Increased serum adiponectin concentrations in amenorrheic physically active women are associated with impaired bone health but not with estrogen exposure

Bone

Volumn 48, Issue 4, 2011, Pages 760-767

  O'Donnell, Emma ^a   De Souza, Mary Jane ^b  

^a UNIVERSITY OF TORONTO   (Canada)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

Adipokines; Adipose tissue; Amenorrhea; Bone; Exercise

Indexed keywords

ADIPONECTIN; ESTROGEN; ESTRONE GLUCURONIDE; GHRELIN; LEPTIN; LIOTHYRONINE;

ADULT; AMENORRHEA; ARTICLE; ATHLETE; BODY FAT; BONE; BONE DENSITY; CLINICAL ARTICLE; CONTROLLED STUDY; ESTROGEN URINE LEVEL; EXERCISE; FEMALE; HORMONE BLOOD LEVEL; HUMAN; OBSERVATIONAL STUDY; OVULATION; PHYSICAL ACTIVITY; PREMENOPAUSE; PROSPECTIVE STUDY; PROTEIN BLOOD LEVEL;

ADIPONECTIN; ADULT; BONE AND BONES; ENERGY METABOLISM; ESTROGENS; EXERCISE; FEMALE; HUMANS; PROSPECTIVE STUDIES;

EID: 79952696231     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2010.12.018     Document Type: Article

References (38)

1. Loucks A.B., Thuma J.R. Luteinizing hormone pulsatility is disrupted at a threshold of energy availability in regularly menstruating women. J Clin Endocrinol Metab 2003, 88:297-311.
2. Williams N.I., Caston-Balderrama A.L., Helmreich D.L., Parfitt D.B., Nosbisch C., Cameron J.L. Longitudinal changes in reproductive hormones and menstrual cyclicity in cynomolgus monkeys during strenuous exercise training: abrupt transition to exercise-induced amenorrhea. Endocrinology 2001, 142:2381-2389.
3. De Souza M.J., Toombs R.J., Scheid J.L., O'Donnell E., West S.L., Williams N.I. High prevalence of subtle and severe menstrual disturbances in exercising women: confirmation using daily hormone measures. Hum Reprod 2010, 25:491-503.
4. Otis C.L., Drinkwater B., Johnson M., Loucks A., Wilmore J. American College of Sports Medicine position stand. The Female Athlete Triad. Med Sci Sports Exerc 1997, 29:i-ix.
5. Laughlin G.A., Yen S.S. Nutritional and endocrine-metabolic aberrations in amenorrheic athletes. J Clin Endocrinol Metab 1996, 81:4301-4309.
6. O'Donnell E., Harvey P.J., Goodman J.M., De Souza M.J. Long-term estrogen deficiency lowers regional blood flow, resting systolic blood pressure, and heart rate in exercising premenopausal women. Am J Physiol Endocrinol Metab 2007, 292:E1401-E1409.
7. De Souza M.J., Lee D.K., VanHeest J.L., Scheid J.L., West S.L., Williams N.I. Severity of energy-related menstrual disturbances increases in proportion to indices of energy conservation in exercising women. Fertil Steril 2007, 88:971-975.
8. Christo K., Cord J., Mendes N., Miller K.K., Goldstein M.A., Klibanski A., et al. Acylated ghrelin and leptin in adolescent athletes with amenorrhea, eumenorrheic athletes and controls: a cross-sectional study. Clin Endocrinol (Oxf) 2008, 69:628-633.
9. Russell M., Stark J., Nayak S., Miller K.K., Herzog D.B., Klibanski A., et al. Peptide YY in adolescent athletes with amenorrhea, eumenorrheic athletes and non-athletic controls. Bone 2009, 45:104-109.
10. Scheid J.L., Williams N.I., West S.L., VanHeest J.L., De Souza M.J. Elevated PYY is associated with energy deficiency and indices of subclinical disordered eating in exercising women with hypothalamic amenorrhea. Appetite 2009, 52:184-192.
11. Rajala M.W., Scherer P.E. Minireview: The adipocyte-at the crossroads of energy homeostasis, inflammation, and atherosclerosis. Endocrinology 2003, 144:3765-3773.
12. Cambuli V.M., Musiu M.C., Incani M., Paderi M., Serpe R., Marras V., et al. Assessment of adiponectin and leptin as biomarkers of positive metabolic outcomes after lifestyle intervention in overweight and obese children. J Clin Endocrinol Metab 2008, 93:3051-3057.
13. Arita Y., Kihara S., Ouchi N., Takahashi M., Maeda K., Miyagawa J., et al. Paradoxical decrease of an adipose-specific protein, adiponectin, in obesity. Biochem Biophys Res Commun 1999, 257:79-83.
14. Misra M., Miller K.K., Cord J., Prabhakaran R., Herzog D.B., Goldstein M., et al. Relationships between serum adipokines, insulin levels, and bone density in girls with anorexia nervosa. J Clin Endocrinol Metab 2007, 92:2046-2052.
15. Tagami T., Satoh N., Usui T., Yamada K., Shimatsu A., Kuzuya H. Adiponectin in anorexia nervosa and bulimia nervosa. J Clin Endocrinol Metab 2004, 89:1833-1837.
16. Perrini S., Laviola L., Cignarelli A., Melchiorre M., De Stefano F., Caccioppoli C., et al. Fat depot-related differences in gene expression, adiponectin secretion, and insulin action and signalling in human adipocytes differentiated in vitro from precursor stromal cells. Diabetologia 2008, 51:155-164.
17. Pannacciulli N., Bunt J.C., Ortega E., Funahashi T., Salbe A.D., Bogardus C., et al. Lower total fasting plasma adiponectin concentrations are associated with higher metabolic rates. J Clin Endocrinol Metab 2006, 91:1600-1603.
18. Cnop M., Havel P.J., Utzschneider K.M., Carr D.B., Sinha M.K., Boyko E.J., et al. Relationship of adiponectin to body fat distribution, insulin sensitivity and plasma lipoproteins: evidence for independent roles of age and sex. Diabetologia 2003, 46:459-469.
19. Chalvatzas N., Dafopoulos K., Kosmas G., Kallitsaris A., Pournaras S., Messinis I.E. Effect of ovarian hormones on serum adiponectin and resistin concentrations. Fertil Steril 2009, 91:1189-1194.
20. O'Donnell E., Harvey P.J., De Souza M.J. Relationships between vascular resistance and energy deficiency, nutritional status and oxidative stress in oestrogen deficient physically active women. Clin Endocrinol Oxf 2009, 70:294-302.
21. De Souza M.J., Miller B.E., Loucks A.B., Luciano A.A., Pescatello L.S., Campbell C.G., et al. High frequency of luteal phase deficiency and anovulation in recreational women runners: blunted elevation in follicle-stimulating hormone observed during luteal-follicular transition. J Clin Endocrinol Metab 1998, 83:4220-4232.
22. Saltin B., Astrand P.O. Maximal oxygen uptake in athletes. J Appl Physiol 1967, 23:353-358.
23. De Souza M.J., Williams N.I. Physiological aspects and clinical sequelae of energy deficiency and hypoestrogenism in exercising women. Hum Reprod Update 2004, 10:433-448.
24. Weir J.B. New methods for calculating metabolic rate with special reference to protein metabolism. J Physiol 1949, 109:1-9.
25. De Souza M.J., Leidy H.J., O'Donnell E., Lasley B., Williams N.I. Fasting ghrelin levels in physically active women: relationship with menstrual disturbances and metabolic hormones. J Clin Endocrinol Metab 2004, 89:3536-3542.
26. Bobbert T., Rochlitz H., Wegewitz U., Akpulat S., Mai K., Weickert M.O., et al. Changes of adiponectin oligomer composition by moderate weight reduction. Diabetes 2005, 54:2712-2719.
27. Kim S.W., Her S.J., Park S.J., Kim D., Park K.S., Lee H.K., et al. Ghrelin stimulates proliferation and differentiation and inhibits apoptosis in osteoblastic MC3T3-E1 cells. Bone 2005, 37:359-369.
28. Thrailkill K.M., Lumpkin C.K., Bunn R.C., Kemp S.F., Fowlkes J.L. Is insulin an anabolic agent in bone? Dissecting the diabetic bone for clues. Am J Physiol Endocrinol Metab 2005, 289:E735-E745.
29. Lee N.J., Wong I.P., Baldock P.A., Herzog H. Leptin as an endocrine signal in bone. Curr Osteoporos Rep 2008, 6:62-66.
30. De Souza M.J., West S.L., Jamal S.A., Hawker G.A., Gundberg C.M., Williams N.I. The presence of both an energy deficiency and estrogen deficiency exacerbate alterations of bone metabolism in exercising women. Bone 2008, 43:140-148.
31. Kaufman B.A., Warren M.P., Dominguez J.E., Wang J., Heymsfield S.B., Pierson R.N. Bone density and amenorrhea in ballet dancers are related to a decreased resting metabolic rate and lower leptin levels. J Clin Endocrinol Metab 2002, 87:2777-2783.
32. Duncan C.S., Blimkie C.J., Cowell C.T., Burke S.T., Briody J.N., Howman-Giles R. Bone mineral density in adolescent female athletes: relationship to exercise type and muscle strength. Med Sci Sports Exerc 2002, 34:286-294.
33. Luo X.H., Guo L.J., Xie H., Yuan L.Q., Wu X.P., Zhou H.D., et al. Adiponectin stimulates RANKL and inhibits OPG expression in human osteoblasts through the MAPK signaling pathway. J Bone Miner Res 2006, 21:1648-1656.
34. Shinoda Y., Yamaguchi M., Ogata N., Akune T., Kubota N., Yamauchi T., et al. Regulation of bone formation by adiponectin through autocrine/paracrine and endocrine pathways. J Cell Biochem 2006, 99:196-208.
35. Sieminska L., Wojciechowska C., Niedziolka D., Marek B., Kos-Kudla B., Kajdaniuk D., et al. Effect of postmenopause and hormone replacement therapy on serum adiponectin levels. Metabolism 2005, 54:1610-1614.
36. Thong F.S., McLean C., Graham T.E. Plasma leptin in female athletes: relationship with body fat, reproductive, nutritional, and endocrine factors. J Appl Physiol 2000, 88:2037-2044.
37. Myburgh K.H., Berman C., Novick I., Noakes T., Lambert E. Decreased resting metabolic rate in ballet dancers with menstrual irregularity. Int J Sport Nutr 1999, 9:285-294.
38. Lenchik L., Register T.C., Hsu F.C., Lohman K., Nicklas B.J., Freedman B.I., et al. Adiponectin as a novel determinant of bone mineral density and visceral fat. Bone 2003, 33:646-651.