sports medicine Volume 41 Issue 2 February 2011

Sports Med 2011; 41 (2): 91-101 0112-1642/11/0002-0091/$49.95/0

CURRENT OPINION

ª 2011 Adis Data Information BV. All rights reserved.

The Menstrual Cycle and Anterior Cruciate Ligament Injury Risk Implications of Menstrual Cycle Variability Jason D. Vescovi School of Kinesiology and Health Science, York University, Toronto, Ontario, Canada

Abstract

The menstrual cycle and associated hormonal fluctuations are considered risk factors for non-contact anterior cruciate ligament (ACL) injuries in female athletes. Researchers have used a ‘normal’ 28-day cycle and relied upon menstrual history questionnaires or a biological sample (i.e. blood, saliva) taken on a single day to identify the phase of the menstrual cycle where an ACL tear has occurred. However, evidence from available studies lack adequate consideration of menstrual cycle variability that exists in the general population and neglect to acknowledge the greater prevalence of subtle menstrual disturbances in physically active and athletic women. Inter- and intrawoman menstrual cycle variability is large for total cycle, follicular phase and luteal phase length ranging from 22 to 36, 9 to 23 and 8 to 17 days, respectively (95% CI). More importantly, subtle menstrual disturbances such as anovulation and luteal phase defects are common in athletic women with a high prevalence of cycle-to-cycle variations. To complicate matters further, menstrual history questionnaires inaccurately quantify cycle length compared with prospective monitoring of cycle length, highlighting the need to implement more sophisticated methods for identifying menstrual cycle/phase characteristics. Regardless of variability and/or the presence of subtle menstrual disturbances, women may still have regularly occurring menses, making it extremely difficult to accurately identify the phase of the menstrual cycle where an ACL tear has occurred based on a menstrual history questionnaire or a single biological sample. Therefore, the assumption that normal ovarian endocrine function is synonymous with regularly occurring menses in physically active and athletic women is unjustified. Thus, definitive conclusions are not warranted regarding the association between the menstrual cycle and non-contact ACL injury risk based on currently available data. Future work in this area must incorporate methods to prospectively evaluate and accurately characterize menstrual cycle characteristics if we are to link the hormonal fluctuations of the menstrual cycle to non-contact ACL injury risk.

1. Introduction The menstrual cycle and sex steroid hormones have been implicated as risk factors for the greater

occurrence of non-contact anterior cruciate ligament (ACL) injuries observed in female athletes compared with male athletes[1-7] (for reviews see Hewett et al.[8] and Renstrom et al.[9]). An apparent

Vescovi

92

non-random distribution of this particular injury across the menstrual cycle suggests that fluctuations in sex steroid hormones during the menstrual cycle are associated with non-contact ACL tears in female athletes. Some clinical investigators have reported more non-contact ACL injuries around the time of ovulation (i.e. late follicular phase) when there is a sharp rise in the concentration of estradiol, compared with the early follicular and luteal phases of the menstrual cycle;[1-4] however, not all reports support this view and indicate ACL injury risk may be greater around menses when both estrogen and progesterone concentrations are low.[5-7] Additionally, numerous studies have attempted to determine if biomechanical,[10,11] musculoskeletal[12,13] and neuromuscular[10,13] properties vary across the menstrual cycle, but outcomes have been equivocal.[12-23] The challenge with many studies is the methods used to determine phases of the menstrual cycle. Consequently, results from these studies make it difficult to discern the role of the menstrual cycle and sex steroid hormones on ACL injury risk as well as risk factors associated with ACL tears. At the molecular level, sex steroid hormones are considered a possible risk factor because they are involved with the regulation of collagen metabolism. It was reported that the size[24] and structural properties[25,26] of the ACL differ between men and women, suggesting that sex differences in the cellular remodelling process may play an important role in how the ACL resists loading conditions. Furthermore, estrogen receptors have been identified on fibroblasts in human ACLs[27] indicating that estrogen could have a direct regulatory effect on fibroblast function, collagen remodelling and, ultimately, alter the structural, material and mechanical properties of the ACL in vivo. Indeed, Liu et al.[28] demonstrated a doseresponse relationship between 17-b estradiol concentration and a reduction of fibroblast proliferation and collagen synthesis in vitro indicating a direct effect of estrogen on collagen remodelling. Shultz et al.[12,14,15] have demonstrated that knee joint laxity varies across the menstrual cycle and is associated with the absolute concentrations of sex steroid hormones, with their model being more predictive when a time delay was considered. Collectively, these findings indicate that it is ª 2011 Adis Data Information BV. All rights reserved.

plausible there could be (i) an immediate or slightly delayed effect on knee joint laxity[12] and potential ACL injury risk, resulting from the regulation of specific proteins involved with collagen and matrix metabolism subsequent to large absolute changes in sex steroid concentrations across the menstrual cycle;[15] or (ii) a chronic effect on the size, shape and quality of the ligament as a result of the accumulated exposure to sex steroid hormones on ligament remodelling. As a result of the conflicting evidence available for an association between a specific phase or particular hormonal fluctuations during the menstrual cycle and non-contact ACL injury risk, as well as with particular risk factors, a consensus has yet to be reached on these topics.[29] One reason for the disparity in findings is that the methods for determining which phase of the menstrual cycle a female athlete is in at the time of injury have relied on questionnaires used to identify cycle day and/or a biological sample taken from a single day. These methods limit the ability to accurately identify the follicular and luteal phases in physically active and athletic women.[30] Additionally, methodological strategies to account for normal intra-individual menstrual cycle variability and/or menstrual dysfunction have been lacking and preclude any definitive conclusions from being made based on currently available research. While there are implications for the accurate assessment of menstrual status and menstrual cycle phases for investigators seeking to determine physiological, biomechanical, structural or functional difference across the various phases of the menstrual cycle, due to space limitations this article will focus on ACL injury risk. The aim of this article is to provide an overview of menstrual cycle variability in young women and, more importantly, to clearly illustrate that normal ovarian function is not synonymous with regularly occurring menses, especially when working with physically active and athletic women.[31,32] 2. Menstrual Cycle Variability The ‘normal’ length of the menstrual cycle or particular phases of the menstrual cycle have been repeatedly used to standardize study outcomes;[4-6] Sports Med 2011; 41 (2)

Menstrual Cycle and ACL Injury Risk

however, there is a substantial body of evidence that illustrates menstrual cycle variability (both intra- and inter-person) is actually the norm.[33-41] Many investigators have reported that the average length of the menstrual cycle is approximately 28 days;[33,34,39,42,43] however, the 95% confidence intervals (CIs) for menstrual cycle length is substantially large. For example, Fehring et al.[34] reported that in 165 women between 21 to 44 years of age, the 95% CI for cycle length was 22–36 days. More recently, Cole et al.[33] demonstrated that in 167 women aged 18–36 years, the 95% CI for cycle length was 23–32 days. In addition to inter-woman cycle variability, intrawoman cycle variability is also an important consideration when attempting to identify phases for a particular cycle. Cycle-to-cycle variability is >7 days, but 100 kg for male judo athletes), it is impossible to establish a single body type or anthropometric profile for all judo athletes.[6] Nevertheless, there is some similarity throughout much of the range in terms of characteristic somatotypes and a predominance of mesomorphy (table I).[8,10] In terms of somatotype, the judo athlete is generally thought to have a profile that accentuates the mesomorphic properties (very high muscularity, low linearity and low fat). Among females, the endomorphic component has values near to the mesomorphic one. However, caution should be exercised when interpreting these results as they could have been influenced by the inclusion of heavyweight athletes. Table II presents the body composition of high-level judo athletes. World and Olympic level male judo athletes usually have 78 kg for females and >100 kg for males). Only one study presented a significant difference in body fat among bestranked judo athletes and lower ranked athletes.[19] 3. Maximal Strength Maximal strength can be defined as the maximal torque that a muscle or a muscle group can generate at a specified or determined velocity.[33] It depends upon the ability of the nervous system to recruit motor units, the ability of the muscle to utilize the energy anaerobically (mainly adenosine triphosphate and phosphocreatine) for muscle contractions, the amount of motor units simultaneously

Table I. Somatotype of high-level judo athletes Athlete characteristics

Endomorphy (mean – SD)

Mesomorphy (mean – SD)

Ectomorphy (mean – SD)

Reference

Hungarian team (n = 18)

3.6 – 1.9

7.0 – 1.5

1.6 – 0.9

Farmosi[7]

Japanese (n = 13)

3.4 – 2.0

8.5 – 1.4

1.0 – 0.6

Kawamura et al.[8]

French (n = 10)

1.2 – 0.5

7.6 – 0.9

1.5 – 0.7

Kawamura et al.[8]

Brazilian team 1999 (n = 7)

2.7 – 1.3

7.9 – 1.6

1.1 – 0.6

Silva et al.[9]

WCP under 71 kg (n = 18)

2.3 – 0.4

5.6 – 0.5

1.9 – 0.4

Claessens et al.[10]

WCP 71–86 kg (n = 9)

3.0 – 0.5

6.0 – 0.7

1.7 – 0.7

Claessens et al.[10]

WCP >86 kg (n = 11)

4.1 – 0.9

6.2 – 0.6

1.3 – 0.4

Claessens et al.[10]

Brazilian university team 1996 (n = 6)

2.7 – 1.8

6.2 – 1.5

1.6 – 1.2

Franchini et al.[11]

Brazilian university team 1996 (n = 7)

4.1 – 1.3

5.0 – 1.1

1.7 – 1.2

Franchini et al.[11]

Brazilian team 1999 (n = 7)

4.3 – 1.3

5.1 – 0.9

1.1 – 1.0

Franchini et al.[12]

Brazilian elite (n = 28)

3.6 – 1.9

5.1 – 1.7

1.5 – 0.9

Mello and Fernandes Filho[13]

Male

Female

WCP = World Championship players.

ª 2011 Adis Data Information BV. All rights reserved.

Sports Med 2011; 41 (2)

Franchini et al.

150

Table II. Percentage body fat in judo athletes Athlete characteristics

Body mass (kg) [mean – SD]

Body fat (%) [mean – SD]

Prediction equation reference

Reference

8.9 – 0.8

Enilina[14]

Farmosi[7]

14.0 – 7.3

[14]

Farmosi[7]

Male Hungarian team (n = 7) Hungarian team (n = 11) Canadian team 1987 (n = 22) US (elite; n = 8)

60–70a >70

b

75.4 – 12.3 91.5 – 2.7

9.3 – 2.1 10.8 – 1.9

Enilina

Lohman

[15]

Thomas et al.[16]

Jackson and Pollock

[17]

Callister et al.[18]

Jackson and Pollock

[17]

Callister et al.[19]

US (elite; n = 18)

83.1 – 3.8

8.3 – 1.0

Canadians (n = 17)

79.3 – 14.6

10.5 – 1.0

Drinkwater and Ross[20]

Little[21]

Brazilian university team (n = 6)

86.9 – 34.4

11.1 – 5.1

Drinkwater and Ross[20]

Franchini et al.[11]

Polish (n = 15)

82.9 – 16.4

13.7 – 3.4

Slaughter et al.[22]

Sterkowicz et al.[23]

Brazilian university team 2000 (n = 13)

89.0 – 16.0

13.7 – 5.2

Drinkwater and Ross

[20]

[25]

Franchini et al.[24] Koury et al.[26]

Brazilian Olympic team 2000 (n = 7)

NR

7.0 – 3.0

Croatians (elite; n = 6)

NR

12.0 – 1.2

NR

Sertic et al.[27]

Brazilian team A (n = 7)

90.6 – 23.8

11.4 – 8.4

Jackson and Pollock[17]

Franchini et al.[6]

Brazilian team B (n = 15)

86.5 – 16.3

10.1 – 5.7

Jackson and Pollock[17]

Franchini et al.[6]

59.1 – 7.9

20.9 – 2.0

Piechaczek[28]

Obuchowicz-Fidelus et al.[29]

Lohman et al.

Female Polish team (n = 22) Canadians (n = 8) US (elite; n = 7)

62.3 – 5.2 56.3 – 0.9

15.2 – 2.1 15.8 – 1.2

Drinkwater and Ross

[20]

Little[21]

Jackson et al.

[30]

Callister et al.[18]

[30]

Callister et al.[19]

US (elite; n = 9)

53.8 – 1.6

15.2 – 1.0

Jackson et al.

Brazilian university team (n = 7)

66.9 – 16.3

16.1 – 3.0

Drinkwater and Ross[20]

Franchini et al.[11]

Brazilian Olympic team 2000 (n = 9)

66.0 – 8.0

22.0 – 5.0

Jackson et al.[30]

Koury et al.[31]

Croatians (n = 8)

NR

16.6 – 4.3

NR

Sertic et al.[27]

a

Athletes body mass ranged from 60 kg to 70 kg.

b

Athletes body mass was >70 kg.

NR = not reported.

active and the size of cross-sectional area of muscle fibres present. Because of the relationship to crosssectional area and size, strength is often analysed relatively to bodyweight; the so-called relative strength is especially informative in bodyweight classified sports such as judo.[34] As muscle contractions might occur in different manners, they will be discussed separately in the next sections. 3.1 Isometric Strength

An isometric action results in no change in muscle length and although force is developed, as no movement occurs, no work is performed.[33] As judo athletes have to grip the opponent’s uniform (judogi), early studies have focused on isometric grip strength. Table III presents the grip strength of different groups of judo athletes. ª 2011 Adis Data Information BV. All rights reserved.

Isometric grip strength has not been investigated in detail for different weight categories, while only two studies[7,36] have addressed this topic. In one study,[36] greater left isometric grip strength was observed in the middle weight category compared with the light weight category. However, there is no mention concerning the number of left-handed athletes in each group, which prevents any conclusion on whether the difference is caused by the weight category or by the number of left-handed athletes in the first group. The other study did not identify any difference among weight categories.[7] A third study presented in table III did not perform any statistical comparison among the different weight groups, but it seems that the isometric strength increases according to the weight category.[35] When correlation analysis is conducted, one study[16] Sports Med 2011; 41 (2)

Physiological Profiles of Elite Judo Athletes

identified a positive relationship (r = 0.76) between body mass and isometric grip strength. Sex differences were reported in only one study.[11] The male group presented higher absolute right and left isometric grip strength compared with the female group. However, when

151

values were presented relative to body mass, no difference was observed. In Canadian judo players,[21] no statistical comparison between male and female athletes was reported, but it is possible to infer that both absolute and relative isometric grip strength were higher for the male group.

Table III. Isometric handgrip strength (IHGS) of judo athletes Study

Athlete characteristics; sex

Right IHGS (kgf) [mean – SD]a

Left IHGS (kgf) [mean – SD]a

Matsumoto et al.[35]

Japanese university athletes (~66 kg); M (n = 12): 1967

43.8

43.8

1968

49.3

49.3

Candidates to the 1967 World Championship

44.9

45.1

1967

50.8

47.7

1968

53.3

52.2

Candidates to the 1967 World Championship

56.8

52.0

1967

55.3

49.5

1968

59.6

55.6

Candidates to the 1967 World Championship

54.2

51.5

All (n = 24)

64.9 – 8.9

59.7 – 8.8