Porter & Schon: Baxter's The Foot and Ankle in Sport, 2nd ed.

Section 2 - Sport Syndromes

Chapter 3 - Stress fractures: their causes and principles of treatment

Peter D. Brukner,Kim L. Bennell

		Introduction
		Epidemiology
		Risk factors for stress fractures
		Diagnosis
		Differential diagnosis
		Treatment
		Conclusion
		References

Introduction

Physical exercise has beneficial effects on a number of physiologic systems, including the skeleton. However, unwise training practices, combined with potential risk factors, may harm these systems. A stress fracture represents one form of breakdown in the skeletal system.^[1] It can be defined as a partial or complete fracture of bone that results from the repeated application of a stress lower than that required to fracture the bone in a single loading situation.^[2]

Historical perspective

Stress fractures were first described in 1855 by Briethaupt, a Prussian military physician who observed foot pain and swelling in young military recruits unaccustomed to the rigors of training. He considered it to be an inflammatory reaction in the tendon sheaths resulting from trauma and called the condition Fussgeschwulst. It was not until the advent of radiographs that the signs and symptoms were attributed to fractures in the metatarsals.^[3] The condition then became known as a “march” fracture because of the close association between marching and the onset of symptoms. Stress fractures were first noticed in civilians in 1921 by Deutschlander,^[4] who reported six cases in women. However, it was not until 1956, more than a century following their identification in military recruits, that they were recognized in athletes.^[5]

A variety of terms have been used over time to describe stress fractures. These include march fractures, Deutschlander's fractures. pied forcé, fatigue fractures, or crack fractures. ^{[0040] [0060] [0070] [0080] [0090] [0100]} Virtually all of these terms have been intended to describe some etiologic attribute of the stress injuries of bone. In recent years the most commonly used term has been stress fracture.

Following the radiographic description of metatarsal stress fractures, many theories were set forth to explain the etiology of this injury. Most of the reports were based on series that were small, and the theories proposed were concerned with either mechanical factors, such as spasm of the interossei, or flat feet, ^{[0040] [0110] [0120]} or with inflammatory reactions, such as nonsuppurative osteomyelitis. ^{[0070] [0080]}

Etiology of stress fractures

It is now recognized that the development of a stress fracture represents the end product of the failure of bone to adapt adequately to the mechanical loads experienced during physical activity. Ground reaction forces and muscular contraction result in bone strain. It is these repetitive strains that are thought to cause a stress fracture. Bone normally responds to strain by increasing the rate of remodeling. In this process, lamellar bone is resorbed by osteoclasts, thereby creating resorption cavities that subsequently are replaced with more dense bone by osteoblasts. Because there is a lag between increased activity of the osteoclasts and osteoblasts, bone is weakened during this time. ^{[0130] [0140]} If sufficient recovery time is allowed, bone mass eventually increases. However, if loading continues, microdamage may accumulate at the weakened region. ^{[0140] [0150]} Remodeling is thought to repair normally occurring microdamage. ^{[0160] [0170]} The processes of microdamage accumulation and bone remodeling, both resulting from bone strain, play an important part in the development of a stress fracture. If microdamage accumulates, repetitive loading continues, and remodeling cannot maintain the integrity of the bone; a stress fracture may result. ^{[0150] [0180] [0190]} This may occur because the microdamage is too extensive to be repaired by normal remodeling, because depressed remodeling processes cannot adequately repair normally occurring microdamage, or because of some combination of these factors.^[18]

Epidemiology

Stress fractures have been reported to occur in association with a variety of sports and physical activities. Clinical impression suggests that stress fractures are more common in weight-bearing activities, particularly those with a running or jumping component. However, it is difficult to compare the incidence of stress fractures in different sports or to identify the sport or activity with the greatest risk because of a lack of sound epidemiologic data. This section reviews the descriptive epidemiology of stress fractures. Most of the literature in this area pertains to female runners and to male military populations. There is no information about stress fracture rates in the general community.

Stress fracture injury rate

Stress fracture rates in athletes

Studies investigating stress fracture rates in athletes are shown in Table 3-1 . ^{[0200] [0210] [0220] [0230] [0240] [0250] [0260] [0270] [0280] [0290] [0300] [0310]} Of these, only two allow a direct comparison of annual stress fracture rates in different sporting populations. ^{[0280] [0290]} Johnson et al.^[28] conducted a 2-year prospective study to investigate sports-related injuries in collegiate male and female athletes. In total, 34 stress fractures were diagnosed during the study period. Track accounted for 64% of stress fractures in women and 50% of stress fractures in men. The stress fracture incidence rate (expressed as a case rate) in males was highest for track (9.7%), followed by lacrosse (4.3%), crew (2.4%), and American football (1.1%). The stress fracture incidence rate in women was highest for track athletes (31.1%), followed by crew (8.2%), basketball (3.6%), lacrosse (3.1%), and soccer (2.6%). No athlete sustained a stress fracture in fencing, hockey, golf, softball, swimming, or tennis.

Table 3-1 -- Stress fracture (SF) rates in athletes expressed as participant rates unless otherwise stated

Reference	Study design	Population	Subject sex & number	Method of data collection	Resp rate of quest (%)	Observation period	Diagnosis of SF	SF rate (%)
Barrow & Saha, 1988[20]	R	Collegiate distance runners	240-F	Self-admin. question	24	Hx	x-ray or BS	37.0
Brunet et al., 1990[21]	R	Recreational/competitive runners	375-F 1130-M	Self-admin. question	NS	Hx	NS	13.2-F 8.3-M
Cameron et al., 1992[22]	R	State/national level runners	263-F 287-M	Self-admin. question	67	Hx	NS	26.6-F 28.0-M
Bennell et al., 1995[23]	R	Track & field athletes	53-F	Self-admin. question	100	Hx	x-ray, BS, or CT	51.5 84.9 *
Bennell et al., 1996[24]	P	Track & field athletes	46-F 49-M	Monitoring	NA	1yr	BS + CT	21.7-F 20.4-M 30.4-F * 24.5-M *
Warren et al., 1986[25]	R	Professional ballet dancers	40-F	Self-admin. question	100	Hx	x-ray or BS	45.0 67.5 *
Frusztajer et al., 1990[26]	R	Ballet dancers	45-F	Interview + question	100	1yr	NS	22.0
Kadel et al., 1992[27]	R	Professional ballet dancers	54-F	Self-admin. question	100	Hx	x-ray or BS	31.5 50.0 *
Johnson et al., 1994[28]	P	Collegiate athletes	321-F 593-M	Monitoring	NA	2yr	x-ray or BS	6.9-F * [†] 2.0-M * [†]
Goldberg & Pecora, 1994[29]	R	Collegiate athletes	≈1200-F ≈1800-M	Review of medical records	NA	3yr	x-ray or BS	2.7-F * [†] 1.4-M * [†]
Pecina et al., 1990[30]	R	Elite ice skaters	42 M/F	Self-admin. question	100	Hx	NS	21.0
Dixon & Fricker, 1993[31]	R	Elite gymnasts	74-F 42-M	Review of medical records	NA	10yr	x-ray or BS	27.0-F * 14.3-M *

From Bennell KL, Brukner PD: Epidemiology and site specificity of stress fractures, Clin Sports Med 16:183, 1997.

BS, Bone scan; CT, computed tomography; F, females; Hx, history; M, males; NA, not applicable; NS, not stated; P, prospective cohort; quest, questionnaire; R, retrospective cohort; resp, response.

*	Stress fracture rates expressed as case rates: number of stress fractures per 100 athletes.
†	Annual incidence.

Goldberg and Pecora^[29] reviewed medical records of stress fractures occurring in collegiate athletes during a 3-year period. Approximate participant numbers were available to allow calculation of estimated incidence case rates in each sport. The greatest incidence occurred in softball (19%), followed by track (11%), basketball (9%), lacrosse (8%), baseball (8%), tennis (8%), and gymnastics (8%). However, participant numbers were small in some of these sports, possibly leading to a bias in incidence rates.

Both studies suggest that track athletes are at one of the highest risks for stress fracture. However, because neither expressed incidence in terms of exposure, it may not be strictly valid to compare the risk of stress fracture in such diverse sports. To our knowledge, there is only one athlete study that has expressed stress fracture incidence rates in terms of exposure.^[24] This 12-month prospective study followed a cohort of 95 track and field athletes. Results showed an overall rate of 0.70 stress fractures per 1000 training hours. Further research is needed to quantify incidence rates in this manner to allow more valid comparison between studies.

Retrospective studies have measured stress fracture rates in specific sporting populations, mostly runners and ballet dancers. ^{[0200] [0210] [0220] [0230] [0250] [0260] [0270] [0290] [0300] [0310]} Variation in reported rates reflects differences in methodology, particularly cohort demographics and method of data collection. A history of stress fracture has been reported by 13% to 52% of female runners. The lowest rate was found in one study that included recreational, as well as competitive, runners. Ballet dancers are another population in which stress fracture rates appear high, with 22% to 45% of dancers reporting a history of stress fracture. However, most studies failed to confirm the accuracy of subject recall, a failure that may introduce bias into the figures reported. Nevertheless, it is clear that stress fracture is a relatively common athletic injury.

Stress fracture rates in the military

Reports of the incidence of stress fractures in male recruits undergoing basic training for periods of 8 to 14 weeks are remarkably similar and generally range from 0.9% to 4.7%. ^{[0320] [0330] [0340] [0350] [0360] [0370] [0380] [0390] [0400]} However, in two particular studies involving the Israeli army, the reported incidence was 31%^[41] and 24%.^[42] The authors attributed this much higher incidence to several factors, including meticulous follow-up, a high index of suspicion, and the use of the radioisotope bone scan for diagnosis. In addition, asymptomatic areas of uptake on bone scan also were classified as lesions, and this would inflate the reported figures. Stress fracture rates in female military recruits during basic training generally are higher than those in males, ranging from 1.1% to 13.9%. ^{[0320] [0330] [0350] [0370] [0390] [0430]}

Stress fracture recurrence rates

Clinically it seems that recurrence of stress fractures at new sites is common. In female track and field athletes, half of those who reported a history of stress fracture had experienced a stress fracture on more than one occasion.^[23] However, few studies have reported recurrence rates in either athletes or the military. When male and female track and field athletes were followed prospectively for 1 year, 60% of those who sustained a stress fracture had a previous stress fracture history.^[24] The athlete recurrence rate in this study was particularly high at 12.6%. A large number of male military recruits were followed for a minimum of 1 year after basic training.^[44] The recurrence rate of stress fractures at a different site in those who had sustained a stress fracture during basic training was 10.6%. In the control group of 60 recruits who did not develop a stress fracture during basic training, the incidence of stress fracture after basic training was only 1.7%. This finding could indicate the persistence of risk factors in susceptible individuals.

Comparison of stress fracture rates in different age groups

It is unclear whether age, as an independent factor, influences the risk of stress fracture because results in the military are conflicting and there are no studies in athletes investigating the incidence of stress fractures in different-aged individuals engaged in identical training. In a retrospective cohort study of 20,422 military recruits, review of clinical records found a positive association between increasing age in the range 17 to 34 years and the incidence of stress fractures in both men and women.^[35] Similar results, even after adjusting for pretraining physical activity, were reported by Gardner et al.^[36] in a large prospective study. These suggest that increasing age, within the range studied, may be associated with a higher incidence of stress fractures. It is surmised that this may be because bone of older individuals is less resistant to fatigue failure. ^{[0450] [0460]}

However, a prospective study by Milgrom et al.^[42] in the Israeli army contradicts the hypothesis that stress fracture incidence increases with age in military recruits. For each year of increase in age from 17 to 26 years, the risk for stress fracture at all sites decreased by 28%. The authors suggested that the decreasing risk with age may be related to increased structural maturity, increased bone density, larger cross-sectional moment of inertia, or changes in bone quality in the older recruits. It also is possible that injury-prone older individuals may be less likely to apply for military training. However, it should be noted that the number of recruits older than the age of 19 was very small in this study.

A case series of 1407 patients presenting to a sports medicine center found that stress fractures or periostitis comprised a greater percentage of injuries in the “younger” group (mean age of 30 years), compared with that in the “older” group (mean age of 57 years).^[47] However, because of the study design, it is not known whether this reflects selection of stress fracture-resistant individuals in the older group, modification of training regimens to lower musculoskeletal stress, or an independent age effect on stress fracture development.

Comparison of stress fracture rates in men and women

It often is suggested that women sustain a disproportionately higher number of stress fractures than men. The relative risk of stress fracture for women compared with men from studies in which stress fracture rates can be directly compared is shown in Table 3-2 . In the military, reported incidence rates during an 8-week training period vary from 1.1% to 13.9% in women and from 0.9% to 3.2% in men. These studies consistently show that female recruits have a greater risk of stress fracture than male recruits, with relative risks ranging from 1.2 to 10. ^{[0320] [0330] [0350] [0370] [0390] [0430]} This increased risk persists even when training loads gradually are increased to moderate levels and when incidence rates are separated by age and race. The most likely explanation for these findings in the military is lower initial physical fitness in the female recruits. Other possible reasons include differences in bone density and geometry, gait, biomechanical features, body composition, and endocrine factors, particularly estrogen status.

Table 3-2 -- Relative risk of stress fracture for women compared with men from studies in which stress fracture rates can be directly compared

Variable	Brunet et al., 1990[21]	Cameron et al., 1992[22]	Johnson et al., 1994[28]	Goldberg & Pecora, 1994[29]	Zernicke et al., 1993[93]
Type of study	R	R	P	R	NS
Sport population	Runners *	Runners	Variety[†]	Variety[†]	Runners
Age, females	33	NS	≈18–22	≈18‐22	≈18‐22
Age, males	39	NS	≈ 8‐22	≈18‐22	≈18‐22
Female number	375	263	321	≈1200	NS
Male number	1130	287	593	≈1800	NS
Observation	History	History	2yr	3yr	12 months
Data collection	Q	Q	Clinic	Records	NS
Response rate	NS	67%	NA	NA	NS
% of SF, females	13.2	26.6	6.9	≈2.7	20‐25
% of SF, males	8.3	28.0	2.0	≈1.4	10.0
Relative risk F:M	1.6	0.95	3.5	≈1.9[‡]	2.2

From Bennell KL, Brukner PD: Epidemiology and site specificity of stress fractures, Clin Sports Med 16:179, 1997.

NA, Not applicable; NS, not stated; P, prospective; Q, questionnaire; R, retrospective.

*	Mainly novice runners.
†	Collegiate athletes.
‡	Population at risk was estimated, therefore providing an approximate incidence rate.

In contrast, a gender difference in stress fracture rates is not as evident in athletic populations. ^{[0210] [0220] [0240] [0280] [0290] [0310]} Studies either show no difference between male and female athletes or a slightly increased risk for women, up to 3.5 times that of men (see Table 3-2 ). A possible confounding variable is that, unlike the military, in which the amount and intensity of basic training is rigidly controlled, it is difficult to assume equivalence of training between men and women in most of these studies. However, Bennell et al.^[24] found no significant difference between gender incidence rates even when expressed in terms of exposure. Women sustained 0.86 stress fractures per 1000 training hours, compared with 0.54 in men. It is feasible that a gender difference in stress fracture risk is reduced in athletes because female athletes may be more conditioned to exercise than female recruits; hence the fitness levels of male and female athletes may be closer.

Comparison of stress fracture rates in different races

Both male and female Caucasians appear to be at greater risk for stress fractures than blacks, with relative risks ranging from 2.3 to 24 ( Table 3-3 ). This may be related to higher bone density in blacks^[48]or to different biomechanical features that may be protective against stress fractures.^[49]

Table 3-3 -- Studies investigating the rates and relative risk of stress fractures (SFs) comparing caucasians (C) and blacks (B). All rates are expressed as participant rates unless stated

Reference	Population	Study design	Number C	Number B	SF rates C (%)	SF Rates B (%)	Relative risk C vs. B
Men
Brudvig et al., 1983[35]	Military	R	NS	NS	1.1	0.2	4.7 *
Gardner et al., 1988[36][†]	Military	P	2050	975	1.6[‡]	0.7[‡]	2.3 *
Milgrom et al., 1994[42]	Military	P	765	18	24.8	0.0	24.8 *
Women
Brudvig et al., 1983[35]	Military	R	NS	NS	11.8	1.4	8.5 *
Barrow & Saha, 1988[20]	Athletes	R	220	12	39.0	17.0	2.3

From Bennell KL, Brukner PD: Epidemiology and site specificity of stress fractures. Clin Sports Med 16:187, 1997.

NS, Not stated; P, prospective cohort; R, retrospective cohort.

*	Statistically significant difference between races.
†	Blacks include all racial and ethnic groups apart from whites.
‡	Stress fracture rates expressed as case rates: number of stress fractures per 100 recruits.

Relative frequency of stress fractures as a proportion of total injuries

Numerous case series have reported that stress fractures comprise between 0.7% and 15.6% of all injuries sustained by athletic populations. ^{[0310] [0500] [0510] [0520] [0530] [0540]}

In those investigating runners only, the relative frequency is much higher, ranging from 6.0% to 15.6%. In track and field athletes, stress fractures appear to comprise a large proportion of overuse injuries: 34.2% in women and 24.4% in men reported by one study,^[24] and 42.0% by men and women combined in another.^[50] In elite gymnasts, stress fractures comprised 18.3% of overuse injuries in women and 9.2% in men.^[31] It seems that the relative frequency of stress fractures is greater in female than in male athletes. The variation in results probably reflects differences in the composition of each case series.

Stress fracture sites

Athletes

Stress fractures are most common in bones of the lower extremity but also occur in nonweight-bearing bones, including the ribs, upper limb, and pelvis. Numerous studies have reported the anatomic distribution of series of stress fractures ^{[0200] [0220] [0240] [0270] [0280] [0290] [0500] [0520] [0530] [0550] [0560] [0570] [0580] [0590] [0600] [0610] [0620] [0630]} ( Table 3-4 ). Although there is great variation in the percentage of stress fractures reported at each bony site, the most common sites appear to be the tibia, metatarsals, and fibula. A number of factors may influence the reported distributions of stress fractures. These include type and level of activity, gender, age, and, in particular, method of diagnosis. For example, tarsal navicular stress fractures rarely are evident on radiographs. If diagnosis is confined to radiographs, these therefore will be underreported in comparison with stress fractures at other sites.

Table 3-4 -- Anatomic distribution of stress fractures (SFs) in athletes expressed as a percentage of the total number of stress fractures in each series

Reference	Sport	No. of SF in series	Diagnosis of SF	Tibia (%)	Fibula (%)	Metatarsal (%)	Navicular (%)	Femur (%)	Pelvis (%)
Brubaker & James, 1974[50]	Runners	17	NS	41.2	17.6	29.4	5.9	0	0
Orava, 1980[52]	Variety	200	x-rays +/- BS	53.5	12.5	18.0	2.0	6.0	1.5
Pagliano & Jackson, 1980[53]	Runners	99	self-report	20.2	15.2	37.4	NS	NS	NS
Taunton et al., 1981[55]	Runners	62	x-rays or BS	55.0	11.3	16.1	3.2	6.5	0
Clement et al., 1981[56]	Runners	87	NS	57.5	9.2	20.7	3.4	4.6	0
Sullivan et al., 1984[57]	Runners	57	x-ray or BS	43.9	21.0	14.0	0	3.5	10.5
Barrow & Saha, 1988[20]	Runners	140	self-report	63.0	9.0	21.0	0.7	4.0	1.4
Hulkko & Orava, 1987[58]	Variety	368	x-ray +/- BS	49.5	12.0	19.8	2.5	6.3	1.9
Matheson et al., 1987[59]	Variety	320	bone scan	49.1	6.6	8.8	NS	7.2	1.6
Courtenay & Bowers, 1990[60]	Variety	108	x-ray or BS	38.0	29.6	18.5	4.6	2.8	0.9
Ha et al., 1991[61]	Variety	169	x-ray or BS	31.5	10.7	7.1	4.7	12.5	4.1
Cameron et al., 1992[22]	Runners	253	self-report	37.5	12.0	22.5	10.0	NS	NS
Benazzo et al., 1992[62]	Track & field	49	x-ray, CT or BS	26.5	12.2	14.3	28.6	0	0
Kadel et al., 1992[27]	Ballet	27	self-report	22.0	0	63.0	NS	4.0	0
Goldberg & Pecora, 1994[29]	Variety	58	x-ray or BS	18.9	12.1	25.9	NS	10.0	3.4
Johnson et al., 1994[28]	Variety	34	x-ray +/- BS	38.2	0	20.6	11.8	23.5	0
Bennell et al., 1996[24]	Track & field	26	BS & CT	45.0	12.0	8.0	15.0	8.0	4.0
Brukner et al., 1996[63]	Variety	180	x-ray, CT or BS	20.0	16.7	23.3	20.0	3.3	1.1

From Bennell KL, Brukner PD: Clin Sports Med 16:190, 1997.

BS, Bone scan; CT, computed tomography; NS, not stated.

Stress fractures develop at skeletal sites that are subjected to repetitive mechanical loading during a particular activity. The site specificity of stress fractures was illustrated in a prospective study in 95 track and field athletes.^[24] Although stress fracture incidence rates were similar in power and endurance athletes, the site distribution differed. Power athletes (sprinters, hurdlers, and jumpers) sustained significantly more foot fractures, whereas endurance athletes (middle-distance and distance runners) sustained more long bone and pelvic fractures. In a series of 180 stress fractures, the percentage distribution of sports among the five most common sites is shown in Table 3-5 .^[63] Dancers were the most common group sustaining metatarsal stress fractures, and track and distance runners sustained the most tibial stress fractures, whereas distance runners and dancers were prominent among fibula stress fractures. Track athletes were by far the most common among the navicular stress fractures. Pars fractures were seen in athletes in field events, racquet sports, cricket, dancing, and basketball. It therefore is apparent that different sports show typical patterns of stress fractures; these are summarized inTable 3-6 .^[64] Other sports associated with certain stress fractures are rowing or golf (rib stress fractures), pitching (humeral fractures), and gymnastics (pars fractures).

Table 3-5 -- Percentage distribution of sports among the most common stress fracture sites

Sport	Metatarsal (n = 42)	Tibia (n = 36)	Fibula (n = 30)	Tarsal navicular (n = 26)	Pars interarticularis (n = 17)
Track	21.4	38.9	16.7	73.1	5.8
Jog/distance running	11.9	41.7	26.7	3.8	0
Dance	42.9	2.8	23.3	0	17.6
Australian football	4.8	8.3	10	7.7	0
Racquet sports	2.4	2.8	6.7	3.8	17.6
Field events	0	0	6.7	0	23.5
Rowing/canoeing	2.4	0	3.3	3.8	0
Triathlon	2.4	0	3.3	3.8	0
Basketball	2.4	0	0	3.8	11.8
Cricket	0	0	0	0	17.6
Aerobics	7.2	0	3.3	0	0
Field hockey	0	0	0	0	5.9
Rugby	0	2.8	0	0	0
Martial arts	2.4	0	0	0	0
Work-related	0	0	0	0	5.9

From Brukner P, et al: Clin J Sport Med 6:85, 1996.

Table 3-6 -- Sports and activities commonly associated with different stress fracture sites

Site of stress fracture	Sport or activity
Coracoid process of scapula	Trapshooting
Scapula	Running with hand-held weights
Humerus	Throwing, racquet sports
Olecranon	Throwing, pitching
Ulna	Racquet sports (especially tennis), gymnastics, volleyball, swimming, softball, wheelchair sports
Ribs, first	Throwing, pitching
Ribs, second to tenth	Rowing, kayaking
Pars interarticularis	Gymnastics, ballet, cricket fast bowling, volleyball, springboard diving
Pubic ramus	Distance running, ballet
Femur, neck	Distance running, jumping, ballet
Femur, shaft	Distance running
Patella	Running, hurdling
Tibia, plateau	Running
Tibia, shaft	Running, ballet
Fibula	Running, aerobics, race walking, ballet
Medial malleolus	Basketball, running
Calcaneus	Long distance military marching
Talus	Pole vaulting
Navicular	Sprinting, middle distance running, hurdling, long/triple jumping, football
Metatarsal, general	Running, ballet, marching
Metatarsal, base second	Ballet
Metatarsal, fifth	Tennis, ballet
Sesamoid bones of foot	Running, ballet, basketball, skating

From Brukner PD, Khan KM: Clinical sports medicine, rev ed 2, Sydney, 2002, McGraw-Hill Book Company.

Conditioned athletes may sustain stress fractures different from those in persons unaccustomed to activity. In a series of 368 fractures, competitive athletes had stress fractures in the tibia significantly more often, whereas recreational athletes had significantly more metatarsal and pelvic bone fractures. ^{[0520] [0580]} It also has been reported that females sustain more metatarsal, ^{[0520] [0580]} pelvic, ^{[0520] [0580]} and navicular stress fractures^[28] than males. Age differences also may play a part; Matheson et al.^[59] found significantly more femoral and tarsal stress fractures in older athletes and more tibial and fibular stress fractures in younger athletes. However, an interaction between age and site of stress fracture was not confirmed in another large series.^[58]

Military recruits

The location of stress fractures in military personnel has appeared to change over the years, probably as a result of changes in training, with a greater emphasis on running instead of marching; changes in footwear, with athletic shoes often replacing combat boots; and changes in initial fitness levels with fitter recruits. Original reports described primarily injuries of the foot, with most diagnosed stress fractures occurring in the metatarsals. ^{[0100] [0650]} However, in the last 2 decades, a greater number of stress fractures have been found in the leg, particularly the tibia, thus more closely approximating that observed in athletic populations. In a recent prospective study in 626 male U.S. Marine Corps recruits, 27 stress fractures were sustained.^[40] The most common site was the tibia (41%), followed by the metatarsals (26%), the femur (19%), and the tarsals (15%). The site distribution of stress fractures in military populations has been well reviewed by Jones et al.^[43]

Risk Factors for Stress Fractures

Risk factors are markers that can be used to identify athletes who are more likely to sustain a stress fracture. Preventative strategies then can be directed toward these individuals. Although the risk factors themselves may not be involved in stress fracture pathogenesis, they directly or indirectly increase the chance of a stress fracture's developing. This occurs by their influence on either the mechanical environment of bone or the remodeling process. Although numerous risk factors for stress fractures have been proposed, research is needed to confirm anecdotal observations. Presently most studies in athletes are case series, confined to injured groups only, or are cross-sectional designs that do not allow the temporal relationship between risk factor and injury to be assessed. Methodologic issues, such as small subject numbers, different definitions of stress fractures, and failure to assess the independent contributions of risk factors also limit their usefulness. There also are few data about risk factors in male athletes. Results from large military epidemiologic studies cannot be readily generalized to athletes because of important differences in training, fitness levels, footwear, and surfaces. However, these may provide additional insights, especially given the deficiencies in the athletic literature.

Genetic predisposition

A large component of the variation in bone mass can be attributed to genetic factors.^[66] Not surprisingly, then, a family history of osteoporosis is considered to be a risk factor for low bone density and osteoporosis in both men and women. ^{[0670] [0680]} Similarly, a significant relationship between a family history of osteoporosis and yearly change in bone density has been demonstrated in studies of runners and nonrunners.^[69] It therefore is feasible that some individuals may be genetically predisposed to stress fractures when exposed to suitable environmental conditions, such as vigorous exercise. This was implied in a case report in which a pair of 18-year-old monozygotic twins undergoing basic military training sustained identical multiple stress fractures in the femoral and tarsal bones.^[70] The authors proposed that identical environmental conditions served to unmask a genetically determined deficiency in the affected bones. Although Myburgh et al.^[71] failed to find a difference in the incidence of a family history of osteoporosis in a group of 25 athletes with stress fractures and a group without stress fractures, this may reflect the small sample. At present, there is little evidence to show that genetic factors predispose an athlete to this injury.

Menstrual disturbances

Because hypoestrogenic postmenopausal women are at an increased risk of developing osteoporotic fractures, it has been suggested that stress fractures may be more prevalent in female athletes with menstrual disturbances. It is feasible that estrogen deficiency could promote stress fracture development by the following:

	•	Accelerating the process of bone remodeling, leading to weakened areas of bone because of the lag period between resorption and formation
	•	Increasing calcium excretion, resulting in greater calcium requirements that may not be adequately met by dietary intake
	•	Causing premature bone loss and hence lower bone density

Although progesterone may be a promoter of bone formation, particularly in cortical bone,^[72] and luteal phase deficiency in athletes is associated with lowered progesterone levels, a possible link between luteal phase deficiency and stress fracture risk has not been sought. Research to date has focused on the relationship between stress fracture incidence and menstrual irregularity (amenorrhea and oligomenorrhea), age of menarche, and use of the oral contraceptive pill (OCP).

The findings of numerous studies suggest that stress fractures are more common in athletes exhibiting menstrual disturbances ^{[0200] [0250] [0260] [0270] [0710] [0730] [0740] [0750] [0760] [0770] [0780]} ( Fig. 3-1 ). Although not all results were statistically significant, power may have been limited by relatively small samples in some studies. In general, athletes with menstrual disturbances had a relative risk for stress fracture that was between two and four times greater than that of their eumenorrheic counterparts. However, in ballet dancers, logistic regression analysis showed that amenorrhea for longer than 6 months’ duration was an independent contributor to the risk of stress fracture, with the estimated risk being 93 times that of a dancer with regular menses.^[27]

Figure 3-1 Studies in which the percentage of athletes with stress fractures could be compared in groups with and without menstrual disturbances. 1, Lindberg et al., 1984[73]; 2, Marcus et al., 1985[74]; 3, Lloyd et al., 1986[75]; 4, Warren et al., 1986[25]; 5, Nelson et al., 1987[76]; 6, Barrow and Saha, 1988[20]; 7, Myburgh et al., 1990[71]; 8, Frusztajer et al., 1990[26]; 9, Grimston et al., 1991[77]; 10, Cameron et al., 1992[22]; 11, Kadel et al., 1992.[27]

The risk of multiple stress fractures also seems to be increased in those with menstrual disturbances. ^{[0200] [0790]} Clark et al.^[79] found that, although amenorrheic and eumenorrheic groups reported a similar prevalence of single stress fractures, 50% of the amenorrheic runners reported multiple stress fractures, compared with only 9% of those regularly menstruating.

Grimston et al.^[80] developed a menstrual index that summarized previous and present menstrual status. They found no relationship between this menstrual index and the incidence of stress fractures in 16 female runners. Conversely, Barrow and Saha^[20] found that lifetime menstrual history did affect the risk of stress fracture. They showed the incidence of stress fracture to be 29% in the regular group and 49% in the very irregular group. The results of a prospective study also demonstrated that those with a lower menstrual index were at greater risk of stress fracture. Myburgh et al.^[71] found that, although athletes with stress fractures had a higher frequency of current menstrual dysfunction than athletes without stress fractures, there was no difference in past menstrual status. This suggests that changes associated with menstrual dysfunction are reversible and do not affect future stress fracture risk if regular menses return.

In summary, it would appear that there is a higher incidence of menstrual disturbances in female athletes with stress fracture than in those without. These findings have led some authors to assume that this is a direct result of decreased bone mineral density (BMD) in athletes with menstrual disturbances. However, athletes with menstrual disturbances also exhibit other risk factors, such as lower calcium intake,^[81] greater training load,^[82] and differences in soft tissue composition.^[83] Because these were not always controlled for in the studies discussed, it is difficult to ascertain which are the contributory factors.

The relationship between age of menarche and risk of stress fracture is uncertain. Some authors have found that athletes with stress fractures have a later age of menarche, ^{[0250] [0840] [0850]} whereas others have found no difference. ^{[0260] [0270] [0710]} In a prospective study, age of menarche was an independent risk factor for stress fracture, with the risk increasing by a factor of 4.1 for every additional year of age at menarche.^[78] However, the mechanism for this relationship is unclear, because a later age of menarche also is associated with an increased likelihood of menstrual disturbance,^[86] a lower energy intake,^[87] decreased body fat or weight,^[87] and excessive premenarcheal training,^[86] all of which could influence stress fracture risk.

Some authors have claimed that the OCP may protect against stress fracture development. Barrow and Saha^[20] found that runners using the OCP for at least 1 year had significantly fewer stress fractures (12%) than nonusers (29%). This was supported by the findings of Myburgh et al.^[71] Although no difference in OCP use was reported in ballet dancers with and without stress fractures,^[27] few dancers were taking the OCP. Because these studies are cross-sectional or retrospective in nature, it is not known whether the athletes were taking the OCP before or following the stress fracture episode. In addition, athletes may or may not take the OCP for reasons that in themselves could influence stress fracture risk. A prospective study did not support a protective effect of OCP use on stress fracture development.^[78] Nevertheless, it is not known whether the risk of stress fracture is decreased in athletes with menstrual disturbances who subsequently take the OCP. This is an important area for future research.

Low bone density

Theoretically, low BMD could contribute to the development of a stress fracture by decreasing the fatigue resistance of bone to loading and by increasing the accumulation of microdamage. ^{[0450] [0880]}Results from a limited number of studies comparing regional bone density in military or athletic groups with and without stress fracture have been inconclusive ^{[0260] [0400] [0710] [0770] [0780] [0840] [0850] [0890] [0900]} ( Table 3-7 ). The discrepancy may reflect differences in populations, type of physical activity, measurement techniques, and bone regions. However, the findings of a 12-month prospective study using dual energy x-ray absorptiometry (DEXA) to measure bone mass indicate that low bone density is a risk factor for stress fractures in women and possibly in men.^[78] Female athletes who sustained tibial stress fractures had 8.1% lower tibia/fibula BMD than athletes without stress fractures (p < .01). In the men, the tibial stress fracture group had 4.0% less tibia/fibula BMD than the nonstress fracture group, although this was not significant (p = .17). However, it is important to note that in this study the athletes with stress fractures still had bone density levels that were similar to or greater than less-active control subjects. This implies that the level of bone density required by athletes for short-term bone health is greater than that required by the general population.

Table 3-7 -- Summary of studies directly investigating the relationship between bone density and stress fractures

Reference	Study design	Subjects	Sex	Sample size	Techn	Sites	Results % diff[†]
Pouilles et al., 1989[89]	CS	Military	M	41-SF 48-NSF	DPA	Femoral neck Ward's triangle Trochanter	-5.7 * -7.1 * -7.4 *
Carbon et al., 1990[85]	CS	Various athletes	F	9-SF 9-NSF	DPA SPA	LSp Femoral neck Distal radius Ultradistal radius	-4.0 * -7.0 -7.7 0.0
Frusztajer et al., 1990[26]	CS	Ballet dancers	F	10-SF 10-NSF	DPA SPA	LSp First metatarsal Radial shaft	-4.1 0.0 0.0
Myburgh et al., 1990[71]	CS	Various athletes	M/F	25-SF 25-NSF (19F, 6M)	DXA	LSp Femoral neck Ward's triangle Trochanter Intertrochanter Proximal femur	-8.5 * -6.7 * -9.0 * -8.6 * -5.5 -6.5 *
Giladi et al., 1987[92]	P	Military	M	91-SF 198-NSF	SPA	Tibial shaft	–6.0
Grimston et al., 1991[77]	CS	Runners	F	6-SF 8-NSF	DPA	LSp Femoral neck Tibial shaft	8.2 * 7.6 * 9.7
Warren et al., 1991[84]	CS	Ballet dancers	F	14-SF 34-NSF	DPA	LSp First metatarsal Distal radius	NS NS NS
Bennell et al., 1996[78]	P	Track & field athletes	F M	10-SF 36-NSF 10-SF 39-NSF	DXA DXA	Upper limb Thor sp LSp Femur Tibia/fibula Foot Upper limb Thor sp LSp Femur Tibia/fibula Foot	-3.3 -6.7 -11.9 * -2.2 -4.2 -6.6 * -4.9 -4.1 -0.8 -2.9 -4.0 -0.3
Beck et al., 199640	P	Military	M	23-SF 587-NSF	DXA	Femur Tibia Fibula	-3.9 * -5.6 * -5.2

CS, Cross-sectional; DPA, dual photon absorptiometry; DXA, dual energy x-ray absorptiometry; F, females; LSp, lumbar spine; M, males; NS, not stated but not significantly different; P, prospective; SPA,single photon absorptiometry; Techn, technique; Thor sp, thoracic spine.

*	Statistically significant.
†	Results are given as the percent difference comparing stress fracture subjects (SF) with nonstress–fracture subjects (NSF).

Bone geometry

Bone geometry influences the ability of the bone to resist mechanical loads. A prospective study of 295 male Israeli military recruits assessed the influence of bone geometry on stress fracture risk. ^{[0910] [0920]} Significantly fewer stress fractures were sustained by those with a greater mediolateral tibial width, measured using standard radiographs, than by those with a narrower tibia. This may be due to a greater area moment of inertia and hence increased ability of the bone to resist bending forces in the anteroposterior direction. However, the incidence of stress fractures did not correlate with cortical thickness. These findings were confirmed by a recent prospective study of 626 U.S. male recruits.^[40] Using DEXA to derive structural geometry, the authors found significantly smaller tibial cross-sectional area, smaller tibial section modulus, and smaller tibial width in the stress fracture cases. These remained after adjusting for body weight differences between groups. There are no data that investigate whether bone geometry predisposes to stress fractures in athletes.

Endocrine factors

Alterations in calcium metabolism could affect bone remodeling and bone density, and theoretically predispose to stress fracture. However, single measurements of serum calcium, parathyroid hormone, 25 OH-vitamin D and 1,25-dihydroxyvitamin D have not been found to differ between stress fracture and nonstress fracture groups in military recruits. ^{[0250] [0710] [0850]} This may reflect sampling procedures or the fact that many of these biochemical parameters are tightly regulated.

Nutritional status

Low calcium intake may contribute to stress fracture development by directly influencing the processes of bone remodeling and bone mineralization or by indirectly affecting soft tissue composition and ovarian function. Other dietary factors, such as fiber, protein, and caffeine intake, may play a role but have not been well studied.

There is limited evidence to suggest that low calcium intake may be associated with an increased risk for stress fracture. ^{[0710] [0930]} Myburgh et al.^[94] found a significantly lower intake of calcium in athletes with shin soreness in comparison with a matched control group. However, because exact diagnoses were not made, stress fracture may not have been the only pathology included in this group. A follow-up study in athletes with scintigraphically diagnosed stress fractures confirmed the original results.^[71] Current calcium intake was significantly lower in the stress fracture group, being 87% of the recommended daily intake (RDI). This is consistent with their reduced consumption of dairy products. The authors claimed that a calcium intake of greater than 800mg/day protects against stress fracture development.

Conversely, other investigators have failed to confirm the relationship between stress fractures and dietary calcium. ^{[0260] [0270] [0780] [0840] [0850] [0950]}

Many ballet dancers were found to consume less than the RDI for calcium regardless of their stress fracture status, ^{[0260] [0270]} implying that other factors may be more important as risk factors in dancers. A calcium index based on the variability in calcium intake during the ages of 12 to 23 years did not differ in runners with and without stress fractures.^[77] In a prospective study of track and field athletes, risk of stress fracture was not associated with current calcium intake, current intake of nutrients known to influence calcium bioavailability and bone mass, or calcium supplementation use. Because the majority of athletes in this study were consuming more than the RDI for calcium, the results suggest that the relative risk of stress fracture is not influenced by daily intakes above this level. This is consistent with the concept of calcium as a threshold nutrient whereby effects on the skeleton are apparent only up to a certain level.^[96] However, it does not rule out an association between calcium deficiency and a higher incidence of stress fracture.

There are no intervention studies assessing the effect of calcium supplementation on stress fracture incidence in athletes. A randomized controlled study in male military recruits showed a similar incidence of stress fractures during a 9-week training program in 247 recruits taking 500mg of calcium daily and in 1151 controls.^[97] However, because both groups had a baseline dietary calcium intake greater than 800mg/day, this may have been sufficient to provide protection against stress fracture. Alternatively, a longer duration of calcium intervention may be necessary for effects to become apparent, particularly at cortical bone sites.

Other nutrients, such as protein, total energy, phosphorus, fiber, sodium, alcohol, and caffeine could potentially affect bone health and therefore stress fracture risk. At present, no associations have been found between these and the incidence of stress fractures in athletes. ^{[0260] [0780] [0840] [0850]}

Dietary behaviors and eating patterns may differ in those with stress fractures. Ballet dancers with stress fractures were more likely to diet and restrict food intake, avoid high-fat dairy foods, consume low-calorie products, have a self-reported history of an eating disorder, and have weight fluctuations down to a lower percentage of ideal body weight than those without stress fractures.^[26] However, scores on a validated test relating to dieting, bulimia and food preoccupation, and oral control (EAT-26) did not differ between ballet dancers or track and field athletes with and without stress fracture. ^{[0250] [0260] [0780]}

Anthropometry and soft tissue composition

Anthropometric characteristics, such as height and weight, and soft tissue composition, such as lean mass and fat mass, theoretically could affect stress fracture risk directly by influencing the forces applied to bones^[98] or indirectly via effects on bone density ^{[0990] [1000]} and menstrual function.^[83]

Unlike the military, in which anthropometric characteristics appear to be related to stress fractures incidence,^[40] no study in athletes has reported a difference in height, weight, body mass index, or fat mass between those with and without stress fractures. ^{[0200] [0210] [0250] [0270] [0750] [0770] [0780] [0850]} Failure to find a relationship in athletes may be due to the relative homogeneity in these characteristics, unlike the military, in which a range of somatotypes would be expected. Another explanation is that the relationship may be nonlinear.

Muscles could play a dual role in stress fracture development. Some investigators consider that muscles act dynamically to cause stress fractures by increasing bone strain at sites of muscle attachment.^{[1010] [1020]} Greater muscle mass with greater ability to generate force would be associated with an increased risk for stress fracture. Others feel that, because muscles act to attenuate and dissipate forces applied to bone,^[103] muscle fatigue or muscle weakness would predispose to stress fracture by causing an increase and redistribution of stress to bone. ^{[0620] [1040]} In the military, leg power was not associated with stress fracture occurrence, although the testing method was relatively crude and nonspecific.^[90] However, recruits with a larger calf muscle circumference developed significantly fewer stress fractures.^[91] This finding also was evident in female athletes, in whom every 1cm decrease in calf girth was associated with a fourfold greater risk of stress fracture^[78] ( Fig. 3-2 ). Using a biomechanical model, Scott and Winter^[105] calculated that, during running, the tibia is subjected to a large forward bending moment as a result of ground reaction force. The calf muscles oppose this large bending moment by applying a backward moment as they contract to control the rotation of the tibia and the lowering of the foot to the ground. The total effect is a smaller bending moment. Extrapolating from this, a stress fracture could result if the calf muscles are unable to produce adequate force to counteract the loading at ground contact and decrease excessive bone strain. The findings of a smaller calf girth in those with stress fractures tend to support the hypothesis that muscles act to protect against rather than cause stress fractures.

Figure 3-2 Plot of the probability of stress fracture at different ages of menarche for different corrected calf girths in female athletes. The plot for small corrected calf girth was calculated using the minimal value measured in the cohort; the average girth was calculated using the mean value; and the large girth was calculated using the maximal value. From Bennell KL, et al: Am J Sports Med 24:814, 1996.

However, there have been no studies comparing muscle mass or muscle strength, particularly peak force production and tendency to fatigue, in athletes with and without stress fractures. Grimston et al.^[106]found that, during the latter stages of a 45-minute run, females with a past history of stress fracture recorded increased ground reaction forces, whereas ground reaction forces did not vary during the run in the control group. The authors surmised that this may indicate differences in fatigue adaptation and muscle activity.

Training

Repetitive mechanical loading arising from athletic training contributes to stress fracture development. However, the contribution of each training component (volume, intensity, frequency, surface, and footwear) to the risk of stress fracture has not been elucidated. Training also may influence bone indirectly through changes in levels of circulating hormones, through effects on soft tissue composition, and through associations with menstrual disturbances.

Large military studies have shown that various training modifications, such as inclusion of rest periods, ^{[0340] [1070]} elimination of running and marching on concrete, ^{[0330] [1080]} use of running shoes rather than combat boots, ^{[0320] [1080]} and reduction of high-impact activity ^{[0320] [0340] [0370] [0380] [1080]} can decrease the incidence of stress fractures in recruits.

In contrast, there is little controlled research in athletes. Most research consists of anecdotal observations or case series in which training parameters are examined only in those athletes with stress fractures. Surveys have reported that up to 86% of athletes can identify some change in their training before the onset of the stress fracture. ^{[0220] [0290] [0570]} Other researchers have blamed training “errors” in a varying proportion of cases but do not adequately define these errors. ^{[0300] [0550] [0600] [1090]} Brunet et al.^[21] surveyed 1505 runners and found that increasing mileage correlated with an increase in stress fractures in women but not in men. An explanation for the apparent gender difference is unclear. Australian track athletes with a past history of stress fracture tended to report more weekly hours of training and running and greater weekly distances in the 5 years preceding the study, compared with those who had never sustained a stress fracture.^[22] In a study of ballet dancers, a dancer who trained for more than 5 hours per day had an estimated risk for stress fracture that was 16 times greater than a dancer who trained for fewer than 5 hours per day.^[27] This study supports a role for training volume as a risk factor for stress fracture, but that factor may be related to increased exposure to injury.

Training surface has long been considered to contribute to stress fracture development.^[5] Anatomic and biomechanical problems can be accentuated by cambered or uneven surfaces, whereas ground reaction forces are increased by less compliant surfaces. ^{[1100] [1110]} In a study of female runners, Zernicke et al.^[93] claimed that those who sustained stress fractures tended to train on harder surfaces but provided no further details. Other researchers also have implicated training surface or change in surface as a risk factor but do not provide substantial evidence in support. ^{[0290] [0570]}

Older or worn running shoes have been related to an increase in stress fractures,^[36] possibly as a result of decreased shock absorption.^[112] However, the use of a shock-absorbing viscoelastic insole made no difference to the incidence of tibial stress fractures in rabbits^[113] or to the overall incidence of stress fractures in military recruits. ^{[0360] [0440] [1140]} It is not clear why Milgrom et al.^[41] found a significant insole effect limited to femoral stress fractures only. Another prospective study showed that a semirigid orthotic device significantly reduced the incidence of femoral stress fractures in recruits with high-arched feet and the incidence of metatarsal fractures in recruits with low-arched feet.^[115] The incidence of tibial stress fractures was not affected by the use of this orthotic device. Because the device had a hindfoot post at 3 degrees varus, altering the biomechanics of the foot, it is difficult to know whether the results of the study can be attributed to this feature or to the shock-absorption capability.

In track and field, clinical observation suggests that the use of running spikes may influence the likelihood of stress fracture. However, little research has focused on the kinetic and kinematic effects of this form of footwear or on the relationship of spikes to stress fracture.

Biomechanics

Biomechanical features may predispose to stress fractures by creating areas of stress concentration in bone or by promoting muscle fatigue. Although various biomechanical features have been examined in military recruits, there are few data pertaining to athletes. Failure to report measurement reliability or to analyze data appropriately makes results difficult to interpret.

High arches (pes cavus) may be associated with an increased risk for stress fracture, particularly at femoral and tibial sites in male military recruits. ^{[1150] [1160] [1170]} In a prospective study, the overall incidence of stress fracture in the low-arched group was 10%, as opposed to 40% in the high-arched group.^[116] A similar trend was noted for tibial and femoral stress fractures. However, assessment of foot type was based on observation in a nonfunctional position, and recruits with extreme pes planus were excluded. Nevertheless, these findings were supported by a study using a contact pressure display method to provide foot-ground pressure patterns and derived stress intensity parameters.^[117] Although there may be a relationship between foot type and stress fracture, this may vary depending on the site of stress fracture. Using radiographs to assess foot type, femoral and tibial stress fractures were more prevalent in the presence of higher arches, whereas the incidence of metatarsal fractures was higher with lower arches.^[115] The authors proposed that, because a low-arched foot is more flexible, it reduces the forces transmitted proximally to the tibia and femur but concentrates the forces in the foot.

Limited observations in athletes tend to differ from military findings. Pes planus (pronated) was the most common foot type in athletes who presented to sports clinics with stress fractures. ^{[0550] [0570]}However, the incidence of pes planus in noninjured athletes was not assessed. In another series of stress fractures, pes planus was more common in tibial and tarsal bone stress fractures and least common in metatarsal stress fractures.^[59] This implies a possible heterogenous effect of biomechanical features on stress fracture risk, depending on the anatomic location of the injured region.

A leg-length discrepancy is another feature that has been postulated as a potential risk factor because of resulting skeletal realignment and asymmetries in loading, bone torsion, and muscle contraction.^[118]Using a radiologic method to assess leg length, Friberg^[119] found that, in 130 cases of stress fracture in military recruits, the longer leg was associated with 73% of tibial, metatarsal, and femoral fractures, whereas 60% of fibular fractures were found in the shorter leg. In a prospective analysis, he observed a positive correlation between the degree of leg-length inequality and the incidence of stress fractures. However, no statistical analyses were performed to assess the significance of these results. A leg-length discrepancy also has been found to be associated with a significant increase in the incidence of stress fractures in athletes. ^{[0210] [0780]} Seventy percent of women who developed stress fractures displayed a leg-length difference of more than 0.5cm, compared with 36% of women without stress fractures.^[78]

Large prospective studies in the Israeli military have included an orthopaedic examination in addition to assessment of other risk factors for stress fractures. ^{[0420] [0900] [1200]} Of the biomechanical variables, only range of hip external rotation was found to correlate with the incidence of stress fracture. Soldiers in whom hip external rotation was greater than 65 degrees were at a higher risk for tibial and total stress fractures than those with a range less than 65 degrees. The risk for tibial stress fracture increased 2% for every 1 degree increase in hip external rotation range.^[42] However, a large prospective study in American recruits failed to confirm these findings.^[121] Greater forefoot varus and restricted ankle joint dorsiflexion also have been associated with an increased risk of stress fracture in military recruits.^[122] The only prospective study to examine a number of clinical biomechanical measurements in athletes, including range of hip rotation and ankle dorsiflexion, calf and hamstring flexibility, lower limb alignment, and static foot posture, did not find any to be useful predictors of stress fracture occurrence.^[78]

Most studies have included static biomechanical measures, which may not adequately reflect the dynamic situation.^[123] Preliminary studies analyzing running gait and using a force platform suggest a possible role for external loading kinetics and load magnitude in the development of a stress fracture. ^{[0770] [1060]} This is an important area for future research.

Diagnosis

In the assessment of a patient presenting with a possible diagnosis of stress fracture, there are three questions that need to be answered:

	1	Is the pain bony in origin?
	2	If so, which bone is involved?
	3	At what stage in the continuum of bone stress is this injury?

To obtain an answer to these three questions, a thorough history, precise examination, and appropriate use of imaging techniques are used. In many cases, the diagnosis of stress fracture will be relatively simple. In others, especially when the affected bone may lie deeply (e.g., femur) or the pattern of pain may be nonspecific (e.g., navicular), the diagnosis can present a challenge for the clinician.

History

The history of the patient with a stress fracture typically is one of insidious onset of activity-related pain. Usually the pain will be described initially as a mild ache occurring after a specific amount of exercise. If the patient continues to exercise, the pain may well become more severe or occur at an earlier stage of exercise. The pain eventually may increase to the point that it limits the quality or quantity of the exercise performed or, occasionally, forces cessation of all activity. In the early stages, pain usually will cease soon after exercise is terminated. However, with continued exercise and increased severity of symptoms, the pain may persist after exercise cessation. Night pain occasionally may occur.

In addition to obtaining a history of the patient's pain and its relation to exercise, it is important to determine the presence of predisposing factors. Therefore a training or activity history is essential. In particular, note should be taken of recent changes in activity level, such as increased quantity of training, increased intensity of training, and changes in surface, equipment (especially shoes), and technique. It may be necessary to obtain information from the patient's coach or trainer. A full dietary history should be taken; particular attention should be paid to the possible presence of eating disorders. In females a menstrual history should be taken, including age of menarche and subsequent menstrual status.

A history of previous similar injury or any other musculoskeletal injury should be obtained. It is essential to obtain a brief history of the patient's general health, medications, and personal habits to ensure that there are no factors that may influence bone health. It also is important to obtain from the history an understanding of the patient's work and sporting commitments. In particular, it is important to know at what level of sport and how serious the patient is about his or her sport, as well what significant sporting commitments are ahead in the short term and medium term.

Physical examination

On physical examination the most obvious feature is localized bony tenderness. Obviously this is easier to determine in bones that are relatively superficial and may be absent in stress fractures of the shaft or neck of femur. It is important to be precise in the palpation of the affected areas, particularly in regions such as the foot, in which there are a number of bones and joints in a relatively small area that may be affected. Occasionally redness and swelling may be present at the site of the stress fracture. There also may be palpable periosteal thickening, especially in a long-standing fracture. Percussion of long bones may result in the production of pain at a point distant from the percussion.

Joint range of motion usually is unaffected except in situations in which the stress fracture is close to the joint surface, such as a stress fracture of the neck of femur.

Some authors have suggested that the presence of pain when therapeutic ultrasound is applied over the area of the stress fracture is of potential use in the detection of stress fractures. ^{[1240] [1250] [1260]}Similarly it is reported that application of a vibrating tuning fork to the affected bone and subsequent increase in pain is indicative of a stress fracture. Our own experience suggests that these methods are not particularly helpful.

The physical examination also must take into account the potential predisposing factors; and, in all stress fractures involving the lower limb, a full biomechanical examination must be performed. Any evidence of leg-length discrepancy, malalignment (especially excessive subtalar pronation), muscle imbalance, weakness, or lack of flexibility should be noted.

Imaging

Imaging plays an important role in supplementing clinical examination to determine the answers to the three questions mentioned at the start of this section on diagnosis. In many cases a clinical diagnosis of stress fracture is sufficient. The classic history of exercise-associated bone pain and typical examination findings of localized bony tenderness have a high correlation with the diagnosis of stress fracture. However, if the diagnosis is uncertain, or in the case of the serious or elite athlete who wishes to continue training if at all possible and requires more specific knowledge of his or her condition, there are various imaging techniques available to the clinician.

Radiography

Radiography has poor sensitivity but high specificity in the diagnosis of stress fractures. The classic radiographic abnormalities seen in a stress fracture are new periosteal bone formation, a visible area of sclerosis, the presence of callus, or a visible fracture line. The diagnosis of stress fracture can be confirmed if any of these radiographic signs are present.

Unfortunately, in the majority of stress fractures there is no obvious radiographic abnormality. The abnormalities on radiography are unlikely to be seen unless symptoms have been present for at least 2 to 3 weeks. In certain cases they may not become evident for up to 3 months, and in a percentage of cases never become abnormal.

Isotopic bone scan (scintigraphy)

If plain radiography demonstrates the presence of a stress fracture, then there seldom is any need to perform further investigations. However, in cases in which there is a high index of suspicion of stress fracture and a negative bone radiograph, the triple-phase bone scan is the next line of investigation. The bone scan is highly sensitive but has low specificity. Prather et al.^[127] stated that the bone scan had a true-positive rate of 100%, and false-negative scans are relatively rare. ^{[1280] [1290]}

Technetium-99 methylene diphosphonate usually is used as the radionuclide substance. Other possibilities include gallium citrate (Ga 67) and indium 111-labeled leukocytes.^[130] The advantage of technetium-99 methylene diphosphonate (MDP) is its short half-life (6 hours), allowing a higher dose to be administered with improved resolution.^[131]

In the first phase of the bone scan, flow images are obtained immediately after the intravenous injection of the tracer. These initial images usually are taken every 2 seconds and correspond roughly to contrast angiography, albeit with much lower spatial and temporal resolution. This first phase of the bone scan evaluates perfusion to bone and soft tissues from the arterial to the venous circulation.

The second phase of the bone scan consists of a static “blood pool” image taken 1 minute after the injection and reflects the degree of hyperemia and capillary permeability of bone and soft tissue. Generally speaking, the more acute and severe the injury, the greater the degree of increased perfusion and blood pool activity.

The third phase of the bone scan is the delayed image taken 3 to 4 hours after injection, when approximately 50% of the tracer has concentrated in the bone matrix through the mechanism of chemisorption to the hydroxyapatite crystals. On the 3-hour delayed image, the uptake of the tracer is proportional to the rate of osteoblastic activity, extraction, and efficiency, as well as to the amount of tracer delivered per unit time or blood flow.^[132] The inclusion of the first and second phases of the bone scan permits the estimation of the age of stress-induced focal bony lesions and the severity of bony injuries and helps to differentiate soft tissue inflammation from bony injury.^[133] As the bony lesion heals, the perfusion returns to normal first, followed by normalization of the blood pool image a few weeks later. Focal increased uptake on the delayed scan resolves last because of ongoing bony remodeling and generally lags well behind the disappearance of pain. As healing continues, the intensity of the uptake diminishes gradually during a 3- to 6-month period following an uncomplicated stress fracture, with a minimal degree of uptake persisting for up to 10 months^[132] or even longer.

Changes on bone scan may be seen as early at 48 to 72 hours after the commencement of symptoms. The radionuclide scan may be positive as early as 7 hours after bone injury.^[134]

The bone scan is virtually 100% sensitive, at least twice as sensitive as x-ray,^[135] and consistently more sensitive that ultrasound,^[136] thermography,^[137] and computerized tomography (CT).^[138] In several studies, only 10% to 25% of bone–scan-positive stress fractures had radiographic evidence of stress fracture. ^{[1390] [1400] [1410] [1420]}

In the appropriate clinical setting, the scintigraphic diagnosis of a stress fracture is defined as focal increased uptake in the third phase of the bone scan. However, bone scintigraphy lacks specificity because other nontraumatic lesions, such as tumor (especially osteoid osteoma), osteomyelitis, bony infarct, and bony dysplasias also can produce localized increased uptake. Therefore it is vitally important to correlate the bone scan appearance with the clinical features.

The radionuclide scan will detect evolving stress fractures at the stage of accelerated remodeling. At that stage, which may be asymptomatic, the uptake usually is of mild intensity, progressing to more intense and better defined uptake as microfractures develop. ^{[0130] [1430]}

In stress fractures all three phases of the triple-phase bone scan are positive. ^{[1330] [1440]} Other bony abnormalities, such as periostitis (shin splints), are positive only on delayed images, ^{[1330] [1450]} whereas certain other overuse soft-tissue injuries would be positive only in the angiogram and blood pool phase, thus allowing one to differentiate between bony and soft-tissue pathology. The characteristic bone scan appearance of a stress fracture is of a sharply marginated or fusiform area of increased uptake involving one cortex or occasionally extending the width of the bone^[13] ( Fig. 3-3 ).

Figure 3-3 Typical bone scan appearance of stress fracture of tibia.

Increased radionuclide uptake often is found in asymptomatic sites. ^{[1080] [1460] [1470]} Originally the presence of increased tracer uptake at nonpainful sites in athletes was interpreted as unrecognized stress fractures. ^{[0130] [1480] [1490]} Other authors postulated that this may be nonspecific stress changes related to bone remodeling,^[133] a false-positive finding,^[150] and an uncertain finding.^[151] Rosen et al.^[148]found asymptomatic uptake in 46% of cases, with focal uptake more common than diffuse uptake.

Matheson et al. in Vancouver, BC,^[152] proposed the concept of bone strain. They noted that the radionuclide bone scan, because of its sensitivity, was able to demonstrate the adaptive changes in bone at any point in the continuum from early remodeling to stress fracture. The term “bone strain” was coined to reflect the true dynamic response of bone to stress and to allow the interpretation of bone changes along the continuum to be correlated with the wide range of presentations seen in clinical practice. They stated that excessive loading from overuse, abnormal biomechanics, reduced shock absorption, or altered gait produced a mechanical stress that is translated into bone remodeling via piezoelectric stimuli. The relative contribution of these factors, as well as the athlete's activity pattern after the onset of remodeling, determines the extent of bone strain seen clinically. Pain during activity may indicate small areas of remodeling, which have low-intensity uptake on bone scan and negative x-rays. On the other hand, pain that persists after exercise and during rest may indicate more extensive remodeling, with intense uptake on scan and possibly abnormal radiographs.

This concept of a continuum of bone strain's existing both clinically and scintigraphically is now widely accepted. It is clear now that bone stress can appear as an area of increased uptake on isotope bone scan before any symptoms occur. It is not clear what percentage of these cases progress to symptomatic bone stress and ultimately to stress fracture if exercise is continued. It also is not clear what treatment is appropriate in these cases of asymptomatic bone stress. Many athletes and dancers in hard training show numerous areas of bone stress on an isotope bone scan. These are indicators of active remodeling and are not necessarily bone at risk for the development of stress fracture.

Attempts have been made to classify the bony continuum into “bone strain” or “asymptomatic stress reaction” and stress fracture. A summary of these features may be seen in Table 3-8 . A scheme for grading bone scan appearance on the basis of severity has been proposed by Zwas et al.^[141] This is shown in Table 3-9 .

Table 3-8 -- Continuum of bony changes with overuse

Clinical features	Bone strain	Stress reaction	Stress fracture
Local pain	Nil
Local tenderness	Nil
X-ray appearance	Normal	Normal	Abnormal (periosteal reaction or cortical defect in cortical bone, sclerosis in trabecular bone)
Radioisotopic bone scan appearance	Increased uptake (mild)	Increased uptake (moderate)	Increased uptake (strongly)
CT scan appearance	Normal	Normal	Features of stress fracture (as for x-ray)
MR appearance	May show increased high signal	Increased high signal	Increased high signal ± cortical defect

From Brukner PD, Khan KM: Clinical sports medicine, rev ed 2, Sydney, 2002, McGraw-Hill Book Company.

CT, Computed tomography; MR, magnetic resonance.

Table 3-9 -- Grading of tibial or long bone stress fractures by bone scan or magnetic resonance imaging (MRI) appearance

Grade	Bone scan appearance	MRI appearance
Grade I	Small, ill-defined cortical area of mildly increased activity	Periosteal edema: mild to moderate on T2-weighted images. Marrow edema: normal on T1- and T2-weighted images.
Grade II	Better defined cortical area of moderately increased activity	Periosteal edema: moderate to severe on T2-weighted images. Marrow edema on T2-weighted images.
Grade III	Wide, fusiform cortical-medullary area of highly increased activity	Periosteal edema: moderate to severe on T2-weighted images. Marrow edema on T1- and T2-weighted images.
Grade IV	Transcortical area of increased activity	Periosteal edema: moderate to severe on T2-weighted images. Marrow edema on T1- and T2-weighted images. Fracture line clearly visible.

Computerized tomography

CT may be useful in differentiating those conditions with increased uptake on bone scan that may mimic stress fracture. These include osteoid osteoma, osteomyelitis with a Brodie's abscess, and other malignancies.

CT scans also are particularly valuable in imaging fractures in which this may be important in treatment. CT scanning of the navicular bone is particularly helpful. ^{[1530] [1540]} CT scanning also may be valuable in detecting fracture lines as evidence of stress fracture in long bones (e.g., metatarsal and tibia) in which plain radiography is normal and isotope bone scan shows increased uptake (see Fig. 3-3 ). CT scanning will enable the clinician to differentiate between a stress fracture, which will be visible on CT scan, and a stress reaction ( Fig. 3-4 ). Particularly in the elite athlete, this may considerably affect his or her rehabilitation program and forthcoming competition program.

Figure 3-4 Computed tomography (CT) appearance of stress fracture of navicular.

Magnetic resonance imaging

Magnetic resonance imaging (MRI), although not imaging cortical bone as well as CT scan, has certain advantages in the imaging of stress fractures. Specific MRI characteristics of stress fracture include new bone formation and fracture lines appearing as very low signal medullary bands that are contiguous with the cortex; surrounding marrow hemorrhage and edema seen as low signal intensity on T1-W images ( Fig. 3-5 ) and as high-signal on T2-W and short T1 inversion and recovery (STIR) images; and periosteal edema and hemorrhage appearing as high signal intensity on T2-W and STIR images.^[155]These changes are seen best if the MRI is performed within 3 weeks of symptoms.^[156] MRI is thought to be more sensitive than conventional radiography. MRI visualizes marrow hemorrhage and edema well, a characteristically difficult finding with CT. Although CT scan visualizes bone detail, another advantage of MR imaging is in distinguishing stress fractures from a suspected bone tumor or infectious process.^[155]

Figure 3-5 Magnetic resonance imaging (MRI) appearance of stress fracture.

Stafford et al.^[157] reported findings of stress fractures in MRI. Zones of decreased signal of T1 images are seen in the affected region, whereas T2-weighted images show increased signal. A low signal line may be seen running through the medullary cavity, presumably corresponding to the zone of localized fracture. Further advances in marrow imaging have occurred, such as STIR sequences that help to better identify such marrow pathology.

The appearance of a stress fracture on MRI is characteristic with intraosseous bands of very low signal intensity that are continuous with the cortex and surrounding areas of decreased signal intensity of the marrow space on T1-weighted images. T2 images show prominent intramedullary areas of high signal intensity and juxtacortical and/or subperiosteal areas of high signal intensity. ^{[1560] [1580]}

Fredericson et al.^[159] proposed a grading scheme for MRI appearances of stress fractures using STIR images. The authors felt that their grades I to IV were equivalent to the bone scan grading described by Zwas et al.,^[141] mentioned in the previous section. In this grading system, grade I indicated mild to moderate periosteal edema on T2-weighted images, only with no focal bone marrow abnormality. Grade II showed more severe periosteal edema, as well as bone marrow edema on T2-weighted images only. Grade III showed moderate to severe edema of both the periosteum and marrow on both T1- and T2-weighted images. Grade IV demonstrated a low signal fracture line on all sequences with changes of severe marrow edema on both T1- and T2-weighted images. Grade IV also may show severe periosteal and moderate muscle edema. The comparison of grading of stress fractures between bone scan^[141] and MRI^[159] is shown in Table 3-9 .

Steinbronn et al.^[158] advocated the use of MRI in patients who have negative radiographs, a positive bone scan, and a diagnosis still not firmly established.

Differential Diagnosis

The differential diagnosis of stress fracture can be divided into nonbony causes or bony causes. Nonbony causes, in particular, relate to muscle or tendon injury; either muscle strain, hematoma or delayed-onset muscle soreness, or tendon inflammation or degenerative change.

Bony pathologies that can mimic stress fracture include tumor and infection. Osteoid osteoma commonly is mistaken for a stress fracture because it presents with pain and a discrete focal area of increased uptake on isotope bone scan. Two distinguishing features of osteoid osteoma are the presence of night pain and the relief of pain with the use of aspirin. In addition, a CT scan or MRI can clearly distinguish the nidus of an osteoid osteoma from the cortical abnormality of a stress fracture.

Treatment

The basis of treatment of stress fractures involves rest from the aggravating activity, a concept known as “relative rest.” The amount of time from a diagnosis of a stress fracture to full return to sport depends on a number of factors, including the site of the fracture, the length of the symptoms, and the stage in the spectrum of bone strain. Most stress fractures with a relatively brief history of symptoms will heal in a straightforward manner, and return to sport should occur within 6 to 8 weeks. However, there is a group of stress fractures that require additional treatment to relative rest, and these are considered later.

The primary aim of initial management of stress fracture is pain relief. This may involve the use of mild analgesics or nonsteroidal anti-inflammatory drugs (NSAIDs). In some cases in which activities of daily living are painful, it may be necessary for the patient with a stress fracture to be nonweight bearing or partial weight bearing on crutches for a period of up to 7 to 10 days. In the majority of cases this is not necessary, and mere avoidance of the aggravating activity will be sufficient.

The rate of resumption of activity should be modified according to symptoms and physical findings. At all time, activity should be pain free; and, if any bony pain occurs, then activity should be ceased for 1 to 2 days and then resumed at a lower level. The patient should be clinically reassessed at regular intervals, in particular looking for bony tenderness.

When activities of daily living are pain free and there is no focal tenderness, then resumption of the aggravating activity can occur on a graduated basis. For lower limb stress fractures in which running is the aggravating activity, we recommend a program that involves initial brisk walking increased by 5 to 10 minutes per day, up to a length of 45 minutes. Once this is achieved without pain, we then recommend introducing initially a period of 5 minutes of slow jogging within the 45-minute walk. Assuming that this increase in activity does not reproduce the patient's symptoms, then the amount of jogging can be increased on a daily basis until the whole 45 minutes is completed at jogging pace. Once this is achieved, then strides can be introduced, initially half-pace and then gradually increasing to full-pace striding. Once full sprinting is pain free, then gradual functional activities, such as hopping, skipping and jumping, twisting, and turning can be introduced gradually. It is important that this process is a graduated one, and it is important to err on the side of caution rather than try to be too hasty.

A typical program for an uncomplicated lower limb stress fracture resuming activity after a period of initial rest and activities of daily living is shown in Figure 3-6 .

Figure 3-6 Activity program following uncomplicated lower limb stress fracture following period of rest and activity of daily living (ADL).

Progress should be monitored clinically by the presence or absence of symptoms and local signs. It usually is not necessary to monitor progress by radiography, scintigraphy, CT, or MRI. Radiologic healing often lags behind clinical healing.

Fitness maintenance

It is important that the athlete with a stress fracture be able to maintain strength and cardiovascular fitness while undergoing the appropriate rehabilitation program. It should be emphasized to the athlete that the rehabilitation program is not designed to maintain or improve the patient's fitness but rather to allow the damaged bone time to heal and gradually develop or regain full strength. Fitness should be maintained in other ways.

The most common ways are biking, swimming, water running, and using upper body weights. These workouts should mimic the athlete's normal training program as much as possible in both duration and intensity. Water running is particularly attractive to runners for this reason. Water running involves the use of a buoyancy vest as a flotation device.

Stretching should be performed to maintain flexibility during the rehabilitation process. Muscle strengthening also is an important component of the rehabilitation phase.

In addition to maintaining these parameters of physiologic fitness, it is possible in most cases for the athlete to maintain specific sports skills. In ball sports these can involve activities either seated or standing still. This active rest approach also greatly assists the athlete psychologically.

Modified risk factors

As with any overuse injury, it is not sufficient merely to treat the stress fracture itself. An essential component of the management of an athlete with an overuse injury involves identification of the factors that have contributed to the injury and, when possible, correction or modification of some of these factors to reduce the risk of the injury's recurring. The fact that stress fractures have a high rate of recurrence is an indication that this part of the management program often is neglected.

The risk factors for the development of stress fractures have been discussed at length in a previous section. Although not yet supported by rigorous scientific evidence, one possible precipitating factor is training errors. Therefore it is important to identify these and to discuss them with the athlete and his or her coach when appropriate. Another important contributing factor may be inadequate equipment, especially running shoes. These shoes may be inappropriate for the particular foot type of the athlete, may have general inadequate support, or may be worn out (see Chapter 26 ).

Biomechanical abnormalities also are thought to be an important factor contributing to the development of overuse injuries in general and stress fractures in particular. Both excessively supinated and excessively pronated feet can be contributing factors in the development of stress fractures. Excessively supinated feet generally give poor absorption and require footwear that gives good absorption. Excessively pronated feet will require appropriate footwear for their foot type and also may require the use of custom-made orthotics (see Chapter 27 ).

It is important that these risk factors are corrected by the time the athlete resumes training. When training resumes, it is important to allow adequate recovery time after hard sessions or hard weeks of training. In view of the history of stress fracture, it is advisable that some form of cross training, for example, swimming and cycling for a runner, be introduced to reduce the stress on the previously injured area and reduce the likelihood of a recurrence.

Stress fractures requiring specific treatment

Although the majority of stress fractures of the foot and ankle will heal without complications in a relatively short time frame, there are a number of stress fractures that require specific additional treatment. These are as follows:

	•	Medial malleolus
	•	Navicular
	•	Base of second metatarsal
	•	Proximal fifth metatarsal
	•	Sesamoids

These “difficult stress” fractures are covered in Chapter 4 .

Pearl

Stress fractures of the second, third, or fourth metatarsals swell and the pain is dorsal, whereas neuromas of the forefoot do not swell and the pain typically is plantar. Most stress fractures of the foot and ankle heal with relative rest. Navicular, fifth metatarsal Jones, base of second, medial malleolus, sesamoid, and lateral process of the talus require more involved care for healing. Stress fractures are fatigue fractures and result from repeated overuse, and they are common in the athlete. For stress fractures, always investigate for eating abnormalities, and in females ask about their menstrual history. Bone scans and MRI are helpful to diagnose a stress fracture early in its presentation (<3 weeks of symptoms).

Conclusion

Stress fractures are a common injury, particularly in runners and in sports that involve a large amount of running. Various risk factors for the development of stress fractures have been proposed; however, the relative importance of these is still uncertain. The diagnosis is primarily on clinical grounds, but imaging can be used to confirm the diagnosis or to assess the extent of the injury. The treatment is straightforward in most cases, but there is a small group of stress fractures that require more specific management.

References

1. Grimston SK, Zernicke RF: Exercise-related stress responses in bone. J Appl Biomech1993; 9:2.
2. Martin AD, Bailey DA: Skeletal integrity in amenorrhoeic athletes. Aust J Sci Med Sport1987; 2:3.
3. Stechow AW: Fussoedem und roentgenstrahlen. Dtsch Mil-Aerztl Zeitg1897; 26:465.
4. Deutschlander C: Ueber eine eigenartige mittelfuszerkrankung. Zentralbl f Chir1921; 48:1422.
5. Devas MB, Sweetnam R: Stress fractures of the fibula: a review of 50 cases in athletes. J Bone Joint Surg1956; 38B:818.
6. Dodd H: Pied force or march foot. Br J Surg1933; 21:131.
7. Roberts SM, Vogt EC: Pseudofracture of the tibia. J Bone Joint Surg1939; 21:891.
8. Weaver JB, Francisco CB: Pseudofractures. A manifestation of non-suppurative osteomyelitis. J Bone Joint Surg1940; 22:610.
9. Burrows HJ: Fatigue fractures of the fibula. J Bone Joint Surg1948; 30B:266.
10. Hullinger CW: Insufficiency fracture of the calcaneus. Similar to march fracture of the metatarsal. J Bone Joint Surg1944; 26:751.
11. Jansen M: March fractures. J Bone Joint Surg1926; 8:262.
12. Sloane D, Sloane MF: March foot. Am J Surg1936; 31:167.
13. Roub LW, et al: Bone stress: a radionuclide imaging perspective. Radiology1979; 132:431.
14. Li G, et al: Radiographic and histologic analyses of stress fracture in rabbit tibias. Am J Sports Med1985; 13:285.
15. Burr DB, et al: Experimental stress fractures of the tibia. J Bone Joint Surg1990; 72:370.
16. Martin RB, Burr DB: A hypothetical mechanism for the stimulation of osteonal remodelling by fatigue damage. J Biomech1982; 15:137.
17. Mori S, Burr DB: Increased intracortical remodeling following fatigue damage. Bone1993; 14:103.
18. Schaffler MB, Radin EL, Burr DB: Mechanical and morphological effects of strain rate on fatigue of compact bone. Bone1989; 10:207.
19. Schaffler MB, Radin EL, Burr DB: Long-term fatigue behavior of compact bone at low strain magnitude and rate. Bone1990; 11:321.
20. Barrow GW, Saha S: Menstrual irregularity and stress fractures in collegiate female distance runners. Am J Sports Med1988; 16:209.
21. Brunet ME, et al: A survey of running injuries in 1505 competitive and recreational runners. J Sports Med Phys Fitness1990; 30:307.
22. Cameron KR, et al: Stress fractures in Australian competitive runners, 1992.
23. Bennell KL, et al: Risk factors for stress fractures in female track-and-field athletes, a retrospective analysis. Clin J Sport Med1995; 5:229.
24. Bennell KL, et al: The incidence and distribution of stress fractures in competitive track and field athletes. Am J Sports Med1996; 26:211.
25. Warren MP, et al: Scoliosis and fractures in young ballet dancers: relation to delayed menarche and secondary amenorrhea. N Engl J Med1986; 314:1348.
26. Frusztajer NT, et al: Nutrition and the incidence of stress fractures in ballet dancers. Am J Clin Nutr1990; 51:779.
27. Kadel NJ, Teitz CC, Kronmal RA: Stress fractures in ballet dancers. Am J Sports Med1992; 20:445.
28. Johnson AW, Weiss CB, Wheeler DL: Stress fractures of the femoral shaft in athletes—more common than expected. A new clinical test. Am J Sports Med1994; 22:248.
29. Goldberg B, Pecora C: Stress fractures. A risk of increased training in freshmen. Phys Sportsmed1994; 22:68.
30. Pecina M, Bojanic I, Dubravcic S: Stress fractures in figure skaters. Am J Sports Med1990; 18:277.
31. Dixon M, Fricker P: Injuries to elite gymnasts over 10yr. Med Sci Sport Exerc1993; 25:1322.
32. Protzman RR, Griffis CG: Stress fractures in men and women undergoing military training. J Bone Joint Surg1977; 59-A:825.
33. Reinker KA, Ozburne S: A comparison of male and female orthopaedic pathology in basic training. Milit Med1979; 144(8):532-536.
34. Scully TJ, Besterman G: Stress fracture—a preventable training injury. Milit Med1982; 147:285.
35. Brudvig TJS, Gudger TD, Oberinger L: Stress fractures in 295 trainees: a one-year study of incidence as related to age, sex, and race. Milit Med1983; 148:666.
36. Gardner LI, et al: Prevention of lower extremity stress fractures: a controlled trial of a shock absorbent insole. Am J Public Health1988; 78:1563.
37. Pester S, Smith PC: Stress fractures in the lower extremities of soldiers in basic training. Orthop Rev1992; 21:297.
38. Taimela S, et al: Risk factors for stress fractures during physical training programs. Clin J Sport Med1992; 2:105.
39. Jones BH, et al: Intrinsic risk factors for exercise-related injuries among male and female army trainees. Am J Sports Med1993; 21:705.
40. Beck TJ, et al: Dual-energy x-ray absorptiomety derived structural geometry for stress fracture prediction in male U.S. Marine Corps recruits. J Bone Miner Res1996; 11:645.
41. Milgrom C, et al: Stress fractures in military recruits. A prospective study showing an unusually high incidence. J Bone Joint Surg1985; 67-B:732.
42. Milgrom C, et al: Youth is a risk factor for stress fracture. A study of 783 infantry recruits. J Bone Joint Surg1994; 76-B:20.
43. Jones H, et al: Exercise-induced stress fractures and stress reactions of bone: epidemiology, etiology, and classification. Exerc Sports Sci Rev1989; 17:379.
44. Milgrom C, et al: The long-term followup of soldiers with stress fractures. Am J Sports Med1985; 13:398.
45. Carter DR, Hayes WC: Fatigue life of compact bone-1. Effects of stress amplitude, temperature and density. J Biomech1976; 9:27.
46. Keller TS, et al: Fatigue of immature baboon cortical bone. J Biomech1985; 18:297.
47. Matheson GO, et al: Musculoskeletal injuries associated with physical activity in older adults. Med Sci Sport Exerc1989; 21:379.
48. Cohn SH, et al: Comparative skeletal mass and radial bone mineral content in black and white women. Metabolism1977; 26:171.
49. Giladi M, et al: The low arch, a protective factor in stress fractures. A prospective study of 295 military recruits. Orthop Rev1985; 14:709.
50. Brubaker CE, James SL: Injuries to runners. J Sports Med1974; 2:189.
51. James SL, Bates BT, Osternig LR: Injuries to runners. Am J Sports Med1978; 6:40.
52. Orava S: Stress fractures. Br J Sports Med1980; 14:40.
53. Pagliano J, Jackson D: The ultimate study of running injuries. Runners World1980;42.November:
54. Witman PA, Melvin M, Nicholas JA: Common problems seen in a metropolitan sports injury clinic. Phys Sportsmed1981; 9:105.
55. Taunton JE, Clement DB, Webber D: Lower extremity stress fractures in athletes. Phys Sportsmed1981; 9:77.
56. Clement DB, et al: A survey of overuse running injuries. Phys Sportsmed1981; 9:47.
57. Sullivan D, et al: Stress fractures in 51 runners. Clin Orthop Rel Res1984; 187:188.
58. Hulkko A, Orava S: Stress fractures in athletes. Int J Sports Med1987; 8:221.
59. Matheson GO, et al: Stress fractures in athletes. A study of 320 cases. Am J Sports Med1987; 15:46.
60. Courtenay BG, Bowers DM: Stress fractures: clinical features and investigation. Med J Aust1990; 153:155.
61. Ha KI, et al: A clinical study of stress fractures in sports activities. Orthopaedics1991; 14:1089.
62. Benazzo F, et al: Stress fractures in track and field athletes. J Sports Traumatol Rel Res1992; 14:51.
63. Brukner P, et al: Stress fractures: a series of 180 cases. Clin J Sport Med1996; 6:85.
64. Brukner P, Khan K: Clinical sports medicine, Sydney, McGraw Hill, 1993.
65. Carlson GD, Wertz RF: March fracture, including others than those of the foot. J Bone Joint Surg1944; 43:48.
66. Pocock NA, et al: Genetic determinants of bone mass in adults. J Clin Invest1987; 80:706.
67. Soroko SB, et al: Family history of osteoporosis and bone mineral density at the axial skeleton: the Rancho Bernardo study. J Bone Miner Res1994; 9:761.
68. Seeman E, et al: Reduced bone mass in daughters of women with osteoporosis. N Engl J Med1989; 320:554.
69. Prior JC, et al: Spinal bone loss and ovulatory disturbances. N Engl J Med1990; 323:1221.
70. Singer A, et al: Multiple identical stress fractures in monozygotic twins. J Bone Joint Surg1990; 72-A:444.
71. Myburgh KH, et al: Low bone density is an etiologic factor for stress fractures in athletes. Ann Intern Med1990; 113:754.
72. Snow GR, Anderson C: The effects of continuous progestogen treatment on cortical bone remodelling activity in beagles. Calcif Tiss Int1985; 37:282.
73. Lindberg JS, et al: Exercise-induced amenorrhea and bone density. Ann Intern Med1984; 101:647.
74. Marcus R, et al: Menstrual function and bone mass in elite women distance runners. Ann Intern Med1985; 102:158.
75. Lloyd T, et al: Women athletes with menstrual irregularity have increased musculoskeletal injuries. Med Sci Sport Exerc1986; 18:374.
76. Nelson ME, et al: Elite women runners: association between menstrual status, weight history and stress fractures. Med Sci Sport Exerc1987; 19:S13.
77. Grimston SK, et al: Bone mass, external loads, and stress fractures in female runners. Int J Sport Biomech1991; 7:293.
78. Bennell KL, et al: Risk factors for stress fractures in track and field athletes: a 12 month prospective study. Am J Sports Med1996; 24:810.
79. Clark N, Nelson M, Evans W: Nutrition education for elite female runners. Phys Sports Med1988; 16:124.
80. Grimston SK, et al: Menstrual, calcium, and training history: relationship to bone health in female runners. Clin Sport Med1990; 2:119.
81. Kaiserauer S, et al: Nutritional, physiological, and menstrual status of distance runners. Med Sci Sport Exerc1989; 21:120.
82. Guler F, Hascelik Z: Menstrual dysfunction rate and delayed menarche in top athletes of team games. Sports Med Training Rehabil1993; 4:99.
83. Wolman RL, Harries MG: Menstrual abnormalities in elite athletes. Clin Sport Med1989; 1:95.
84. Warren MP, et al: Lack of bone accretion and amenorrhea: evidence for a relative osteopenia in weight bearing bones. J Clin Endocrinol Metab1991; 72:847.
85. Carbon R, et al: Bone density of elite female athletes with stress fractures. Med J Aust1990; 153:373.
86. Frisch RE, et al: Delayed menarche and amenorrhea of college athletes in relation to age of onset of training. JAMA1981; 246:1559.
87. Moisan J, Meyer F, Gingras S: A nested case-control study of the correlates of early menarche. Am J Epidemiol1990; 132:953.
88. Carter DR, et al: Fatigue behaviour of adult cortical bone: the influence of mean strain and strain range. Acta Orthop Scand1981; 52:481.
89. Pouilles JM, et al: Femoral bone density in young male adults with stress fractures. Bone1989; 10:105.
90. Giladi M, et al: Stress fractures: identifiable risk factors. Am J Sports Med1991; 19:647.
91. Milgrom C, et al: The area moment of inertia of the tibia: a risk factor for stress fractures. J Biomech1989; 22:1243.
92. Giladi M, et al: Stress fractures and tibial bone width. A risk factor. J Bone Joint Surg1987; 69-B:326.
93. Zernicke R, et al: Stress fracture risk assessment among elite collegiate women runners. International Society of Biomechanics XIVth Congress, 1993:1012.
94. Myburgh KH, Grobler N, Noakes TD: Factors associated with shin soreness in athletes. Phys Sportsmed1988; 16:129-134.
95. Grimston SK, et al: The application of historical data for evaluation of osteopenia in female runners: the menstrual index. Clin Sports Med1990; 2:108.
96. Matkovic V, Heaney RP: Calcium balance during human growth: evidence for threshold behaviour. Am J Clin Nutr1992; 55:992.
97. Schwellnus MP, Jordaan G: Does calcium supplementation prevent bone stress injuries? A clinical trial. Int J Sport Nutr1992; 2:165.
98. Frederick EC, Hagy JL: Factors affecting peak vertical ground reaction forces in running. Int J Sport Biomech1986; 2:41.
99. Lindsay R, et al: Bone mass and body composition in normal women. J Bone Miner Res1992; 7:55.
100. Elliot JR, et al: Historical assessment of risk factors in screening for osteopenia in a normal Caucasian population. Austr New Z J Med1993; 23:458.
101. Meyer SA, Saltzman CL, Albright JP: Stress fractures of the foot and leg. Clin Sports Med1993; 12:395.
102. Stanitski CL, McMaster JH, Scranton PE: On the nature of stress fractures. Am J Sports Med1978; 6:391.
103. Voloshin A, Wosk J: An in vivo study of low back pain and shock absorption in the human locomotor system. J Biomech1982; 15:21.
104. Clement DB: Tibial stress syndrome in athletes. J Sports Med1974; 2:81.
105. Scott SH, Winter DA: Internal forces at chronic running injury sites. Med Sci Sport Exerc1990; 22:357.
106. Grimston SK, et al: External loads throughout a 45 minute run in stress fracture and non-stress fracture runners. J Biomech1994; 27:668.
107. Worthen BM, Yanklowitz BAD: The pathophysiology and treatment of stress fractures in military personnel. J Am Podiatr Med Assoc1978; 68:317.
108. Greaney RB, et al: Distribution and natural history of stress fractures in U.S. marine recruits. Radiology1983; 146:339.
109. McBryde AM: Stress fractures in runners. Clin Sports Med1985; 4:737.
110. McMahon TA, Greene PR: The influence of track compliance on running. J Biomech1979; 12:893.
111. Steele JR, Milburn PD: Effect of different synthetic sport surfaces on ground reactions forces at landing in netball. Int J Sport Biomech1988; 4:130.
112. Cook SD, Brinker MR, Poche M: Running shoes. Sports Med1990; 10:1.
113. Milgrom C, et al: The effect of a viscoelastic orthotic on the incidence of tibial stress fractures in an animal model. Foot Ankle1990; 10:276.
114. Schwellnus MP, Jordaan G, Noakes TD: Prevention of common overuse injuries by the use of shock absorbing insoles. Am J Sports Med1990; 18:636.
115. Simkin A, et al: Combined effect of foot arch structure and an orthotic device on stress fractures. Foot Ankle1989; 10:25.
116. Giladi M, et al: The low arch, a protective factor in stress fractures. A prospective study of 295 military recruits. Orthop Rev1985; 14:709-712.
117. Brosh T, Arcan M: Toward early detection of the tendency to stress fractures. Clin Biomech1994; 9:111.
118. D'Amico JC, Dinowitz HD, Polchaninoff M: Limb length discrepancy: an electrodynographic analysis. J Am Podiatr Med Assoc1985; 75:639.
119. Friberg O: Leg length asymmetry in stress fractures. A clinical and radiological study. J Sports Med1982; 22:485.
120. Milgrom C, et al: Stress fractures in military recruits. A prospective study showing an unusually high incidence. J Bone Joint Surg1985; 67-B:732.
121. Montgomery LC, et al: Orthopedic history and examination in the etiology of overuse injuries. Med Sci Sport Ex1989; 21:237-243.
122. Hughes LY: Biomechanical analysis of the foot and ankle for predisposition to developing stress fractures. J Orthop Sports Phys Ther1985; 7:96.
123. Hamill J, et al: Relationship between selected static and dynamic lower extremity measures. Clin Biomech1989; 4:217.
124. Cole JP, Gossman D: Ultrasonic stimulation of low lumbar nerve roots as a diagnostic procedure: a preliminary report. Clin Orthop1979; 153:126.
125. Delacerda FG: A case study: application of ultrasound to determine a stress fracture of the fibula. J Orthop Sports Phys Ther1981; 2:134.
126. Moss A, Mowat AG: Ultrasonic assessment of stress fractures. Br Med J1983; 286:1478.
127. Prather JL, et al: Scintigraphic findings in stress fractures. J Bone Joint Surg1977; 59-A:869.
128. Milgrom C, et al: Negative bone scan and impending tibial stress fractures. A report of three cases. Am J Sports Med1984; 12:488.
129. Keene JS, Lash EG: Negative bone scan in a femoral neck stress fracture. Am J Sports Med1992; 20:234.
130. Monteleone G: Stress fractures in the athlete. Orthop Clin North Am1995; 26:423.
131. Batillas J, Vasilas A, Pizzi WF: Bone scanning in the detection of occult fractures. J Trauma1981; 21:564.
132. Ammann W, Matheson GO: Radionuclide bone imaging in the detection of stress fractures. Clin J Sports Med1991; 1:115.
133. Rupani HD, et al: Three-phase radionuclide bone imaging in sports medicine. Radiology1985; 156:187.
134. Rosenthall L, Hill RO, Chuang S: Observation on the use of 99mTc-phosphate imaging in peripheral bone trauma. Radiology1976; 119:637.
135. Saunders AJS, et al: Stress lesions of the lower leg and foot. Clin Radiol1979; 30:649.
136. Giladi M, Ziv Y, Aharonson Z: Comparison between radiography, bone scan and ultrasound in the diagnosis of stress fractures. Milit Med1984; 149:459.
137. Devereaux MD, et al: The diagnosis of the stress fractures in athletes. JAMA1984; 252:531.
138. Somer K, Meurman KOA: Computed tomography of stress fractures. J Comp Assoc Tomogr1982; 6:109.
139. Prather JL, et al: Scintigraphic findings in stress fractures. J Bone Joint Surg1974; 59-A:869.
140. Matheson GO, et al: Scintigraphic uptake of 99mTc at non-painful sites in athletes with stress fractures. The concept of bone strain. Sports Med1987; 4:65.
141. Zwas ST, Elkanovitch R, Frank G: Interpretation and classification of bone scintigraphic findings in stress fractures. J Nucl Med1987; 28:452.
142. Clement DB, et al: Exercise-induced stress injuries to the femur. Int J Sports Med1993; 14:347.
143. Wilcox JR, Moniot AL, Green JP: Bone scanning in the evaluation of exercise-related stress injuries. Radiology1977; 123:699.
144. Martire JR: The role of nuclear medicine bone scan in evaluating pain in athletic injuries. Clin Sports Med1987; 6:13.
145. Sterling JC, et al: Stress fractures in the athlete. Diagnosis and management. Sports Med1992; 14:336.
146. Meurman KOA, Elfving S: Stress fracture of the cuneiform bones. Br J Radiol1980; 53:157.
147. Lombardo SJ, Benson DW: Stress fractures of the femur in runners. Am J Sports Med1982; 10:219.
148. Rosen PR, Micheli LJ, Treves S: Early scintigraphic diagnosis of bone stress and fractures in athletic adolescents. Pediatrics1982; 70:11.
149. Daffner RH, Martinez S, Gehweiler JA: Stress fractures in runners. JAMA1982; 247:1039.
150. Geslien GE, et al: Early detection of stress fractures using 99m Tc-polyphosphate. Radiology1976; 121:683.
151. Butler JE, Brown SL, McConnell BG: Subtrochanteric stress fractures in runners. Am J Sports Med1982; 10:228.
152. Matheson GO, et al: Scintigraphic uptake of 99m Tc at non-painful sites in athletes with stress fractures. Sports Med1987; 4:65.
153. Khan KM, et al: Outcome of conservative and surgical management of navicular stress fracture in athletes. Am J Sports Med1992; 20:657.
154. Kiss ZA, Khan KM, Fuller PJ: Stress fractures of the tarsal navicular bone: CT findings in 55 cases. Am J Roentgenol1993; 160:111.
155. Terrell PN, Davies AM: Magnetic resonance appearances of fatigue fractures of the long bones of the lower limb. Br J Radiol1994; 67:332.
156. Lee JK, Yao L: Stress fractures: MR imaging. Radiology1988; 169:217.
157. Stafford SA, et al: MRI in stress fractures. Am J Roentgenol1986; 147:553.
158. Steinbronn DJ, Bennett GL, Kay DB: The use of magnetic resonance imaging in the diagnosis of stress fractures of the foot and ankle: four case reports. Foot Ankle1994; 15:80.
159. Fredericson M, et al: Tibial stress reaction in runners. Correlation of clinical symptoms and scintigraphy with a new magnetic resonance imaging grading system. Am J Sports Med1995; 23:472.