Effect of Estrogen on Musculoskeletal Performance and Injury Risk

Nkechinyere Chidi-Ogbolu, Keith Baar, Nkechinyere Chidi-Ogbolu, Keith Baar

Abstract

Estrogen has a dramatic effect on musculoskeletal function. Beyond the known relationship between estrogen and bone, it directly affects the structure and function of other musculoskeletal tissues such as muscle, tendon, and ligament. In these other musculoskeletal tissues, estrogen improves muscle mass and strength, and increases the collagen content of connective tissues. However, unlike bone and muscle where estrogen improves function, in tendons and ligaments estrogen decreases stiffness, and this directly affects performance and injury rates. High estrogen levels can decrease power and performance and make women more prone for catastrophic ligament injury. The goal of the current work is to review the research that forms the basis of our understanding how estrogen affects muscle, tendon, and ligament and how hormonal manipulation can be used to optimize performance and promote female participation in an active lifestyle at any age.

Keywords: ACL; estrogen; exercise; injury risk; ligament; muscle; tendon.

Figures

Figure 1
Figure 1
Hormonal fluctuation during (A) a normal menstrual cycle, (B) while taking an oral contraceptive (OC) containing both estrogen and progesterone, and (C) in the years before and after menopause.
Figure 2
Figure 2
Relationship between estrogen and ACL rupture in a normal cycle. The rate of anterior cruciate ligament (ACL) rupture in relation to female hormones throughout a standard menstrual cycle. Note that with the ovulatory rise in estrogen there is a concomitant rise in ACL ruptures. Adapted from Wojtys et al. (2002).
Figure 3
Figure 3
High estrogen decreasing engineered ligament stiffness due to inhibition of lysyl oxidase. (A) Collagen content, (B) tangent modulus, and (C) lysyl oxidase (LOX) activity in ligaments engineered from human ACL cells isolated from women following 24 or 48 h of treatment of the constructs with physiologically high (500 pg/ml) of estrogen. Note that even though there is a slight rise in collagen, the stiffness of the grafts decreases concomitant with an increase in estrogen in the media. *indicates different than control (p < 0.05), whereas †indicates different than 24 h (p < 0.05). Adapted from Lee C. A. et al. (2015).
Figure 4
Figure 4
Differential measures of collagen incorporation and synthesis with estrogen replacement and exercise. The rate of (A) collagen incorporation of proline into the patellar tendon or (B) the appearance of the N-terminal propeptide of collagen I in post-menopausal women ± estrogen replacement therapy (ERT) and exercise. Note that with ERT collagen incorporation is higher in the same women where collagen synthesis is repressed. Further, exercise tends to decrease collagen incorporation and synthesis in controls, whereas ERT users show no effect on incorporation or a large drop in collagen synthesis. Symbols (*P < 0.01, **P < 0.001) show significance determined by unpaired t-test Control vs. ERT. These data suggest that there is a large methodological discrepancy between the two measures. Adapted from Hansen et al. (2009b).

References

    1. Adachi N., Nawata K., Maeta M., Kurozawa Y. (2008). Relationship of the menstrual cycle phase to anterior cruciate ligament injuries in teenaged female athletes. Arch. Orthop. Trauma Surg. 128, 473–478. 10.1007/s00402-007-0461-1
    1. Arendt E., Dick R. (1995). Knee injury patterns among men and women in collegiate basketball and soccer: NCAA data and review of literature. Am. J. Sports Med. 23, 694–701. 10.1177/036354659502300611
    1. Baltgalvis K. A., Greising S. M., Warren G. L., Lowe D. A. (2010). Estrogen regulates estrogen receptors and antioxidant gene expression in mouse skeletal muscle. PLoS ONE 5:e10164. 10.1371/journal.pone.0010164
    1. Bamman M. M., Hill V. J., Adams G. R., Haddad F., Wetzstein C. J., Gower B. A., et al. . (2003). Gender differences in resistance-training-induced myofiber hypertrophy among older adults. J. Gerontol. Ser. A Biol. Sci. Med. Sci. 58, B108–B116. 10.1093/gerona/58.2.B108
    1. Barros R. P., Gustafsson J. Å. (2011). Estrogen receptors and the metabolic network. Cell Metabol. 14, 289–299. 10.1016/j.cmet.2011.08.005
    1. Bassey E. J., Fiatarone M. A., O'Neill E. F., Kelly M., Evans W. J., Lipsitz L. A. (1992). Leg extensor power and functional performance in very old men and women. Clin. Sci. 82, 321–327. 10.1042/cs0820321
    1. Beydoun H. A., Beydoun M., Wiggins N., Stadtmauer L. (2012). Relationship of obesity-related disturbances with LH/FSH ratio among post-menopausal women in the United States. Maturitas 71, 55–61. 10.1016/j.maturitas.2011.10.010
    1. Beynnon B. D., Johnson R. J., Braun S., Sargent M., Bernstein I. M., Skelly J. M., et al. . (2006). The relationship between menstrual cycle phase and anterior cruciate ligament injury: a case-control study of recreational alpine skiers. Am. J. Sports Med. 34, 757–764. 10.1177/0363546505282624
    1. Blackstock C. D., Higashi Y., Sukhanov S., Shai S. Y., Stefanovic B., Tabony A. M., et al. . (2014). Insulin-like growth factor-1 increases synthesis of collagen type I via induction of the mRNA-binding protein LARP6 expression and binding to the 5′ stem-loop of COL1a1 and COL1a2 mRNA. J. Biol. Chem. 289, 7264–74. 10.1074/jbc.M113.518951
    1. Bridgeman J. T., Zhang Y., Donahue H., Wade A. M., Juliano P. J. (2010). Estrogen receptor expression in posterior tibial tendon dysfunction: a pilot study. Foot Ankle Int. 31, 1081–1084. 10.3113/FAI.2010.1081
    1. Brockett C. L., David L. M., Proske U. W. E. (2004). Predicting hamstring strain injury in elite athletes. Med. Sci. Sports Exerc. 36, 379–387. 10.1249/01.MSS.0000117165.75832.05
    1. Camporez J. P., Jornayvaz F. R., Lee H. Y., Kanda S., Guigni B. A., Kahn M., et al. . (2013). Cellular mechanism by which estradiol protects female ovariectomized mice from high-fat diet-induced hepatic and muscle insulin resistance. Endocrinology 154, 1021–1028. 10.1210/en.2012-1989
    1. Carcia C. R., Shultz S. J., Granata K. P., Gansneder B. M., Perrin D. H. (2004). Knee ligament behavior following a controlled loading protocol does not differ by menstrual cycle day. Clin. Biomech. 19, 1048–1054. 10.1016/j.clinbiomech.2004.07.006
    1. Cauley J. A. (2015). Estrogen and bone health in men and women. Steroids 99, 11–15. 10.1016/j.steroids.2014.12.010
    1. Chen M. H., Hu C. K., Chen P. R., Chen Y. S., Sun J. S., Chen M. H. (2014). Dose-dependent regulation of cell proliferation and collagen degradation by estradiol on ligamentum flavum. BMC Musculoskel. Disord. 15:238. 10.1186/1471-2474-15-238
    1. Clarkson P. M., Monica J. H. (2002). Exercise-induced muscle damage in humans. Am. J. Phys. Med. Rehabil. 81, S52–S69. 10.1097/00002060-200211001-00007
    1. Cook J. L., Bass S. L., Black J. E. (2007). Hormone therapy is associated with smaller Achilles tendon diameter in active post-menopausal women. Scand. J. Med. Sci. Sports 17, 128–132. 10.1111/j.1600-0838.2006.00543.x
    1. Corman B., Duriez M., Poitevin P., Heudes D., Bruneval P., Tedgui A., et al. . (1998). Aminoguanidine prevents age-related arterial stiffening and cardiac hypertrophy. Proc. Natl. Acad. Sci. 95, 1301–1306. 10.1073/pnas.95.3.1301
    1. Cui J., Shen Y., Li R. (2013). Estrogen synthesis and signaling pathways during aging: from periphery to brain. Trends Mol. Med. 19, 197–209. 10.1016/j.molmed.2012.12.007
    1. Deie M., Sakamaki Y., Sumen Y., Urabe Y., Ikuta Y. (2002). Anterior knee laxity in young women varies with their menstrual cycle. Int. Orthop. 26, 154–156. 10.1007/s00264-001-0326-0
    1. Dieli-Conwright C. M., Spektor T. M., Rice J. C., Sattler F. R., Todd Schroeder E. (2009). Influence of hormone replacement therapy on eccentric exercise induced myogenic gene expression in postmenopausal women. J. Appl. Physiol. 107, 1381–1388. 10.1152/japplphysiol.00590.2009
    1. Dyer D. G., Dunn J. A., Thorpe S. R., Bailie K. E., Lyons T. J., McCance D. R., et al. . (1993). Accumulation of Maillard reaction products in skin collagen in diabetes and aging. J. Clin. Invest. 91, 2463–2469. 10.1172/JCI116481
    1. Edouard P., Branco P., Alonso J. M. (2016). Muscle injury is the principal injury type and hamstring muscle injury is the first injury diagnosis during top-level international athletics championships between 2007 and 2015. Br. J. Sports Med. 50, 619–630. 10.1136/bjsports-2015-095559
    1. Enns D. L., Tiidus P. M. (2010). The influence of estrogen on skeletal muscle. Sports Med. 40, 41–58. 10.2165/11319760-000000000-00000
    1. Finni T., Kovanen V., Ronkainen P. H., Pöllänen E., Bashford G. R., Kaprio J., et al. . (2009). Combination of hormone replacement therapy and high physical activity is associated with differences in Achilles tendon size in monozygotic female twin pairs. J. Appl. Physiol. 106, 1332–1337. 10.1152/japplphysiol.91439.2008
    1. Frank C. B. (2004). Ligament structure, physiology and function. J. Musculoskel. Neuronal Interact. 4, 199–201.
    1. Frontera W. R., Hughes V. A., Lutz K. J., Evans W. J. (1991). A cross-sectional study of muscle strength and mass in 45-to 78-yr-old men and women. J. Appl. Physiol. 71, 644–650. 10.1152/jappl.1991.71.2.644
    1. Gray A. M., Zbgniew G., Jacques G. B. (2016). Effects of oral contraceptive use on anterior cruciate ligament injury epidemiology. Med. Sci. Sports Exerc. 48, 648–654. 10.1249/MSS.0000000000000806
    1. Griffiths R. I. (1991). Shortening of muscle fibres during stretch of the active cat medial gastrocnemius muscle: the role of tendon compliance. J. Physiol. 436, 219–236. 10.1113/jphysiol.1991.sp018547
    1. Hägglund M., Markus W., Ekstrand J. (2009). Injuries among male and female elite football players. Scand. J. Med. Sci. Sports 19, 819–827. 10.1111/j.1600-0838.2008.00861.x
    1. Häkkinen K., Pakarinen A. (1993). Muscle strength and serum testosterone, cortisol and SHBG concentrations in middle-aged and elderly men and women. Acta Physiol. Scand. 148, 199–207. 10.1111/j.1748-1716.1993.tb09549.x
    1. Hama H., Yamamuro T., Takeda T. (1976). Experimental studies on connective tissue of the capsular ligament: influences of aging and sex hormones. Acta Orthop. Scand. 47, 473–479. 10.3109/17453677608988723
    1. Hammes H. P., Martin S., Federlin K., Geisen K., Brownlee M. (1991). Aminoguanidine treatment inhibits the development of experimental diabetic retinopathy. Proc. Natl. Acad. Sci. 88, 11555–11558. 10.1073/pnas.88.24.11555
    1. Hansen M. (2018). Female hormones: do they influence muscle and tendon protein metabolism?. Proc. Nutr. Soc. 77, 32–41. 10.1017/S0029665117001951
    1. Hansen M., Boesen A., Holm L., Flyvbjerg A., Langberg H., Kjaer M. (2013). Local administration of insulin-like growth factor-I (IGF-I) stimulates tendon collagen synthesis in humans. Scand. J. Med. Sci. Sports 23, 614–619. 10.1111/j.1600-0838.2011.01431.x
    1. Hansen M., Kjaer M. (2014). Influence of sex and estrogen on musculotendinous protein turnover at rest and after exercise. Exerc. Sport Sci. Rev. 42, 183–192. 10.1249/JES.0000000000000026
    1. Hansen M., Kjaer M. (2016). Sex hormones and tendon, Metabolic Influences on Risk for Tendon Disorders, ed Ackermann P., Hart D. A. (Cham: Springer; ), 139–149.
    1. Hansen M., Kongsgaard M., Holm L., Skovgaard D., Magnusson S. P., Qvortrup K., et al. . (2009b). Effect of estrogen on tendon collagen synthesis, tendon structural characteristics, and biomechanical properties in postmenopausal women. J. Appl. Physiol. 106, 1385–1393. 10.1152/japplphysiol.90935.2008
    1. Hansen M., Koskinen S. O., Petersen S. G., Doessing S., Frystyk J., Flyvbjerg A., et al. . (2008). Ethinyl oestradiol administration in women suppresses synthesis of collagen in tendon in response to exercise. J. Physiol. 586, 3005–3016. 10.1113/jphysiol.2007.147348
    1. Hansen M., Langberg H., Holm L., Miller B. F., Petersen S. G., Doessing S., et al. . (2011). Effect of administration of oral contraceptives on the synthesis and breakdown of myofibrillar proteins in young women. Scand. J. Med. Sci. Sports 21, 62–72. 10.1111/j.1600-0838.2009.01002.x
    1. Hansen M., Miller B. F., Holm L., Doessing S., Petersen S. G., Skovgaard D., et al. . (2009a). Effect of administration of oral contraceptives in vivo on collagen synthesis in tendon and muscle connective tissue in young women. J. Appl. Physiol. 106, 1435–1443. 10.1152/japplphysiol.90933.2008
    1. Hansen M., Skovgaard D., Reitelseder S., Holm L., Langbjerg H., Kjaer M. (2012). Effects of estrogen replacement and lower androgen status on skeletal muscle collagen and myofibrillar protein synthesis in postmenopausal women. J. Gerontol. Ser. A Biomed. Sci. Med. Sci. 67, 1005–1013. 10.1093/gerona/gls007
    1. Heikura I. A., Uusitalo A. L. T., Stellingwerff T., Bergland D., Mero A. A., Burke L. M. (2017). Low energy availability is difficult to assess but outcomes have large impact on bone injury rates in elite distance athletes. Int. J. Sport Nutr. Exerc. Metab. 28, 403–411. 10.1123/ijsnem.2017-0313
    1. Heitz N. A., Eisenman P. A., Beck C. L., Walker J. A. (1999). Hormonal changes throughout the menstrual cycle and increased anterior cruciate ligament laxity in females. J. Athl. Train. 34:144–149.
    1. Heldring N., Pike A., Andersson S., Matthews J., Cheng G., Hartman J., et al. . (2007). Estrogen receptors: how do they signal and what are their targets. Physiol. Rev. 87, 905–931. 10.1152/physrev.00026.2006
    1. Herzberg S. D., Motu'apuaka ML Lambert, W., Fu R., Brady J., Guise J-M. (2017). The effect of menstrual cycle and contraceptives on ACL injuries and laxity: a systematic review and meta-analysis. Orthop. J. Sports Med. 5:2325967117718781. 10.1177/2325967117718781
    1. Holmes G. B., Johnny L. (2006). Etiologic factors associated with symptomatic achilles tendinopathy. Foot Ankle Int. 27, 952–959. 10.1177/107110070602701115
    1. Irie T., Takahata M., Majima T., Abe Y., Komatsu M., Iwasaki N., et al. . (2010). Effect of selective estrogen receptor modulator/raloxifene analogue on proliferation and collagen metabolism of tendon fibroblast. Connect. Tissue Res. 51, 179–187. 10.3109/03008200903204669
    1. Kitajima Y., Ono Y. (2016). Estrogens maintain skeletal muscle and satellite cell functions. J. Endocrinol. 229, 267–75. 10.1530/JOE-15-0476
    1. Kjaer M. (2004). Role of extracellular matrix in adaptation of tendon and skeletal muscle to mechanical loading. Physiol. Rev. 84, 649–698. 10.1152/physrev.00031.2003
    1. Kjaer M., Langberg H., Heinemeier K., Bayer M. L., Hansen M., Holm L., et al. . (2009). From mechanical loading to collagen synthesis, structural changes and function in human tendon. Scand. J. Med. Sci. Sports 19, 500–510. 10.1111/j.1600-0838.2009.00986.x
    1. Kumar S., Lata K., Mukhopadhyay S., Mukherjee T. K. (2010). Role of estrogen receptors in pro-oxidative and anti-oxidative actions of estrogens: a perspective. Biochim. Biophys. Acta Gen. Subjects 1800, 1127–1135. 10.1016/j.bbagen.2010.04.011
    1. LaStayo P. C., Woolf J. M., Lewek M. D., Snyder-Mackler L., Reich T., Lindstedt S. L. (2003). Eccentric muscle contractions: their contribution to injury, prevention, rehabilitation, and sport. J. Orthop. Sports Phys. Ther. 33, 557–571. 10.2519/jospt.2003.33.10.557
    1. Laurent G. J. (1987). Dynamic state of collagen: pathways of collagen degradation in vivo and their possible role in regulation of collagen mass. Am. J. Physiol. Cell Physiol. 252, C1–C9. 10.1152/ajpcell.1987.252.1.C1
    1. Leblanc D. R., Schneider M., Angele P., Vollmer G., Docheva D. (2017). The effect of estrogen on tendon and ligament metabolism and function. J. Steroid Biochem. Mol. Biol. 172, 106–116. 10.1016/j.jsbmb.2017.06.008
    1. Lee C. A., Lee-Barthel A., Marquino L., Sandoval N., Marcotte G. R., Baar K. (2015). Estrogen inhibits lysyl oxidase and decreases mechanical function in engineered ligaments. J. Appl. Physiol. 118, 1250–1257. 10.1152/japplphysiol.00823.2014
    1. Lee C. Y., Liu X., Smith C. L., Zhang X., Hsu H. C., Wang D. Y., et al. . (2004a). The combined regulation of estrogen and cyclic tension on fibroblast biosynthesis derived from anterior cruciate ligament. Matrix Biol. 23, 323–329. 10.1016/j.matbio.2004.07.004
    1. Lee C. Y., Smith C. L., Zhang X., Hsu H. C., Wang D. Y., Luo Z. P. (2004b). Tensile forces attenuate estrogen-stimulated collagen synthesis in the ACL. Biochem. Biophys. Res. Commun. 317, 1221–1225. 10.1016/j.bbrc.2004.03.174
    1. Lee H., Jerrold S. P., JongEun Y. (2015). Do oral contraceptives alter knee ligament damage with heavy exercise? Tohoku J. Exp. Med. 237, 51–56. 10.1620/tjem.237.51
    1. Lee H., Petrofsky J. S., Daher N., Berk L., Laymon M., Khowailed I. A. (2013). Anterior cruciate ligament elasticity and force for flexion during the menstrual cycle. Med. Sci. Monit. 19, 1080–1088. 10.12659/MSM.889393
    1. Lefevre N, Bohu Y., Klouche S., Lecocq J., Herman S. (2013). Anterior cruciate ligament tear during the menstrual cycle in female recreational skiers. Orthop. Traumatol. Surg. Res. 99, 571–575. 10.1016/j.otsr.2013.02.005
    1. Ling-Ling E., Xu W. H., Feng L., Liu Y., Cai D. Q., Wen N., et al. (2016). Estrogen enhances the bone regeneration potential of periodontal ligament stem cells derived from osteoporotic rats and seeded on nano-hydroxyapatite/collagen/poly (L-lactide). Int. J. Mol. Med. 37, 1475–1486. 10.3892/ijmm.2016.2559
    1. Liu S. H., al-Shaikh R., Panossian V., Yang R. S., Nelson S. D., Soleiman N., et al. . (1996). Primary immunolocalization of estrogen and progesterone target cells in the human anterior cruciate ligament. J. Orthop. Res. 14, 526–533. 10.1002/jor.1100140405
    1. Liu S. H., Al-Shaikh R. A., Panossian V., Finerman G. A., Lane J. M. (1997). Estrogen affects the cellular metabolism of the anterior cruciate ligament: a potential explanation for female athletic injury. Am. J. Sports Med. 25, 704–709. 10.1177/036354659702500521
    1. Luo T., Kim J. K. (2016). The role of estrogen and estrogen receptors on cardiomyocytes: an overview. Can. J. Cardiol. 32, 1017–1025. 10.1016/j.cjca.2015.10.021
    1. Magnusson S. P., Hansen M., Langberg H., Miller B., Haraldsson B., Westh E. K., et al. . (2007). The adaptability of tendon to loading differs in men and women. Int. J. Exp. Pathol. 88, 237–240. 10.1111/j.1365-2613.2007.00551.x
    1. Mamalis A., Markopoulou C., Lagou A., Vrotsos I. (2011). Oestrogen regulates proliferation, osteoblastic differentiation, collagen synthesis and periostin gene expression in human periodontal ligament cells through oestrogen receptor beta. Arch. Oral Biol. 56, 446–455. 10.1016/j.archoralbio.2010.11.001
    1. Marturano J. E., Xylas J. F., Sridharan G. V., Georgakoudi I., Kuo C. K. (2014). Lysyl oxidase-mediated collagen crosslinks may be assessed as markers of functional properties of tendon tissue formation. Acta Biomater. 10, 1370–1379. 10.1016/j.actbio.2013.11.024
    1. McClung J. M., Davis J. M., Wilson M. A., Goldsmith E. C., Carson J. A. (2006). Estrogen status and skeletal muscle recovery from disuse atrophy. J. Appl. Physiol. 100, 2012–2023. 10.1152/japplphysiol.01583.2005
    1. Miller B. F., Hansen M., Olesen J. L., Flyvbjerg A., Schwarz P., Babraj J. A., et al. . (2006). No effect of menstrual cycle on myofibrillar and connective tissue protein synthesis in contracting skeletal muscle. Am. J. Physiol. Endocrinol. Metabol. 290, E163–E168. 10.1152/ajpendo.00300.2005
    1. Miller B. F., Hansen M., Olesen J. L., Schwarz P., Babraj J. A., Smith K., et al. . (2007). Tendon collagen synthesis at rest and after exercise in women. J. Appl. Physiol. 102, 541–546. 10.1152/japplphysiol.00797.2006
    1. Miller B. F., Olesen J. L., Hansen M., Døssing S., Crameri R. M., Welling R. J., et al. . (2005). Coordinated collagen and muscle protein synthesis in human patella tendon and quadriceps muscle after exercise. J. Physiol. 567, 1021–1033. 10.1113/jphysiol.2005.093690
    1. Minahan C., Joyce S., Bulmer A. C., Cronin N., Sabapathy S. (2015). The influence of estradiol on muscle damage and leg strength after intense eccentric exercise. Eur. J. Appl. Physiol. 115, 1493–1500. 10.1007/s00421-015-3133-9
    1. Mishell D. R., Thorneycroft I. H., Nakamura R. M., Nagata Y., Stone S. C. (1972). Serum estradiol in women ingesting combination oral contraceptive steroids. Am. J. Obst. Gynecol. 114, 923–928. 10.1016/0002-9378(72)90098-1
    1. Myer G. D., Ford K. R., Paterno M. V., Nick T. G., Hewett T. E. (2008). The effects of generalized joint laxity on risk of anterior cruciate ligament injury in young female athletes. Am. J. Sports Med. 36, 1073–1080. 10.1177/0363546507313572
    1. Nelson L. R., Bulun S. E. (2001). Estrogen production and action. J. Am. Acad. Dermatol. 45, S116–S124. 10.1067/mjd.2001.117432
    1. Park S. K., Stefanyshyn D. J., Loitz-Ramage B., Hart D. A., Ronsky J. L. (2009). Changing hormone levels during the menstrual cycle affect knee laxity and stiffness in healthy female subjects. Am. J. Sports Med. 37, 588–598. 10.1177/0363546508326713
    1. Pingel J., Langberg H., Skovgård D., Koskinen S., Flyvbjerg A., Frystyk J., et al. . (2012). Effects of transdermal estrogen on collagen turnover at rest and in response to exercise in postmenopausal women. J. Appl. Physiol. 113, 1040–1047. 10.1152/japplphysiol.01463.2011
    1. Pöllänen E., Fey V., Törmäkangas T., Ronkainen P. H., Taaffe D. R., Takala T., et al. . (2010). Power training and postmenopausal hormone therapy affect transcriptional control of specific co-regulated gene clusters in skeletal muscle. Age 32, 347–363. 10.1007/s11357-010-9140-1
    1. Rahr-Wagner L., Thillemann T. M., Mehnert F., Pedersen A. B., Lind M. (2014). Is the use of oral contraceptives associated with operatively treated anterior cruciate ligament injury? A case-control study from the danish knee ligament reconstruction registry. Am. J. Sports Med. 42, 2897–2905. 10.1177/0363546514557240
    1. Ramesh R., Von Arx O., Azzopardi T., Schranz P. J. (2005). The risk of anterior cruciate ligament rupture with generalised joint laxity. Bone Joint J. 87, 800–803. 10.1302/0301-620X.87B6.15833
    1. Ramos J. E., Al-Nakkash L., Peterson A., Gump B. S., Janjulia T., Moore M. S., et al. . (2012). The soy isoflavonegenistein inhibits the reduction in Achilles tendon collagen content induced by ovariectomy in rats. Scand. J. Med. Sci. Sports 22, e108–e114. 10.1111/j.1600-0838.2012.01516.x
    1. Reddy G. K., Lisa S.-B., Chukuka S. (2002). Enwemeka. Glycation-induced matrix stability in the rabbit achilles tendon. Arch. Biochem. Biophys. 399, 174–180. 10.1006/abbi.2001.2747
    1. Rice C. L., Cunningham D. A., Paterson D. H., Rechnitzer P. A. (1989). Strength in an elderly population. Arch. Phys. Med. Rehabil. 70, 391–397.
    1. Ronkainen P. H., Kovanen V., Alén M., Pöllänen E., Palonen E. M., Ankarberg-Lindgren C., et al. . (2009). Postmenopausal hormone replacement therapy modifies skeletal muscle composition and function: a study with monozygotic twin pairs. J. Appl. Physiol. 107, 25–33. 10.1152/japplphysiol.91518.2008
    1. Ruedl G., Ploner P., Linortner I., Schranz A., Fink C., Sommersacher R., et al. . (2009). Are oral contraceptive use and menstrual cycle phase related to anterior cruciate ligament injury risk in female recreational skiers? Knee Surg. Sports Traumatol. Arthroscopy 17, 1065–1069. 10.1007/s00167-009-0786-0
    1. Savage K. J., Priscilla M. C. (2002). Oral contraceptive use and exercise-induced muscle damage and recovery. Contraception 66, 67–71. 10.1016/S0010-7824(02)00320-7
    1. Seneviratne A., Attia E., Williams R. J., Rodeo S. A., Hannafin J. A. (2004). The effect of estrogen on ovine anterior cruciate ligament fibroblasts: cell proliferation and collagen synthesis. Am. J. Sports Med. 32, 1613–1618. 10.1177/0363546503262179
    1. Sewright K. A., Hubal M. J., Kearns A., Holbrook M. T., Clarkson P. M. (2008). Sex differences in response to maximal eccentric exercise. Med. Sci. Sports Exerc. 40, 242–251. 10.1249/mss.0b013e31815aedda
    1. Shultz S. J., Levine B. J., Nguyen A. D., Kim H., Montgomery M. M., Perrin D. H. (2010). A comparison of cyclic variations in anterior knee laxity, genu recurvatum, and general joint laxity across the menstrual cycle. J. Orthop. Res. 28, 1411–1417. 10.1002/jor.21145
    1. Shultz S. J., Randy J. S., Beynnon B. D. (2011). Variations in varus/valgus and internal/external rotational knee laxity and stiffness across the menstrual cycle. J. Orthop. Res. 29, 318–325. 10.1002/jor.21243
    1. Shultz S. J., Sander T. C., Kirk S. E., Perrin D. H. (2005). Sex differences in knee joint laxity change across the female menstrual cycle. J. Sports Med. Phys. Fit. 45, 594–603. 10.1249/00005768-200405001-00719
    1. Shultz S. J., Schmitz R. J., Kong Y., Dudley W. N., Beynnon B. D., Nguyen A. D., et al. . (2012a). Cyclic variations in multiplanar knee laxity influence landing biomechanics. Med. Sci. Sports Exer. 44, 900–909. 10.1249/MSS.0b013e31823bfb25
    1. Shultz S. J., Wideman L., Montgomery M. M., Beasley K. N., Nindl B. C. (2012b). Changes in serum collagen markers, IGF-I, and knee joint laxity across the menstrual cycle. J. Orthop. Res. 30, 1405–1412. 10.1002/jor.22093
    1. Siegel R. C. (1976). Collagen cross-linking. Synthesis of collagen cross-links in vitro with highly purified lysyl oxidase. J. Biol. Chem. 251, 5786–5792.
    1. Siegel R. C., Fu J. C. (1976). Collagen cross-linking. Purification and substrate specificity of lysyl oxidase. J. Biol. Chem. 251, 5779–5785.
    1. Sipilä S., Taaffe D. R., Cheng S., Puolakka J., Toivanen J., Suominen H. (2001). Effects of hormone replacement therapy and high-impact physical exercise on skeletal muscle in post-menopausal women: a randomized placebo-controlled study. Clin. Sci. 101, 147–157. 10.1042/cs1010147
    1. Smith G. I., Yoshino J., Reeds D. N., Bradley D., Burrows R. E., Heisey H. D., et al. . (2014). Testosterone and progesterone, but not estradiol, stimulate muscle protein synthesis in postmenopausal women. J. Clin. Endocrinol. Metab. 99, 256–265. 10.1210/jc.2013-2835
    1. Spangenburg E. E., Geiger P. C., Leinwand L. A., Lowe D. A. (2012). Regulation of physiological and metabolic function of muscle by female sex steroids. Med. Sci. Sports Exerc. 44, 1653–1662. 10.1249/MSS.0b013e31825871fa
    1. Svensson R. B., Mulder H., Kovanen V., Magnusson S. P. (2013). Fracture mechanics of collagen fibrils: influence of natural cross-links. Biophys. J. 104, 2476–2484. 10.1016/j.bpj.2013.04.033
    1. Taaffe D. R., Newman A. B., Haggerty C. L., Colbert L. H., de Rekeneire N., Visser M., et al. . (2005). Estrogen replacement, muscle composition, and physical function: the health ABC study. Med. Sci. Sports Exerc. 37, 1741–1747. 10.1249/01.mss.0000181678.28092.31
    1. Teixeira P. J., Going S. B., Houtkooper L. B., Metcalfe L. L., Blew R. M., Flint-Wagner H. G., et al. . (2003). Resistance training in postmenopausal women with and without hormone therapy. Med. Sci. Sports Exerc. 35, 555–562. 10.1249/01.MSS.0000058437.17262.11
    1. Torres M. J., Kew K. A., Ryan T. E., Pennington E. R., Lin C. T., Buddo K. A., et al. . (2018). 17β-estradiol directly lowers mitochondrial membrane microviscosity and improves bioenergetic function in skeletal muscle. Cell Metab. 27, 167–179. 10.1016/j.cmet.2017.10.003
    1. Valencia A. P., Schappal A. E., Morris E. M., Thyfault J. P., Lowe D. A., Spangenburg E. E. (2016). The presence of the ovary prevents hepatic mitochondrial oxidative stress in young and aged female mice through glutathione peroxidase 1. Exp. Gerontol. 73, 14–22. 10.1016/j.exger.2015.11.011
    1. West D. W., Lee-Barthel A., McIntyre T., Shamim B., Lee C. A., Baar K. (2015). The exercise-induced biochemical milieu enhances collagen content and tensile strength of engineered ligaments. J. Physiol. 593, 4665–4675. 10.1113/JP270737
    1. Westh E., Kongsgaard M., Bojsen-Moller J., Aagaard P., Hansen M., Kjaer M., et al. . (2008). Effect of habitual exercise on the structural and mechanical properties of human tendon, in vivo, in men and women. Scand. J. Med. Sci. Sports. 18, 23–30. 10.1111/j.1600-0838.2007.00638.x
    1. Wojtys E. M., Huston L. J., Boynton M. D., Spindler K. P., Lindenfeld T. N. (2002). The effect of the menstrual cycle on anterior cruciate ligament injuries in women as determined by hormone levels. Am. J. Sports Med. 30, 182–188. 10.1177/03635465020300020601
    1. Wojtys E. M., Huston L. J., Lindenfeld T. N., Hewett T. E., Greenfield M. L. (1998). Association between the menstrual cycle and anterior cruciate ligament injuries in female athletes. Am. J. Sports Med. 26, 614–619. 10.1177/03635465980260050301
    1. Yao J., Brinton R. D. (2012). Estrogen regulation of mitochondrial bioenergetics: implications for prevention of Alzheimer's disease. Adv. Pharmacol. 64, 327–371. 10.1016/B978-0-12-394816-8.00010-6
    1. Yu W. D., Liu S. H., Hatch J. D., Panossian V., Finerman G. A. (1999). Effect of estrogen on cellular metabolism of the human anterior cruciate ligament. Clin. Orthop. Relat. Res. 366, 229–238. 10.1097/00003086-199909000-00030
    1. Zhao R., Xu Z., Zhao M. (2015). Effects of oestrogen treatment on skeletal response to exercise in the hips and spine in postmenopausal women: a meta-analysis. Sports Med. 45, 1163–1173. 10.1007/s40279-015-0338-3

Source: PubMed

3
Iratkozz fel