April 2016

Influence of estrogen on the plantar fascia

4Plantar-iStock82830367Reported effects of estrogen on knee ligaments and the Achilles tendon raise questions about how the plantar fascia might be altered during the menstrual cycle and how those changes might affect injury risk. This original study was designed to address that question.

By Jerrold Petrofsky, PhD, JD; and Haneul Lee, PT, DSc

The plantar fascia serves as an elastic cushion for weight applied to the foot and also helps increase stability in the ankle.1,2 It is a thick fibrous connective tissue that originates at the medial tuberosity of the calcaneus and inserts into the proximal phalanges.2 The central portion is the thickest; it attaches at the posterior aspect of the medial tuberosity of the calcaneus posterior to the origin of the flexor digitorum brevis tendon, and is 1.5 to 2 cm in width, distally, at the level of the metatarsophalangeal joints. The central portion of the plantar aponeurosis divides into five fascicles, one for each of the toes.1,3 The lateral portion of the plantar aponeurosis is 1 to 1.5 cm in width; it arises from the lateral aspect of the medial tuberosity of the calcaneus, and its distal medial and lateral bands attach to the plantar plate of the fourth toe and to the base of the fifth metatarsal, respectively.

Although the plantar fascia does not differ anatomically between men and women, comparing lower extremity function for both sexes produces a number of interesting statistics. Men experience more plantar loading than women, especially at the midfoot, during a cutting task.4 Women have significantly higher rates of anterior cruciate ligament (ACL) injuries and anterior knee pain than men.5-7 Previous studies have shown that ACL injuries are associated with changes in anterior and posterior cruciate ligament laxity due to changes in body temperature during the menstrual cycle and the effect of beta estrogen receptors on these two ligaments.8-11

Although a higher rate of plantar fasciitis in women than men has been reported in the military, little has been done to examine the effect of estrogen on the plantar fascia.

Increased tissue temperature increases the laxity of ligaments in the body.12,13 Such increases in core and shell temperature are associated with the latter half of the menstrual cycle in women not taking oral contraceptives.14-16 The increase in estrogen just before ovulation at midcycle also increases laxity of the anterior and posterior cruciate ligaments.9 This increase in laxity makes the knee unstable, which can lead to compensatory increased activity of the medial and lateral quadriceps muscles.8 In spite of compensation, knee injuries in runners peak at ovulation.10 Ankle injuries are also more common in women than men, and presumably involve a similar mechanism.17

Although more running-related injuries are seen in men than in women,18 and a significantly higher rate of plantar fasciitis in women than men has been reported in a military population,19 little has been done to examine the effect of estrogen on the plantar fascia. Greater postural sway in the early follicular phase of the menstrual cycle has been reported.20 This could be due to a complex interaction between knee and ankle laxity, as cited above. In another study, Ericksen and Gribble found more inversion-eversion laxity in women than in men, but no effects of the menstrual cycle.21 However, they examined their study participants five days before and five days after ovulation; estradiol peaks at ovulation and then falls. Other research has found that center of pressure path length and velocity were significantly higher at ovulation than at menstruation, suggesting altered neuromuscular control strategies; this was not seen in birth control users.22 In a similar manner, for the Achilles tendon, strain of the tendon was greater in women with a normal menstrual cycle and abolished when women used birth control pills.23

Our research

These investigations into the effect of estrogen on the knee ligaments and the Achilles tendon raise questions about how the ligaments in the foot, such as the plantar fascia, might be altered during the menstrual cycle. It stands to reason that, if these same estrogen receptors are found in the plantar fascia, the ligament will be most flexible at ovulation. This, combined with the known effects of estrogen on more proximal aspects of the kinetic chain, should have the added effect of impairing postural control at ovulation.

To test this hypothesis, we examined plantar laxity, elasticity, and thickness in women compared with men over the same time period. The men were controls to account for measurement variation due to environmental factors.

Methods

The participants in this study were 15 healthy women with a regular menstrual cycle and 15 men, all aged between of 18 and 30 years. Participants did not have any orthopedic abnormalities or injuries to the knee or foot and were screened to confirm normal arches and exclude those with flat feet. Basic characteristics are described in Table 1; the only statistically significant difference between genders was for body weight (p < .01). All participants signed a statement of informed consent as approved by the institutional review board of Loma Linda University in California.

All participants were advised of the study goals, protocol, and inclusion and exclusion criteria. We made two different estimates of plantar fascia elasticity based on the assumption that plantar fascia elasticity would affect foot length and fascia thickness. First, the foot was loaded at two different weights (half body weight and full body weight) and foot length from the longest toe to the heel was measured on a powdered polypropylene sheet. We also measured plantar fascia thickness with no load and full body weight to assess the elasticity of the plantar fascia. We measured all participants at two time points, 14 days apart, to correspond with the early luteal phase and ovulation in the female participants.

plantar-table1We measured foot length with the participant standing on a talcum-powdered polypropylene sheet. This allowed the foot to have a natural shape while we measured its length, since the friction is low. We measured the length of the foot with a digital caliper that could be extended up to 300 mm under two conditions, unilateral stance and bilateral stance.

Musculoskeletal ultrasound is a useful imaging tool for confirming a diagnosis of plantar fasciitis and for measuring plantar fascia thickness before and after a treatment regimen to gauge the treatment’s efficacy. The standard “normal,” or asymptomatic, thickness value reported for the plantar fascia is 2.3 to 4 mm, averaging 3.4 mm.24 Acoustic coupling gel was applied to the plantar surface of the foot, and each foot was evaluated sonographically with a L14-6 MHz linear array transducer. The plantar fascia was examined with the patient in two positions: prone, with the foot hanging over the edge of the examination table and the ankle in a neutral position; and while standing on a platform. The ultrasound probe was applied vertically to the plantar aspect of the heel. The sagittal thickness of the proximal insertion of the plantar fascia was measured at a standard reference point 5 mm from the proximal insertion at the anterior aspect of the inferior border of the calcaneus.

We analyzed data using SPSS for Windows version 22.0. Characteristics of the participants were summarized using mean and standard deviation. T-tests and ANOVA (analysis of variance) were used to compare means. The level of significance was set at less than .05.

Results

Figure 1. Change in foot length for each gender over time. Average foot length in 15 female and 15 male participants taken when standing on both legs (half body weight) or full body weight (standing on one leg). Foot length was measured in women at menstruation and ovulation and in men 14 days apart (males time 1 and 2).

Figure 1. Change in foot length for each gender over time. Average foot length in 15 female and 15 male participants taken when standing on both legs (half body weight) or full body weight (standing on one leg). Foot length was measured in women at menstruation and ovulation and in men 14 days apart (males time 1 and 2).

The results of the experiments are shown graphically in figures 1 and 2. As shown in Figure 1, foot length was significantly greater in men than in women (p < .01). The change in the length of the foot with weight while standing was also different in men and women. For the women, the change in foot length with weightbearing varied during the menstrual cycle; in the early luteal phase, the average change in length from partial to full weightbearing was 3.5 ± 1.4 mm, whereas at ovulation it was 5 ± 2.5 mm. This difference was significant (p < .01).

When indexing the foot length change from partial to full weightbearing, an elasticity index can be derived: .12 ± .04 mm/kg body weight for the early luteal phase and .17 ± .08 mm/kg body weight for ovulation. This difference was about 50% at ovulation and under the influence of estrogen. For the men this elasticity index averaged .07 ± .003 mm/kg body weight and was the same at the two time points.

Plantar fascia thickness helps explain some of this. As shown in Figure 2, plantar fascia thickness was greater in men than women (p < .01), and women showed a significant reduction in thickness with weightbearing during the early luteal phase.

Discussion

Figure 2. Plantar fascia thickness for each gender over time. The average thickness of the plantar fascia in 15 female and 15 male participants when standing on both feet (full body weight) or lying down (unloaded) at two time points 14 days apart.

Figure 2. Plantar fascia thickness for each gender over time. The average thickness of the plantar fascia in 15 female and 15 male participants when standing on both feet (full body weight) or lying down (unloaded) at two time points 14 days apart.

It has been well established that there are estrogen receptors on the anterior and posterior cruciate ligaments, the Achilles tendon, skeletal muscle, and the nervous system.10,13,23 There are both alpha and beta receptors in tendons, ligaments, and skeletal muscle altering neuromuscular control and myofascial force transmission pathways during the menstrual cycle.25-27 There are 17-β estradiol receptors in human connective tissues28,29 that cause relaxation of connective tissues such as the ACL at the time of ovulation, when estradiol concentration peaks.10,13 The effect of estrogen on these receptors affects the female neuromuscular system both directly, by altering motor control, and indirectly, by altering elasticity at ovulation.30

In our investigation, we found that, as others have shown in the Achilles tendon and knee ligaments, there was a significant increase in elasticity of the plantar fascia at ovulation. Men demonstrated thicker plantar ligaments than women, with no change in elasticity over a two-week time period. These data on the men clearly show the change in elasticity seen in the women is not an artifact of the measurements.

Since central body (core) temperature also increases at ovulation31-33 some of the elasticity effect may be due to an increase in tissue temperature. However, we are not aware of any reports of deep tissue temperature measurements in the foot during the menstrual cycle, and this will require further study. Further, if environmental temperature changes due to the season, this may impact the measurements. Body temperature changes throughout the day, presenting another confounding variable. Both of these variables would lead to variation in the measurements. Another limitation of the study is the small number of participants. It would be good in the future to examine three populations of women: one with a normal menstrual cycle, one on the birth control pill (in whom, presumably, the variation in elasticity would not be seen), and finally a group of postmenopausal women.

It seems likely that laxity fluctuations in women affect motor control and injury risk in the foot. We have previously reported that static balance is reduced at ovulation in women,34 which may be due to the increase in laxity since the plantar fascia plays a role in balance during gait.35 Chronic ankle instability, which has been reported to be more common in female athletes than male athletes at both the high school and collegiate levels,17 is also associated with postural control deficits. Ericksen and Gribble found better postural control in men than women, but found no association between postural control and the menstrual cycle.21 However, no studies have yet looked at this possible association in patients with chronic ankle instability.

Conclusion

In female athletes, foot and ankle injuries occur much more frequently than ACL injuries,36 but the medical literature on hormonal changes with the menstrual cycle and injury risk factors in women has focused primarily on the knee. Because ligament laxity in women can be managed clinically using oral contraceptive pills, this potential risk factor for foot and ankle injuries deserves clinical consideration and further research.

Jerrold Petrofsky, PhD, JD, is a professor of physical therapy at Touro University in Henderson, NV, and is on the pain management advisory board for Pfizer Pharmaceuticals. Haneul Lee, PT, DSc, is assistant professor and director of research in the Department of Physical Therapy at Gachon University in Incheon, Korea.  

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