November 2013

Achilles tendon rupture: The influence of gender

11Achilles-iStock1773499v2The literature suggests that women are less likely than men to experience an Achilles tendon rupture. This may be because women are less capable of generating the large eccentric contractions necessary for rupturing the tendon. Estrogen may also play a protective role.

By Joseph L. Laratta, MD, and J. Turner Vosseller, MD

The Achilles tendon, the common tendon of the gastrocnemius and soleus muscles, is the largest and strongest tendon in the human body. The Achilles tendon is also the most commonly ruptured tendon in the body.1 Although the exact mechanism of rupture is not fully understood, generally speaking, two conditions must be present in the tendon for it to rupture: preexisting degeneration and an eccentric contraction of sufficient force for rupture.

The increasing participation of female athletes in sports in the US is largely attributable to the passage of Title IX of the Education Amendments of 1972 that mandated institutional support for women’s programs.2 The increased participation of girls and women in athletic activities has led to increased recognition and diagnosis of sports injuries in women. While some injuries are more common in women than in men, the incidence of Achilles tendon rupture appears to be less common in women.3 Ligamentous injury in the knee of female athletes has been more specifically investigated than injury in the Achilles tendon, allowing a better establishment of demographic and potential precipitating factors.4

As female athletic involvement continues to grow, physicians will be presented with injury patterns in women comparable to those of men in similar sports, though the likelihood of injury and causative factors may be different. A thorough understanding of the anatomy and mechanism of injury is paramount. However, the role of gender differences in neuromuscular control, biomechanics, genetics, and endocrinology are still being determined.

Achilles tendon anatomy and function

The Achilles tendon, not unlike other tendons, is composed of organized type I collagen fibers, which transmit tension from muscle to bone. The Achilles tendon origin begins near the midcalf and is the distal condensation of the soleus muscle with the gastrocnemius muscle, which inserts posteriorly on the calcaneus.5 These two muscles together make the triceps surae muscle–tendon complex, which acts to plantar flex the ankle through the Achilles tendon. The innervation of the Achilles tendon and sheath comes primarily from branches of the sural cutaneous nerve.6 The vascular supply of the tendon is age-dependent, decreasing with age.7 The posterior tibial artery supplies the tendon proximally and distally, whereas the peroneal artery supplies the midsection. Some cadaveric studies suggest a watershed area approximately 2 cm to 6 cm above the Achilles’ insertion, although this has not been supported in vivo.8

Epidemiology of Achilles tendinopathy

The incidence of Achilles rupture is 7 out of 100,000 in the general population and 12 out of 100,000 in competitive athletes.9 Achilles tendon injuries predominantly affect active young people participating in athletic activities that require quick bursts of energy. Many musculoskeletal injuries occur with a greater frequency among women. Indeed, Jones et al have shown women undergoing basic army training sustain more musculoskeletal injuries than their male counterparts, though most of those injuries were overuse injuries.10 With respect to the knee, many studies have demonstrated an increased incidence of ligamentous injures and a correspondingly increased number of surgeries for female athletes compared with male athletes.11-13 However, the incidence of Achilles tendon rupture is lower in women than in men, with a male-to-female ratio ranging between 1.67:1 and 6.90:1.14-18 More recent data suggest the true ratio is likely on the upper end of that spectrum.3

Mechanism of Achilles tendon injury

11Achilles-iStock28037790v2As noted, Achilles tendon rupture requires two things: first, degeneration (or tendinopathy) of the tendon, and second, an eccentric contraction of sufficient force to tear the tendon apart. Tendinopathy is a failed healing response. The healing response is haphazard, with disruption of collagen fibers, increased noncollagenous matrix, and disorganized proliferation of tenocytes.19,20 Jozsa et al first noted a link between Achilles tendon degeneration and rupture.1 Maffuli subsequently expanded on this work and has shown ruptured tendons are clearly more histologically degenerated than both non­ruptured tendons and tendons of people with Achilles tendinosis.21

An eccentric contraction is one in which the muscle contracts while it is lengthening. In essence, the degenerated Achilles tendon is quite literally pulled apart by a strong contraction performed while the tendon is lengthening. Numerous authors have noted the correlation between athletic activity of various types and Achilles tendon injury, with rates of injury associated with athletic activity ranging from 59% to 81%.12,15,16,22 Most recently, Vosseller et al noted that men most commonly rupture their Achilles tendons while playing basketball, while women most commonly experience such rupture playing tennis.16

Maffuli et al suggested patients with degeneration and those without degeneration are really two distinct populations, with those with degeneration having some unclear risk factor or factors predisposing to rupture not present in the other population.23 Furthermore, data show patients with symptomatic Achilles tendinosis are typically older than those who rupture the tendon. Vosseller et al showed the mean age of patients with Achilles ruptures is 43.8 years, while the mean age for those with nonacute pathology (i.e., Achilles tendinosis) was 55.1 years.16 Perhaps those patients who present with painful tendinotic tendons are those who are at risk for rupture but have not yet experienced an eccentric contraction of sufficient force to rupture the tendon.

Genetic considerations in tendon injury

As mentioned, nearly all intrinsic risk factors for injury have a genetic element. A family history of Achilles tendinopathy raises the risk of pathology nearly fivefold.24 Nine studies have investigated an association of specific genes with Achilles tendinopathy, specifically whether specific variants of genes are over- or under-expressed in Achilles tendinopathy. The genes implicated include COL1A1, COL5A1, COL12A1, and COL14A1, respectively encoding type I, V, XII, and XIV collagen proteins. Other genes encoding matrix metalloproteinases (MMPs) and inflammatory signaling molecules (IL-1β, IL-6) are also implicated.25-33

Some studies reveal a link between ABO blood group and chronic Achilles pathology, though it is more likely due to the fact that the genes for blood group are in close proximity on chromosome 9q34 to the COL5A1 gene and other genes involved directly in Achilles biology.34 The COL5A1 gene encodes for the α1 chain of type V collagen that intercalates with type I collagen fibrils and is believed to regulate fibril diameters.35

Specifically, research has shown the CC genotype of the BstUI restriction fragment length polymorphism (RFLP) within the 3′-untranslated region (UTR) of the COL5A1 gene is significantly underrepresented in participants with chronic Achilles tendinopathy.26,27 Posthumus et al showed a predilection for the CC genotype in a population of female, but not male, athletes with anterior cruciate ligament (ACL)  pathology.36 However, it would be premature to attempt to link these findings directly to risk of Achilles rupture in female athletes without further supporting data.

Metabolic considerations in tendon injury

Medical comorbidities can be associated with increased risk of Achilles injury in rabbits and, possibly, in humans. Diabetes is associated with an increased rate of advanced glycation end products (AGEs) that form covalent links within collagen fibers, altering their stability and accelerating degeneration.37,38

Tendon damage in obese individuals is often due to two distinct mechanisms: increased load-bearing tension and systemic dysmetabolism. Adiposity functions as an endocrine organ and releases bioactive peptides such as leptin, adiponectin, and lipocalin that influence mesenchymal cell phenotypes, and therefore may directly modulate tendon structure.39 In the 20th century the prevalence of obesity in the US among adult men has been greater than that among adult women.40 Moreover, overweight men tend to have more visceral fat, which substantially increases the risk of heart disease, metabolic syndrome, and diabetes.41

Biomechanical considerations

The adaptability of a tendon to loading differs across gender with respect to collagen metabolism and mechanical properties of tendon fascicles. It has been shown that well-trained men had larger patellar tendon cross-sectional areas than untrained men, though this difference was not observed in women.42 Thus, tendons in men may adapt to physical loading with increased collagen synthesis and hypertrophy while such phenomena may not be detectable in women.

Magnusson et al further demonstrated that collagen fascicles from men reached higher levels of ultimate stress than those from women, and that the tangent modulus for male fascicles exceeded those of women.38 In addition to intrinsic properties of tendons, different foot-strike patterns during running and jumping may affect Achilles tendon loading, force, and rate of injury. Rearfoot strike (RFS) patterns, in which the heel contacts the ground first, have been demonstrated to decrease peak force and average loading rate on the Achilles tendon compared with nonrearfoot strike patterns.43 Bertelsen et al showed women had an increased tendency to use a RFS pattern, thus experiencing lower force and loading rate, compared with men.44

Sex hormones in tendon injury

It is accepted that sex hormones, such as estrogen and progesterone, have effects on soft tissues through alteration of gene expression. Sex hormones have not been thoroughly studied in Achilles tendons, but have been explored in relation to ACL rupture. ACL rupture incidence is increased during the ovulatory phase of the menstrual cycle, when estrogen levels are most elevated.45 Wojtys et al further noted that oral contraceptive use decreases the injury incidence peak observed during the ovulatory phase.46

Although ligaments differ from tendons in terms of origin and insertion, both share similar mechanical function and a similar hierarchical structure that allows them to be used interchangeably in reconstructive surgery. The basic architecture consists of type I collagen arranged in a cross-linked triple-helix structure forming fibrils further organized into fascicles and further organized into the ligament or tendon proper.

Higher endogenous estrogen levels in women have been associated with lower collagen synthesis rates and, therefore, smaller tendon cross-sectional area.47 Estrogen receptors have been identified on posterior tibial tendon and flexor digitorum longus tenocytes in both male and female patients and in healthy and diseased hosts.48 Thus, sex hormones may influence the structure and function of these tendons and possibly other tendons, such as the Achilles tendon. Recent evidence suggests that estrogen attenuates fibroblast biosynthesis and may decrease collagen density in the tendon, thus decreasing tendon resistance to injury.49

Conversely, however, Bryant et al demonstrated that acute fluctuations in plasma estrogen across the menstrual cycle did not alter the strain behavior of the Achilles tendon.50 Furthermore, Burgess et al showed no difference in the mechanical properties of patellar and medial gastrocnemius tendons with acute fluctuations in either estrogen or progesterone.51,52

Chronic estrogen exposure, however, has been shown to result ultimately in less Achilles tendon strain.46 Moreover, studies on rat skeletal muscle demonstrate the inhibitory effect of female sex hormones on skeletal muscle fiber diameter, which may decrease the ability of the muscle to produce an eccentric load capable of rupturing the tendon.53

Prevention

Eccentric calf exercises have primarily been the subject of research involving the treatment of midportion Achilles tendinopathy, but may also be beneficial for prevention of injury. Identification of neuromuscular imbalances, particularly highly dominant dominant legs and single-leg stance deficits, is paramount in formulating an effective preventive exercise regimen.54,55

Jumping and landing strategies with respect to unbalanced weightbearing and dangerous maneuvers should be examined closely and addressed with repetitive movements aimed at building muscle memory. Men in general have greater muscle mass and are capable of generating greater force of contraction, and may more easily exceed the maximal tensile strength of the tendon than women. However, because the pathophysiology of injury is similar across gender and the most consistently identifiable risk factor for rupture is participation in athletic activity, both would likely benefit from appropriate preventive exercise programs.

Extrinsic factors can always be modified to decrease the risk of any musculoskeletal injury. Activity modification is likely the most important prevention strategy for Achilles pathology as an eccentric contraction is always required for rupture. Alteration in shoes, orthotic equipment, and playing surface may also be beneficial in preventing injury, though their effectiveness has not been studied adequately.

Conclusions

The literature shows women have a lower risk of Achilles tendon rupture compared to men. Women generally are less capable of generating the large eccentric contractions necessary for rupturing the tendon. Furthermore, estrogen may play a protective role. The risk factors for tendinosis currently are not clear. Further work to shed light on those risk factors may provide greater insight into why these injuries occur less frequently in women.

Joseph L. Laratta, MD, is a resident in the Columbia University Medical Center Orthopaedic Residency training program in New York City. J. Turner Vosseller, MD, is an associate professor of orthopaedic surgery at Columbia University Medical Center.

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