Advertisement

Breast Cancer Research and Treatment

, Volume 152, Issue 3, pp 637–643 | Cite as

Effect of weight loss on bone health in overweight/obese postmenopausal breast cancer survivors

  • Adetunji T. ToriolaEmail author
  • Jingxia Liu
  • Patricia A. Ganz
  • Graham A. Colditz
  • Lin Yang
  • Sonya Izadi
  • Michael J. Naughton
  • Anna L. Schwartz
  • Kathleen Y. Wolin
Epidemiology

Abstract

Current guidelines recommend weight loss in obese cancer survivors. Weight loss, however, has adverse effects on bone health in obese individuals without cancer but this has not been evaluated in breast cancer survivors. We investigated the associations of intentional weight loss with bone mineral density (BMD) and bone turn-over markers in overweight/obese postmenopausal breast cancer survivors. Participants were overweight/obese breast cancer survivors (N = 81) with stage I, II or IIIA disease enrolled in the St. Louis site of a multi-site Exercise and Nutrition to Enhance Recovery and Good health for You (ENERGY) study; a randomized-controlled clinical trial designed to achieve a sustained ≥7 % loss in body weight at 2 years. Weight loss was achieved through dietary modification with the addition of physical activity. Generalized estimating equations were used to assess differences in mean values between follow-up and baseline. Mean weight decreased by 3 and 2.3 % between baseline and 6-month follow-up, and 12-month follow-up, respectively. There were decreases in osteocalcin (10.6 %, p value < 0.001), PINP (14.5 %, p value < 0.001), NTx (19.2 % p value < 0.001), and RANK (48.5 %, p value < 0.001), but not BALP and CTX-1 levels between baseline and 12-month follow-up. No significant changes occurred in mean T-scores, pelvis and lumbar spine BMD between baseline and 12-month follow-up. A 2.3 % weight loss over 12 months among overweight/obese women with early-stage breast cancer does not appear to have deleterious effect on bone health, and might even have beneficial effect. These findings warrant confirmation, particularly among breast cancer survivors with a larger magnitude of weight loss.

Keywords

Breast cancer Bone health Obesity Weight loss Bone mineral density 

Notes

Acknowledgments

Research reported in this publication was supported by grants R21CA161105 and CA148791 from the National Cancer Institute and the Washington University Institute of Clinical, Translational Sciences Grant UL1TR000448 from the National Center for Advancing Translational Sciences (NCATS) of the National Institutes of Health (NIH), and the Biostatistics Core at Siteman Cancer Center. The content is solely the responsibility of the authors and does not necessarily represent the official view of the NIH. Adetunji T. Toriola is supported by the Washington University School of Medicine, Barnes-Jewish Hospital Foundation, Siteman Cancer Center and a Faculty Diversity Award. The authors would also like to recognize the women who participated in the sub-site project of the ENERGY trial.

Complaince with Ethical Standards

Conflict of interests

The authors declare that they have no conflict of interest.

References

  1. 1.
    Chan DS, Vieira AR, Aune D, Bandera EV, Greenwood DC, McTiernan A, Navarro Rosenblatt D, Thune I, Vieira R, Norat T (2014) Body mass index and survival in women with breast cancer-systematic literature review and meta-analysis of 82 follow-up studies. Ann Oncol. doi: 10.1093/annonc/mdu042 PubMedCentralGoogle Scholar
  2. 2.
    Chao D, Espeland MA, Farmer D, Register TC, Lenchik L, Applegate WB, Ettinger WH Jr (2000) Effect of voluntary weight loss on bone mineral density in older overweight women. J Am Geriatr Soc 48:753–759CrossRefPubMedGoogle Scholar
  3. 3.
    Cheung AM, Heisey R, Srighanthan J (2013) Breast cancer and osteoporosis. Curr Opin Endocrinol Diabetes Obes 20:532–538. doi: 10.1097/01.med.0000436195.10599.dd CrossRefPubMedGoogle Scholar
  4. 4.
    Delmas PD, Eastell R, Garnero P, Seibel MJ, Stepan J, Committee of Scientific Advisors of the International Osteoporosis Foundation (2000) The use of biochemical markers of bone turnover in osteoporosis. Osteoporos Int 11(Suppl 6):S2–17CrossRefPubMedGoogle Scholar
  5. 5.
    DeSantis CE, Lin CC, Mariotto AB, Siegel RL, Stein KD, Kramer JL, Alteri R, Robbins AS, Jemal A (2014) Cancer treatment and survivorship statistics, 2014. CA Cancer J Clin 64:252–271. doi: 10.3322/caac.21235 CrossRefPubMedGoogle Scholar
  6. 6.
    Eastell R, Adams JE, Coleman RE, Howell A, Hannon RA, Cuzick J, Mackey JR, Beckmann MW, Clack G (2008) Effect of anastrozole on bone mineral density: 5-year results from the anastrozole, tamoxifen, alone or in combination trial 18233230. J Clin Oncol 26:1051–1057. doi: 10.1200/JCO.2007.11.0726 CrossRefPubMedGoogle Scholar
  7. 7.
    Forsen L, Berntsen GK, Meyer HE, Tell GS, Fonnebo V, Group NCR (2008) Differences in precision in bone mineral density measured by SXA and DXA: the NOREPOS study. Eur J Epidemiol 23:615–624. doi: 10.1007/s10654-008-9271-1 CrossRefPubMedGoogle Scholar
  8. 8.
    Garnero P (2009) Bone markers in osteoporosis. Curr Osteoporos Rep 7:84–90CrossRefPubMedGoogle Scholar
  9. 9.
    Garnero P, Sornay-Rendu E, Claustrat B, Delmas PD (2000) Biochemical markers of bone turnover, endogenous hormones and the risk of fractures in postmenopausal women: the OFELY study. J Bone Miner Res 15:1526–1536. doi: 10.1359/jbmr.2000.15.8.1526 CrossRefPubMedGoogle Scholar
  10. 10.
    Gerdhem P, Ivaska KK, Alatalo SL, Halleen JM, Hellman J, Isaksson A, Pettersson K, Vaananen HK, Akesson K, Obrant KJ (2004) Biochemical markers of bone metabolism and prediction of fracture in elderly women. J Bone Miner Res 19:386–393. doi: 10.1359/JBMR.0301244 CrossRefPubMedGoogle Scholar
  11. 11.
    Harris ST, Gertz BJ, Genant HK, Eyre DR, Survill TT, Ventura JN, DeBrock J, Ricerca E, Chesnut CH 3rd (1993) The effect of short term treatment with alendronate on vertebral density and biochemical markers of bone remodeling in early postmenopausal women. J Clin Endocrinol Metab 76:1399–1406. doi: 10.1210/jcem.76.6.8501142 PubMedGoogle Scholar
  12. 12.
    Hinton PS, LeCheminant JD, Smith BK, Rector RS, Donnelly JE (2009) Weight loss-induced alterations in serum markers of bone turnover persist during weight maintenance in obese men and women. J Am Coll Nutr 28:565–573CrossRefPubMedGoogle Scholar
  13. 13.
    Hinton PS, Rector RS, Linden MA, Warner SO, Dellsperger KC, Chockalingam A, Whaley-Connell AT, Liu Y, Thomas TR (2012) Weight-loss-associated changes in bone mineral density and bone turnover after partial weight regain with or without aerobic exercise in obese women. Eur J Clin Nutr 66:606–612. doi: 10.1038/ejcn.2011.212 PubMedCentralCrossRefPubMedGoogle Scholar
  14. 14.
    Lacey DL, Timms E, Tan HL, Kelley MJ, Dunstan CR, Burgess T, Elliott R, Colombero A, Elliott G, Scully S, Hsu H, Sullivan J, Hawkins N, Davy E, Capparelli C, Eli A, Qian YX, Kaufman S, Sarosi I, Shalhoub V, Senaldi G, Guo J, Delaney J, Boyle WJ (1998) Osteoprotegerin ligand is a cytokine that regulates osteoclast differentiation and activation. Cell 93:165–176CrossRefPubMedGoogle Scholar
  15. 15.
    Miller PD, Bonnick SL, Rosen CJ (1996) Consensus of an international panel on the clinical utility of bone mass measurements in the detection of low bone mass in the adult population. Calcif Tissue Int 58:207–214CrossRefPubMedGoogle Scholar
  16. 16.
    Miller PD, Delmas PD, Lindsay R, Watts NB, Luckey M, Adachi J, Saag K, Greenspan SL, Seeman E, Boonen S, Meeves S, Lang TF, Bilezikian JP (2008) Open-label study to determine how prior therapy with alendronate or risedronate in postmenopausal women with osteoporosis influences the clinical effectiveness of teriparatide I. Early responsiveness of women with osteoporosis to teriparatide after therapy with alendronate or risedronate. J Clin Endocrinol Metab 93:3785–3793. doi: 10.1210/jc.2008-0353 CrossRefPubMedGoogle Scholar
  17. 17.
    Nakagawa N, Kinosaki M, Yamaguchi K, Shima N, Yasuda H, Yano K, Morinaga T, Higashio K (1998) RANK is the essential signaling receptor for osteoclast differentiation factor in osteoclastogenesis. Biochem Biophys Res Commun 253:395–400. doi: 10.1006/bbrc.1998.9788 CrossRefPubMedGoogle Scholar
  18. 18.
    National Comprehensive Cancer Network (NCCN) (2011) NCCN clinical practice guidelines in oncology: breast cancer. http://www.nccn.org/professionals/physician_gls/f_guidelines.asp. Accessed Nov 2011
  19. 19.
    Naylor K, Eastell R (2012) Bone turnover markers: use in osteoporosis. Nat Rev Rheumatol 8:379–389. doi: 10.1038/nrrheum.2012.86 CrossRefPubMedGoogle Scholar
  20. 20.
    Peppone LJ, Mustian KM, Janelsins MC, Palesh OG, Rosier RN, Piazza KM, Purnell JQ, Darling TV, Morrow GR (2010) Effects of a structured weight-bearing exercise program on bone metabolism among breast cancer survivors: a feasibility trial. Clin Breast Cancer 10:224–229. doi: 10.3816/CBC.2010.n.030 PubMedCentralCrossRefPubMedGoogle Scholar
  21. 21.
    Reid IR, Ames R, Evans MC, Sharpe S, Gamble G, France JT, Lim TM, Cundy TF (1992) Determinants of total body and regional bone mineral density in normal postmenopausal women: a key role for fat mass. J Clin Endocrinol Metab 75:45–51. doi: 10.1210/jcem.75.1.1619030 PubMedGoogle Scholar
  22. 22.
    Rock CL, Byers TE, Colditz GA, Demark-Wahnefried W, Ganz PA, Wolin KY, Elias A, Krontiras H, Liu J, Naughton M, Pakiz B, Parker BA, Sedjo RL, Wyatt H, Exercise and Nutrition to Enhance Recovery and Good Health for You (ENERGY) Trial (2013) Reducing breast cancer recurrence with weight loss, a vanguard trial: the Exercise and Nutrition to Enhance Recovery and Good health for You (ENERGY) Trial. Contemp Clin Trials 34:282–295. doi: 10.1016/j.cct.2012.12.003 PubMedCentralCrossRefPubMedGoogle Scholar
  23. 23.
    Rock CL, Doyle C, Demark-Wahnefried W, Meyerhardt J, Courneya KS, Schwartz AL, Bandera EV, Hamilton KK, Grant B, McCullough M, Byers T, Gansler T (2012) Nutrition and physical activity guidelines for cancer survivors. CA Cancer J Clin 62:243–274. doi: 10.3322/caac.21142 CrossRefPubMedGoogle Scholar
  24. 24.
    Rosner B (1983) Percentage points for a generalized ESD many-outlier procedure. Technometrics 25:165–172. doi: 10.2307/1268549 CrossRefGoogle Scholar
  25. 25.
    Ross PD, Knowlton W (1998) Rapid bone loss is associated with increased levels of biochemical markers. J Bone Miner Res 13:297–302. doi: 10.1359/jbmr.1998.13.2.297 CrossRefPubMedGoogle Scholar
  26. 26.
    Sornay-Rendu E, Munoz F, Garnero P, Duboeuf F, Delmas PD (2005) Identification of osteopenic women at high risk of fracture: the OFELY study. J Bone Miner Res 20:1813–1819. doi: 10.1359/JBMR.050609 CrossRefPubMedGoogle Scholar
  27. 27.
    Spencer H, Kramer L (1986) NIH consensus conference: osteoporosis. Factors contributing to osteoporosis. J Nutr 116:316–319PubMedGoogle Scholar
  28. 28.
    Swaminathan R (2001) Biochemical markers of bone turnover. Clin Chim Acta 313:95–105CrossRefPubMedGoogle Scholar
  29. 29.
    Tromp AM, Ooms ME, Popp-Snijders C, Roos JC, Lips P (2000) Predictors of fractures in elderly women. Osteoporos Int 11:134–140. doi: 10.1007/PL00004174 CrossRefPubMedGoogle Scholar
  30. 30.
    Villareal DT, Fontana L, Weiss EP, Racette SB, Steger-May K, Schechtman KB, Klein S, Holloszy JO (2006) Bone mineral density response to caloric restriction-induced weight loss or exercise-induced weight loss: a randomized controlled trial. Arch Intern Med 166:2502–2510. doi: 10.1001/archinte.166.22.2502 CrossRefPubMedGoogle Scholar
  31. 31.
    Villareal DT, Shah K, Banks MR, Sinacore DR, Klein S (2008) Effect of weight loss and exercise therapy on bone metabolism and mass in obese older adults: a 1-year randomized controlled trial. J Clin Endocrinol Metab 93:2181–2187. doi: 10.1210/jc.2007-1473 PubMedCentralCrossRefPubMedGoogle Scholar
  32. 32.
    Waltman NL, Twiss JJ, Ott CD, Gross GJ, Lindsey AM, Moore TE, Berg K, Kupzyk K (2010) The effect of weight training on bone mineral density and bone turnover in postmenopausal breast cancer survivors with bone loss: a 24-month randomized controlled trial. Osteoporos Int 21:1361–1369. doi: 10.1007/s00198-009-1083-y CrossRefPubMedGoogle Scholar
  33. 33.
    Zhao LJ, Jiang H, Papasian CJ, Maulik D, Drees B, Hamilton J, Deng HW (2008) Correlation of obesity and osteoporosis: effect of fat mass on the determination of osteoporosis. J Bone Miner Res 23:17–29. doi: 10.1359/jbmr.070813 PubMedCentralCrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Adetunji T. Toriola
    • 1
    Email author
  • Jingxia Liu
    • 2
  • Patricia A. Ganz
    • 3
  • Graham A. Colditz
    • 1
  • Lin Yang
    • 1
  • Sonya Izadi
    • 1
  • Michael J. Naughton
    • 4
  • Anna L. Schwartz
    • 5
  • Kathleen Y. Wolin
    • 6
  1. 1.Division of Public Health Sciences, and Siteman Cancer Center, Department of SurgeryWashington University School of MedicineSaint LouisUSA
  2. 2.Division of BiostatisticsWashington University School of MedicineSaint LouisUSA
  3. 3.University of California Los Angeles Jonsson Comprehensive Cancer CenterLos AngelesUSA
  4. 4.Division of Oncology, Section of Medical Oncology and Siteman Cancer CenterWashington University School of MedicineSaint LouisUSA
  5. 5.Arizona State UniversityArizonaUSA
  6. 6.Coeus HealthChicagoUSA

Personalised recommendations