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Anterior cruciate ligament laxity related to the menstrual cycle: an updated systematic review of the literature.

Introduction

The physical disability and long rehabilitation process associated with anterior cruciate ligament (ACL) injury can be both psychologically and financially devastating to the individual, ultimately resulting in a decreased quality of life. (1) Female athletes have a higher rate of ACL injury than do men, and many of these injuries require extensive surgical and rehabilitative interventions, with a financial burden to the American healthcare system estimated to approach $650 million annually. (1) Bearing that in mind, it is imperative to understand the mechanisms leading to such an injury in an effort to prevent its occurrence and its subsequent sequelae. Although both men and women are susceptible, the literature states that women have a 4 to 6 fold increased incidence of ACL injury. (2,3) Notwithstanding the fact that a definitive etiology for this discrepancy between the sexes has not been established, proposed theories to account for it include: neuromuscular and biomechanical factors (differences in pelvis width/increased Q-angles in females, smaller femoral notch widths in females, increased female hamstring flexibility, and imbalanced hamstrings-to-quadriceps strength leading to differences in landing patterns); psychological factors (women may be more prone to maladaptive perfectionism leading to overtraining and burnout) and nutritional differences (higher frequency of food restriction and decreased calcium intake among females compared to males). (1,3,4) An additional theory posits increased ligament laxity is related to hormonal fluctuations during the menstrual cycle. (1)

The menstrual cycle is controlled by the pituitary-hypothalamic-ovarian axis and involves the complex interaction of estrogen, progesterone, relaxin and testosterone. (1) Typically, each menstrual cycle spans 28 days, beginning with the follicular phase from days 1-9 during which estrogen predominates, followed by the ovulatory phase spanning days 10-14, where estrogen continues to prevail and reaches its peak. (1) The cycle ends with the luteal phase extending from days 15-28 during which time progesterone levels surpass that of estrogen levels. (1) Relaxin is secreted during the follicular and luteal phases, reaching its peak during the luteal phase. (5) Lastly, testosterone fluctuates throughout the cycle, and functions to contribute to the formation of estrogen. (6) Although the hormones that predominate during each phase are consistent among all women with normal functioning cycles, the levels of each hormone varies among individuals. (3)

The hormones controlling the menstrual cycle are thought to affect the overall integrity of the ACL by altering its structure. (7) In general, these hormones decrease the tensile properties of the ACL by binding to specific receptors on it. (7) Specifically estrogen, when bound to receptors on the ACL, has been shown to decrease fibroblast proliferation, subsequently decreasing collagen production. (7) This could theoretically result in a greater incidence of ACL injuries during the pre-ovulatory phase spanning days 1-14 of the menstrual cycle, when estrogen predominates. This theory has been supported by a case-control study in which female recreational skiers who sustained a non-contact ACL injury demonstrated a two-fold increase in injury rates during the pre-ovulatory phase compared to the uninjured controls. (8) However, other studies have reported contradictory results that refute the theory that hormonal variations during the menstrual cycle contribute to ligament laxity. For example, Van Luren et al (9) reported arthrometric analysis of ACL laxity that failed to demonstrate any variation in ACL laxity throughout the menstrual cycle. In addition, Belanger and colleagues (10) examined 18 female subjects and were unable to establish an association between increased ACL laxity and the menstrual phase.

The objective of this article is to review the literature regarding changes to anterior cruciate ligament laxity during the menstrual cycle, building on previous reviews by Zazulac et al (1) and Hewett et al (2). A better understanding of the mechanism of injury may allow clinicians to identify females who are at greatest risk of ACL injury and subsequently contribute to injury prevention in female athletes.

Methods

A literature search was performed using the following electronic databases: Index to Chiropractic Literature, MEDLINE, CINAHL and Rehabilitation & Sports Medicine Source, through EBSCO Publishing. We combined controlled vocabulary terms with text words. In MEDLINE we exploded and searched the MeSH term menstrual cycle, which included fertile period, follicular phase, luteal phase and menstruation, and menstruation, and combined these terms with the MeSH term anterior cruciate ligament injury. Text words for these concepts included anterior cruciate ligament tear and anterior cruciate ligament injuries. This yielded 27 articles. Citations from specific articles (reference tracking) were then searched independently through selected databases followed by hand searching throughout the periodicals. Reference tracking yielded one article. Periodical searching yielded no eligible articles.

Inclusion/Exclusion Criteria

Inclusion criteria were as follows: female subjects of reproductive age; published between 1998 and August 2011; papers written in the English language and studies using human subjects only. Articles that focused on therapy for ACL injuries were excluded. Papers were also excluded if they had been reviewed in the most recent literature review by Hewett et al in 2007. (2) Using these inclusion/exclusion criteria 13 articles were selected for review.

Quality Appraisal

The methodological quality of the studies that met the selection criteria was assessed using a modified version of an instrument developed by Sackett (see Table 1). (11) Since the majority of research on the topic of ACL laxity and menstrual hormonal fluctuations is limited to observational study designs rather than randomized clinical trials, the 'assignment of patients' and 'follow-up levels' criteria were not included in our grading as they were deemed incompatible with the majority of the research designs. As a result, the instrument was modified and scored out of 38 rather than 50.

The eligible articles were randomly assigned to four authors (LB, DB, JC, SC). Each accepted article was reviewed by two authors independently. The data from all accepted articles were recorded onto a data extraction sheet by the authors as part of their review. The authors checked and edited all entries for accuracy and consistency. Recorded data included study authors and quality score, details of the study design, sample, interventions, outcome measures, and main results/conclusions of the study. Any discrepancies of scores between the authors were settled via discussion until consensus was reached.

Results

Thirteen articles met the inclusion criteria (see Table 2). (12-24) After methodological quality assessment of each article using the modified Sackett grading instrument, papers were allocated scores out of a possible 38 points (Table 3). Of the 13 articles, 9 articles investigated ACL injuries throughout the menstrual cycle and 4 articles investigated the issue of ACL laxity throughout the menstrual cycle (see Tables 4a and 4b respectively). Articles are listed in descending order of their score. In the event two or more articles had the same score, they were arranged alphabetically. A brief summary of each of the 13 articles graded in this study is provided in Table 4a and 4b.

The accepted studies, determined by Sackett et al, scored between 30 and 13 out of a possible 38 points on the Modified Sackett Score (MSS) instrument (Table 2,3). Eight (12-19) of the thirteen studies reported that knee ligament laxity changes throughout the menstrual cycle, although the phase during which this ligamentous laxity occurred varies throughout the cycle. Ruedl et al (MSS = 23/39) (12), Adachi et al (MSS = 22) (13), Wojtys et al (MSS = 17) (14) and Park-b et al (MSS = 13) (15) all reported increased knee laxity during the ovulatory phase and Beynnon et al (MSS = 30) (16) reported increased knee laxity during the pre-ovulatory phase (compared to post-ovulatory phase). However,

Schult et al (MSS = 25) (17) and Deie et al (MSS = 20) (18) reported increased knee laxity during the follicular phase and Parka (MSS = 15) (19) reported increases knee laxity during the luteal phase of the menstrual cycle.

On the other hand, five studies (20-24) did not report any statistically significant changes in knee laxity during the menstrual cycle. Eiling et al (MSS = 27) (20) reported that there was no statistically significant effect on anterior knee ligament laxity throughout the menstrual cycle and that 'musculoskeletal stiffness' was lower during the ovulatory phase of the menstrual cycle as compared to day one of menstruation and the mid-follicular phase. Two studies compared men to women with respect to knee laxity. The study by Deie et al (18) reported there was no statistical difference in the anterior knee movement of 8 men assessed during the same three week period as 16 women and the study by Pollard et al (21) that compared 12 men to 12 women reported that, while knee laxity increased following exercise, there was no difference across the sexes.

Discussions

Zazulak et al conducted a systematic review similar to ours in 2006. (1) Those researchers were able to retrieve nine studies. Subjects included collegiate athletes, high-school athletes, recreational athletes, non-athletes and 'unspecified' sport participants. Cohort sizes ranged from 7 to 41. Anterior tibiofemoral movement was measured in all studies using KT 1000 or KT 2000 arthrometers. (1)

In that review, six of the nine reviewed studies reported no statistically significant effect of the menstrual cycle on ACL laxity. However, the reviewers reminded the reader that the majority of these six studies based their observations on a single sampled day of the cycle, or randomly sampled across the cycle without hormonal or cycle landmark confirmation. (1) Of the three studies that did report increased laxity of ACL during the menstrual cycle, all three reported it occurred during the ovulatory or post-ovulatory (luteal) phase (1), a finding similar to what we found among the 13 articles we reviewed. Despite diversity in the literature, Zazulak et al (1) suggested that the three studies which found a positive association between the menstrual cycle and ligament laxity were superior in study design, methodology and consistency compared to the 6 studies which failed to show any association, thereby concluding that the menstrual cycle may have a significant effect on anterior knee laxity.

Hewett et al (2) performed a similar systematic review to the one by Zazulak et al (1), with the primary difference being that Hewett et al reviewed articles that investigated the effects of the menstrual cycle on anterior cruciate ligament injury risk among high-risk female athletes, whereas Zazulek et al investigated the effect of the menstrual cycle on anterior knee laxity. In the Hewett et al (2) review, seven studies met the study's inclusion criteria. Hewett et al (2) reported that all seven articles favoured an effect of the first half of the menstrual cycle for the increased ACL injuries, most commonly during the pre-ovulatory phase. These authors also reported that the use of oral contraceptives in combination with neuromuscular training may increase the stability of the knee joint and decrease the risk of injury to female athletes. (2) Hewett et al suggested that disproportionate or isolated quadriceps recruitment can create forces higher than those required for ACL failure. (3) Therefore, neuromuscular training should focus on balancing hamstrings-to-quadriceps strength and recruitment in order to increase stability of the knee.

While Zazulak et al (2) focused on knee laxity and Hewett et al (1) focused on injury, this most recent review looked at a combination of both laxity and injury. The results of our review are in agreeance with Zazulak et al (2) and Hewett et al (1), supporting an effect of menstrual cycle on anterior cruciate ligament laxity. While the association between ligament laxity and hormonal fluctuations during the menstrual cycle has been suggested, there remains discrepancy concerning which phase of the menstrual cycle is associated with greater ligament laxity. The current review found that the majority of studies (4 studies out of 8) that reported a positive association between increased laxity, injury and the menstrual cycle implicated the ovulatory phase as the most significant time for laxity to occur. These findings are somewhat in concordance with the conclusions of Zazulak et al (2), who identified the greatest laxity during the ovulatory and post-ovulatory phases. In contrast, Hewett et al (1) identified that the greatest injury risk occurred during the pre-ovulatory phase.

Overall, limited evidence from the three reviews supports the theory that ACL ligament laxity varies with the fluctuations of the hormonal cycle, thus predisposing female athletes to ACL injury. What remains to be clarified is what phase of the cycle females are most at risk. Future research should aim to clarify whether this fluctuation in ligament laxity is consistent amongst all women with hormonal fluctuations throughout their cycle, or whether ligament laxity is dependent on the absolute or relative hormonal level changes throughout a woman's cycle. Future studies can address this issue by focusing more stringently on measuring hormone levels and by examining women over a longer period of time (more than one cycle) to try and establish whether a trend in hormonal levels and ligament laxity can be established and a phase of increased risk identified.

Limitations

Many limitations were encountered throughout the review of the recent literature. Limitations included: the majority of the research was conducted during only one menstrual cycle per participant, which does not account for variation from cycle to cycle; there was no standardized definition of the phases of the menstrual cycle, resulting in variation of the phases from paper to paper; typically only one knee was assessed per participant and therefore the results cannot be confidently distinguished from conditions that may have been pre-existent in that knee; the majority of studies were conducted exclusively on women with normal 28-day cycles and; women who were on oral contraceptives were often excluded by design. The average woman, and the elite athlete, are not so easily categorized-especially since menstruation may cease among some high performance athletes with low body mass indexes, and thus the results reported in these studies may not be extrapolated to the female population most at-risk of ACL injury.

Other limitations of this review are that we only searched for articles in English and did not go further back than 1998, since that was where other similar reviewers ended. Another limitation was our use of an adapted Sacket instrument for the purposes of this review. Although it had face validity to do so, to the best of our knowledge there is no evidence that specifically supports the validity of the modifications we made to Sackett's original instrument. Furthermore, this tool does not assess important aspects including confounding factors, participation rates, study population consistency or selection bias. Lastly, 5 of the 13 studies accepted in this review are cross-sectional and therefore cannot be used to determine any cause and effect relationship between menstrual cycle and knee ligament laxity.

Conclusions

There is preliminary evidence to suggest that ligamentous laxity of the knee changes throughout the course of a women's menstrual cycle, with the majority of studies reporting the greatest change is during the ovulatory phase. However it is important to note that the evidence remains inconsistent and is based predominantly on studies of low methodological quality. Certainly better clinical trials need to be conducted that follow women over several menstrual cycles and that include women not on a standard 28-day cycle. Moreover, clinical trials investigating changes to ACL laxity should assess both knees. That said, this review, as well as the previously published study by Hewitt et al (2,3), suggest that healthcare professionals caution their female patients that injury may occur during different phases of their menstrual cycle--particularly the ovulatory phase. It may be prudent for female athletes to take the necessary precautions when exercising vigorously during certain stages of their menstrual cycle. Since it does appear that at least some women may experience ligament laxity during different phases of their menstrual cycle, patients can be encouraged to diarize any injuries they may sustain and monitor if they typically occur during a particular phase of their menstrual cycle. In addition, due to the lack of consensus on the phase at which increased laxity and injury occurs, healthcare professionals can provide greater benefit than a warning of the possibility of increased laxity with the implementation of a training program that focuses on balancing lower limb musculature strength as a preventative measure.

References

(1.) Zazulak B, Paterno M, Myer G et al. The effects of the menstrual cycle on anterior knee laxity: a systematic review. Sports Med. 2006; 36(10):847-862.

(2.) Hewett T, Zazulak B, Myer G. Effects of the menstrual cycle on anterior cruciate ligament injury risk: a systematic review. Am J Sports Med. 2007; 35(4): 659-668.

(3.) Hewett T, Myer G, Ford K. Anterior cruciate ligament injuries in female athletes: Part 1, mechanisms and risk factors. Am J Sports Med. 2006; 34(2):299-311.

(4.) Elliot D, Goldberg L, Kuehl K. Young women's anterior cruciate ligament injuries: an expanded model and prevention paradigm. Sports Med. 2010; 40(5):367-376.

(5.) Wreje U, Kristiansson P, Aberg H et al. Serum levels of relaxin during the menstrual cycle and oral contraceptive use. GynecolObstert Invest. 1995; 39(3): 197-200.

(6.) Mathor M, Achado S, Wajchenberg B et al. Free plasma testosterone levels during the normal menstrual cycle. J Endocrinol Invest. 1985; 8(5), 437-441.

(7.) Yu W, Liu S, Hatch J et al. Effect of estrogen on cellular metabolism of the human anterior cruciate ligament. Clin Orthop 1999; 366: 229-238.

(8.) Ruedl G, Ploner P, Linortner I et al. Are oral contraceptive use and menstrual cycle phase related to anterior cruciate ligament injury risk in female recreational skiers? Knee Surg Sport Tr A. 2009; 17(9):1065-1069.

(9.) Van Lunen B, Roberts J, Branch J et al. Association of menstrual-cycle hormone changes with anterior cruciate ligament laxity measurements. J Athlet Train. 2003; 38(4): 298.

(10.) Belanger M, Moore D, Crisco J et al. Knee laxity does not vary with the menstrual cycle, before or after exercise. Am J Sports Med. 2004; 32(5):1150-1157.

(11.) Sackett DC, Willams MC, Rosenbery JA. Evidence base Medicine: What is it and what it isn't. BMJ. 1996; 312:7172.

(12.) Ruedl G, Ploner P, Linortner I et al. Are oral contraceptive use and menstrual cycle phase related to anterior cruciate ligament injury risk in female recreational skiers? Knee Surg Sports Tr A. 2009; 29(17):1065-1069.

(13.) Adachi N, Nawata K, Maeta M et al. Relationship of the menstrual cycle phase to anterior cruciate ligament injuries in teenaged female athletes. Arch Orthop Trauma Surg. 2008; 128:473-478.

(14.) Wojtys E, Huston L, Lindenfeld T et al. Association between the menstrual cycle and anterior cruciate ligament injuries in female athletes. Am J Sport Med. 1998; 26: 614-619.

(15.) Park SK, Stefanyshyn D, Loitz-Ramage B et al. Changing hormone levels during the menstrual cycle affect knee laxity and stiffness in healthy female subjects. Am J Sport Med. 2009; 37: 588-598.

(16.) Beynnon B, Johnson R, Braun S et al. The relationship between menstrual cycle phase and anterior cruciate ligament injury: A case-control study of recreational alpine skiers. Am J Sport Med. 2006; 34:757-764.

(17.) Shultz S, Gansneder B, Sander T et al. Absolute serum hormone levels predict the magnitude of change in anterior knee laxity across the menstrual cycle. J Ortho Res. 2006; 24:124-131.

(18.) Deie M, Sakamaki Y, Sumen Y et al. Anterior knee laxity in young women varies with their menstrual cycle. Int Orthop. 2002; 5(26):154-156.

(19.) Park S, Stefanyshyn D, Ramage B et al. Relationship between knee joint laxity and knee joint mechanics during the menstrual cycle. Br J Sports Med. 2009; 43: 174-179.

(20.) Eiling E, Bryant A, Petersen W et al. Effects of menstrual-cycle hormone fluctuations on musculotendinous stiffness and knee joint laxity. Knee Surg Sport Tr A. 2007; 15:126-132.

(21.) Pollard C, Braun B, Hamill J. Influence of gender, estrogen and exercise on anterior knee laxity. Clin Biomech. 2006; 21:1060-1066.

(22.) Abt J, Sell T, Laudner K et al. Neuromuscular and biomechanical characteristics do not vary across the menstrual cycle. Knee Surg Sports Tr A. 2007; 15:901-907.

(23.) Hertel J, Williams N, Olmsted-Kramer L et al. Neuromuscular performance and knee laxity do not change across the menstrual cycle in female athletes. Knee Surg Sports Tr A. 2006; 14: 817-822.

(24.) Park SK, Stefanyshyn D, Ramage B, Hart D, Ronsky J. Alterations in knee joint laxity during the menstrual cycle in healthy women leads to increases in joint loads during selected athletic movements. Am J Sports Med. 2009; 37:1169-1177.

Lesley Belanger, BA, DC

Dawn Burt, BSc (Hons), DC

Julia Callaghan, BSc (Hons), DC

Sheena Clifton, BSc, DC

Brian J. Gleberzon, DC, MHSc *

* Professor & Chair, Department of Chiropractic Therapeutics, CMCC 6100 Leslie St, Toronto, Ontario. M2H 3J1


Table 1:
Instrument Categories Used to Grade Articles for this Review

Grading Criteria:

Baseline values of          No mention of baseline values    score 0;
groups (/8)                 baseline values mentioned but    score 4;
                            not statistically significant
                            baseline values mentioned and    score 8.
                            not statistically significant

Relevance of outcomes       No mention of outcomes and       score 0;
and clinical significance   clinical significance
(/7)                        subjective outcome measures      score 3;
                            objective outcome measures       score 5;
                            both subjective and objective    score 7.
                            outcome measures

Prognostic stratification   No clear mention of study        score 0;
(comorbidity and risk       inclusion or exclusion
factors) (/6)               criteria
                            inadequate mention of            score 3;
                            inclusion or exclusion
                            criteria
                            complete mention and             score 6.
                            description of inclusion
                            and exclusion criteria

Blinding strategies (/5)    No blinding strategies           score 0;
                            mentioned
                            single blinded study without     score 2;
                            method described and
                            appropriate
                            single blinded study with        score 3;
                            method described and
                            appropriate
                            double blinded study without     score 4;
                            method described and
                            appropriate
                            double blinded study with        score 5.
                            method described and
                            appropriate

Contamination/              No mention of ways to control    score 0;
co-intervention (/4)        for contamination or
                            co-intervention
                            some patients received some      score 2;
                            sort of contamination or
                            co-intervention assumed that
                            no contamination or
                            co-intervention took place
                            due to immediate follow-up       score 3;

                            contamination and                score 4.
                            co-intervention closely
                            monitored and accounted for

Compliance of subjects      No mention or detail given       score 0;
to study procedures (/4)    to compliance of study
                            subjects
                            compliance and                   score 1;
                            co-intervention of patients
                            monitored but not closely
                            monitored
                            some patients were compliant     score 2;
                            and did not receive co
                            -interventions and was
                            closely monitored and
                            detailed
                            compliance of subjects was       score 3;
                            assumed due to immediate
                            follow-up
                            all patients were compliant      score 4.
                            and closely monitored and
                            detailed

Drop-out rates              No mention of drop-out rates     score 0;
of subjects (/3)            drop-out rates mentioned         score 1;
                            no drop-out rates assumed        score 2;
                            due to immediate follow-up
                            number and reason for drop       score 3.
                            -outs described

Publication date of         Published prior to 2000          score 0;
research                    published after 2000             score 1.

Total Score: /38

Table 3:

                        Beynnon   Eiling   Shultz   Park et al.
                        et al.    et al.   et al.      2009
                         2006      2007     2005       AJSM
                         AJSM     KSSTA     JOR        37(6)

Baseline Values            8        8        4           8
  of Groups (/8)
Relevance of Outcomes      7        7        5           5
  & Clinical
  Significance (/7)
Prognostic                 6        6        6           3
  Stratification
  (Comorbidity and
  Risk factors) (/6)
Blinding                   0        3        3           0
  Strategies (/5)
Contamination/             3        2        4           4
  Co-Intervention
  (/4)
Compliance of              3        0        1           1
  Subjects to Study
  Procedures (/4)
Drop-out Rates of          2        0        1           1
  Subjects (/3)
Date of Publication        1        1        1           1
Total (/38)               30        27       25         23

                        Ruedl    Adachi   Pollard    Deie    Hertel
                        et al.   et al.   et al.    et al.   et al.
                         2009     2008     2006      2002     2006
                        KSSTA     AOTS      CB        IO     KSSTA

Baseline Values           8        4         4        8        4
  of Groups (/8)
Relevance of Outcomes     3        3         5        5        7
  & Clinical
  Significance (/7)
Prognostic                6        6         6        3        3
  Stratification
  (Comorbidity and
  Risk factors) (/6)
Blinding                  0        0         0        0        0
  Strategies (/5)
Contamination/            0        3         4        0        0
  Co-Intervention
  (/4)
Compliance of             3        3         0        0        1
  Subjects to Study
  Procedures (/4)
Drop-out Rates of         2        2         0        3        3
  Subjects (/3)
Date of Publication       1        1         1        1        1
Total (/38)               23       22       20        20       19

                         Abt     Wojtys    Park     Park
                        et al.   et al.   et al.   et al.
                         2007     1998     2009     2008
                        KSSTA     AJSM     AJSM     BJSM

Baseline Values           4        4        4        4
  of Groups (/8)
Relevance of Outcomes     5        3        5        5
  & Clinical
  Significance (/7)
Prognostic                6        3        3        3
  Stratification
  (Comorbidity and
  Risk factors) (/6)
Blinding                  0        0        0        0
  Strategies (/5)
Contamination/            0        2        2        0
  Co-Intervention
  (/4)
Compliance of             0        3        0        0
  Subjects to Study
  Procedures (/4)
Drop-out Rates of         3        2        0        0
  Subjects (/3)
Date of Publication       1        0        1        1
Total (/38)               19       17       15       13

* AJSM--American Journal of Sports Medicine

* KSSTA--Knee Surgery, Sports Traumology, Arthroscopy

* AOTS--Archives of Orthopaedic and Trauma Surgery

* BJSM--British Journal of Sports Medicine

* CB--Clinical Biomechanics

* IO--International Orthopaedics

* JOR--Journal of Orthopedic Research

Table 4a:

Studies Investigating ACL Laxity

Reference         Objective              Study Design      Score/38

Eiling et al      1. To examine          Cross-sectional   27
  2007            changes in             Study
                  lower limb
                  musculotendinous
                  stiffness (MTS)
                  over the course
                  of the menstrual
                  cycle

                  2. Investigate the
                  interaction of
                  warm-up on
                  MTS

Schultz et al     To investigate         Cross-sectional   25
  2005            if hormone             study
                  levels across the
                  menstrual cycle
                  can affect
                  anterior knee
                  laxity

Park et al        To investigate         Controlled        23
  2009            whether the            laboratory
  (Alterations    hormonal cycle         study.
  in knee         has an influence
  joint...)       on knee joint
                  mechanism and
                  whether increased
                  knee joint loading
                  during the
                  menstrual cycle
                  affects knee joint
                  mechanics.

Pollard et al     To investigate the     Observational     20
  2006            collective effects     Study
                  of gender, estrogen
                  and exercise on
                  anterior knee
                  laxity in active
                  individuals

Deie et al        To determine           Case-Control      20
  2002            whether ACL laxity     study.
                  in women changes
                  significantly
                  during their
                  menstrual cycles

Hertel et al      To investigate         Cross-sectional   19
  2006            changes in             study.
                  neuromuscular
                  control and
                  laxity at the
                  knee across the
                  menstrual cycle

Abt et al         To determine if        Cross-sectional   19
  2007            changes in the         study.
                  levels of
                  estradiol and
                  progesterone
                  significantly
                  alter fine motor
                  coordination,
                  postural
                  stability knee
                  strength and knee
                  joint kinematics
                  and kinetics
                  between the menses,
                  post-ovulatory,
                  and mid-luteal
                  phases of the
                  menstrual cycle.

Park et al        To determine           Observational     15
  2009            whether changing       Study
                  hormone levels
                  influence joint
                  laxity and stiffness
                  of a non-contractile
                  knee joint and knee
                  joint structures
                  using a new
                  analysis technique.
                  To determine
                  whether subsets of
                  women exist who
                  demonstrate or do
                  not demonstrate
                  changes in knee
                  laxity in response
                  to circulating
                  hormone levels
                  throughout their
                  menstrual cycle.

Park et al        To investigate         Cross-sectional   13
  2009            whether changing       study
  (Relationship   knee laxity during
  between.)       the menstrual cycle
                  correlates with
                  changing knee joint
                  loads in a cutting
                  maneuver

Reference         Patients/Conditions

Eiling et al      11 adolescent females.
  2007            Played netball for minimum 5 yrs.

                  * eight A-grade players and state
                  representatives

                  * two B-grade players and two
                  C-grade players
                  The average age, height and
                  weight of the subjects was:

                  * 16.3 [+ or -] 0.65 years

                  * 164.12 [+ or -] 6.2 cm and 60.72
                  [+ or -] 6.3 kg
                  Trained min 2 hrs per week.
                  Consistent menstrual cycles for
                  3 mths.

                  Menarche >1 yr ago.
                  No use of contraceptives or other
                  hormones for 3 mths.
                  No history of serious lower limb
                  injury.
                  Normal joint ROM.

Schultz et al     22 females with normal
  2005            self-reported menstrual history in
                  the previous 6 months
                  Between the ages of 18 and 30,
                  with a body mass index (BMI =
                  weight/height2) less than or equal
                  to 30 Inclusion:

                  * no history of pregnancy

                  * no use of oral contraceptives
                  or other hormone-stimulating
                  medications for 6 months

                  * non-smoking behavior

                  * two healthy knees with no prior
                  history of joint injury or surgery,
                  no medical conditions affecting
                  the connective tissue

                  * physical activity limited to 7 h
                  or less per week.
                  Exclusion:

                  * experienced an anovulatory
                  cycle or missed three or more
                  consecutive days of testing
Park et al        26 healthy women:
  2009
  (Alterations    * age 22.7 [+ or -] 3.3 years
  in knee
  joint...)       * height, 170.1 [+ or -] 7.1 cm

                  * mass, 65.0 [+ or -] 9.3 kg

                  * body mass index (BMI), 22.4
                  [+ or -] 2.5

                  * average menstrual cycle, 28.9
                  [+ or -] 2.7 days

                  * activity level, 8.7 [+ or -] 4.4
                  h/wk Inclusion:

                  * required that the subject have a
                  normal menstrual cycle

                  * no history of oral contraceptive
                  use, and no previous knee injury
                  Refrain from exercise 6 hrs prior to
                  testing.
Pollard et al     12 women: age 24.8 years
  2006            12 men: age 24.3 years

                  -- All 24 men and women had a
                  history of participating in high
                  school and/or recreational cutting
                  and landing sports which included
                  basketball, volleyball, field hockey
                  and soccer.

                  -- Inclusion criteria: subjects had
                  to have performed moderate
                  exercise at least 4 times a
                  week for at least 45 mins in
                  duration for 2 months prior to
                  participation in the study, had
                  to have no history of significant
                  lower extremity injury, were
                  injury-free at the time of data
                  collection, females had to have
                  not taken oral contraceptives
                  for the past 6 months and had
                  experienced a normal 27-31 day
                  cycle for the past 3 months.

                  -- Exclusion: if they had
                  participated in collegiate level
                  athletics at any time

Deie et al        16 women, aged 21-23 (average
  2002            age of 21.6 years)
                  8 men No BCP
                  Regular menses (28[+ or -]4 days)
                  No previous knee injury

Hertel et al      -- 14 female collegiate athletes
  2006
                  * age 19.3 [+ or -] 1.3 years

                  * height 163.6 [+ or -] 8.5 cm

                  * mass 59.4 [+ or -] 6.8 kg.

                  -- normal ovulatory menstrual
                  cycles (28-35 day cycles) with
                  confirmed ovulation

                  -- not taking oral contraceptives

                  -- no history of serious knee injury

                  -- Subjects participated in either
                  competitive soccer or stunt
                  cheerleading

Abt et al         10 physically active females were
  2007            recruited from the local university

                  * Age: 21.4 [+ or -] 1.4 years

                  * Height: 1.67 [+ or -] 0.06 m

                  * Mass: 59.9 [+ or -] 7.4 kg
                  who do not use oral
                  contraceptives.

                  -- subjects were screened for:

                  * history of injury

                  * nutritional practices

                  * menstrual dysfunction

                  * thyroid dysfunction, and
                  physical activity.
                  Exclusion:

                  * mid-luteal progesterone level
                  less than 10 ng/ml

                  * history of serious knee injury
                  or other lower extremity injury
                  within the prior 6 months

                  * previous or current eating
                  disorder

                  * previous or current menstrual
                  dysfunction

Park et al        26 women
  2009
                  * age, 22.7 [+ or -] 3.3 years

                  * height, 170.1 [+ or -] 7.1 cm

                  * mass, 65.0 [+ or -] 9.3 kg

                  * body mass index (BMI), 22.4
                  [+ or -] 2.5

                  * average menstrual cycle, 28.9
                  [+ or -] 2.7 days

                  * and activity level, 8.7 [+ or -]
                  4.4 h/wk.

                  * Most subjects regularly
                  participated in a sports activity
                  at a recreational level.
                  Inclusion:

                  * no previous knee injuries

                  * never been pregnant

                  * have regular menstrual cycles
                  (approximately 28 days) with no
                  missed cycles over the previous 24
                  months

                  * no oral contraceptive use for the
                  previous 6 months
Park et al        25 healthy women:
  2009
  (Relationship   * mean age 22.7 years
  between.)
                  * height 170.2 cm

                  * mass 64.7 kg

                  * body mass index 22.3 menstrual
                  cycle 28.9 days

                  * activity levels 8.7 h/week
                  The subjects regularly participated
                  in sports activity at a recreational
                  level.
                  Inclusion:

                  * a normal menstrual cycle

                  * no history of oral contraceptive
                  use

                  * no knee injury within the
                  preceding 6 months

Reference         Methods

Eiling et al      Subjects documented menstrual
  2007            history for 3 months prior and post
                  testing,
                  Each subject tested at each of the
                  4 phases of the cycle:

                  -- blood levels for LH, FSH,
                  estradiol and progesterone.

                  -- ACL laxity using KT-2000.

                  -- MTS assessed before and after
                  5 min cycling warm up using
                  unilateral hopping on force
                  plate.

Schultz et al     Measured blood levels of estradiol,
  2005            progesterone and testosterone.
                  Then measured knee joint laxity
                  with an arthrometer

Park et al        Blood samples drawn at 3 different
  2009            phases of the menstrual cycle in
  (Alterations    each subject.
  in knee         Knee joint loading was then
  joint...)       measured during each phase using
                  the KT-2000 arthrometer.
                  Motion analysis testing of the knee
                  was then performed.

Pollard et al     All subjects came to the lab
  2006            prior to data collection for a
                  pre-collection session to familiarize
                  them with the KT-1000. Female
                  subjects were given ovulation kits
                  that detect the surge of LH
                  immediately preceding ovulation
                  to determine the time of ovulation.
                  Each completed an informed consent
                  and was instructed to refrain from
                  exercise prior to data collection on
                  that day. Females assigned to start
                  data collection at the onset of
                  menses or the onset of ovulation and
                  completed 5 day data collections
                  following the same protocol each
                  which occurred at a specific time to
                  correlate with different phases of
                  the menstrual cycle--onset menses,
                  10 and 12 days post onset, 7 and 9
                  days post ovulation. Male subjects
                  started collection on a day of
                  convenience and completed 3 data
                  collections following the same
                  protocol as females, 10-12 days
                  apart

Deie et al        Measurements of their knees
  2002            using KT-2000 arthrometer were
                  performed 2-3 times every week over
                  4 consecutive weeks. Women measured
                  their basal body temp daily for 4
                  weeks and estradiol and progesterone
                  levels in their blood weekly. From
                  their BBT or estradiol and
                  progesterone levels the follicular,
                  ovulatory, and luteal phases were
                  delineated. 342 measurements were
                  made. 158 measurements = follicular
                  phase, 56 = ovulatory, 128 = luteal
                  phase
                  -- Men's measurements of their
                  knees using KT-2000 were
                  performed 3 times a week
                  over a 3 week period. 144
                  measurements were taken
                  with 48 measurements in each
                  of the first, second and third
                  phases (based on when the
                  measurement was taken in
                  what week)
Hertel et al      Urine hormone levels and
  2006            ovulation measured.
                  Neuromuscular performance and
                  laxity of knee were measured in
                  each phase of the cycle.

Abt et al         Measured single leg postural
  2007            stability, fine motor coordination,
                  knee strength, knee biomechanics,
                  and serum estradiol and
                  progesterone.

Park et al        Each completed a blood draw
  2009            and laxity tests at 3 different
                  times during her menstrual cycle.
                  Blood samples were collected to
                  determine the levels of estradiol
                  and progesterone, indicating an
                  appropriate phase of testing.
                  Passive laxity and stiffness were
                  measured using arthrometer

Park et al        Serum hormone concentrations
  2009            were assessed and knee joint laxity
  (Relationship   was measured during the follicular,
  between.)       ovulation and luteal phases.
                  Performed 10 trials of a cutting
                  maneuver.

Reference         Main Outcome Measures

Eiling et al      1. Blood levels LH, FSH, estradiol
  2007            and progesterone.

                  * The levels were analysed
                  which allowed the levels to be
                  matched with the testing date

                  * If the values of the hormone
                  analysis were not within
                  the documented ranges for
                  the specific phase, it was
                  assumed that either the
                  test date was miscalculated
                  or that the cycle was
                  anovulatory

                  * In both cases, the subject was
                  re-tested for that particular
                  phase in the subsequent
                  cycle.

                  2. KT-2000

                  * The knee was placed in 30
                  deg. of flexion as the subject
                  lay supine on a bench

                  3. Force plate

                  * Following a warm-up of
                  5 min of cycling at 50 W
                  together with ten run-ups
                  and netball landings subjects
                  were instructed to perform a
                  unilateral hop on a force plate
                  in time with a metronome at
                  a frequency of 2.2 Hz
Schultz et al     Minimum and peak levels of
  2005            blood estradiol, progesterone,
                  and testosterone.
                  Knee laxity using an arthrometer

Park et al        Blood serum estradiol and
  2009            progesterone.
  (Alterations    KT-2000
  in knee
  joint...)

Pollard et al     Exercise:
  2006
                  * Subjects ran on a treadmill for
                  15 min at a self-selected pace.

                  * The subject was asked to set
                  the pace to correspond to what
                  they would consider "moderately
                  hard". Once this pace was
                  established, it was used
                  throughout the rest of the data
                  collections.

                  * For each subsequent treadmill
                  run, the subject was instructed
                  to warm up during the first three
                  minutes and to reach the
                  predetermined pace by the end of
                  3 min.

                  * immediately following the
                  treadmill run, subjects were
                  instructed to perform three
                  dynamic lower extremity tasks
                  consisting of the following: two
                  minutes of weaving (grapevine)
                  along a 20 m long runway; two
                  minutes of left and right cutting
                  along 2 m wide runway; and, 25
                  jump downs from a 46 cm step.
                  KT-1000 arthrometer.
                  Blood samples: looking at
                  estrogen levels across the
                  menstrual cycles
Deie et al        Arthrometer
  2002            Basal body temp
                  Blood samples

Hertel et al      Hormone levels.
  2006            Peak flexion and extension torque.
                  Hamstring: quadriceps strength.
                  Joint position sense.
                  Centre of pressure velocity.
                  Anterior knee laxity.

Abt et al         Estradiol
  2007            Progesterone
                  Fine motor coordination
                  Postural stability
                  Hamstring: quad strength
                  Knee flexion and valgus excursion
                  Peak proximal ant tibial shear
                  force Flexion and valgus moments
                  at peak proximal ant tibial shear
                  force

Park et al        Self reported menstrual history
  2009            Arthrometer

                  Measured for estradiol and
                  progesterone

Park et al        Knee joint laxity
  2009            Peak knee angle
  (Relationship   Knee joint moment
  between.)       Knee joint impulse
                  Blood hormone levels

Reference         Main Results/Conclusions

Eiling et al      No statistically significant
  2007            effect of the menstrual
                  cycle on anterior knee
                  laxity.

                  MTS significantly
                  decreased following
                  warm up.

                  * Repeated measures
                  ANOVA revealed
                  significant (P < 0.05)
                  main effects of
                  test-session and
                  warm-up on MTS for the
                  dominant leg.

                  * MTS was found to
                  significantly decrease
                  by 4.2% following the
                  warm-up intervention
                  It was significantly lower
                  during the ovulatory
                  phase compared to day
                  one of menstruation and
                  mid-follicular phase, 8.7
                  and 4.5%.

Schultz et al     The minimum
  2005            concentrations of estradiol
                  and progesterone in the
                  early follicular phase
                  are important factors in
                  determining sensitivity of
                  the knee joint's response
                  to changing hormone
                  levels.
                  When minimum
                  progesterone
                  concentrations were
                  higher and minimum
                  estradiol concentrations
                  were lower during the
                  early follicular phase,
                  females experienced
                  greater increases in knee
                  laxity across the menstrual
                  cycle with attainment
                  of peak estradiol and
                  testosterone levels post
                  ovulation.
Park et al        No significant difference
  2009            in knee joint mechanics
  (Alterations    between phases. However,
  in knee         increased knee joint laxity
  joint...)       was associated with higher
                  knee joint loads during
                  movements.

Pollard et al     Knee laxity increased
  2006            following exercise but did
                  not differ across genders.

Deie et al        In men, no statistical
  2002            significance with anterior
                  movement through the 3 week
                  period. In women, anterior
                  or terminal stiffness was
                  higher in the follicular
                  phase than the ovulatory
                  phase, which was in turn
                  higher than the luteal
                  phase.

Hertel et al      Neuromuscular control
  2006            and knee joint laxity do
                  not change substantially
                  across the menstrual cycle
                  despite varying estrogen
                  and progesterone levels.

Abt et al         Neuromuscular
  2007            and biomechanical
                  characteristics are not
                  influenced by estradiol
                  and progesterone
                  fluctuations

Park et al        Lowest hormones in
  2009            follicular phase, highest in
                  luteal phase

                  Lowest estradiol and
                  progesterone were in
                  follicular and highest were
                  in luteal phase

                  -- Greater knee laxity at
                  89N was recorded in
                  ovulation compared to
                  luteal phase

                  -- Max knee laxity during
                  ovulation significantly
                  exceeded max laxity during
                  follicular phase

Park et al        Increased knee laxity
  2009            was observed during
  (Relationship   ovulation compared with
  between.)       the luteal phase, but no
                  significant changes in knee
                  mechanics corresponding
                  to menstrual phases were
                  found.

Table 4b:

Studies Investigating ACL Injury

Reference   Objective              Study Design    Score/38

Beynnon     To determine the       Case-control    30
  et al     relationship between   study
  2006      the menstrual cycle
            and ACL injury

Ruedl       1. investigate a       Case-control    23
  et al     possible protective    Study
  2009      effect of oral
            contraceptive use
            against ACL injuries
            in rec. skiers
            2. compare the
            frequencies of
            non-contact ACL
            injuries in the
            preovulatory phase
            with that in the
            postovulatory phase

Adachi      To determine if        Case-control    22
  et al     non-contact ACL        Study
  2008      injuries occurred
            randomly or
            correlate with a
            specific phase of
            the menstrual
            cycle in teenaged
            female athletes

Wojtys      To investigate         Observational   17
  et al     the variation in       Study
  1998      ACL injury rates
            during the female
            monthly cycle

Reference   Patients/Conditions

Beynnon     200 subjects, female only
  et al
  2006

Ruedl       93 females With non-contact
  et al      ACL injuries 93 female
  2009      recreational skiers with a
            non-contact ACL injury and
            93 age matched controls

Adachi      18 females aged 11-18
  et al     ACL injury (non-contact)
  2008      confirmed by MRI.
            No history of pregnancy.
            No use of oral
            contraceptives or hormone
            stimulating meds.
            Consistent menstrual cycle
            last 6 months.
            Competitive or recreational
            athlete.

Wojtys      28 women with ACL tears
  et al     in the last 3 months.
  1998

Reference   Methods

Beynnon     Direct measurement of blood
  et al     concentrations of progesterone
  2006      and estradiol at time of
            injury. Self reported menstrual
            history.

Ruedl       MRI was used to diagnose ACL
  et al     injury. Only non-contact ACL
  2009      injuries were included. On and
            off pill users were included.
            Female recreational alpine
            skiers are treated in a ski
            clinic, which is located in
            close proximity to the ski
            resort.

Adachi      Subjects completed a
  et al     questionnaire that documented
  2008      injury history, menstrual
            history and activity level at
            each phase of the cycle to
            determine in which phase their
            injury occurred.

Wojtys      Women with a history of either
  et al     irregular or missed menstrual
  1998      cycles were excluded and only
            patients with noncontact ACL
            injuries were included.

            -- 28 met these criteria and
            were asked to fill out a
            questionnaire and provide
            their age, height, weight,
            level and freq. of sports
            participation, and previous
            knee injuries. Asked to
            document the date and mechanism
            of acute ACL injury, including
            the number of minutes played
            before the injury occurred,
            whether the injury occurred
            during a practice or game and
            the nature of the ACL injury.
            Each woman was asked to provide
            a detailed history of her
            menstrual cycle, frequency and
            regularity, date of last
            period and average length,
            premenstrual symptoms and oral
            contraceptive or hormone
            replacement use.

Reference   Main Outcome Measures

Beynnon     Serum levels of progesterone
  et al     and estradiol. Menstrual
  2006      history.

Ruedl       Questionnaire, with
  et al     information on:
  2009
            * Age

            * Height

            * Weight

            * Previous knee injuries
            of either leg
            A second questionnaire
            developed and validated by
            Wojtys et al. was used:

            * age at the start of
            menstruation

            * date of last menstruation

            * average length of
            menstruation

            * the use of oral
            contraceptives
Adachi      Questionnaire:
  et al
  2008      * injury history

            * menstrual history

            * subjective activity
            levels on each phase of the
            menstrual cycle

            A second questionnaire
            developed by Wojtys et al.
            was used to document:

            * age

            * height

            * weight

            * detailed history of the
            menstrual cycle (including
            frequency and regularity,
            date of last menstrual
            period, average length of
            cycle, premenstrual and
            menstrual symptoms, and
            oral contraceptives)
Wojtys      Questionnaire:
  et al
  1998      * age

            * height

            * weight

            * level and frequency of
            sports participation

            * previous knee injuries

            * date and mechanism of the
            acute ACL injury (including
            the number of minutes
            played before the injury
            occurred, whether the injury
            occurred during a practice
            or game situation, and the
            nature of the ACL injury

            * history of menstrual cycle
            (frequency, regularity, date
            of last menstrual period,
            average length of cycle,
            premenstrual symptoms, and
            oral contraceptive use

Reference   Main Results/Conclusions

Beynnon     The risk of sustaining an
  et al     ACL tear increases during
  2006      the pre-ovulatory phase
            of the menstrual cycle as
            compared to the
            post-ovulatory phase (3x)
Ruedl       ACL injury is greater in
  et al     the pre-ovulatory phase.
  2009      Use of oral contraceptives
            and previous knee injuries
            showed no association with
            ACL injury rate.

Adachi      Significant statistical
  et al     association was found
  2008      between the phase of
            the menstrual cycle and
            time of ACL injuries.
            More injuries occurred
            during the ovulation
            phase (72%). Few
            injuries in luteal and
            follicular phases.

Wojtys      The association
  et al     between the ovulatory
  1998      phase and the rate of
            ACL injury is statistically
            significant. Further
            information needed.
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Article Details
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Author:Belanger, Lesley; Burt, Dawn; Callaghan, Julia; Clifton, Sheena; Gleberzon, Brian J.
Publication:Journal of the Canadian Chiropractic Association
Article Type:Report
Geographic Code:1CANA
Date:Jan 1, 2013
Words:7162
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