65,66,67,68,69]. In response to these studies, AAMI has published new recommendations, which begin to lower the maximum microbial contaminant levels in dialysis fluids. In these new recommendations, water and conventional dialysate have the same maximum contaminant levels (200 cfu/ml and 2 endotoxin units per ml (Eu/ml)). They also have included standards for ultrapure dialysate and dialysate for infusion (Table 23-4) [40].

TABLE 23-4
AAMI MICROBIAL QUALITY STANDARDS FOR DIALYSIS FLUIDS

Microbial Bioburden

Endotoxin

Type of Fluid

Maximum Contaminant Level

Action Level

Maximum Contaminant Level

Action Level

a Compliance with a maximum bacterial level of 10-6 cfu/ml cannot be demonstrated by culturing but by processes developed by the machine manufacturers.

Water for all purposes

200 CFU/ml

50 CFU/ml

2 Eu/ml

1 Eu/ml

Conventional dialysate

200 CFU/ml

50 CFU/ml

2 Eu/ml

1 Eu/ml

Ultrapure dialysate

1 CFU/10 ml

0.03 Eu/ml

Dialysate for infusion

1 CFU/1000 la

0.03 Eu/ml

The microbiological assay is quantitative rather than qualitative, and a standard technique for enumeration should be used; the standard recommended method is membrane filtration [40]. Water samples should be collected at a point that is as close as possible to where water enters the dialysate concentrate-proportioning unit. Samples should be collected at least monthly for established units and weekly for new units until an established pattern is determined. Repeat samples should be collected when microbial counts exceed the action level (Table 23-4) and after disinfection changes have been instituted. Dialysis fluid samples should be collected at the start or termination of dialysis close to the point where the dialysis fluid either enters or leaves the dialyzer. These types of samples also should be taken at least once monthly and after suspected pyrogenic reactions or changes in the water treatment system or disinfection protocols.

Samples should be assayed within 30 minutes or refrigerated (4°C) and assayed within 24 hours of collection. Total viable counts (standard plate counts) are the objective of the assays, and conventional laboratory procedures, such as membrane filtration technique or spread plate, can

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be used; calibrated loops should not be used because they sample a small volume and are inaccurate. Although standard methods such as agar, blood agar, and trypticase soy agar were considered equivalent in the earlier recommendations of the AAMI, research has since shown that many gram-negative bacterial flora of bicarbonate dialysis fluid require a small amount of NaCl for optimal growth. Consequently, trypticase soy agar currently is considered the culture medium of choice; other acceptable media include standard methods of agar and plate count agar (also known as TGYE). Colonies should be counted after 48 hours of incubation at 35°C–37°C (95°C–98.6°F) [40,60,61,70,71]. This method indicates water and dialysate fluid quality only and is not to be confused with total heterotrophic plate counts, which require much longer incubation times at 28°C. There has been discussion in the dialysis community that these methods infact under estimate the actual contamination of dialysis fluids [72,73].

In the event of an outbreak investigation, the assay may need to be qualitative and quantitative, and samples may have to be cultured using additional microbiological culture media and methods as is the case with nontuberculous mycobacteria and fungi (Table 23-2). In such instances, plates should be incubated for 5–14 days.

If centers reprocess dialyzers for reuse on the same patient, water used to rinse dialyzers and prepare dialyzer disinfectants also should be assayed at least monthly in the manner described previously. It is recommended that microbial or endotoxin contaminations not exceed 200 cfu/ml and 2 eu/ml (Table 23-4) [40,74].

Pyrogenic Reactions and Septicemia/Fungemia

Pyrogenic reactions and gram-negative sepsis are the most common complications associated with high levels of gram-negative bacterial contamination of dialysis fluid. Pyrogenic reactions can result from either the passage of bacterial endotoxin (lipopolysaccharide) in the dialysis fluid across the dialyzer membrane [75,76,77,78,79] or the transmembrane stimulation of cytokine production in the patient's blood by endotoxins in the dialysis fluid [80,81]. In other instances, endotoxins can enter the bloodstream directly with fluids that are contaminated with gram-negative bacteria [51,82]. Studies indicate that chronic hemodialysis patients have enhanced cytokine response compared to nonhemodialysis patients, which may account for the high rate of fatal sepsis in uremic patients [83].

The higher the level of bacteria and endotoxin in dialysis fluid, the higher the probability that bacteria or endotoxin will pass through the dialysis membrane or stimulate cytokine production. In an outbreak of febrile reactions among patients undergoing dialysis, the attack rates were directly proportional to the level of bacterial contamination in the dialysis fluid [19]. Prospective studies also demonstrated a lower pyrogenic reaction rate among patients when they underwent dialysis with dialysis fluid that had been filtered and from which most bacteria had been removed compared to patients who underwent dialysis with dialysis fluid that was highly contaminated (mean 19,000 cfu/ml) [84,85].

In 1997, 21% of U.S. hemodialysis centers reported at least one pyrogenic reaction in the absence of septicemia in patients undergoing dialysis [13]. This reported rate was fairly stable from 1989–1997 (range: 19–22%) [13]. An active surveillance system is essential for early detection and control of these complications. Clinical reactions should be defined as they occur because doing so may be the first clue that a problem exists. In addition, the dialysis system should be microbiologically monitored periodically by methods described previously.

Among 11 outbreaks of bacteremia and pyrogenic reactions not related to dialyzer reuse investigated by the CDC, inadequate disinfection of the water distribution or storage system was implicated in 4 of them (Table 23-5). The most recent outbreaks occurred at centers using dialysis machines having a port to dispose of dialyzer priming fluid (waste handling option) [89,90,91,95,96, CDC unpublished data, 2006]. One-way check valves in the waste-handling option had not been maintained, checked for competency, or disinfected as recommended, allowing backflow from the drain, contamination of the port, and backflow of fluid into the patients' blood lines.

Surveillance of Pyrogenic Reactions and Infections

Pyrogenic reactions in patients undergoing dialysis are associated with shaking chills, fever, and hypotension. Depending on the type of dialysis system and the level of initial contamination, the onset of an elevated temperature and chills can occur 1–5 hours after the initiation of dialysis and usually are associated with a decrease in systolic blood pressure of at least 30 millimeters of mercury (mm Hg). Other less frequent but characteristic symptoms may include headache, myalgia, nausea, and vomiting. We define a case of pyrogenic reaction as the onset of objective chills (visible rigors), fever (oral temperature ≥37.8°C [100°F]), or both in a patient who was afebrile (oral temperature ≤37.0°C [98.6°F]) and who had no signs or symptoms of infection before the dialysis treatment [33,54,82,85].

Differentiating gram-negative bacterial sepsis from a pyrogenic reaction can be difficult because the initial signs and symptoms of the two conditions are identical. The most reliable means of detecting sepsis is by culturing blood taken at the time of the reaction. However, because the results of these cultures take at least 18–24 hours to obtain and because therapy for sepsis should not be withheld for this length of time, other less reliable criteria must be used. Many pyrogenic reactions are not associated with bacteremia, and the preceding signs and symptoms generally abate within a few hours after dialysis has been

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stopped. With gram-negative bacterial sepsis, fever and chills may persist, and hypotension is more refractory to therapy [33,82].

TABLE 23-5
CDC INVESTIGATED OUTBREAKS OF BACTEREMIA, FUNGEMIA, OR PYROGENIC REACTIONS UNRELATED TO HEMODIALYZER REUSE

Description

Cause(s) of Outbreak

Corrective Measure

Reference

Pyrogenic reactions in 49 patients

Untreated city (tap) water with high level of endotoxin

Install reverse osmosis system

[33]

Pyrogenic reactions in 45 patients

Inadequate disinfection of the fluid distribution system

Increase disinfection frequency and contact time for the disinfectant

[86]

Pyrogenic reactions in 14 patients; two bacteremias; one death

Reverse osmosis water storage tank contaminated with bacteria

Remove or properly disinfect and maintain storage tank

[18]

Pyrogenic reactions in 6 patients; 7 bacteremias

Inadequate disinfection of water distribution system and dialysis machines; improper microbial assay procedure

Use correct microbial assay procedure; disinfect water distribution system and dialysis machines according to manufacturer's recommendations

[87]

Bacteremia in 35 patients with central vein catheters (CVC)

CVCs used as primary access; median duration of infected catheters was 311 days; improper aseptic technique

Use CVCs only when necessary; use appropriate aseptic techniques when inserting and performing catheter care

[88]

Three pyrogenic reactions and 10 bacteremias in patients treated on machines with a port (WHO) for disposal of dialyzer priming fluid

Incompetent valve allowing backflow from the drain to the WHO and contamination of the blood lines; bacterial contamination of the WHO

Routine maintenance, disinfection, and determination of valve competency of the WHO

[89, 90]

Bacteremia in 10 patients treated on machines with a port for disposal of dialyzer prime

Incompetent valve allowing backflow from the drain to the WHO and contamination of the blood lines; bacterial contamination of the WHO

Routine maintenance, disinfection, and determination of valve competency of the WHO

[89, 91]

Outbreak of pyrogenic reactions and gram-negative bacteremia in 11 patients (four with bacteremia)

Water distribution system and machines not routinely disinfected according to manufacturer's recommendations; water and dialysate samples cultured using calibrated loops and blood agar plates

Disinfect machines according to manufacturer's instructions; include water distribution system in the weekly disinfection of the system; perform environmental monitoring of dialysis fluids using recommended methods

[92]

In a one-month period, 10 bacteremias and 6 pyrogenic reactions occurred in patients at a hemodialysis center

Preservative-free, single-use vials of epoetin alfa punctured multiple times, and residual epoetin alfa from multiple vials pooled and administered to patients

Follow manufacturer's recommendations for use of preservative free injectable medications

[93]

Phialemonium curvatum access infections in four hemodialysis patients; two died of systemic disease

Observations at the facility noted some irregularities in site prep for needle insertion; all affected patients had synthetic grafts; one environmental culture was positive of P. curvatum (condensate pan of HVAC) serving the dialysis facility

Review infection control practices; clean and disinfect the condensate HVAC system where water accumulates; perform surveillance on patients

[CDC unpublished data, 94]

Phialemonium curvatum blood stream infections in patients treated on the same hemodialysis machine

Patients dialyzed on a machine with a WHO port; P. curvatum isolated from treated water supplied to the station where the dialysis machine was located; water distribution system is disinfected once per year and cultures monitoring dialysis fluids were not performed on a routine basis

Eliminate dead legs in the distribution loop and disinfect the water distribution system on a regular schedule; follow manufacturer's instruction for disinfection and maintenance

[CDC unpublished data]

The early detection of pyrogenic reactions or gram-negative sepsis depends on a thorough understanding of the signs and symptoms of these entities by the dialysis staff and on the careful charting of the patient's symptoms and changes in blood pressure and temperature. The following diagnostic procedures are recommended for patients who meet the criteria of a pyrogenic reaction: a careful physical examination to rule out other causes of chills and fever (e.g., pneumonia, vascular access infection, urinary tract infection); blood cultures, other diagnostic tests (e.g., chest radiograph), and cultures as clinically indicated; collection of dialysis fluid from the dialyzer (downstream side) for quantitative and qualitative bacteriologic assays; and recording the incident in a log or other permanent record. Determining the cause of these episodes is important because they may be the first indication of a remediable problem.

Hemodialyzer Reuse

In the early 1960s, the most common dialyzer used in dialysis centers was the Kiil plate dialyzer, which was cleaned and disinfected after each patient use and supplied with a new set of cuprophane membranes. The dialyzer housing, however, was reused each time. With the development of disposable coil and hollow-fiber dialyzers, the use of the Kiil dialyzer was discontinued. Disposable dialyzers are medical devices that are supplied in a sterile state and were initially intended by the manufacturer for one-time use and since 1995 have required specific labeling that identified single use or multiple use [97]. In recent years, as a cost-saving effort, more centers are reusing dialyzers on the same patient after employing an appropriate disinfection procedure. Although it has caused some controversy, this is now standard practice in the dialysis community. From 1976–1983, the percentage of U.S. dialysis centers that reported reuse of disposable dialyzers increased from 18–52%. This upward trend in reuse continued until 1997 when 82% of centers reported that they reused disposable dialyzers on ≥1 patients [13]. In 1997, the average number of times a dialysis center reused dialyzers was 17 (range, 1–65). The mean number of times a dialyzer was reused was 38 (range, 1–179) [13]. Dialysis centers most likely to report reuse of dialyzers were those with larger patient populations (>40), those located in free-standing facilities, and those operated for profit compared with centers with smaller patient populations, those located in hospitals, and those not operated for profit [5,7,8,10,13]. However, within the last 6 years, one of the large U.S. dialysis provider organizations made a decision to discontinue reuse, which would account for the drop in reuse as of 2002 to 63% of facilities [2] and may eventually fall to the share of the dialysis market not represented by this provider.

CDC's surveillance project has not shown a correlation between HBV incidence or anti-Hepatitis C Virus (HCV) prevalence and dialyzer reuse. A study has shown a statistical association between the reuse of dialyzers disinfected with glutaraldehyde or peracetic acid/hydrogen peroxide and increased death rates at dialysis centers [98]. However, other factors may have contributed to what appears to be a causal relationship between reuse and a higher death rate, or the association may be due to unmeasured confounding factors [99,100,101].

In 1986, the U.S. Public Health Service (PHS) subsumed the AAMI's guidelines for reusing hemodialyzers [74] and recommended them as PHS guidance to the CMS, which, in turn, made them conditions for participation in Medicare/Medicaid. In effect, the AAMI guidelines, which became PHS guidance, resulted in CMS regulations. In general, if the procedures involved in reprocessing hemodialyzers are performed according to established and strict protocols, patients do not appear to have harmful effects. However, the practice of reusing disposable hemodialyzers should not be considered risk free. Outbreaks of patient infections and pyrogenic reactions associated with user error have occurred (Table 23-3). Many of these episodes were the result of inadequate reprocessing procedures, such as the use of incorrect concentrations of chemical germicides and failure to maintain standards for water quality [102]. In addition, in 1986, six dialysis centers reported outbreaks of pyrogenic reactions and septicemia that were associated with the use of a new germicide, the active ingredient of which was chlorine dioxide. That germicide, although efficacious for disinfecting dialyzers, appeared to degrade the integrity of cellulosic dialyzer membranes to such an extent that leaks in the membranes developed [103]. Centers that reported using this germicide employed manual reprocessing systems, and most of these centers reused their dialyzers >20 times.

In each of 3 successive years (1985–1988), reprocessing dialyzers in a manual reprocessing system was shown consistently to be significantly associated with a higher reported frequency of pyrogenic reactions, even with the use of other germicides, and was not necessarily related to the absolute number of reuses [4,104]. Some dialyzer membrane defects may go undetected when manual reprocessing systems are used because testing for dialyzer membrane integrity, as with an air-pressure leak test, generally is not performed with this type of system [105]. It is emphasized that adverse reactions associated with reuse of dialyzers are accentuated in dialysis centers that are having problems and that, for the most part, only a small number of centers are experiencing an increased risk with dialyzers that are reused >20 times or that include a manual reprocessing system. In 1993, only a modest and insignificant association between dialyzer reuse and reporting of pyrogenic reactions at U.S. hemodialysis centers occurred [10].

The procedures used in dialysis centers for reprocessing hemodialyzers usually cannot be classified as sterilization

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procedures but constitute high-level disinfection [70,105]. In 1983, most centers in the United States (94%) used 2% aqueous formaldehyde with a contact time of approximately 36 hours for high-level disinfection of disposable dialyzers [5]. Although this procedure may be satisfactory against the presumed microbiologic challenge of gram-negative water bacteria, it is inadequate for the highly germicide-resistant nontuberculous mycobacteria (Table 23-2).

CDC investigated an outbreak of infections caused by nontuberculous mycobacteria during which 27 infections occurred among 140 patients [27]. The source of the nontuberculous mycobacteria appeared to be the water used in processing the dialyzers. It was evident that 2% formaldehyde did not effectively inactivate populations of these mycobacteria within 36 hours. It was subsequently shown that 4% formaldehyde with a minimum contact time of 24 hours can inactivate high numbers of nontuberculous mycobacteria; as a consequence, 4% formaldehyde is recommended as a minimum solution for disinfection of dialyzers [70,105,106].

A similar outbreak of systemic mycobacterial infections in five dialysis patients, resulting in two deaths, occurred when high-flux dialyzers were contaminated with mycobacteria during manual reprocessing and were then disinfected with a commercial dialyzer disinfectant prepared at a concentration that did not ensure complete inactivation of mycobacteria [29]. These two outbreaks emphasize the need to use dialyzer disinfectants at concentrations that are effective against the more chemically resistant microorganisms, such as mycobacteria.

Formaldehyde (a chemical solution obtained from chemical supply houses) for reprocessing dialyzers is now considered to be both environmentally hazardous and hazardous to use in the dialysis setting; it has recently been classified as a human carcinogen (cancer-causing substance) by the International Agency for Research on Cancer and as a probable human carcinogen by the U.S. Environmental Protection Agency. The use of formaldehyde in the dialysis setting has been decreasing due to limits on the allowable amounts in the wastewater stream and to reduce potential occupational and patient exposures. During 1983–2002, the centers using formaldehyde for reprocessing dialyzers decreased from 94% to 22% while the use of peracetic acid increased to 72% [2]. A number of chemical germicides specifically formulated for reprocessing hemodialyzers have been shown to be effective and are approved by the Food and Drug Administration (FDA).

Pyrogenic reactions in dialysis patients caused by reprocessing dialyzers with water that did not meet AAMI standards have been frequently associated with epidemics investigated by the CDC (Table 23-3). In most of these outbreaks, the water used to rinse dialyzers or to prepare dialyzer disinfectants exceeded allowable AAMI microbial or endotoxin standards because the water distribution system was not disinfected frequently, the disinfectant was improperly prepared, or routine microbiologic assays were improperly performed.

The California Department of Health Services conducted a series of investigations of outbreaks of bloodstream infections (BSIs) associated with dialyzer reuse in 2001 and 2002. It found that the BSI clusters caused by Stenotrophomonas maltophilia, Burkholderia cepacia complex, Ralstonia pickettii, or Candida parapsilosis were more likely to occur in dialysis facilities that refrigerated dialyzers before reprocessing them [107].

High-Flux Dialysis

High-flux dialysis is a very efficient hemodialysis treatment that uses dialyzer membranes with hydraulic permeabilities 5–10 times greater than those of conventional dialyzer membranes. By using highly permeable membranes in dialyzers that have larger membrane surface areas than conventional dialyzers and higher blood flow rates, dialysis treatment times can be reduced from 4–5 hours to 2–3 hours. Between 1988 and 1999, the U.S. hemodialysis centers reported using high-flux dialyzer membranes on at least some patients increased from 23% to approximately 58% [5,108]. Because high-flux membranes are so permeable, there is concern that bacteria or endotoxin in the dialysate may penetrate these membranes, causing infections or pyrogenic reactions in the patient. Another concern is that high-flux dialysis requires the use of bicarbonate dialysate, which, unlike the acetate-based dialysate used almost exclusively since the 1970s, is prepared from a concentrate that can support rapid bacterial growth. Acetate dialysate is prepared from a single concentrate with such a high salt molarity (4.8 M) that most bacteria cannot grow in it. Bicarbonate dialysate, in contrast, must be prepared from two concentrates, an acid concentrate with a pH of 2.8 that is not conducive to bacterial growth and a bicarbonate concentrate with a relatively neutral pH and a salt molarity of 1.2 molar (M). Because the bicarbonate concentration will support rapid bacterial growth [25,109], its use can increase bacterial and endotoxin concentrations in the dialysate and, theoretically, may contribute to an increase in pyrogenic reactions, especially when it is used during high-flux dialysis.

Some of this concern may be justified. In 1980s and 1990s, surveillance data showed a significant association between use of high-flux dialysis and reporting of pyrogenic reactions during dialysis [5,6,7,8,9,10]. However, a prospective study of pyrogenic reactions in patients receiving >27,000 conventional, high-efficiency, or high-flux dialysis treatments with a bicarbonate dialysate containing high concentrations of bacteria and endotoxin found no association between pyrogenic reactions and the type of dialysis treatment [84,85]. Although there seem to be conflicting data on the relationship between high-flux dialysis and pyrogenic reactions, centers providing

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high-flux dialysis should be especially mindful of ensuring that dialysate meets AAMI microbial standards (Table 23-4).

Other Infections

Vascular Access Site Infections

Hemodialysis procedures depend on direct and repeated access to large blood vessels that can provide rapid extracorporeal blood flow. Scribner developed a method for vascular access by surgically inserting plastic tubes, one into an artery and one into a vein. After treatment, the circulatory access would be kept open by connecting the two tubes outside the body using a small U-shaped device, which would shunt the blood from the tube in the artery back to the tube in the vein [110,111]. Although the external arteriovenous (AV) shunts were the foundation on which modern dialysis grew, their use in recent years has been limited to patients who require temporary access to treatment. The material used for these shunts can be biologic or synthetic. External shunts are primarily used for those in emergent need for continuous renal replacement therapy (CRRT) when catheters (central or femoral lines cannot be placed [112]). Three primary types of vascular access are used for hemodialysis therapy: native AV fistulas, AV grafts, and central hemodialysis catheters [113].

The AV fistula is believed to provide the best long-term access to circulation with the least number of complications. However, only 33% of all U.S. hemodialysis patients have AV fistulas; 42% have AV grafts, and 26% use a central line for dialysis. The use of central venous catheters (CVCs) for vascular access has doubled since 1995 while the use of AV grafts has declined from 65% to 42% of patients. AV fistula use has increased from 22% of patients in 1995 to 33% of patients in 2002 [2].

Access site infections are particularly important because they can cause disseminated bacteremia/fungemia or loss of the access. Local signs of vascular access infection include erythema, warmth, induration, swelling, tenderness, skin breakdown, loculated fluid, or purulent exudate [114,115,116,117]. Vascular access site infections may account for 15–20% of all access-related complications. In general, the length of time that a catheter is left in place and the duration of cannulation can be important factors predisposing to infection. In addition, the type of fistula, nature of the access site dressing, number of needle access events, movement of the site, and personal hygiene of the patient may play a role in the acquisition of infection. BSIs can occur, either by migration of bacteria down the outer surface of a hemodialysis catheter (tunnel) or by contamination of the lumen of the catheter during attachment or detachment during dialysis. Infections of the vascular access site can lead to sepsis, septic pulmonary emboli, endocarditis, or meningitis. No controlled prospective studies have been performed; thus, reported rates of access site infections among hemodialysis patients vary. Although the most frequent pathogens are Staphylococcus aureus or S. epidermidis, gram-negative bacteria also can be responsible for access site infections, especially if the site is in the patient's lower extremities. Transmission of these types of bacterial infections among patients or from staff members to patients in the hemodialysis center setting is primarily due to cross-contamination, which results in colonization and subsequent infection in a subset of these patients. Transmission can be controlled by good hand-hygiene and gloving techniques as well as good puncture techniques [118,119,120,121,122,123,124].

Figure 23-1 Rates of blood stream infection by access type—Dialysis Surveillance Network, 1999–2005.

For many years, central (subclavian or jugular) catheters have been used for temporary venous access for hemodialysis. Recent technical improvements have made it feasible to use these catheters for permanent access, usually in patients for whom no other access is available [125]. However, CVCs have high rates of failure due to thrombosis and infection (Figure 23-1) [125]. In 1991, CDC investigated 35 BSIs among 68 patients receiving

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hemodialysis through CVCs; one patient died and one developed endocarditis and required aortic valve replacement [126].

Infections Associated with Peritoneal Dialysis

As mentioned earlier, approximately 6–7% of U.S. ESRD patients were treated by peritoneal dialysis at the end of 2003 [1]. In peritoneal dialysis, the patient's peritoneal membrane is used to dialyze waste products from the patient's blood. In the mid-1970s, the development of automated peritoneal dialysis systems made intermittent peritoneal dialysis a viable alternative to hemodialysis for long-term management of ESRD patients. Currently, this approach has been replaced by chronic ambulatory peritoneal dialysis (CAPD), continuous-cycling peritoneal dialysis (CCPD), and chronic intermittent peritoneal dialysis (CIPD) in which presterilized dialysis fluid is either introduced by gravity or is cycled into a patient's peritoneal cavity. In CAPD, commercially available sterile dialysate in a plastic bag is self-administered by the patient who has a surgically implanted catheter. The exchanges are done every 4 hours, and the patient can be mobile between exchanges [127]. The most persistent problem in the management of patients treated by peritoneal dialysis is peritonitis [128,129].

In the past, automated peritoneal machines were used to create dialysate from tap water. To prevent the growth of pathogenic microorganisms that cause infection, automated peritoneal dialysis machines had to be cleaned and maintained properly. In theory, the incidence of peritonitis should be low because the machine functions as a closed system. However, the machines may themselves provide a reservoir for pathogens that cause peritonitis. Several outbreaks of bacterial peritonitis among patients receiving intermittent peritoneal dialysis have been reported, and the etiologic agents have included Mycobacterium chelonei–like organisms or Pseudomonas cepacia [30,131]. Both organisms can grow in water; investigation of these outbreaks revealed that machines were inadequately cleaned and disinfected and that the product water and dialysis fluid contained the microorganisms responsible for peritonitis [132]. In addition, one group of organisms, the nontuberculous mycobacteria such as M. chelonae, is significantly and extraordinarily resistant to the commonly used disinfectants [133]. Berkelman et al. recommended a set of guidelines that can ensure the production of sterile dialysis fluid and reduce the likelihood of outbreaks of peritonitis for dialysis centers using automated peritoneal dialysis machines [135]. The precise details and protocols differ for each machine type, and the reader is referred to the guidelines for a more complete discussion [134]. It should be noted that, for all practical purposes, the use of these automated peritoneal dialysis machines has been discontinued in the United States, and the preceding information is cited for completeness and for historical considerations.

With CAPD, CCPD, or CIPD, catheter-related infections and peritonitis remain the most common cause of morbidity among peritoneal dialysis patients, contribute significantly to the cost of this treatment, and are the primary reason for the abandonment of peritoneal dialysis. Incidence rates for peritonitis vary widely among centers and among modalities. In general, peritonitis has dramatically decreased from the inception of CAPD; rates >0.5 episodes per patient per year are still common [135,136,137,138]. The use of CCPD or CIPD in centers with experienced staff, patients, and patient caregivers has resulted in substantially reduced infection rates compared to CAPD. The weak link with peritoneal dialysis and the present catheter technology is the associated risk of tunnel or exit site infections. These infections occur at a rate of 0.7 episodes per patient per year [128,138,139,140].

Clinical symptoms of peritoneal infection usually appear 12–36 hours after bacterial contamination of the peritoneal cavity. Symptoms include nausea, vomiting, and abdominal pain. Later, vague abdominal tenderness may progress to severe, diffuse, or localized pain associated with fever, abdominal distention, and gastrointestinal dysfunction. The clinical diagnosis should be confirmed by bacteriologic analysis of the peritoneal fluid. Cloudy peritoneal fluid often is the first sign of infection.

The etiologic agents of peritonitis associated with conventional peritoneal dialysis usually are S. epidermidis, S. aureus, and other gram-positive bacteria, which collectively account for 55–80% of episodes; 17–30% of episodes are caused by gram-negative organisms such as Enterobacteriaceae, Pseudomonas aeruginosa, Burkholderia cepacia, and Acinetobacter species; in a few instances (10%), peritonitis is caused by fungi, yeast, mycobacteria, or anaerobic bacteria. Approximately 10% of episodes will be culture negative [128,141,142].

The primary strategy for controlling peritonitis is to prevent contamination of the dialysis fluid that enters the peritoneal cavity and to prevent tunnel and exit site infections. Prevention involves (1) aseptic manipulation of the sterile disposable plastic lines leading into the abdominal catheter that deliver the dialysis fluid into the peritoneal cavity, (2) a system for aseptic connection of the tubing containing the sterile dialysis fluid and the patient's catheter, and (3) appropriate access site care [143,144].

Noninfectious Complications

First-Use and Allergic Reactions

A variety of symptoms attributed to hypersensitivity reactions may occur during dialysis. Symptoms variously reported include increased or decreased blood pressure, dyspnea, cough, conjunctival injection, flushing, urticaria, headache, and pains in the chest, back, and limbs. Such symptoms are more common during the first use of a dialyzer and have been termed the “first-use syndrome” [145,146]. These reactions are more common with

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cuprophan dialyzers; some may be attributable to residual ethylene oxide in dialyzers [147,148,149]. During 1992–1993, such reactions were reported by 24–27% of dialysis centers and were most strongly associated with the use of cuprophan and regenerated cellulose membranes [10]. Reports of first-use syndrome have decreased from 43% of centers in 1984 to 23% of centers in 1997 [13].

In 1990, several outbreaks of anaphylactoid reactions associated with angiotensin-converting enzyme (ACE) inhibitors were reported. Reactions occurred within 10 minutes of initiating dialysis and included nausea, abdominal cramps, burning, flushing, swelling of the face or tongue, angioedema, shortness of breath, and hypotension. One outbreak was linked to the reuse of dialyzers [150], but other reports implicated polyacrylonitrile (PAN) dialyzers in the reactions [151,152,153,154]. In 1992, the FDA issued a safety alert regarding anaphylactoid reactions in patients on ACE inhibitors, especially those using PAN dialyzers [155].

Dialysis Dementia

Dialysis encephalopathy, or dialysis dementia, is a disorder that affects dialysis patients who, for a variety of reasons, are subjected to water that has a relatively high content of aluminum, such as community water supplies treated with alum. This complication was first described in 1972 by Alfrey et al. [156]. Schreeder et al. [157] first demonstrated the role of aluminum as a significant contributing factor in this disorder in an epidemiologic study. Case definitions of dialysis encephalopathy include three different groups of objective findings:

  1. Speech impairment (stuttering, stammering, dysnomia, hypofluency, mutism).
  2. Seizure disorder (generalized tonic-clonic, focal, or multifocal seizures).
  3. Motor disturbance (myoclonic jerks, motor apraxia, immobility).

Schreeder et al. [157] showed that patients were at increased risk of dialysis dementia when the aluminum content of water used to prepare dialysate was high (>100 ng/L). The number of episodes of dialysis dementia reported to CDC has decreased from 0.4% in the years 1980 and 1983–1985 to 0.1% in 1990 (N = 129; case-fatality rate = 21%) [7]. Although it is not clear what was responsible for this decrease, we believe it may be related to increased awareness in the dialysis community of the requirement for good water treatment systems. In 1980, only 26% of U.S. hemodialysis centers reported that they employed a reverse osmosis system, either alone or with deionization in their water treatment systems. By 1988, 91% of the centers were using reverse osmosis alone or in combination with deionization as an integral part of their water treatment system [5]. Control of dialysis dementia revolves around adequate water treatment systems and invariably requires the use of reverse osmosis, either alone or with deionization.

It also is important to ensure that all components of the water treatment and dialysis fluid preparation and delivery systems be compatible with all fluid with which they are in contact in order to eliminate the possibility of leaching of harmful substances. In one outbreak, 58/85 (68%) dialysis patients at a dialysis center were diagnosed with acute or chronic aluminum intoxication that resulted in three deaths. Investigation revealed that the acidified portion (pH = 2.7) of the bicarbonate-based dialysate solution was passed through a pump with an aluminum housing, and aluminum was leached out of the pump and into the dialysate solution in concentrations exceeding 200 ppm and was present in the dialysis fluid [158].

Toxic Reactions

Chemicals in water or as residuals in dialysis fluid can affect dialysis patients. Certain chemicals in water may not be toxic when ingested by humans, but the hemodialysis patient may be exposed directly to 150 L of water per treatment. Two examples will illustrate this problem.

Occasionally, suppliers of community water change their water disinfection patterns by increasing chlorine dosages or by using monochloramine. These changes usually occur without the knowledge of the dialysis staff. Monochloramine (combined chlorine) in water used to prepare dialysis fluid must be removed or the patient will experience acute hemolysis. Patients will be exposed to this chemical if the correct water treatment system component (activated carbon) is not present or operating in the dialysis center. In one instance, a dialysis center changed from acetate to bicarbonate dialysate, adding an additional reverse osmosis unit and tanks for preparation and dilution of the dialysate. No changes were made to increase the capacity of the carbon filter, and within a few weeks, approximately 100 of the center's dialysis patients were exposed to chloramine-contaminated dialysate when the undersized carbon filters failed. A total of 41 patients required transfusion to treat hemolytic anemia caused by the chloramine exposure [34].

Another example of chemical intoxication occurred when a city water treatment plant accidentally fed excessive levels of fluoride into the community water supply, resulting in the death of one dialysis patient and acute illness in several other patients in a hemodialysis center receiving this community water supply. The center's water treatment system was not adequate to remove excessive fluoride from water [159].

In both of the preceding examples, a properly designed water treatment system consisting of adequate carbon filtration for the fluid flow and volume plus the use of reverse osmosis, deionization, and ultrafiltration would have prevented toxic reactions.

There also have been instances in which a disinfectant, such as formaldehyde, was not sufficiently removed from dialysis systems, and patients were exposed to the chemical.

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This can be prevented by monitoring the system for complete rinsing using a chemical assay sensitive to the chemical.

A summary of toxic reactions in hemodialysis patients that have been investigated by the CDC is given in Table 23-6.

TABLE 23-6
CDC-INVESTIGATED OUTBREAKS OF CHEMICAL INTOXICATIONS IN HEMODIALYSIS FACILITIES

Description

Cause(s) of Outbreak

Corrective Measure

Reference

Hemolytic anemia in 41 patients

Monochloramine in city water not removed completely by carbon filters

Size carbon adsorption media and place in series configuration (worker + polisher); monitor chloramines before each patient shift

[34]

Decreased hemoglobin in 3 pediatric patients

Disinfectant (30% hydrogen peroxide) not adequately rinsed from the water distribution system

Thoroughly rinse germicide from the system; use an appropriate test kit to confirm rinse out

[160]

Severe hypotension in 9 patients

Dialysate contaminated with sodium azide from new ultrafilters

Rinse system after modification or installation of new components; use equipment suitable for medical use

[161]

Aluminum intoxication in 27

Exhausted deionization tanks unable to remove aluminum from city water

Monitor deionization tanks daily; install reverse osmosis system

[162]

Formaldehyde intoxication in 5 patients, 1 death

Disinfectant not properly rinsed from the system

Eliminate stagnant flow areas; test for residual germicide

[163]

Aluminum intoxication in 27; 3 deaths

Aluminum pump was used to transfer acid concentrate to the treatment area

Use components that do not leach harmful substances into dialysis fluids.

[158]

Fluoride intoxication in 8; 1 death

Excess fluoride in city water; no water treatment by center

Install reverse osmosis system

[159]

Fluoride intoxication in 9 patients; 3 deaths

Exhausted deionization tanks discharge a bolus of fluoride

Deionization tanks should be monitored by resistivity meters with audible and visual alarms

[164, 165]

126 patients were exposed to microcystins in the dialysate; 47 patients died

Untreated water delivered to dialysis facility by tanker truck; by water system

Install appropriate water treatment equipment (granular activated carbon and reverse osmosis)

[166]

Sudden death in at least 50 patients in Spain, Croatia, Italy, Germany, Taiwan, Colombia and the United States

A perfluorohydrocarbon-based performance fluid used to detect in manufacturing the dialyzers was not adequately rinsed from all of the dialyzers

Improve quality control mechanisms at the manufacturing level before release of products; improve dialyzer priming at the facility level

[167, 168, CDC unpublished data, 2001]

16 patients exposed to volatile sulfur compounds; 2 deaths

Volatile sulfur-containing compounds (ie, methanethiol, carbon disulfide, dimethyldisulfide, and sulfur dioxide) were detected by gas chromatography and mass spectrometry in 8 of 12 water samples from the RO unit

Water treatment system including reverse osmosis system should be maintained; include distribution loop when disinfecting the reverse osmosis

[169]

Blood Borne Viruses: Viral Hepatitis and Acquired Immunodeficiency Syndrome

Introduction

Shortly after the art and science of hemodialysis was institutionalized, it was recognized that both patients and staff members were at risk of acquiring viral hepatitis. The development and use of specific serologic testing identified HBV, and later HCV, as those most likely to be transmitted within the hemodialysis environment. Other blood borne pathogens that need to be considered as potentially transmissible in hemodialysis centers include hepatitis delta virus (HDV) and human immunodeficiency virus (HIV). The CDC has conducted 19 investigations involving the transmission of blood borne pathogens (Table 23-7). Hepatitis A virus (HAV), which is spread by the fecal-oral route and rarely by blood, has not been associated with hemodialysis.

Since HBV is the most efficiently transmitted blood borne virus in the dialysis setting, long-standing precautions developed for and shown to be effective in its control will be used, in part, as a model for the prevention of transmission of other blood borne infections. The primary rationale is that infection control practices that effectively control HBV transmission also would be effective

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for other blood borne viruses such as HCV and HIV because their efficiency of transmission is much less than that of HBV.

TABLE 23-7
TRANSMISSION OF BLOOD BORNE PATHOGENS IN HEMODIALYSIS FACILITIES

Description

Cause(s) of Outbreak

Corrective Measure

Reference

26 patients seroconverted to HBsAg positive over a 10-month period

Leakage of coil dialyzer membranes and use of a dialysis machine employing a recirculating bath

Separate HBsAg-positive patients and their equipment from other patients

[170]

19 Patients and 1 staff seroconverted to HBsAg positive during a 14-month period

No specific cause determined; false positive HBsAg results caused some susceptible patients to be dialyzed with HBsAg-positive patients

Laboratory confirmation of HBsAg-positive results; strict adherence to glove use and use of separate equipment

[171]

24 patients and 6 staff seroconvert to HBsAg positive during 10-month period

Staff not wearing gloves; surfaces not properly cleaned and disinfected; improper handling of needles/sharps resulting in many needlesticks

Separation of HBsAg-positive patients and equipment from other patients; proper precautions by staff (e.g. glove use; handling of needles/sharps)

[172]

13 patients and 1 staff seroconverted to HBsAg positive during a 1-month period

Extrinsic contamination of intravenous medication being prepared adjacent to area where blood work handled

Separate medication preparation area and blood processing for diagnostic tests

[173]

10 patients seroconverted from HBsAg positive in 1 month

Extrinsic contamination of a multidose intravenous medication vial shared by HBsAg-positive and negative patients

No sharing of supplies, equipment, and medications between patients

[174]

8 patients seroconverted to HBsAg positive during a 5-month period

Sporadic screening for HBsAg; HBsAg carriers not separated

Monthly screening of HBsAg-positive patients from other patients and have dedicated equipment and staff; vaccination of susceptible

[CDC unpublished data]

7 patients seroconverted to HBsAg positive during 3-month period

Same staff caring for HBsAg-positive and negative patients

Separation of HBsAg-positive patients from other patients; same staff should not care for HBsAg-positive and negative patients on the same shift

[175]

8 patients seroconverted to HBsAg positive during 1 month

Not consistently using pressure transducer protectors; same staff members cared for HBsAg-positive and negative patients on the same shift

Use pressure transducer protectors and replace after each use; same staff should not care for HBsAg-positive and negative patients on the same shift

[176]

14 patients seroconverted to HBsAg positive during a 6-week period

Failure to review results on admission and monthly HBsAg testing; inconsistent hand washing and use of gloves; adjacent clean and contaminated areas; <20% of patients vaccinated

Proper infection control precautions for dialysis units; routine review of serologic testing; hepatitis B vaccination of all susceptible patients

[177]

7 patients seroconvert to HBsAg positive during a 2-month period

Same staff member cared for both HBsAg-positive and negative patients on the same shift; common medication and supply carts were moved between patient stations, and medication vials were shared; no patients were vaccinated

Dedicate staff for HBsAg-positive patients; no sharing of medications or supplies between any patients; centralized medication and supply areas; hepatitis B vaccination of all susceptible patients

[177]

4 patients seroconverted to HBsAg positive during a 3-month period

Transmission appeared to occur during hospitalization at an acute facility

Vaccinated all susceptible patients against hepatitis B

[177]

11 patients seroconverted to HBsAg positive during a 3-month period

Staff, equipment, and supplies were shared between HBsAg-positive and negative patients; no patients vaccinated

Dedicate staff for HBsAg-positive patients; no sharing of medications or supplies between any patients; hepatitis B vaccination of all susceptible patients

[177]

2 patients seroconverted to HBsAg positive during a 4-month period

Same staff member cared for both HBsAg-positive and negative patients; no patients were vaccinated

Dedicate staff for HBsAg-positive patients; vaccinate all susceptible patients

[178]

36 patients with elevated liver enzymes consistent with non-A, non-B hepatitis

Environmental contamination with blood

Monthly liver enzyme screening; proper precautions (i.e., gloves) by staff

[179]

35 patients with elevated liver enzymes consistent with non-A, non-B hepatitis during a 22-month period; 82% of probable cases were anti-HCV positive

Inconsistent use of infection control precautions, especially hand washing and glove use

Strict compliance to aseptic techniques and dialysis unit precautions

[180]

HCV infection developed in 7/41 (17.1%) patients; shift specific attack rates of 29% to 36%

Multidose vials left on top of machine and used by multiple patients; cleaning and disinfection of surfaces and equipment not routinely done; arterial lines for draining prime waste dropped into bucket that was not routinely cleaned or emptied between patients

Strict compliance with infection control precautions recommended for all patients; routine testing for HCV

[181]

HCV infection developed in 5/75 (6.7%) of patients

Sharing equipment and supplies between chronically infected and susceptible patients; gloves not routinely used; clean and contaminated areas not separated

Strict compliance with infection control precautions recommended for all patients

[182]

HCV infection developed in 3/23 (13%) of patients

Supply carts moved between stations and contained both clean supplies and blood-contaminated items; medications prepared in the same area used for disposal of used injection equipment

Strict compliance with infection control precautions recommended for all patients

[183]

13 patients found to be HIV positive; 9 seroconverted after the admission of a known HIV-positive patient

Access needles reprocessed by soaking in a common container with a low-level disinfectant, benzalkonium chloride; access needles reused on different patients

Do not reuse access needles

[184]

39 patients at 2 dialysis centers developed HIV infection

Sharing of syringes among patients was observed at both centers

Do not share syringes between patients; infection control guidelines for hemodialysis settings

[185]

Viral Hepatitis

Hepatitis B Virus

Epidemiology

Hepatitis B Virus (HBV) is transmitted by percutaneous or per mucosal exposure to infectious blood or body fluids that contain blood. Hepatitis B surface antigen (HBsAg)-positive persons who also are positive for hepatitis B e antigen (HBeAg) have an extraordinary level of HBV circulating in their blood, approximately 108 virions per milliliter. With virus titers this high, body fluids containing serum or blood also may contain appreciable levels of HBV, and HBV can be present on environmental surfaces in the absence of any visible blood and still contain 102–103 infectious virions per milliliter [186]. Furthermore, HBV is relatively stable in the environment, and has been shown to remain viable for at least 7 days on environmental surfaces at room temperature [187]. Thus, wherever there is a good deal of blood exposure, the risk of HBV transmission can be high if proper control measures are not practiced. This is especially true in a hemodialysis center setting.

In the past, HBV infection could be acquired by patients in a dialysis unit by transfusion of infectious blood or blood products. This is very unlikely now since all blood is screened for HBsAg and antibody to hepatitis B core antigen (anti-HBc) and with the use of erythropoietin in dialysis patients. Dialysis patients, once infected, frequently become chronically infected but asymptomatic and are sources of HBV contamination of many environmental surfaces.

Given the extraordinarily high level of HBV in blood, the various modes of HBV transmission can be categorized based on efficiency as follows:

  1. Direct percutaneous inoculation of HBV by needle from contaminated blood, serum, or plasma.
  2. Percutaneous transfer of blood, serum, or plasma, such as may occur through cuts, scratches, abrasions, or other breaks in the skin.

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  1. Transfer of infected blood, serum, or plasma onto mucosal surfaces such as may occur through inadvertent introduction of these fluids into the mouth or eyes.
  2. Introduction of other known infectious secretions, such as saliva and peritoneal fluid, onto mucosal surfaces.
  3. Indirect transfer of HBV from blood, serum, or plasma by means of environmental surface contamination.

There is no epidemiologic or laboratory evidence of airborne HBV transmission [188,189], and no disease transmission occurs by the intestinal route. Splashes of infectious blood that enter the oral cavity may result in HBV infection because the virus enters the vascular system through the buccal cavity but not the intestinal tract.

V transmission can occur by a number of routes in the hemodialysis center setting. Staff members may become infected with HBV through accidental needle punctures or breaks in their skin or mucous membranes. These staff members have frequent and continuous contact with blood and blood-contaminated surfaces. Dialysis patients may acquire HBV infection in several ways, including (1) internally contaminated dialysis equipment (e.g., venous pressure gauges or venous pressure isolators or filters used to prevent reflux of blood into gauges) not routinely changed after each use, (2) injections (by contamination of the site of injection or the material being injected), or (3) breaks in the skin or mucous membranes that have contact with blood-contaminated objects. Patients who are dialyzed in centers that routinely reuse dialyzers are not at increased risk of HBV infection because of this practice [190].

There is no documentation that HBV has been transmitted from infected hemodialysis staff members to dialysis patients. Hypothetically, this route of transmission is possible but not likely because infectious blood and body fluids of dialysis personnel are not readily accessible to patients. However, dialysis staff members may physically carry HBV from infected patients to susceptible patients by means of contaminated hands, gloves, and other objects.

Environmental surfaces in the hemodialysis center can play a role in HBV transmission. It has been shown that HBsAg, which is considered a “footprint” of HBV, can be detected on environmental surfaces (especially those often touched) in dialysis center settings [186]. For example, HBsAg has been detected on clamps, scissors, dialysis machine control knobs, doorknobs, and other surfaces. If these surfaces or objects are not cleaned or disinfected frequently and are shared among patients using the same or neighboring machines, an almost unnoticeable infection transmission route is created. Although dialysis staff members may routinely change gloves after caring for each patient, a new pair of gloves can become contaminated when the staff member touches surfaces previously contaminated with blood from an HBsAg-positive patient. HBV can be transmitted from patient to patient when a staff member wearing the contaminated gloves searches for the patient's best site of injection by applying finger pressure or by otherwise contaminating that site before injection. When donning a pair of new gloves, staff members should refrain from touching any environmental surfaces before performing the injection on the patient. Other environmental sources of contamination include shared items, such as multiple dose medication vials that can become contaminated with blood and serve as sources of patient-to-patient transmission.

This potential for the environmentally mediated mode of virus transmission rather than any phenomenon dealing with internal contamination of dialysis machines is the basis for the infection control strategies recommended for preventing HBV transmission in dialysis centers.

Surveillance data from the CDC show that, between 1972 and 1974, the incidence of HBsAg positivity among patients or staff increased by >100% to 6.2% and 5.2%, respectively [191,192]. In a separate survey of 15 hemodialysis centers during the same 2-year period, Szmuness et al. [193] showed that the point prevalence of a positive test for HBsAg was 16.8% among patients and 2.4% among staff. During this time, HBV infection in dialysis units had become highly endemic, and outbreaks were common because of the presence of chronically infected patients who were asymptomatic, the absence of sufficient disease and serologic surveillance systems to detect these chronic infections, and the lack of infection control measures to prevent transmission [170,172].

Subsequently, infection control strategies were developed to incorporated precautions for preventing exposures to blood and body fluids among both patients and staff with several extra precautions [194]. As will be discussed, these extra precautions included routinely testing all dialysis patients and staff members for HBsAg, dialyzing HBsAg-positive patients in separate areas or rooms in the dialysis center using dedicated dialysis machines and staff, rather than including HBsAg-positive patients in dialyzer reuse programs.

Continued nationwide surveillance by the CDC found that, by 1983, the incidence of HBV infection had declined to 0.5% among both patients and staff members [195]. Over the same period, the proportion of centers using separation practices increased from 75% to 86%, and the proportion of centers that screened patients monthly for HBsAg increased from 57% to 84%. In addition, the risk of acquiring HBV infection for patients was shown to be highest in those centers that provided dialysis to HBsAg-positive patients but did not separate these patients by room and machine. Other investigators also have shown that segregation of HBsAg-positive patients and their equipment reduces the incidence of HBV infection in hemodialysis units [196,197]. The success of separation practices in preventing HBV transmission can be linked to other control recommendations, including frequent serologic surveillance. Routine serologic surveillance facilitates the rapid identification of patients who become HBsAg-positive,

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which allows for the rapid implementation of isolation procedures before cross-infection can occur.

In 2002, the prevalence of HBsAg positivity among patients was 1.0%, a figure that has not changed substantially during the past decade. Similarly, the incidence of HBV infection in hemodialysis patients has not changed substantially during the past decade and in 2002 was 0.12% [2]. In 1994, an increasing number of centers reported to CDC episodes of HBV transmission among their patients. During a 5-month period in 1994 alone, five HBV outbreaks in chronic hemodialysis centers were investigated by CDC and/or state and local health authorities [177]. All were the result of failure to follow ≥1 recommended infection control practices for the prevention of HBV transmission in these settings including the failure to routinely screen patients for HBsAg or routinely review results of testing to detect infected patients; assignment of staff to the simultaneous care of infected and susceptible patients; and sharing supplies, particularly multidose medication vials, among patients. These same factors have typically been responsible for most other hemodialysis-associated HBV outbreaks reported in the past [170,172,175]. In addition, few patients in these centers had received HBV vaccine. Although HBV vaccine has been recommended for all hemodialysis patients since it became available in 1982, it has been shown to reduce the costs of serologic screening [198]. From 1983–2002, the percentage that had ever received at least three doses of HBV vaccine increased from 5.4% to 56% among patients and from 26.1% to 90% among staff [2]. As these outbreaks illustrate, the generally low incidence of HBV infection among hemodialysis patients does not preclude the need to maintain infection control measures that were specifically formulated to prevent the transmission of blood borne pathogens in these settings.

Screening and Diagnostic Tests

Several well-defined antigen-antibody systems are associated with HBV infection, including HBsAg and anti-HBs; hepatitis B core antigen (HBcAg) and anti-HBc; and HBeAg and antibody to HBeAg (anti-HBe). Serologic assays are commercially available for all of these except HBcAg because no free HBcAg circulates in blood. One or more of these serologic markers are present during different phases of HBV infection (Table 23-8) [199].

TABLE 23-8
INTERPRETATION OF SEROLOGIC TEST RESULTS FOR HEPATITIS B VIRUS INFECTION

Serological Markers

HBsAga

Total Anti-HBcb

IgMc Anti-HBc

Anti-HBSd

Interpretation

a Hepatitis B surface antigen.
b Antibody to hepatitis B core antigen.
c Immunoglobulin M.
d Antibody to hepatitis B surface antigen.
e Transient HBsAg positivity (lasting <18 days) might be detected in some patients during vaccination.

Susceptible, never infected

+

Acute infection, early incubatione

+

+

+

Acute infection

+

+

Acute resolving infection

+

+

Past infection, recovered and immune

+

+

Chronic infection

+

False positive (i.e., susceptible), past infection, or “low-level” chronic infection

+

Immune if titer is >10 mIU/mL

The presence of HBsAg indicates ongoing HBV infection and potential infectiousness. In newly infected persons, HBsAg is present in serum 30–60 days after exposure to HBV and persists for variable periods. Transient HBsAg positivity (lasting <18 days) can be detected in some patients during vaccination [200,201]. Anti-HBc develops in all HBV infections, appearing at onset of symptoms or liver test abnormalities in acute HBV infection, rising rapidly to high levels, and persisting for life. Acute or recently acquired infection can be distinguished by the presence of the immunoglobulin M (IgM) class of anti-HBc, which persists for approximately 6 months.

In persons who recover from HBV infection, HBsAg is eliminated from the blood, usually in 2–3 months, and anti-HBs develop during convalescence. The presence of anti-HBs indicates immunity from HBV infection. After recovery from natural infection, most persons will be positive for both anti-HBs and anti-HBc whereas only anti-HBs develop in persons who are successfully HBV vaccinated. Persons who do not recover from HBV infection and become chronically infected remain positive for HBsAg (and anti-HBc), although a small proportion (0.3% per year) eventually clear HBsAg and might develop anti-HBs [202].

In some persons, the only HBV serologic marker detected is anti-HBc (i.e., isolated anti-HBc). Among most asymptomatic persons in the United States tested for HBV infection, an average of 2% (range: <0.1–6%) test positive for isolated anti-HBc [203]; among injecting-drug users, however, the rate is 24% [204]. In general, the frequency of isolated anti-HBc is directly related to the frequency of previous HBV infection in the population and can have several explanations. This pattern can occur after HBV infection among persons who have recovered but whose anti-HBs levels have waned or among persons who failed to develop anti-HBs. Persons in the latter category include those who circulate HBsAg at levels not detectable

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by current commercial assays. However, HBV DNA has been detected in <10% of persons with isolated anti-HBc, and these persons are unlikely to be infectious to others except under unusual circumstances involving direct percutaneous exposure to large quantities of blood (e.g., transfusion) [205]. In most persons with isolated anti-HBc, the result appears to be a false positive. Data from several studies have demonstrated that a primary anti-HBs response develops in most of these persons after a three-dose series of HBV vaccine [206,207]. No published data exist on response to HBV vaccination among hemodialysis patients with this serologic pattern.

A third antigen, HBeAg, can be detected in serum of persons with acute or chronic HBV infection. The presence of HBeAg correlates with viral replication and high levels of virus (i.e., high infectivity). Anti-HBe correlates with the loss of replicating virus and with lower levels of virus. However, all HBsAg-positive persons should be considered potentially infectious, regardless of their HBeAg or anti-HBe status.

Hepatitis C

Epidemiology

Data are limited on the current incidence or prevalence of HCV infection among maintenance hemodialysis patients. In 2002, 63% of dialysis centers tested patients for anti-HCV, and 11.5% reported having ≥1 patient who became anti-HCV positive in 2002 The incidence rate in 2002 was 0.34%; among centers that tested for anti-HCV, the prevalence of anti-HCV among patients was 7.8%, a decrease of 25.7% since 1995 [2]. In the facilities that tested, the reported incidence was 0.34%, and the prevalence was 7.8% (range among ESRD networks, 5.7% to 9.8%). Only 11.5% of dialysis facilities reported newly acquired HCV infection among their patients. Higher incidence rates have been reported from cohort studies of U.S. dialysis patients (<1–3%), Japan (<2%), or Europe (3–10%) [208,209,210,211,212,213,214,215,216]. Higher prevalence rates (10–76%) also have been reported in individual facilities [208,217,218,219,220,221,222].

HCV is most efficiently transmitted by direct percutaneous exposure to blood, and like HBV, the chronically infected person is central to the epidemiology of HCV transmission. Hemodialysis staff members have rates of anti-HCV comparable to those (1–2%) reported in other healthcare workers [223]. Risk factors associated with HCV infection among hemodialysis patients include blood transfusions from unscreened donors and years on dialysis [208,219,224,225]. The number of years on dialysis is the major risk factor that is independently associated with higher HCV infection rates. As the time patients spent on dialysis increased, their prevalence of HCV infection increased from an average of 12% for patients receiving dialysis <5 years to an average of 37% for patients receiving dialysis >5 years [208,219,226,227].

These studies and investigations of dialysis-associated HCV outbreaks indicate that HCV transmission most likely occurs because of inadequate infection control practices. During 1999 to 2000, CDC investigated three outbreaks of HCV infection among patients in chronic hemodialysis centers [CDC, unpublished data, 1999, 2000]. In two of the outbreaks, multiple HCV transmissions occurred during periods of 16–24 months (attack rates: 6.6–17.5%), and seroconversions were associated with receiving dialysis immediately after a chronically infected patient. Multiple opportunities for cross-contamination among patients were observed including (1) equipment and supplies that were not disinfected between patient use, (2) use of common medication carts to prepare and distribute medications at patient stations, (3) sharing of multidose vials, which were placed at patients' stations on the top of the hemodialysis machine, (4) contaminated priming buckets that were not routinely changed or cleaned and disinfected between patients; (5) machine surfaces that were not routinely cleaned and disinfected between patients; and (6) blood spills that were not cleaned up promptly. In the third outbreak, there were multiple infections clustered at one point in time (attack rate of 27%), suggesting a common exposure event. Multiple opportunities for cross-contamination from chronically infected patients also were observed in this unit. In particular, supply carts were moved from station to station and contained both clean supplies and blood-contaminated items, including small biohazard containers, sharps disposal boxes, and used Vacutainers containing patients' blood.

Other risk factors for acquiring HCV include injection drug use, exposure to an HCV-infected sexual partner or household contact, multiple sexual partners, and perinatal exposure [223,228]. The efficiency of transmission in settings involving sexual or household exposure to infected contacts is low, and the magnitude of risk and the circumstances under which these exposures result in transmission are not well defined.

Screening and Diagnostic Tests

FDA-licensed or approved anti-HCV screening tests used in the United States comprise three immunoassays; two enzyme immunoassays (EIA) and one enhanced chemiluminescence immunoassay (CIA) [229,230]. Although no true confirmatory test has been developed, supplemental tests for specificity are available. The FDA-licensed or approved supplemental tests include a serologic anti-HCV assay, the strip immunoblot assay (Chiron RIBA® HCV 3.0 SIA, Chiron Corp., Emeryville, California), and nucleic acid tests (NAT) for HCV RNA (including reverse transcriptase polymerase chain reaction [RT-PCR] amplification [231] and transcription mediated amplification [TMA]).

Anti-HCV testing includes initial screening with an EIA immunoassay. However, interpretation of the results of EIAs that screen for anti-HCV is limited by several factors: (1) these assays will not detect anti-HCV in approximately 10% of persons infected with HCV, (2) these assays do not distinguish between acute, chronic, or past infection,

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(3) in the acute phase of hepatitis C, the interval between onset of illness and seroconversion may be prolonged, and (4) in populations with a low prevalence of infection, the rate of false positivity for anti-HCV is high. If the screening test is positive, supplemental testing with a test with high specificity should be performed to verify the results. Among hemodialysis patients, the proportion of false-positive screening test results averages approximately 15% [229]. For this reason, one should not rely exclusively on a positive anti-HCV screening test to determine whether a person has been infected with HCV.

TABLE 23-9
RECOMMENDATIONS FOR REPORTING RESULTS OF TESTING FOR ANTIBODY TO HEPATITIS C VIRUS (ANTI-HCV) BY TYPE OF REFLEX SUPPLEMENTAL TESTING PERFORMED

Anti-HCV Screening Test Result

Supplemental Test Result

Interpretation

Comments

Negative

Not applicable

Anti-HCV-negative

Not infected with HCV unless recent infection is suspected or other evidence exists to indicate HCV infection

Positive with high signal-to-cut-off ration

Not done

Anti-HCV-positive

Probably indicates past or present infection; supplemental serological testing not performed; samples with high signal-to-cut-off rations usually (≥95%) confirm positive, but <5 of every 100 might represent false positives; more specific testing may be requested if indicated.

Positive

Recombinant immunoblot assay (RIBA®) positive

Anti-HCV positive

Indicates past or present HCV infection

Positive

RIBA negative

Anti-HCV negative

Not infected with HCV unless recent infection is suspected or other evidence exists to indicate HCV infection

Positive

RIBA indeterminate

Anti-HCV indeterminate

HCV antibody and infection status cannot be determined; another sample should be collected for repeat anti-HCV testing (>1 month) or for HCV RNA testing

Positive

Nucleic acid test (NAT) positive

Anti-HCV positive, HCV-RNA positive

Indicates active HCV infection

Positive

NAT negative RIBA positive

Anti-HCV positive, HCV-RNA negative

Presence of anti-HCV indicates past or present infection; single negative HCV-RNA result does not rule out active infection

Positive

NAT negative RIBA negative

Anti-HCV negative, HCV-RNA negative

Not infected with HCV

Positive

NAT negative RIBA indeterminate

Anti-HCV indeterminate, HCV-RNA negative

Screening test anti-HCV result probable false positive, which indicates no HCV infection

Routine testing of hemodialysis patients for anti-HCV on admission and every 6 months thereafter has been recommended since 2001 [232]. For routine HCV testing of hemodialysis patients, the anti-HCV screening immunoassay is recommended, and if positive, supplemental anti HCV testing using RIBA (Table 23-9). RIBA is recommended rather than NAT because serologic assay can be performed on the same serum or plasma sample collected for the screening anti-HCV screening assay. In addition, in certain situations, the HCV RNA result can be negative in persons with active infection. As the titer of anti-HCV increases during acute infection, the titer of HCV RNA declines [233]. Thus, HCV RNA is not detectable in certain persons during the acute phase of their infection, but this finding can be transient and chronic infection can develop [234]. In addition, intermittent HCV positivity has been observed among patients with chronic HCV infection [235,236,237]. Therefore, the significance of a single negative HCV RNA result is unknown, and the need for further investigation or follow-up is determined by verifying anti-HCV status. Detection of HCV RNA also requires that serum or plasma sample be collected and handled in a manner suitable for NAT and that testing be performed in a laboratory with appropriate facilities established for NAT testing [229]. Although in rare instances, detection of HCV RNA might be the only evidence of HCV infection, a recent study conducted among almost 3,000 U.S. hemodialysis patients found that only 0.07% were HCV RNA positive but antibody negative [CDC, unpublished data].

Delta Hepatitis

Delta hepatitis is caused by the HDV, a relatively small defective virus that causes infection only in persons

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with active HBV infection. The prevalence of HDV infection is low in the United States with rates <1% among HBsAg-positive persons in the general population and >10% among HBsAg-positive persons with repeated percutaneous exposures (e.g., injecting drug users, persons with hemophilia) [238]. Areas of the world with high endemic rates of HDV infection include southern Italy, parts of Africa, and the Amazon basin.

Few data exist on the prevalence of HDV infection among chronic hemodialysis patients; a few studies have reported nonexistent to low prevalence among hemodialysis patients [239,240]. In endemic areas, prevalence rates may be relatively high among hemodialysis patients who are HBsAg-positive [241]. Only one transmission of HDV has been reported in the United States [242]. In this episode, transmission occurred from a patient who was chronically infected with HBV and HDV to an HBsAg-positive patient after a massive bleeding incident; both patients received dialysis at the same station.

HDV infection may occur as either co-infection with HBV or as a superinfection in a person with chronic HBV infection. Co-infections usually resolve, but superinfection frequently results in chronic HDV infection and severe disease. High mortality rates are associated with both types of infection. A serologic test that measures total antibody to HDV is commercially available.

Human Immunodeficiency Virus (HIV) Infection

During 1985–2002, the U.S. hemodialysis centers that reported providing chronic hemodialysis for patients with HIV infection increased from 11% to 39%, and the patients with known HIV infection increased from 0.3% to 1.5% [2]. Although the proportion of patients with HIV infection has remained fairly stable during the past decade, the number of infected patients has increased, as has the number of centers treating patients with HIV infection. HIV is transmitted by blood and other body fluids that contain blood. No patient-to-patient transmission of HIV has been reported in a U.S. hemodialysis center. However, there have been reports of transmission of HIV among patients in other countries. All of these outbreaks have been attributed to several breaks in infection control: (1) reusing access needles and inadequately disinfected equipment [184], (2) sharing of syringes among patients [185], and (3) sharing dialyzers among different patients [243]. HIV infection usually is diagnosed with assays that measure antibody to HIV, and a repeatedly positive EIA test should be confirmed by Western blot or other confirmatory test.

Preventing Infections Among Chronic Hemodialysis Patients

Preventing transmission among chronic hemodialysis patients of blood borne viruses and pathogenic bacteria from both recognized and unrecognized sources of infection requires implementation of a comprehensive infection control program. The components of such a program include infection control practices specifically designed for the hemodialysis setting, including routine serologic testing and immunization, surveillance, and training and education. CDC has published recommendations describing these components in detail [232].

The infection control practices recommended for hemodialysis units (Table 23-10) will reduce opportunities for patient-to-patient transmission of infectious agents, directly or indirectly via contaminated devices, equipment and supplies, environmental surfaces, and hands of personnel. These practices should be carried out routinely for all patients in the chronic hemodialysis setting because of the increased potential for blood contamination during hemodialysis and because many patients are colonized or infected with pathogenic bacteria.

Such practices include additional measures to prevent HBV transmission because of the high titer of HBV and its ability to survive on environmental surfaces (Table 23-10). The potential for environmentally mediated transmission of HBV rather than internal contamination of dialysis machines is the focus of infection control strategies for preventing HBV transmission in dialysis centers. For patients at increased risk for transmission of pathogenic bacteria, including antimicrobial-resistant strains, additional precautions also might be necessary in some circumstances. Furthermore, surveillance for infections and other adverse events is required to monitor the effectiveness of infection control practices, and training and education of both staff members and patients are critical to ensure that appropriate infection control behaviors and techniques are fully implemented.

In each chronic hemodialysis unit, policies and practices should be reviewed and updated to ensure that infection control practices recommended for hemodialysis units are implemented and rigorously followed. Intensive efforts must be made to educate new staff members and reeducate existing staff members regarding these practices. Readers should consult the CDC recommendations for details on these practices [232].

Routine Testing

All chronic hemodialysis patients should be routinely tested for HBV and HCV infection and the results promptly reviewed to ensure that patients are managed appropriately based on their testing results (Tables 23-10, 23-11). Test results (positive and negative) must be communicated to other units or hospitals when patients are transferred for care. Routine testing for HDV and HIV infection for purposes of infection control is not recommended.

Before admission to the hemodialysis unit, the HBV serologic status (i.e., HBsAg, total anti-HBc, and anti-HBs) of all patients should be known. Test results for patients

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transferred from another unit should be obtained before hand. If a patient's HBV serologic status is not known at the time of admission, testing should be completed within 7 days. The hemodialysis unit should ensure that the laboratory performing the testing for anti-HBs can detect a 10 milli-International Units per mL (mIU/mL) concentration to determine protective levels of antibody.

TABLE 23-10
RECOMMENDATIONS FOR PREVENTING INFECTIONS IN HEMODIALYSIS CENTERS

Infection control precautions for all patients

Wear disposable gloves when caring for the patient or touching the patient's equipment at the dialysis station; remove gloves and perform hand hygiene between each patient or station.

Items taken into the dialysis station should be disposed of, dedicated for use only on a single patient, or cleaned and disinfected before being taken to a common clean area or used on another patient.

When multiple-dose medication vials are used (including vials containing diluents), prepare individual patient doses in a clean (centralized) area away from dialysis stations and deliver separately to each patient. Do not carry multiple-dose medication vials from station to station.

Do not use common medication carts to deliver medications to patients. Do not carry medication vials, syringes, alcohol swabs, or supplies in pockets. If trays are used to deliver medications to individual patients, they must be cleaned between patients.

Clean areas should be clearly designated for the preparation, handling, and storage of medications and unused supplies and equipment. Clean areas should be clearly separated from contaminated areas where used supplies and equipment are handled. Do not handle and store medications or clean supplies in the same or an adjacent area where used equipment or blood samples are handled.

Use external venous and arterial pressure transducer protectors for each patient treatment to prevent blood contamination of the dialysis machines' pressure monitors. Change the external transducer protectors between each patient treatment, and do not reuse them. Internal transducer protectors do not need to be changed routinely between patients.

Clean and disinfect the dialysis station, all frequently touched surfaces, Discard all fluid and clean and disinfect all surfaces and containers associated with the prime waste (including chairs, beds, tables, machines, buckets attached to the machines) between patients.

For dialyzers and blood tubing that will be reprocessed, cap dialyzer ports and clamp tubing. Place all used dialyzers and tubing in leak proof containers for transport from station to reprocessing or disposal area.

Vaccinate all susceptible patients against hepatitis B; test for anti-HBs 1–2 months after last dose. If <10 mIU/ml consider patient susceptible, revaccinate with an additional three doses, and retest for anti-HBs. If ≥10 mIU/ml, consider patient immune, and retest annually. Give booster dose of vaccine if anti-HBs declines to <10 mIU/mL and continue to retest annually.

Additional precautions of HBsAg-positive patients

Dialyze HBsAg-positive patients in a separate room using separate machines, equipment, instruments, and supplies.

Staff members caring for HBsAg-positive patients should not care for HBV-susceptible patients at the same time (e.g., during the same shift or during patient changeover).

TABLE 23-11
SCHEDULE FOR ROUTINE TESTING FOR HEPATITIS B VIRUS (HBV) AND HEPATITIS C VIRUS (HCV) INFECTIONS

Patient Status

On Admission

Monthly

Semiannual

Annual

a Results of HBV testing should be known before the patient begins dialysis.
b HBsAg, hepatitis B surface antigen; anti-HBc, antibody to hepatitis B core antigen; anti-HBs, antibody to hepatitis B surface antigen; anti-HCV, antibody to hepatitis C virus; ALT, alanine aminotransferase.

All patients

HBsAg,a Anti-HBca (total), Anti-HBs,aAnti-HCV, ALTb

HBV susceptible, including nonresponders to vaccine

HBsAg

Anti-HBs positive (≥10 milli-International Units/ml), anti-HBc negative

Anti-HBs

Anti-HBs and anti-HBc positive

No additional HBV testing needed

Anti-HCV negative

ALT

Anti-HCV

Routine HCV testing should include the use of both a screening immunoassay to test for anti-HCV and supplemental or confirmatory testing with an additional, more specific assay. Use of NAT for HCV RNA as the primary test for routine screening is not recommended because few HCV infections will be identified in anti-HCV negative patients. However, if ALT levels are persistently abnormal in anti-HCV negative patients in the absence of another etiology, testing for HCV RNA should be considered. Blood samples collected for NAT should not contain heparin, which interferes with the accurate performance of this assay.

HBV vaccination is an essential component of prevention in the hemodialysis setting. All susceptible patients and staff should receive HBV vaccine. Susceptible patients who have not yet received HBV vaccine, are in the process of being vaccinated, or have not adequately responded to vaccination should continue to be tested regularly for HBsAg. Detailed recommendations for vaccination and follow-up of hemodialysis patients have been published elsewhere [232].

Management of Infected Patients

HBV

HBsAg-positive patients should undergo dialysis in a separate room designated only for them. They should use separate machines, equipment, and supplies, and—most important—staff members should not care for both HBsAg-positive and susceptible patients at the same time or while the HBsAg-positive patient is in the treatment area. Dialyzers should not be reused on HBsAg-positive patients. Because HBV is efficiently transmitted through occupational exposure to blood, reprocessing dialyzers from HBsAg-positive patients might place HBV-susceptible staff members at increased risk for infection.

HBV chronically infected patients (i.e., those who are HBsAg positive, total anti-HBc positive, and IgM anti-HBc negative) are infectious to others and are at risk for chronic liver disease. These patients should be counseled regarding preventing transmission to others, and their household and sexual partners should receive HBV vaccine and should be evaluated (by consultation or referral, if appropriate) for the presence or development of chronic liver disease according to current medical practice guidelines. Persons with chronic liver disease should be vaccinated against HAV if susceptible.

HBV chronically infected patients do not require any routine follow-up testing for purposes of infection control. However, annual testing for HBsAg is reasonable to detect the small percentage of HBV-infected patients who might lose their HBsAg.

HCV

HCV-positive patients do not have to be isolated from other patients or dialyzed separately on dedicated machines. The purpose of routine testing is to monitor potential transmission within centers and ensure that appropriate practices are being properly and consistently used. Furthermore, HCV-positive patients can participate in dialyzer reuse programs. Unlike HBV, HCV is not transmitted efficiently through occupational exposures. Thus, reprocessing dialyzers from HCV-positive patients should not place staff members at increased risk for infection.

HCV-positive persons should be evaluated (by consultation or referral, if appropriate) for the presence or development of chronic liver disease according to current medical practice guidelines. They also should receive information concerning how they can prevent further harm to their liver and prevent transmitting HCV to others [244,245]. Persons with chronic liver disease should be vaccinated against HAV if susceptible.

HDV

Because HDV depends on an HBV-infected host for replication, prevention of HBV infection will prevent HDV infection in a person susceptible to it. Patients known to be infected with HDV should be isolated from all other dialysis patients, especially those who are HBsAg positive.

HIV

Infection control precautions recommended for all hemo-dialysis patients are sufficient to prevent HIV transmission between/among patients. HIV-infected patients do not have to be isolated from other patients or dialyzed separately on dedicated machines. In addition, they can participate in dialyzer reuse programs. Because HIV is not transmitted efficiently through occupational exposures, reprocessing dialyzers from HIV-positive patients should not place staff members at increased risk for infection.

Bacterial/Fungal Infections

Contact transmission can be prevented by hand hygiene [246], glove use, and disinfection of environmental surfaces. Infection control precautions recommended for all hemodialysis patients are adequate to prevent transmission for most patients infected/colonized with pathogenic bacteria, including antimicrobial-resistant strains. However, additional precautions should be considered for treatment of patients who might be at increased risk for transmitting pathogenic bacteria. Such patients include those with either an infected skin wound with drainage that is not contained by dressings (the drainage does not have to be culture positive for MRSA, VRE, or any specific pathogen) or fecal incontinence or diarrhea uncontrolled with personal hygiene measures. For these patients, consider using the

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following additional precautions: (1) staff members treating the patient should wear a separate gown over their usual clothing and remove the gown when finished caring for the patient and (2) dialyze the patient at a station with as few adjacent stations as possible (e.g., at the end or corner of the unit) [232].

Vancomycin is used commonly in dialysis patients in part because vancomycin can be conveniently administered to patients when they come in for hemodialysis treatments. Prudent antimicrobial use is an important component of preventing the spread of vancomycin resistance [247]. This CDC guideline states that vancomycin is not indicated for therapy (chosen for dosing convenience) of infections due to ß-lactam sensitive gram-positive microorganisms in patients with renal failure. Depending on the situation, alternative antimicrobials (e.g., cephalosporins) with dosing intervals >48 hours, which would allow postdialytic dosing, could be used. Recent studies suggest that cefazolin given three times a week in the dialysis unit provides adequate blood levels and could be used to treat many infections in hemodialysis patients [248,249].

Disinfection, Sterilization, and Environmental Hygiene

Good cleaning, disinfection, and sterilization procedures are important components of infection control in the hemodialysis center. The procedures do not differ from those recommended for other healthcare settings [250,251], but the high potential for blood contamination makes the hemodialysis setting unique. Additionally, the need for routine aseptic access of the patient's vascular system makes the hemodialysis unit more similar to a surgical suite than to a standard hospital room. Medical items are categorized as critical (e.g., needles and catheters), which are introduced directly into the bloodstream or normally sterile areas of the body; semicritical (e.g., fiberoptic endoscopes), which come in contact with intact mucous membranes; and noncritical (e.g., blood pressure cuffs), which touch only intact skin [246,250].

Cleaning and housekeeping in the dialysis center have two goals: to remove soil and waste on a regular basis, thereby preventing the accumulation of potentially infectious material, and to maintain an environment that is conducive to good patient care. Crowding patients and overtaxing staff members may increase the likelihood of microbial transmission. Adequate cleaning may be difficult if there are multiple wires, tubes, and hoses in a small area. There should be enough space to move completely around each patient's dialysis station without interfering with the neighboring stations. When space is limited, the following can improve accessibility for cleaning: eliminating unneeded items; arranging required items in an orderly manner; and removing excess lengths of tubes, hoses, and wires from the floor. Because of the special requirements for cleaning in the dialysis center, staff should be specially trained in this task.

After each patient treatment, frequently touched environmental surfaces, including external surfaces of the dialysis machine, should be cleaned (with a good detergent) or disinfected (with a detergent germicide). It is the cleaning step that is important for interrupting the cross-contamination transmission routes. Antiseptics, such as formulations with povidone iodine, hexachlorophene, or chlorhexidine, should not be used because they are formulated for use on skin and are not designed for use on hard surfaces.

There is no evidence that medical waste is any more infectious than residential waste or has caused disease in the community [252]. Wastes from a hemodialysis center that are actually or potentially contaminated with blood should be considered infectious and handled accordingly. Eventually, these items of solid waste should be disposed of properly in an incinerator or sanitary landfill, depending on state or local laws.

Standard protocols for sterilization and disinfection are adequate for processing any items or devices contaminated with blood. Historically, there has been a tendency to use “overkill” strategies for instrument sterilization or disinfection and housekeeping protocols. This is not necessary. The floors in a dialysis center are routinely contaminated with blood, but the protocol for floor cleaning is the same as for floors in other healthcare settings. Usually, this involves the use of a good detergent germicide; the formulation can contain a low or intermediate level disinfectant.

Blood borne viruses, such as HBV and HIV, are inactivated by any standard sterilization systems such as standard steam autoclave cycles of 121°C (249.8°F) for 15 minutes, ethylene oxide gas [250], and low temperature hydrogen peroxide gas plasma [253]. Large blood spills should be cleaned to remove visible material, and then the area should receive low- to intermediate-level disinfection after the directions of the germicide manufacturer.

Blood and other specimens, such as peritoneal fluid, from all patients should be handled with care. Peritoneal fluid can contain high levels of HBV and should be handled in the same manner as the patient's blood. Consequently, if the center performs peritoneal dialysis, the same criteria for separating HBsAg-positive patients who are undergoing hemodialysis apply to those undergoing peritoneal dialysis.

HBV has not been grown in tissue cultures, and without a viral assay system, studies on the precise resistance of this virus to various chemical germicides and heat have not been performed. However, the resistance of HBV to both heat and chemical germicides may approach that of some other viruses and bacteria, but certainly not that of the bacterial endospore or the tubercle bacillus. Furthermore, studies have shown that HBV is not resistant to commonly used high level and intermediate level disinfectants [254,255].

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Blood contamination of venous pressure monitors has been implicated in HBV transmission [176]. Therefore, if venous pressure transducer filters are used, they should not be reused.

In single-pass artificial kidney machines, the internal fluid pathways are not subject to contamination with blood. Although the fluid pathways that exhaust dialysis fluid from the dialyzer may become contaminated with blood in the event of a dialyzer leak, it is unlikely that this blood contamination will reach a subsequent patient. Therefore, disinfection and rinsing procedures should be designed to control contamination with bacterial rather than blood borne pathogens.

For dialysis machines that use a dialysate recirculating system (e.g., some ultrafiltration control machines and those that regenerate the dialysate), a blood leak in a dialyzer, especially a massive leak, can result in contamination of a number of surfaces that will contact the dialysis fluid of subsequent patients. However, the procedures that are normally practiced after each use of a recirculating machine—draining of the dialysis fluid, subsequent rinsing, and disinfection—will reduce the level of contamination below infectious levels. In addition, an intact dialyzer membrane will not allow passage of bacteria or viruses. Consequently, if a blood leak does occur with either type of dialysis machine, the standard disinfection procedure used for machines in the dialysis center to control bacterial contamination also will prevent transmission of blood borne pathogens.

References

  1. U.S. Renal Data System. USRDS 2005 Annual data report: Atlas of end-stage renal disease in the United States, National Institutes of Health, National Institute of Diabetes and Digestive and Kidney Diseases. Bethesda: 2005.
  2. Finelli L, Miller JT, Tokars JI, et al. National surveillance of dialysis-associated diseases in the United States, 2002. Seminars Dialysis2005;18:52–61.
  3. Alter MJ, Favero MS, Petersen NJ, et al. National surveillance of dialysis-associated hepatitis and other diseases, 1976 and 1980. Dialysis Transplant1983:12:860–61, 864–65, 868.
  4. Alter MJ, Favero MS, Miller JK, et al. National surveillance of dialysis-associated diseases in the United States, 1987. ASAIO Trans1989;35:820–31.
  5. Alter MJ, Favero MS, Moyer LA, et al. National surveillance of dialysis-associated diseases in the United States, 1988. ASAIO Trans1990;36:107–18.
  6. Alter MJ, Favero MS, Moyer LA, Bland LA. National surveillance of dialysis-associated diseases in the United States, 1989. ASAIO Trans1991;37:97–109.
  7. Tokars JI, Alter MJ, Favero MS, et al. National surveillance of hemodialysis associated diseases in the United States, 1990. ASAIO J1993;39:71–80.
  8. Tokars JI, Alter MJ, Favero MS, et al. National surveillance of dialysis associated diseases in the United States, 1991. ASAIO J1993;39:966–75.
  9. Tokars JI, Alter MJ, Favero MS, et al. National surveillance of dialysis associated diseases in the United States, 1992. ASAIO J1994;40:1020–31.
  10. Tokars JI, Alter MJ, Favero MS, et al. National surveillance of dialysis associated diseases in the United States, 1993. ASAIO J1996;42:219–29.
  11. Tokars JI, Alter MJ, Miller E, et al. National surveillance of dialysis associated diseases in the United States, 1994. ASAIO J1997;43:108–19.
  12. Tokars JI, Miller ER, Alter MJ, Arduino MJ. National surveillance of dialysis associated diseases in the United States, 1995. ASAIO J1998;44:98–107.
  13. Tokars JI, Miller ER, Alter MJ, Arduino MJ. National surveillance of dialysis-associated diseases in the United States, 1997. Seminars Dialysis2000;13:75–85.
  14. Tokars JI, Frank M, Alter MJ, Arduino MJ. National surveillance of dialysis-associated diseases in the United States, 2000. Seminars Dialysis2002;15:162–71.
  15. Tokars JI, Finelli L, Alter MJ, Arduino MJ. National surveillance of dialysis-associated diseases in the United States, 2001. Seminars Dialysis2004;17:310–19.
  16. Favero MS, Carson LA, Bond WW, Petersen NJ. Pseudomonas aeruginosa: Growth in distilled water from hospitals. Science1971;173:836–38.
  17. Favero MS, Carson LA, Bond WW, Petersen NJ. Factors that influence microbial contamination of fluids associated with hemodialysis machines. Appl Microbiol1974;28:822–30.
  18. Favero MS, Petersen NJ, Boyer KM, et al. Microbial contamination of renal dialysis systems and associated health risks. Trans Am Soc Artif Intern Organs1974;20A:175–83.
  19. Favero MS, Petersen NJ, Carson LA, et al. Gram-negative water bacteria in hemodialysis systems. Health Lab Sci1975;12:321–34.
  20. Carson LA, Petersen NJ, Favero MS. Use of the Limulus amoebocyte lysate assay system for detection of bacterial endotoxin in fluids associated with hemodialysis procedures. In: Cohen E, ed. Biomedical applications of the horseshoe crab (limulidae). New York: Alan R. Liss, 1979:453–64.
  21. Petersen NJ, Boyer KM, Carson LA, Favero MS. Pyrogenic reactions from inadequate disinfection of a dialysis fluid distribution system. Dialysis Transplant1978;7:52–57
  22. Phillips G, Hudson S, Stewart WK. Persistence of microflora in biofilm within fluid pathways of contemporary haemodialysis monitors (Gambro AK-10). J Hosp Infect1994;27:117–25.
  23. Lonnemann G. When good water goes bad: How it happens, clinical consequences and possible solutions. Blood Purif2004;22:124–29.
  24. Hoenich NA, Ronco C, Levin R. The importance of water quality and haemodialysis fluid composition. Blood Purif2006;24:11–18.
  25. Arduino MJ, Bland LA, Favero MS. Microbiology of bicarbonate dialysate. Nephrol News Issues1992;5:7–8
  26. Bland LA, Favero MS. Microbial contamination control strategies for hemodialysis systems. JCAHO Plant Technol Safety Series1989;3:30–36
  27. Bolan G, Reingold AL, Carson LA, et al. Infections with Mycobacterium chelonei in patients receiving dialysis and using processed hemodialyzers. J Infect Dis1985;52:1013–19.
  28. Carson LA, Bland LA, Cusick LB, et al. Prevalence of nontuberculous mycobacteria in water supplies of hemodialysis centers. Appl Environ Microbiol1988;54:3122–25.
  29. Lowry PW, Beck-Sague CM, Bland LA, et al. Mycobacterium chelonae infection among patients receiving high-flux dialysis in a hemodialysis clinic in California. J Infect Dis1990;161:85–90.
  30. Band JD, Ward JI, Fraser DW, et al. Two outbreaks of peritonitis due to a Mycobacterium chelonei-like organism associated with intermittent chronic peritoneal dialysis. J Infect Dis1982;145:9–17.
  31. Poty F, Denis C, Baufine-Ducrocq H. Nosocomial Pseudomonas pickettii infection: Danger of the use of ion-exchange resins. Presse Med1987;16:1185–87.
  32. Carson LA, Bland LA, Cusick LB, et al. Factors affecting endotoxin levels in fluids associated with hemodialysis procedures. In: Novitsky TJ, Watson SW, eds. Detection of bacterial endotoxins with the Limulus amoebocyte lysate test. New York: Alan R. Liss, 1987:223–34.
  33. Hindman SH, Favero MS, Carson LA, et al. Pyrogenic reactions during hemodialysis caused by extramural endotoxin. Lancet1975;2:732–34.
  34. Tipple MA, Shusterman N, Bland LA, et al. Illness in hemodialysis patients after exposure to chloramine contaminated dialysate. ASAIO Trans1991;37:588–91.

P.367

  1. Calderaro RV, Heller L. Outbreak of hemolytic reactions associated with chlorine and chloramine residuals in hemodialysis water. Rev Saude Publica2001;35:481–86.
  2. Arduino MJ. CDC investigations of noninfectious outbreaks of adverse events in hemodialysis facilities, 1979–1999. Seminars Dialysis2000;13:86–91.
  3. Fenves AZ, Gipson JS, Pancorvo C. Chloramine-induced methemoglobinemia in a hemodialysis patient. Seminars Dialysis2000;13:327–29.
  4. Villforth JC. FDA safety alert: Chloramine contamination of hemodialysis water supplies. Am J Kidney Dis1988;11:447.
  5. Association for the Advancement of Medical Instrumentation. American national standard: Water treatment equipment for hemodialysis applications. ANSI/AAMI RD62-2001. Arlington, VA: Association for the Advancement of Medical Instrumentation, 2001.
  6. Association for the Advancement of Medical Instrumentation. American national standard: Dialysate for hemodialysis. ANSI/AAMI RD52-2004. Arlington, VA: Association for the Advancement of Medical Instrumentation, 2004.
  7. Stamm JM, Engelhard WE, Parsons JE. Microbiological study of softener resins. Appl Microbiol1969;18:376–86.
  8. Martiny H, Wlodavezyz K, Harms G, Rueden H. The use of UV-irradiation for the disinfection of water. I. Communication: Microbiological investigations in drinking water. Zb Bak Hyg B1988;185:350–67.
  9. Martiny H, Brust H, Rueden H. The use of UV radiation for the disinfection of water. IV. Microbiological studies of the UV sensitivity of different aged cells of E. faecium, E. coli and P. aeruginosa. Zbl Hyg Umweltmed1990;190:39–50.
  10. Carson LA, and Petersen NJ. Photoreactivation of Pseudomonas cepacia after ultraviolet exposure: A potential source of contamination in ultraviolet-treated waters. J Clin Microbiol1975;1:462–64.
  11. Favero MS. Microbiological contaminants. In: Proceedings of the Association for the Advancement of Medical Instrumentation Technology Assessment Conference: Issues in hemodialysis. Arlington, VA: Association for the Advancement of Medical Instrumentation, 1981:30–33.
  12. Anderson RL, Holland BW, Carr JK, et al. Effect of disinfectants on pseudomonads colonized on interior surface of PVC pipes. Am J Public Health1990;80:17–21.
  13. Arduino MJ. Microbiologic quality of water used for hemodialysis. Contemp Dial Nephrol1996;17:17–19.
  14. Arduino MJ, Favero MS. Microbiologic aspects of hemodialysis. In: Water quality for hemodialysis. Arlington, VA: Association for the Advancement of Medical Instrumentation, 1998:16–22.
  15. Centers for Disease Control and Prevention. Clusters of bacteremia and pyrogenic reactions in hemodialysis patients. Epidemic Investigation Report EPI 86-65, April 22, 1987. Atlanta: CDC,
  16. Beck-Sague CM, Jarvis WR, Bland LA, et al. Outbreak of gram-negative bacteremia and pyrogenic reactions in a hemodialysis center. Am J Nephrol1990;10:397–403.
  17. Murphy J, Parker T, Carson L, et al. Outbreaks of bacteremia in hemodialysis patients associated with alteration of dialyzer membranes following chemical disinfection. ASAIO Trans1987;16:51.
  18. Welbel SF, Schoendorf K, Bland LA, et al. An outbreak of gram-negative bloodstream infections in chronic hemodialysis patients. Am J Nephrol1995;15:1–4.
  19. Centers for Disease Control. Pyrogenic reactions in patients undergoing high-flux hemodialysis, California. Epidemic Investigation Report EPI 86-80, June 1, 1987. Atlanta: CDC, 1987.
  20. Gordon S, Tipple M, Bland L, Jarvis W. Pyrogenic reactions associated with the reuse of disposable hollow fiber hemodialyzers. JAMA1988;260:2077–81.
  21. Rudnick JR, Arduino MJ, Bland LA, et al. Pyrogenic reactions associated with hemodialysis reuse. Artif Organs1995;19:289–94.
  22. Townsend TR, Siok-Bi W, Bartlett J. Disinfection of hemodialysis machines. Dialysis Transplant1985;14:274, 78, 80, 82–83, 87.
  23. Amato RL. Water treatment for hemodialysis—updated to include the latest AAMI standards for dialysate (RD52: 2004) continuing. Nephrol Nurs J2005;32:151–67.
  24. Smeets E, Kooman J, van der Sande F, et al. Prevention of biofilm formation in dialysis water treatment systems. Kidney Int2003; 2003;63:1574–76.
  25. Amato RL, Curtis J. The practical application of ozone in dialysis. Nephrol News Issues2002;16:27–30.
  26. Favero MS, Petersen NJ. Microbiologic guidelines for hemodialysis systems. Dialysis Transplant1977;6:34–36.
  27. Association for the Advancement of Medical Instrumentation. American national standard for hemodialysis systems. ANSI/AAMI RD5-1992. Arlington, VA: Association for the Advancement of Medical Instrumentation, 1992.
  28. Sitter T, Bergner A, Schiffl H. Dialysate related cytokine induction and response to recombinant human erythropoietin in haemodialysis patients. Nephrol Dial Transplant2000;15:1207–11.
  29. Vaslaki LR, Berta K, Major L, et al. On-line hemodiafiltration does not induce inflammatory response in end-stage renal disease patients: Results from a multicenter cross-over study. Artif Organs2005;29:406–12.
  30. Lacson E Jr., Levin NW. C-reactive protein and end-stage renal disease. Seminars Dialysis2004;17:438–48.
  31. Hsu PY, Lin CL, Yu CC, et al. Ultrapure dialysate improves iron utilization and erythropoietin response in chronic hemodialysis patients—a prospective cross-over study. J Nephrol2004;17:693–700.
  32. Kleophas W, Haastert B, Backus G, et al. Long-term experience with an ultrapure individual dialysis fluid with a batch type machine. Nephrol Dial Transplant1998;13:3118–25.
  33. Baz M, Durand C, Ragon A, et al. Using ultrapure water in hemodialysis delays carpal tunnel syndrome. Int J Artif Organs1991;14:681–85.
  34. Richardson D. Clinical factors influencing sensitivity and response to epoetin. Nephrol Dial Transplant2002;17:53–59.
  35. Schiffl H, Lang SM, Stratakis D, Fischer R. Effects of ultrapure dialysis fluid on nutritional status and inflammatory parameters. Nephrol Dial Transplant2001;16:1863–69.
  36. Favero MS, Bland LA. Microbiologic principles applied to reprocessing hemodialyzers. In: Deane N, Wineman RJ, Bemis JA, eds. Guide to reprocessing of hemodialyzers. Boston: Martinus Nijhoff, 1986:63–73.
  37. Arduino MJ, Bland LA, Aguero SM, et al. Comparison of microbiologic assay methods for hemodialysis fluids. J Clin Microbiol1991;29:592–94.
  38. Klein E, Pass T, Harding GB, et al. Microbial and endotoxin contamination in water and dialysate in the central United States. Artif Organs1990;14:85–94.
  39. van der Linde K, Lim BT, Rondeel JM, et al. Improved bacteriological surveillance of haemodialysis fluids: A comparison between Tryptic soy agar and Reasoner's 2A media.Nephrol Dial Transplant1999;14:2433–37.
  40. Association for the Advancement of Medical Instrumentation. American national standard: Reuse of hemodialyzers ANSI/AAMI RD47-2002/A 1:2003.Arlington, VA: Association for the Advancement of Medical Instrumentation, 2003.
  41. Gazenfeldt-Gazit E, Elaihou HE. Endotoxin antibodies in patients on maintenance hemodialysis. Israel J Med Sci1969;5:1032–36.
  42. Lonnemann G, Behme TC, Lenzner B, et al. Permeability of dialyzer membranes to TNF-α inducing substances derived from water bacteria. Kidney Int1992;42:61–68.
  43. Laude-Sharpe M, Canoff M, Simard L, et al. Induction of IL-1 during hemodialysis: Trans-membrane passage of intact endotoxin (LPS). Kidney Int1990;38:1089–94.
  44. Kumano K, Yokota S, Nanbu M, Sakai T. Do cytokine-inducing substances penetrate through dialysis membranes and stimulate monocytes? Kidney Int Suppl1993;41:S205–8.
  45. Yamagami S, Adachi T, Sugimura T, et al. Detection of endotoxin antibody in long-term dialysis patients. Int J Artif Organs1990;13:205–10.
  46. Henderson LW, Koch KM, Dinarello CA, et al. Hemodialysis hypotension: The interleukin hypothesis. Blood Purif1983;1:3–8.
  47. Port FK, VanDerKerkhove KM, Kunkel SL, Kluger MJ. The role of dialysate in the stimulation of interleukin-1 production during clinical hemodialysis. Am J Kidney Dis1987;10:118–22.

P.368

  1. Kantor RJ, Carson LA, Graham DR, et al. Outbreak of pyrogenic reactions at a dialysis center: Association with infusion of heparinized saline solution. Am J Med1983;74:449–56.
  2. Powell AC, Bland LA, Oettinger CW, et al. Enhanced release of TNF-α, but not IL-1β, from uremic blood after endotoxin stimulation. Lymphokine Cytokine Res1991;10:343–46.
  3. Pegues DA, Oettinger CU, Bland LA, et al. A prospective study of pyrogenic reactions in hemodialysis patients using bicarbonate dialysis fluids filtered to remove bacteria and endotoxin. J Am Soc Nephrol1992;3:1002–7.
  4. Gordon SM, Oettinger CW, Bland LA, et al. Pyrogenic reactions in patients receiving conventional, high-efficiency or high-flux hemodialysis with bicarbonate dialysate containing high concentrations of bacteria and endotoxin. J Am Soc Nephrol1992;2:1436–44.
  5. Petersen NJ, Boyer KM, Carson LA, et al. Pyrogenic reactions from inadequate disinfection of a dialysis fluid distribution system. Dialysis Transplant1978;7:52, 57–60.
  6. Centers for Disease Control and Prevention. Pyrogenic reactions and gram-negative bacteremia in a hemodialysis center. Epidemic investigation report EPI 91-37. Atlanta: CDC, 1991.
  7. Centers for Disease Control and Prevention. Bacteremia in hemodialysis patients. Epidemic Investigation Report EPI 92-10. Atlanta: CDC, 1992.
  8. Centers for Disease Control and Prevention. Outbreaks of gram negative bacterial bloodstream infections traced to probable contamination of hemodialysis machines—Canada, 1995; United States, 1997; and Israel, 1997. MMWR1998;47:55–59.
  9. Jochimsen EM, Frenette C, Delorme M, et al. A cluster of bloodstream infections and pyrogenic reactions among hemodialysis patients traced to dialysis machine waste-handling option units. Am J Nephrol1998;18:485–89.
  10. Wang SA, Levine RB, Carson LA, et al. An outbreak of gram-negative bacteremia in hemodialysis patients traced to hemodialysis machine waste drain ports. Infect Control Hosp Epidemiol1999;20:746–51.
  11. Jackson BM, Beck-Sague CM, Bland LA, et al. Outbreak of pyrogenic reactions and gram-negative bacteremia in a hemodialysis center. Am J Nephrol1994;14:85–89.
  12. Grohskopf LA, Roth VR, Feikin DR, et al. Serratia liquefaciens bloodstream infections from contamination of epoetin alfa at a hemodialysis center. N Engl J Med2001; 17;344:1491–97.
  13. Proia LA, Hayden MK, Kammeyer PL, et al. Phialemonium: An emerging mold pathogen that caused 4 cases of hemodialysis-associated endovascular infection. Clin Infect Dis2004;39:373–79.
  14. Arnow PM, Garcia-Houchins S, Neagle MB, et al. An outbreak of bloodstream infections arising from hemodialysis equipment. J Infect Dis1998;178:783–91.
  15. Block C, Backenroth R, Gershon E, et al. Outbreak of bloodstream infections associated with dialysis machine waste ports in a hemodialysis facility. Eur J Clin Microbiol Infect Dis1999;18:723–25.
  16. Food and Drug Administration. Guidance for hemodialyzer reuse. Rockville: Food and Drug Administration, Center for Devices and Radiologic Health, 1995.
  17. Held PJ, Wolfe RA, Gaylin DS, et al. Analysis of the association of dialyzer reuse practices and patient outcomes. Am J Kidney Dis1994;23:692–708.
  18. Collins AJ, Ma JZ, Constantini EG, Everson SE. Dialysis unit and patient characteristics associated with reuse practices and mortality: 1989–1993. J Am Soc Nephrol1998;9:2108–17.
  19. Collins AJ, Liu J, Ebben JP. Dialyser reuse-associated mortality and hospitalization risk in incident Medicare haemodialysis patients, 1998–1999. Nephrol Dial Transplant2004;19:1245–51.
  20. Feldman HI, Bilker WB, Hackett MH, et al. Association of dialyzer reuse with hospitalization and survival rates among U.S. hemodialysis patients: Do comorbidities matter? J Clin Epidemiol1999;52:209–17.
  21. Roth VR, Jarvis WR. Outbreaks of infection and/or pyrogenic reactions in dialysis patients. Seminars Dialysis2000;13:92–96.
  22. Centers for Disease Control. Bacteremia associated with reuse of disposable hollow-fiber hemodialyzers. MMWR1986;35:417–18.
  23. Alter MJ, Favero MS, Miller JK, et al. Reuse of hemodialyzers. Results of nationwide surveillance for adverse effects. JAMA1988;260:2073–76.
  24. Bland L, Alter M, Favero M, et al. Hemodialyzer reuse: Practices in the United States and implications for infection control. ASAIO Trans1985;31:556–59.
  25. Favero MS. Distinguishing between high level disinfection, reprocessing, and sterilization. In: Association for the Advancement of Medical Instrumentation, Reuse of disposables: Implications for quality health care and cost containment. Technical Assessment Report No. 6. Arlington, VA: AAMI, 1983:19–20.
  26. Rosenberg J. Primary blood stream infections associated with dialyzer reuse in California dialysis centers. Proceedings of the 43rd Annual Meeting of the Infectious Diseases Society of America. IDSA, Alexandria, VA, 2005.
  27. Tokars JI, Miller ER, Alter MJ, Arduino MJ. National surveillance of dialysis-associated diseases in the United States, 1999. Atlanta: Centers for Disease Control and Prevention, 2001.
  28. Bland LA, Ridgeway MR, Aguero SM, et al. Potential bacteriologic and endotoxin hazards associated with liquid bicarbonate concentration. ASAIO Trans1987;33:542–45.
  29. Quinton W, Dillard D, Scribner DH. Cannulation of blood vessels for prolonged hemodialysis. Trans Soc Artif intern Organs1960;6:104–13.
  30. Foran RF, Golding AL, Treiman RL, et al. Quinton-Scribner cannulas for hemodialysis. Review of four years' experience. Calif Med1970;112:8–13.
  31. Coronel F, Herrero JA, Mateos P, et al. Long-term experience with the Thomas shunt, the forgotten permanent vascular access for haemodialysis. Nephrol Dial Transplant2001;16:1845–49.
  32. Bell PRF, Veitch PS. Vascular access for hemodialysis. In: Jacobson HR, Striker GE, Klahr S, eds. The principles and practice of nephrology. Philadelphia: BC Decker, 1991:26–44.
  33. Bonomo RA, Rice D, Whalen C, et al. Risk factors associated with permanent access-site infections in chronic hemodialysis patients. Infect Control Hosp Epidemiol1997;18:757–61.
  34. Kaplowitz LG, Comstock JA, Landwehr DM, et al. A prospective study of infections in hemodialysis patients: Patient hygiene and other risk factors for infection. Infect Control Hosp Epidemiol1988;9:534–41.
  35. Tokars JI, Miller ER, Stein G. New national surveillance system for hemodialysis-associated infections: Initial results. Am J Infect Control2002;30:288–95.
  36. Padberg FT Jr, Lee BC, Curl GR. Hemoaccess site infection. Surg Gynecol Obstet1992;174:103–8.
  37. Mehta S. Statistical summary of clinical results of vascular access procedures for hemodialysis. In: Jacobson HR, Striker GE, Klahr S, eds. The priciples and practice of nephrology. Philadelphia: BC Decker, 1991:145–57.
  38. Whelchel JD. Central venous hemodialysis access catheters: A review of technical considerations and complications. In: Sommer BG, Henry ML, eds. Vascular Access for Hemodialysis II. Chicago: WL. Gore and Associates and Precept Press, 1991:123–38.
  39. Goldstein MB. Prevention of sepsis from central vein dialysis catheters. Seminars Dialysis1992;5:106–8.
  40. Counts CS. Potential complications of the internal vascular access: Implications for nursing care. Dialysis Transplant1993;22:75–79.
  41. Dryden MS, Samson A, Ludlam HA, Wing AJ. Infective complications associated with the use of the Quinton Permacath for long-term central vascular access in hemodialysis. J Hosp Infect1991;19:257–62.
  42. Carlisle EJF, Blake P, McCarthy F, et al. Septicemia in long-term jugular hemodialysis catheters: Eradicating infection by changing the catheter over a guidewire. Int J Artif Organs1991;14:150–53.
  43. Saxena A, Panhotra BR. Haemodialysis catheter-related bloodstream infections: Current treatment options and strategies for prevention. Swiss Med Wkly2005;135:127–38.
  44. Klevens M, Tokars JI, Andrus MA. Electronic reporting of infections associated with hemodialysis. Nephrol News Issues2005;19:37–38, 43.

P.369

  1. Welbel SF, Williams D, Ray B, et al. Central venous catheter-associated bloodstream infections in a dialysis unit, Texas. In: Abstracts of the 1993 Epidemic Intelligence Service Conference, Atlanta, April 19–23, 1993. Washington, DC: Department of Health and Human Services, 1993:59.
  2. Gokal R, Khanna R, Krediet R Th, and Nolph KD. Textbook of peritoneal dialysis. 2nd ed. Dordrecht: Kluwer Academic Publishers, 2000.
  3. Peterson P, Matzke G, Keane WF. Current concepts in the management of peritonitis in patients undergoing continuous ambulatory peritoneal dialysis. Rev Infect Dis1987;9:604–12.
  4. Walshe JJ, Morse GD. Infectious complications of peritoneal dialysis. In: Nissenson AR, Fine RN, Gentile DE, eds. Clinical DialysisNorwalk,CT: Appleton, 1990:301–18.
  5. Piraino B. Peritoneal dialysis infections recommendations. Contrib Nephrol2006;150:181–86.
  6. Berkelman RL, Godley J, Weber JA, et al. Pseudomonas cepacia peritonitis associated with contamination of automatic peritoneal dialysis machines. Ann Intern Med1982;96:456–58.
  7. Petersen NJ, Carson LA, Favero MS. Microbiological quality of water in an automatic peritoneal dialysis system. Dialysis Transplant1977;6:38–40, 86.
  8. Carson LA, Petersen NJ, Favero MS, Aguero SM. Growth characteristics of atypical mycobacteria in water and their comparative resistance to disinfection. Appl Environ Microbiol1978;36:839–46.
  9. Berkelman RL, Band JD, Petersen NJ. Recommendations for the care of automated peritoneal dialysis machines: Can the risk of peritonitis be reduced? Infect Control1984;5:85–87.
  10. Zelenitsky S, Barns L, Findlay I, et al. Analysis of microbiological trends in peritoneal dialysis-related peritonitis from 1991 to 1998. Am J Kidney Dis2000;36:1009–13.
  11. Oxton LL, Zimmerman SW, Roecker EB, Wakeen M. Risk factors for peritoneal dialysis-related infections. Perit Dial Int1994;14:137–44.
  12. Salusky IB, Holloway M. Selection of peritoneal dialysis for pediatric patients. Perit Dial Int1994;17:S35–37.
  13. Vas S, Oreopoulos DG. Infections in patients undergoing peritoneal dialysis. Infect Dis Clin North Am2000;15:743–74.
  14. Copley JB. Prevention of peritoneal dialysis catheter-related infections. Am J Kidney Dis1987;10:401–7.
  15. Thodis E, Passadakis P, Ossareh S, et al. Peritoneal catheter exit-site infections: Predisposing factors, prevention and treatment. Int J Artif Organs2003;26:698–714.
  16. Vas S. Microbiologic aspects of chronic ambulatory peritoneal dialysis. Kidney Int1983;23:83–92.
  17. Szeto CC, Chow VC, Chow KM, et al. Enterobacteriaceae peritonitis complicating peritoneal dialysis: A review of 210 consecutive cases. Kidney Int2006;69:1245–52.
  18. Pegues DA, Arduino MJ, Bland LA, Jarvis WR. Infectious complications in continuous ambulatory peritoneal dialysis. Asepsis1989;11:6–12.
  19. Piraino B, Bailie GR, Bernardini J, et al. Ad Hoc Advisory Committee. Peritoneal dialysis-related infections recommendations: 2005 update. Perit Dial Int2005;25:107–31.
  20. Hakim RM, Breillatt J, Lazarus JM, Port FK. Complement activation and hypersensitivity reactions to dialysis membranes. N Engl J Med1984;311:878–82.
  21. Villarroel F. First-use syndrome in patients treated with hollow-fiber dialyzers. Blood Purif1987;5:112–4.
  22. Ing TS, Ivanovich PT, Daugirdas JT. First-use syndrome and hypersensitivity during hemodialysis: Some pieces of the puzzle are falling into place. Artif Organs1987;11:79–81.
  23. Daugirdas JT, Potempa LD, Dinh N, et al. Plate, coil, and hollow-fiber cuprammonium cellulose dialyzers: Discrepancy between incidence of anaphylactic reactions and degree of complement activation. Artif Organs1987;11:140–43.
  24. Daugirdas JT, Ing TS. First-use reactions during hemodialysis: A definition of subtypes. Kidney Int Suppl1988;24:S37–43.
  25. Pegues DA, Beck-Sague CM, Woollen SW, et al. Anaphylactoid reactions associated with reuse of hollow-fiber hemodialyzers and ACE inhibitors. Kidney Int1992;42:1232–37.
  26. Teileans C, Madhoun P, Lenaers M, Schandene L. Anaphylactic reactions during hemodialysis on AN69 membranes in patients receiving ACE inhibitors. Kidney Int1990;38:982–84.
  27. Verresen L, Waer M, Vanrenterghem Y, Michielsen P. Angiotensin converting enzyme inhibitors and anaphylactoid reactions to high-flux membrane dialysis. Lancet1990;336:1360–62.
  28. van Es A, Henny FC, Lobatto S. Angiotensin-converting enzyme inhibitors and anaphylactic reactions to high-flux membrane dialysis. Lancet1991;337:112–13.
  29. Jadoul M, Struyven J, Stragier A, Van Ypersele De Strihou C. Angiotensin-converting enzyme inhibitors and anaphylactic reactions to high-flux membrane dialysis [Letter].Lancet1991;337:112.
  30. Federal Drug Administration. Anaphylactoid reactions associated with ACE inhibitors and dialyzer membranes. FDA Safety Alert, March 6, 1992.
  31. Alfrey AC, Mishell JM, Burks J, et al. Syndrome of dyspraxia and multifocal seizures associated with chronic hemodialysis. Trans Am Soc Artif Intern Organs1972;18:257–61, 266–67.
  32. Schreeder MT, Favero MS, Hughes JR, et al. Dialysis encephalopathy and aluminum exposure: an epidemiologic analysis. J Chronic Dis1983;36:581–93.
  33. Burwen DR, Olsen SM, Bland LA, et al. Epidemic aluminum intoxication in hemodialysis patients traced to use of an aluminum pump. Kidney Int1995;48:469–74.
  34. Centers for Disease Control and Prevention. Fluoride intoxication in a dialysis unit—Maryland. MMWR1980;29:134–36.
  35. Gordon SM, Bland LA, Alexander SR, et al. Hemolysis associated with hydrogen peroxide at a pediatric dialysis center. Am J Nephrol1990;10:123–27.
  36. Gordon SM, Drachman J, Bland LA, et al. Epidemic hypotension in a dialysis center caused by sodium azide. Kidney Int1990;37:110–15.
  37. Centers for Disease Control. Dialysis dementia from aluminum. Epidemic Investigation Report EPI 81-39. Atlanta: CDC, 1982.
  38. Centers for Disease Control. Formaldehyde intoxication associated with hemodialysis—California. Epidemic investigation report EPI 81-73. Atlanta: CDC, 1984.
  39. Arnow PM, Bland LA, Garcia-Houchins S, et al. An outbreak of fatal fluoride intoxication in a long-term hemodialysis unit. Ann Intern Med1994;121:339–44.
  40. Bland LA, Arnow PM, Arduino MJ, et al. Potential hazards of deionization systems used for water purification in hemodialysis. Artif Organs1996;20:2–7.
  41. Jochimsen EM, Carmichael WW, An JS, et al. Liver failure and death after exposure to microcystins at a hemodialysis center in Brazil. N Engl J Med1998 26;338:873–78.
  42. Food and Drug Administration. FDA investigating roles of Baxter's recalled dialyzers in dialysis patient deaths. Medical Device RecallsNovember 7, 2001.
  43. No author. Caunaud B. performance liquid test as a cause for sudden deaths of dialysis patients: Perfluorohydrocarbon, a previously unrecognized hazard for dialysis patients. Nephrol Dial Transplant2002;17:545–48.
  44. Selenic D, Alvarado-Ramy F, Arduino M, et al. Epidemic parenteral exposure to volatile sulfur-containing compounds at a hemodialysis center. Infect Control Hosp Epidemiol2004;25:256–61.
  45. Snydman DR, Bryan JA, London WT, et al. Transmission of hepatitis B associated with hemodialysis: Role of malfunction (blood leaks) inside dialysis machines. J Infect Dis1976;134:562–70.
  46. Kantor RJ, Hadler SC, Schreeder MT, et al. Outbreak of hepatitis B in a dialysis unit, complicated by false positive HBsAg test results. Dial Transplant1979;8:232–35.
  47. Snydman DR, Bryan JA, Macon EJ, Gregg MB. Hemodialysis-associated hepatitis: Report of an epidemic with further evidence on mechanisms of transmission. Am J Epidemiol1976;104; 563–70.
  48. Carl M, Francis DP, Maynard JE. A common source outbreak of hepatitis B in a hemodialysis unit. Dialysis Transplant1983;12:222–29.
  49. Alter MJ, Ahtone J, Maynard JE. Hepatitis B virus transmission associated with a multiple dose vial in a hemodialysis unit. Am J Med1983;99:330–33.
  50. Niu MT, Penberthy LT, Alter MJ, et al. Hemodialysis-associated hepatitis B: Report of an outbreak. Dialysis Transplant1989;18:542–55.

P.370

  1. Centers for Disease Control and Prevention. Outbreak of hepatitis B in a dialysis center. Epidemic investigation report EPI 91-17.Atlanta: CDC, 1993.
  2. Centers for Disease Control and Prevention. Outbreaks of hepatitis B virus infection among hemodialysis patients—California, Nebraska, and Texas, 1994. MMWR1996;45:285–89.
  3. Hutin YJ, Goldstein ST, Varma JK, et al. An outbreak of hospital acquired hepatitis B virus infection among patients receiving chronic hemodialysis. Infect Control Hosp Epidemiol1999;20:731–35.
  4. Centers for Disease Control. Non-A, Non-B hepatitis in a dialysis center, Nashville Tennessee. Epidemic investigation report EPI 78–96. Phoenix: CDC, 1979.
  5. Niu MT, Alter MJ, Kristensen C, et al. Outbreak of hemodialysis-associated non-A, non-B hepatitis and correlation with antibody to hepatitis C virus. Am J Kidney Dis1992;19:345–52.
  6. Centers for Disease Control and Prevention. Possible ongoing transmission of hepatitis C virus in a hemodialysis unit. Epidemic investigation report EPI 99-38. Atlanta: CDC, 1999.
  7. Centers for Disease Control and Prevention. Transmission of hepatitis C virus among hemodialysis patients. Epidemic investigation report EPI-2000. Atlanta: CDC, 2000.
  8. Centers for Disease Control and Prevention. Transmission of hepatitis C virus in a hemodialysis unit. Epidemic investigation report EPI-2000-64. Atlanta: CDC, 2000.
  9. Velandia M, Fridkin SK, Cardenas V, et al. Transmission of HIV in dialysis centre. Lancet1995;345:1417–22.
  10. El Sayed NM, Gomatos PJ, Beck-Sague CM, et al. Epidemic transmission of human immunodeficiency virus in renal dialysis centers in Egypt. J Infect Dis2000;181:91–97.
  11. Favero MS, Maynard JE, Petersen NJ, et al. Hepatitis B antigen on environmental surfaces [Letter]. Lancet1973;2:1455.
  12. Bond WW, Favero MS, Petersen NJ, et al. Survival of hepatitis B virus after drying and storage for one week. Lancet1981;1:550–51.
  13. Petersen NJ. An assessment of the airborne route in hepatitis B transmission. Ann NY Acad Sci1980;353:157–66.
  14. Favero MS, Bolyard EA. Microbiologic considerations, disinfection and sterilization strategies and the potential for airborne transmission of bloodborne pathogens. Surgical Clinics North America1995;75:1071–89.
  15. Favero MS, Deane N, Leger RT, Sosin AE. Effect of multiple use of dialyzers on hepatitis B incidence in patients and staff. JAMA1981;245:166–67.
  16. Snydman DR, Bryan JA, Hanson B. Hemodialysis-associated hepatitis in the United States—1972. J Infect Dis1975;132:109–13.
  17. Snydman DR, Bregman D, Bryan JA. Hemodialysis-associated hepatitis in the United States, 1974. J Infect Dis1977;135:687–91.
  18. Szmuness W, Prince AM, Grady GF, et al. Hepatitis B infection. A point prevalence study in 15 US dialysis centers. JAMA1974;227:901–6.
  19. Centers for Disease Control and Prevention. Control measures for hepatitis B in dialysis centers. In: Viral Hepatitis Investigation and Control Series. Atlanta: CDC, 1977.
  20. Alter MJ, Favero MS, Maynard JE. Impact of infection control strategies on the incidence of dialysis-associated hepatitis in the United States. J Infect Dis1986;153:1149–51.
  21. Marmion BP, Burrell CJ, Tonkin RW, Dickson J. Dialysis-associated hepatitis in Edinburgh: 1969–1978. Rev Infect Dis1982;4:619–37.
  22. Najem GR, Louria DB, Thind IS, Lavenhar MA, Gocke DJ, Basking SE, Miller AM, Frankel HJ, Notkin MG, Weiner B. Control of hepatitis B infection. The role of surveillance and an isolation hemodialysis center. JAMA1981;245(2):153–57.
  23. Alter MJ, Favero MS, Francis DP. Cost benefit of vaccination for hepatitis B in hemodialysis centers. J Infect Dis1983;148:770–71.
  24. Hoofnagle JH, Di Bisceglie AM. Serologic diagnosis of acute and chronic viral hepatitis. Semin Liver Dis1991;11:73–83.
  25. Kloster B, Kramer R, Eastlund T, et al. Hepatitis B surface antigenemia in blood donors following vaccination. Transfusion1995;35:475–77.
  26. Lunn ER, Hoggarth BJ, Cook WJ. Prolonged hepatitis B surface antigenemia after vaccination. Pediatrics2000;105:E81.
  27. McMahon BJ, Alberts SR, Wainwright RB, et al. Hepatitis B-related sequelae: Prospective study in 1400 hepatitis B surface antigen—positive Alaska Native carriers. Arch Intern Med1990;150:1051–54.
  28. Hadler SC, Murphy B, Schable CA, et al. Epidemiological analysis of the significance of low-positive test results for antibody to hepatitis B surface and core antigens. J Clin Microbiol1984;19:521–25.
  29. Levine OS, Vlahov D, Koehler J, et al. Seroepidemiology of hepatitis B virus in a population of injecting drug users: Association with drug injection patterns. Am J Epidemiol1995;142:331–41.
  30. Silva AE, McMahon BJ, Parkinson AJ, et al. Hepatitis B virus DNA in persons with isolated antibody to hepatitis B core antigen who subsequently received hepatitis B vaccine.Clin Infect Dis1998;26:895–97.
  31. McMahon BJ, Parkinson AJ, Helminiak C, et al. Response to hepatitis B vaccine of persons positive for antibody to hepatitis B core antigen. Gastroenterology1992;103:590–94.
  32. Lai C-L, Lau JYN, Yeoh E-K, et al. Significance of isolated anti-HBc seropositivity by ELISA: Implications and the role of radioimmunioassay. J Med Virol1992;36:180–83.
  33. Niu MT, Coleman PJ, Alter MJ. Multicenter study of hepatitis C virus infection in chronic hemodialysis patients and hemodialysis center staff members. Am J Kidney Dis1993;22:568–73.
  34. Sypsa V, Psichogiou M, Katsoulidou A, et al. Incidence and patterns of hepatitis C virus seroconversion in a cohort of hemodialysis patients. Am J Kidney Dis2005;45:334–43.
  35. Fabrizi F, Martin P, Dixit V, et al. Acquisition of hepatitis C virus in hemodialysis patients: A prospective study by branched DNA signal amplification assay. Am J Kidney Dis1998;31:647–54.
  36. Petrosillo N, Gilli P, Serraino D, et al. Prevalence of infected patients and understaffing have a role in hepatitis C virus transmission in dialysis. Am J Kidney Dis2001;37:1004–10.
  37. dos Santos JP, Loureiro A, Cendoroglo Neto M, Pereira BJ. Impact of dialysis room and reuse strategies on the incidence of hepatitis C virus infection in haemodialysis units.Nephrol Dial Transplant1996;11:2017–22.
  38. Forns X, Fernandez-Llama P, Pons M, et al. Incidence and risk factors of hepatitis C virus infection in a haemodialysis unit. Nephrol Dial Transplant1997;12:736–40.
  39. Hmaied F, Ben Mamou M, Saune-Sandres K, et al. Hepatitis C virus infection among dialysis patients in Tunisia: Incidence and molecular evidence for nosocomial transmission. J Med Virol2006;78:185–91.
  40. Kobayashi M, Tanaka E, Oguchi H, et al. Prospective follow-up study of hepatitis C virus infection in patients undergoing maintenance haemodialysis: Comparison among haemodialysis units. J Gastroenterol Hepatol1998;13:604–9.
  41. McLaughlin KJ, Cameron SO, Good T, et al. Nosocomial transmission of hepatitis C virus within a British dialysis centre. Nephrol Dial Transplant1997;12:304–9.
  42. Silva LK, Silva MB, Rodart IF, et al. Prevalence of hepatitis C virus (HCV) infection and HCV genotypes of hemodialysis patients in Salvador, Northeastern Brazil. Braz J Med Biol Res2006;39:595–602.
  43. Chandra M, Khaja MN, Hussain MM, et al. Prevalence of hepatitis B and hepatitis C viral infections in Indian patients with chronic renal failure. Intervirology2004;47:374–76.
  44. Sivapalasingam S, Malak SF, Sullivan JF, et al. High prevalence of hepatitis C infection among patients receiving hemodialysis at an urban dialysis center. Infect Control Hosp Epidemiol2002;23:319–24.
  45. Carneiro MA, Martins RM, Teles SA, et al. Hepatitis C prevalence and risk factors in hemodialysis patients in Central Brazil: A survey by polymerase chain reaction and serological methods. Mem Inst Oswaldo Cruz2001;96:765–69.
  46. Covic A, Iancu L, Apetrei C, et al. Hepatitis virus infection in haemodialysis patients from Moldavia. Nephrol Dial Transplant1999;14:40–45.
  47. Fissell RB, Bragg-Gresham JL, Woods JD, et al. Patterns of hepatitis C prevalence and seroconversion in hemodialysis units from three continents: The DOPPS. Kidney Int2004;65:2335–42.
  48. Alter MJ. Epidemiology of hepatitis C in the west. Sem Liv Dis1995;15:5–14.

P.371

  1. Khokhar N, Alam AY, Naz F, et al. Risk factors for hepatitis C virus infection in patients on long-term hemodialysis. J Coll Physicians Surg Pak2005;15:326–28.
  2. Othman B, Monem F. Prevalence of antibodies to hepatitis C virus among hemodialysis patients in Damascus, Syria. Infection2001;29:262–65.
  3. Hardy NM, Sandroni S, Danielson S, Wilson WJ. Antibody to hepatitis C virus increases with time on hemodialysis. Clin Nephrol1992;38:44–48.
  4. Selgas R, Martinez-Zapico R, Bajo MA, et al. Prevalence of hepatitis C antibodies (HCV) in a dialysis population at one center. Perit Dial Int1992;12:28–30.
  5. Alter MJ. Prevention of spread of hepatitis C. Hepatology2002;365(suppl 1):S93–98.
  6. Dufour DR, Talastas M, Fernandez MD, Harris B. Chemiluminescence assay improves specificity of hepatitis C antibody detection. Clin Chem2003;49:940–44.
  7. Centers for Disease Control and Prevention. Guidelines for laboratory testing and result reporting of antibody to hepatitis c virus. MMWR2003;52(RR-03):1–16.
  8. Houghton M, Weiner A, Han J, et al. Molecular biology of the hepatitis C viruses: Implications for diagnosis, development and control of viral disease. Hepatology1991;14:381–88.
  9. Centers for Disease Control and Prevention. Recommendations for preventing transmission of infections among chronic hemodialysis patients. MMWR2001;50(RR-5):1–43.
  10. Busch MP, Kleinman SH, Jackson B, et al. Committee report. Nucleic acid amplification testing of blood donors for transfusion-transmitted infectious diseases: Report of the Interorganizational Task Force on Nucleic Acid Amplification Testing of Blood Donors. Transfusion2000;40:143–59.
  11. Williams IT, Gretch D, Fleenor M, et al. Hepatitis C virus RNA concentration and chronic hepatitis in a cohort of patients followed after developing acute hepatitis C. In: Margolis HS, Alter MJ, Liang TJ, et al, eds. Viral hepatitis and liver disease. Atlanta: International Press, 2002:341–44.
  12. Alter MJ, Margolis HS, Krawczynski K, et al. The natural history of community-acquired hepatitis C in the United States. The Sentinel Counties Chronic non-A, non-B Hepatitis Study Team. N Engl J Med1992;327:1899–905.
  13. Thomas DL, Astemborski J, Rai RM, et al. The natural history of hepatitis C virus infection: Host, viral, and environmental factors. JAMA2000;284:450–56.
  14. Larghi A, Zuin M, Crosignani A, et al. Outcome of an outbreak of acute hepatitis C among healthy volunteers participating in pharmacokinetics studies. Hepatology2002;36:993–1000.
  15. Hadler SC, Fields HA. Hepatitis delta virus. In: Belshe RB, ed. Textbook of human virology. St Louis: Mosby Year Book, 1991:749–65.
  16. Pol S, Dubois F, Mattlinger B, et al. Absence of hepatitis delta virus infection in chronic hemodialysis and kidney transplant patients in France. Transplantation1992;54:1096–97.
  17. Aghanashinikar PN, al-Dhahry SH, al-Marhuby HA, et al. Prevalence of hepatitis B, hepatitis delta, and human immunodeficiency virus infections in Omani patients with renal diseases. Transplant Proc1992;24:1913–4.
  18. Rezvan H, Forouzandeh B, Taroyan S, et al. A study on delta virus infection and its clinical impact in Iran. Infection1990;18:26–28.
  19. Lettau LA, Alfred HJ, Glew RH, et al. Nosocomial transmission of delta hepatitis. Ann Intern Med1986;104:631–35.
  20. Dyer E. Argentinian doctors accused of spreading AIDS. BMJ1993;307:584.
  21. Centers for disease Control. Recommendations for preventing transmission of hepatitis C virus (HCV infection and HCV-related chronic diseases. MMWR1998;47(RR-19):1–39.
  22. National Institutes of Health. Chronic hepatitis C: Current disease management. Washington, DC: National Institute of Diabetes, Digestive, and Kidney Diseases, 2000:1–21.
  23. Boyce JM, Pittet D. Guideline for hand hygiene in healthcare-settings. Recommendations of the Healthcare Infection Control Practices Advisory Committee and the HICPAC/SHEA/APIC/IDSA Hand Hygiene Task Force. Am J infect Control2002;30:S1–46.
  24. Centers for Disease Control and Prevention. Recommendations for preventing the spread of vancomycin resistance. MMWR1995;44 (RR-12):1–13.
  25. Fogel MA, Nussbaum PB, Feintzeig ID, et al. Cefazolin in chronic hemodialysis patients: A safe, effective alternative to vancomycin. Am J Kidney Dis1998;32:401–9.
  26. Marx MA, Frye RF, Matzke GR, Golper TA. Cefazolin as empiric therapy in hemodialysis-related infections: Efficacy and blood concentrations. Am J Kidney Dis1998;32:410–14.
  27. Favero MS, Bond WW. Chemical disinfection of medical and surgical materials. In: Block SS, ed. Disinfection, sterilization, and preservation. 4th ed. Philadelphia: Lea & febiger, 1991:617–41.
  28. Favero MS, Bolyard EA. Microbiologic considerations. Disinfection and sterilization strategies and the potential for airborne transmission of bloodborne pathogens. Surg Clin North Am1995;75:1071–89.
  29. Centers for Disease Control. Recommendations for prevention of HIV transmission in healthcare facilities. MMWR1987;36:1S–18S.
  30. Roberts C, Antonoplos P. Inactivation of human immunodeficiency virus type 1, hepatitis A virus, respiratory syncytial virus, vaccinia virus, herpes simplex virus type 1, and poliovirus type 2 by hydrogen peroxide gas plasma sterilization. Am J Infect Control1998;26:94–101.
  31. Bond WW, Favero MS, Petersen NJ, Ebert JW. Inactivation of hepatitis B virus by intermediate-to-high-level disinfectant chemicals. J Clin Microbiol. 1983;18:535–38.
  32. Sattar SA, Tetro J, Springthorpe VS, Giulivi A. Preventing the spread of hepatitis B and C viruses: Where are germicides relevant? Am J Infect Control2001;29:187–97.


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