Skip to main content

Advertisement

SpringerLink
Log in

Favorable modulation of benign breast tissue and serum risk biomarkers is associated with >10 % weight loss in postmenopausal women

  • Clinical trial
  • Published:
Breast Cancer Research and Treatment Aims and scope Submit manuscript

Abstract

We conducted a phase II feasibility study of a 6-month behavioral weight loss intervention in postmenopausal overweight and obese women at increased risk for breast cancer and the effects of weight loss on anthropomorphic, blood, and benign breast tissue biomarkers. 67 women were screened by random peri-areolar fine-needle aspiration, 27 were registered and 24 participated in the interventional phase. The 24 biomarker evaluable women had a median baseline BMI of 34.2 kg/m2 and lost a median of 11 % of their initial weight. Significant tissue biomarker modulation after the 6-month intervention was noted for Ki-67 (if restricted to the 15 women with any Ki-67 at baseline, p = 0.041), adiponectin to leptin ratio (p = 0.003); and cyclin B1 (p = 0.001), phosphorylated retinoblastoma (p = 0.005), and ribosomal S6 (p = 0.004) proteins. Favorable modulation for serum markers was observed for sex hormone-binding globulin (p < 0.001), bioavailable estradiol (p < 0.001), bioavailable testosterone (p = 0.033), insulin (p = 0.018), adiponectin (p = 0.001), leptin (p < 0.001), the adiponectin to leptin ratio (p < 0.001), C-reactive protein (p = 0.002), and hepatocyte growth factor (p = 0.011). When subdivided by <10 or >10 % weight loss, change in percent total body and android (visceral) fat, physical activity, and the majority of the serum and tissue biomarkers were significantly modulated only for women with >10 % weight loss from baseline. Some factors such as serum PAI-1 and breast tissue pS2 (estrogen-inducible gene) mRNA were not significantly modulated overall but were when considering only those with >10 % weight loss. In conclusion, a median weight loss of 11 % over 6 months resulted in favorable modulation of a number of anthropomorphic, breast tissue and serum risk and mechanistic markers. Weight loss of 10 % or more should likely be the goal for breast cancer risk reduction studies in obese women.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Huang Z, Hankinson SE, Colditz GA et al (1997) Dual effects of weight and weight gain on breast cancer risk. JAMA 278:1407–1411

    Article  PubMed  CAS  Google Scholar 

  2. Ahn J, Schatzkin A, Lacey JV Jr, Albanes D, Ballard-Barbash R, Adams KF et al (2007) Adiposity, adult weight change, and postmenopausal breast cancer risk. Arch Intern Med 167:2091–2102

    Article  PubMed  Google Scholar 

  3. Harvie M, Howell A, Vierkant RA, Kumar N, Cerhan JR, Kelemen LE et al (2005) Association of gain and loss of weight before and after menopause with risk of postmenopausal breast cancer in the Iowa women’s health study. Cancer Epidemiol Biomarkers Prev 14:656–661

    Article  PubMed  Google Scholar 

  4. Lahmann PH, Schulz M, Hoffmann K, Boeing H, Tjønneland A, Olsen A et al (2005) Long-term weight change and breast cancer risk: the European prospective investigation into cancer and nutrition (EPIC). Br J Cancer 93:582–589

    Article  PubMed  CAS  Google Scholar 

  5. Eliassen AH, Colditz GA, Rosner B, Willett WC, Hankinson SE (2006) Adult weight change and risk of postmenopausal breast cancer. JAMA 296:193–201

    Article  PubMed  CAS  Google Scholar 

  6. Manders P, Pijpe A, Hooning MJ, Kluijt I, Vasen HF, Hoogerbrugge N et al (2011) Body weight and risk of breast cancer in BRCA1/2 mutation carriers. Breast Cancer Res Treat 126:193–202

    Article  PubMed  CAS  Google Scholar 

  7. Subbaramaiah K, Howe LR, Bhardwaj P, Du B, Gravaghi C, Yantiss RK et al (2011) Obesity is associated with inflammation and elevated aromatase expression in the mouse mammary gland. Cancer Prev Res 4:329–346

    Article  CAS  Google Scholar 

  8. Subbaramaiah K, Morris PG, Zhou ZK, Morrow M, Du B, Giri D et al (2012) Increased levels of COX-2 and prostaglandin E2 contribute to elevated aromatase expression in inflamed breast tissue of obese women. Cancer Discov 2:356–365

    Article  PubMed  CAS  Google Scholar 

  9. Endogenous Hormones and Breast Cancer Collaborative Group, Key TJ, Appleby PN, Reeves GK, Roddam AW, Helzlsouer KJ, Alberg AJ et al (2011) Circulating sex hormones and breast cancer risk factors in postmenopausal women: reanalysis of 13 studies. Br J Cancer 105:709–722

    Article  Google Scholar 

  10. Morris PG, Hudis CA, Morrow M, Falcone DJ, Zhou XK (2011) Inflammation and increased aromatase expression occur in the breast tissue of obese women with breast cancer. Cancer Prev Res 4:1021–1029

    Article  CAS  Google Scholar 

  11. Hammarstedt A, Graham TE (2012) Kahn BB (2012) Adipose tissue dysregulation and reduced insulin sensitivity in non-obese individuals with enlarged abdominal adipose cells. Diabetol Metab Syndr. 4(1):42

    Article  PubMed  CAS  Google Scholar 

  12. Coelho M, Oliveira T, Fernandes R (2013) Biochemistry of adipose tissue: an endocrine organ. Arch Med Sci 9:191–200

    Article  PubMed  CAS  Google Scholar 

  13. Schairer C, Hill D, Sturgeon SR, Fears T, Pollak M, Mies C, Ziegler RG, Hoover RN, Sherman ME (2004) Serum concentrations of IGF-I, IGFBP-3 and c-peptide and risk of hyperplasia and cancer of the breast in postmenopausal women. Int J Cancer 108:773–779

    Article  PubMed  CAS  Google Scholar 

  14. Probst-Hensch NM, Steiner JH, Schraml P, Varga Z, Zürrer-Härdi U, Storz M, Korol D, Fehr MK, Fink D, Pestalozzi BC, Lütolf UM, Theurillat JP, Moch H (2010) IGFBP2 and IGFBP3 protein expressions in human breast cancer: association with hormonal factors and obesity. Clin Cancer Res 16:1025–1032

    Article  PubMed  CAS  Google Scholar 

  15. Hursting SD, Digiovanni J, Dannenberg AJ, Azrad M, Leroith D, Demark-Wahnefried W, Kakarala M, Brodie A, Berger NA (2012) Obesity, energy balance, and cancer: new opportunities for prevention. Cancer Prev Res 5:1260–1272

    Article  CAS  Google Scholar 

  16. Bruning PF, Bonfrer JM, van Noord PA, Hart AA, Jong-Bakker M, Nooijen WJ (1992) Insulin resistance and breast-cancer risk. Int J Cancer 52:511–516

    Article  PubMed  CAS  Google Scholar 

  17. Sieri S, Pala V, Brighenti F, Pellegrini N, Muti P, Micheli A et al (2007) Dietary glycemic index, glycemic load, and the risk of breast cancer in an Italian prospective cohort study. Am J Clin Nutr 86:1160–1166

    PubMed  CAS  Google Scholar 

  18. Tworoger SS, Eliassen AH, Kelesidis T et al (2007) Plasma adiponectin concentrations and risk of incident breast cancer. J Clin Endocrinol Metab 92:1510–1516

    Article  PubMed  CAS  Google Scholar 

  19. Vona-Davis L, Rose DP (2007) Adipokines as endocrine, paracrine, and autocrine factors in breast cancer risk and progression. Endocr Relat Cancer 14:189–206

    Article  PubMed  CAS  Google Scholar 

  20. Becker S, Dossus L, Kaaks R (2009) Obesity related hyperinsulinaemia and hyperglycaemia and cancer development. Arch Physiol Biochem 115:86–96

    Article  PubMed  CAS  Google Scholar 

  21. Maccio A, Madeddu C, Mantovani G (2009) Adipose tissue as target organ in the treatment of hormone-dependent breast cancer: new therapeutic perspectives. Obes Rev 10:660–670

    Article  PubMed  CAS  Google Scholar 

  22. Taliaferro-Smith L, Nagalingam A, Zhong D, Zhou W, Saxena NK, Sharma D (2009) LKB1 is required for adiponectin-mediated modulation of AMPK-S6 K axis and inhibition of migration and invasion of breast cancer cells. Oncogene 28:2621–2633

    Article  PubMed  CAS  Google Scholar 

  23. Grossmann ME, Ray A, Nkhata KJ, Malakhov DA, Rogozina OP, Dogan S, Cleary MP (2010) Obesity and breast cancer: status of leptin and adiponectin in pathological processes. Cancer Metastasis Rev 29:641–653

    Article  PubMed  CAS  Google Scholar 

  24. Roberts DL, Dive C, Renehan AG (2010) Biological mechanisms linking obesity and cancer risk: new perspectives. Ann Rev Med 61:301–316

    Article  PubMed  CAS  Google Scholar 

  25. Mazzali G, Di Francesco V, Zoico E, Fantin F, Zamboni G, Benati C, Bambara V, Negri M, Bosello O, Zamboni M (2006) Interrelations between fat distribution, muscle lipid content, adipocytokines, and insulin resistance: effect of moderate weight loss in older women. Am J Clin Nutr 84:1193–1199

    PubMed  CAS  Google Scholar 

  26. Harvie MN, Bokhari S, Shenton A, Ashcroft L, Evans G, Swindell R, Howell A (2007) Adult weight gain and central obesity in women with and without a family history of breast cancer: a case control study. Fam Cancer 6:287–294

    Article  PubMed  Google Scholar 

  27. Zamboni M, Di Francesco V, Garbin U, Fratta Pasini A, Mazzali G, Stranieri C, Zoico E, Fantin F, Bosello O, Cominacini L (2007) Adiponectin gene expression and adipocyte NF-kappaB transcriptional activity in elderly overweight and obese women: inter-relationships with fat distribution, hs-CRP, leptin and insulin resistance. Int J Obes 31:1104–1109

    Article  CAS  Google Scholar 

  28. Karelis AD (2011) Obesity: to be obese: does it matter if you are metabolically healthy? Nat Rev Endocrinol 7:699–700

    Article  PubMed  Google Scholar 

  29. Shuster A, Patlas M, Pinthus JH, Mourtzakis M (2012) The clinical importance of visceral adiposity: a critical review of methods for visceral adipose tissue analysis. Br J Radiol 85:1–10

    Article  PubMed  CAS  Google Scholar 

  30. Mason C, Katzmarzyk PT (2010) Waist circumference thresholds for the prediction of cardiometabolic risk: is measurement site important? Eur J Clin Nutr 64:862–867

    Article  PubMed  CAS  Google Scholar 

  31. Byers T, Sedjo RL (2011) Does intentional weight loss reduce cancer risk? Diabetes Obes Metab 12:1063–1072

    Article  Google Scholar 

  32. Sjöström L, Gummesson A, Sjöström CD, Narbro K, Peltonen M, Wedel H, Bengtsson C, Bouchard C, Carlsson B, Dahlgren S, Jacobson P, Karason K, Karlsson J, Larsson B, Lindroos AK, Lönroth H, Näslund I, Olbers T, Stenlöf K, Torgerson J, Carlsson LM; Swedish Obese Subjects Study (2009) Effects of bariatric surgery on cancer incidence in obese patients in Sweden (Swedish Obese Subjects Study): a prospective, controlled intervention trial. Lancet Oncol 10:653–662

    Article  Google Scholar 

  33. Sjöström L, Gummesson A, Sjöström CD, Narbro K, Peltonen M, Wedel H, Bengtsson C, Bouchard C, Carlsson B, Dahlgren S, Jacobson P, Karason K, Karlsson J, Larsson B, Lindroos AK, Lönroth H, Näslund I, Olbers T, Stenlöf K, Torgerson J, Carlsson LM; Swedish Obese Subjects Study (1998) Executive summary of the clinical guidelines on the identification, evaluation, and treatment of overweight and obesity in adults. Arch Intern Med 158:1867–1885

    Google Scholar 

  34. Parker ED, Folsom AR (2003) Intentional weight loss and incidence of obesity related cancers: the Iowa Women’s Health Study. Int J Obes Relat Metab Disord 27:1447–1452

    Article  PubMed  CAS  Google Scholar 

  35. Leblanc ES, O’Connor E, Whitlock EP, Patnode CD, Kapka T (2011) Effectiveness of primary care-relevant treatments for obesity in adults: a systematic evidence review for the US Preventive Services Task Force. Ann Intern Med 155:434–447

    Article  PubMed  Google Scholar 

  36. Moyer VA, U.S. Preventive Services Task Force (2012) Screening for and management of obesity in adults: US Preventive Services Task Force recommendation statement. Ann Intern Med 157:373–378

    Google Scholar 

  37. Donnelly JE, Smith BK, Dunn L, Mayo MM, Jacobsen DJ, Stewart EE, Gibson C, Sullivan DK (2007) Comparison of a phone vs clinic approach to achieve 10 % weight loss. Int J Obes 31:1270–1276

    Article  CAS  Google Scholar 

  38. Fabian CJ, Kimler BF, Zalles CM, Klemp JR, Kamel S, Zeiger S, Mayo MS (2000) Short-term prediction of breast cancer by random peri-areolar fine needle aspiration cytology and Gail risk. J Natl Cancer Inst 92:1217–1227

    Article  PubMed  CAS  Google Scholar 

  39. Fabian CJ, Kimler BF, Zalles CM, Klemp JR, Petroff BK, Khan QJ, Sharma P, Setchell KD, Zhao X, Phillips TA, Metheny T, Hughes JR, Yeh HW, Johnson KA (2010) Reduction in Ki-67 in benign breast tissue of high-risk women with the lignan secoisolariciresinol diglycoside. Cancer Prev Res 3:1342–1350

    Article  CAS  Google Scholar 

  40. Masood S, Frykberg ER, McLellan GL, Scalapino MC, Mitchum DG, Bullard JB (1990) Prospective evaluation of radiologically directed fine-needle aspiration biopsy of nonpalpable breast lesions. Cancer 66:1480–1487

    Article  PubMed  CAS  Google Scholar 

  41. Khan QJ, Kimler BF, Clark J, Metheny T, Zalles CM, Fabian CJ (2005) Ki-67 expression in benign breast ductal cells obtained by random periareolar fine needle aspiration. Cancer Epidemiol Biomarkers Prev 14:786–789

    Article  PubMed  CAS  Google Scholar 

  42. National Task Force on the Prevention and Treatment of Obesity, Dieting and the development of eating disorders in overweight and obese adults (2000) Arch Intern Med 160:2581–2589

  43. Vermeulen A, Verdonck G (1992) Representativeness of a single point plasma testosterone level for the long term hormonal milieu in men. J Clin Endocrinol Metab 74:939–942

    Article  PubMed  CAS  Google Scholar 

  44. Phillips TA, Fabian CJ, Kimler BF, Petroff BK (2013) Assessment of RNA in human breast tissue sampled by random periareolar fine needle aspiration and ductal lavage and processed as fixed or frozen specimens. Reprod Biol 13:75–81

    Article  PubMed  Google Scholar 

  45. Hennessy BT, Lu Y, Gonzalez-Angulo AM, Carey MS, Myhre S, Ju Z, Davies MA, Liu W, Coombes K, Meric-Bernstam F, Bedrosian I, McGahren M, Agarwal R, Zhang F, Overgaard J, Alsner J, Neve RM, Kuo WL, Gray JW, Borresen-Dale AL, Mills GB (2010) A technical assessment of the utility of reverse phase protein arrays for the study of the functional proteome in non-microdissected human breast cancers. Clin Proteomics 6:129–151

    Article  PubMed  CAS  Google Scholar 

  46. Moore T, Beltran L, Carbajal S, Strom S, Traag J, Hursting SD, DiGiovanni J (2008) Dietary energy balance modulates signaling through the Akt/mammalian target of rapamycin pathways in multiple epithelial tissues. Cancer Prev Res 1:65–76

    Article  CAS  Google Scholar 

  47. Mason C, Xiao L, Duggan C, Imayama I, Foster-Schubert KE, Kong A, Campbell KL, Wang CY, Alfano CM, Blackburn GL, Pollack M, McTiernan A (2013) Effects of dietary weight loss and exercise on insulin-like growth factor-1 and insulin-like growth factor binding protein-3 in postmenopausal women. Cancer Epidemiol Biomarkers Prev 22:1457–1463

    Article  PubMed  CAS  Google Scholar 

  48. Sidle A, Palaty C, Dirks P, Wiggan O, Kiess M, Gill RM, Wong AK, Hamel PA (1996) Activity of the retinoblastoma family proteins, pRB, p107, and p130, during cellular proliferation and differentiation. Crit Rev Biochem Mol Biol 31:237–271

    Article  PubMed  CAS  Google Scholar 

  49. García-Tuñón I, Ricote M, Ruiz A, Fraile B, Paniagua R, Royuela M (2006) Cell cycle control related proteins (p53, p21, and Rb) and transforming growth factor beta (TGFbeta) in benign and carcinomatous (in situ and infiltrating) human breast: implications in malignant transformations. Cancer Invest 24:119–125

    Article  PubMed  Google Scholar 

  50. Khan S, Brougham CL, Ryan J, Sahrudin A, O’Neill G, Wall D, Curran C, Newell J, Kerin MJ (2013) Dwyer RM (2013) miR-379 regulates cyclin B1 expression and is decreased in breast cancer. PLoS One 8(7):e68753

    Article  PubMed  CAS  Google Scholar 

  51. Magnuson B, Ekim B, Fingar DC (2012) Regulation and function of ribosomal protein S6 kinase (S6 K) within mTOR signalling networks. Biochem J 441:1–21

    Article  PubMed  CAS  Google Scholar 

  52. Stanton AL, Bernaards CA, Ganz PA (2005) The BCPT symptom scales: a measure of physical symptoms for women diagnosed with or at risk for breast cancer. J Natl Cancer Inst 97:448–456

    Article  PubMed  Google Scholar 

  53. Mendoza TR, Wang XS, Cleeland CS, Morrissey M, Johnson BA, Wendt JK, Huber SL (1999) The rapid assessment of fatigue severity in cancer patients: use of the Brief Fatigue Inventory. Cancer 85:1186–1196

    Article  PubMed  CAS  Google Scholar 

  54. Sloan JA, Loprinzi CL, Novotny PJ, Barton DL, Lavasseur BI, Windschitl H (2001) Methodologic lessons learned from hot flash studies. J Clin Oncol 19:4280–4290

    PubMed  CAS  Google Scholar 

  55. Klempel MC, Varaday KA (2011) Reliability of leptin but not adiponectin as a biomarker for diet induced weight loss in humans. Nutr Rev 69:145–154

    Article  PubMed  Google Scholar 

  56. Campbell KL, Foster-Schubert KE, Alfano CM, Wang CC, Wang CY, Duggan CR, Mason C, Imayama I, Kong A, Xiao L, Bain CE, Blackburn GL, Stanczyk FZ, McTiernan (2012) Reduced-calorie dietary weight loss, exercise, and sex hormones in postmenopausal women: randomized controlled trial. J Clin Oncol 30:2314–2326

    Article  PubMed  CAS  Google Scholar 

  57. Imayama I, Ulrich CM, Alfano CM, Wang C, Xiao L, Wener MH, Campbell KL, Duggan C, Foster-Schubert KE, Kong A, Mason CE, Wang CY, Blackburn GL, Bain CE, Thompson HJ, McTiernan A (2012) Effects of a caloric restriction weight loss diet and exercise on inflammatory biomarkers in overweight/obese postmenopausal women: a randomized controlled trial. Cancer Res 72:2314–2326

    Article  PubMed  CAS  Google Scholar 

  58. Abbenhardt C, McTiernan A, Alfano CM, Wener MH, Campbell KL, Duggan C, Foster-Schubert KE, Kong A, Toriola AT, Potter JD, Mason C, Xiao L, Blackburn GL, Bain C, Ulrich CM (2013) Effects of individual and combined dietary weight loss and exercise interventions in postmenopausal women on adiponectin and leptin levels. J Intern Med 274:115–163

    Article  Google Scholar 

  59. Grossmann ME, Ray A, Dogan S, Mizuno NK, Cleary MP (2008) Balance of adiponectin and leptin modulates breast cancer cell growth. Cell Res 18:1154–1156

    Article  PubMed  CAS  Google Scholar 

  60. Ollberding NJ, Kim Y, Shvetsov YB, Wilkens LR, Franke AA, Cooney RV, Maskarinec G, Hernandez BY, Henderson BE, Le Marchand L, Kolonel LN, Goodman MT (2013) Prediagnostic leptin, adiponectin, C-reactive protein, and the risk of postmenopausal breast cancer. Cancer Prev Res 6:188–195

    Article  CAS  Google Scholar 

  61. Santen RJ, Boyd NF, Chlebowski RT, Cummings S, Cuzick J, Dowsett M, Easton D, Forbes JF, Key T, Hankinson SE, Howell A, Ingle J; Breast Cancer Prevention Collaborative Group (2007) Critical assessment of new risk factors for breast cancer: considerations for development of an improved risk prediction model. Endocr Relat Cancer 14:169–187

    Article  Google Scholar 

  62. Prieto-Hontoria PL, Pérez-Matute P, Fernández-Galilea M, Bustos M, Martínez JA, Moreno-Aliaga MJ (2011) Role of obesity-associated dysfunctional adipose tissue in cancer: a molecular nutrition approach. Biochim Biophys Acta 807:664–678

    Google Scholar 

  63. Goodwin PJ, Ennis M, Pritchard KI, Trudeau ME, Koo J, Taylor SK, Hood N (2012) Insulin- and obesity-related variables in early-stage breast cancer: correlations and time course of prognostic associations. J Clin Oncol 30:164–171

    Article  Google Scholar 

  64. Fabian CJ, Kimler BF, Mayo MS, Khan SA (2005) Breast tissue sampling for risk assessment and prevention. Endocr Relat Cancer 12:185–213

    Article  PubMed  CAS  Google Scholar 

  65. Hartmann LC, Sellers TA, Frost MH, Lingle WL, Degnim AC, Ghosh K, Vierkant RA, Maloney SD, Pankratz VS, Hillman DW, Suman VJ, Johnson J, Blake C, Tlsty T, Vachon CM, Melton LJ 3rd, Visscher DW (2005) Benign breast disease and the risk of breast cancer. N Engl J Med 353:229–237

    Article  PubMed  CAS  Google Scholar 

  66. Shaaban AM, Sloane JP, West CR, Foster CS (2002) Breast cancer risk in usual ductal hyperplasia is defined by estrogen receptor alpha and Ki-67 expression. Am J Pathol 160:597–604

    Article  PubMed  Google Scholar 

  67. Santisteban M, Reynolds C, Barr Fritcher EG, Frost MH, Vierkant RA, Anderson SS, Degnim AC, Visscher DW, Pankratz VS, Hartmann LC (2010) Ki67: a time-varying biomarker of risk of breast cancer in atypical hyperplasia. Breast Cancer Res Treat 121:431–437

    Article  PubMed  CAS  Google Scholar 

  68. Ibarra-Drendall C, Wilke LG, Zalles C, Scott V, Archer LE, Lem S, Yee LD, Lester J, Kulkarni S, Murekeyisoni C, Wood M, Wilson K, Garber J, Gentry C, Stouder A, Broadwater G, Baker JC Jr, Vasilatos SN, Owens E, Rabiner S, Barron AC, Seewaldt VL (2009) Reproducibility of random periareolar fine needle aspiration in a multi-institutional Cancer and Leukemia Group B (CALGB) cross-sectional study. Cancer Epidemiol Biomarkers Prev 18:1379–1385

    Article  PubMed  Google Scholar 

  69. Hofseth LJ, Raafat AM, Osuch JR, Pathak DR, Slomski CA, Haslam SZ (1999) Hormone replacement therapy with estrogen or estrogen plus medroxyprogesterone acetate is associated with increased epithelial proliferation in the normal postmenopausal breast. J Clin Endocrinol Metab 84:4559–4565

    Article  PubMed  CAS  Google Scholar 

  70. Befort CA, Austin H, Klemp JR (2011) Weight control needs and experiences among rural breast cancer survivors. Psychooncology 20:1069–1075

    Article  PubMed  Google Scholar 

  71. Befort CA, Klemp JR, Austin HL, Perri MG, Schmitz KH, Sullivan DK, Fabian CJ (2012) Outcomes of a weight loss intervention among rural breast cancer survivors. Breast Cancer Res Treat 132:631–639

    Article  PubMed  Google Scholar 

  72. Ogden J (2000) The correlates of long-term weight loss: a group comparison study of obesity. Int J Obes Relat Metab Disord 24:1018–1025

    Article  PubMed  CAS  Google Scholar 

  73. Wing RR, Phelan S (2005) Long-term weight loss maintenance. Am J Clin Nutr 82(1 Suppl):222S–225S

    PubMed  CAS  Google Scholar 

  74. Milsom VA, Middleton KM, Perri M (2011) Successful long-term weight loss maintenance in a rural population. Clin Interv Aging 6:303–309

    Article  PubMed  Google Scholar 

  75. Middleton KM, Patidar SM, Perri MG (2012) The impact of extended care on the long-term maintenance of weight loss: a systematic review and meta-analysis. Obes Rev 13:509–517

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

Supported by grants 5R21CA121106 from NIH, and the Breast Cancer Research Foundation (KUMC); 5R01CA129409 from NIH (UT Austin); and CA16672 from NIH (MD Anderson Cancer Center). The University of Virginia Center for Research in Reproduction Ligand Assay and Analysis Core is supported by the Eunice Kennedy Shriver NICHD/NIH (SCCPIR) Grant U54-HD28934. Health Management Resources provided discounted packaged meals and shakes.

Conflict of interest

Authors have no conflicts of interest to declare.

Author information

Authors and Affiliations

  1. Department of Internal Medicine, University of Kansas Medical Center, 3901 Rainbow Boulevard, Kansas City, KS, 66160, USA

    Carol J. Fabian, Joseph E. Donnelly, Jennifer R. Klemp, Brian K. Petroff, Teresa A. Phillips, Trina Metheny & Sonya Aversman

  2. Department of Radiation Oncology, University of Kansas Medical Center, 3901 Rainbow Boulevard, Kansas City, KS, 66160, USA

    Bruce F. Kimler

  3. Department of Dietetics and Nutrition, University of Kansas Medical Center, 3901 Rainbow Boulevard, Kansas City, KS, 66160, USA

    Debra K. Sullivan

  4. Department of Biostatistics, University of Kansas Medical Center, 3901 Rainbow Boulevard, Kansas City, KS, 66160, USA

    Hung-wen Yeh

  5. Mercy Hospital, 3663 S Miami Ave, Miami, FL, 33133, USA

    Carola M. Zalles

  6. Department of Systems Biology, University of Texas MD Anderson Cancer Center, 1515 Holcombe Blvd., Houston, TX, 77030, USA

    Gordon B. Mills

  7. Department of Nutritional Sciences, University of Texas at Austin, 1 University Station, A2703, Austin, TX, 78712, USA

    Stephen D. Hursting

Authors
  1. Carol J. Fabian
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bruce F. Kimler
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Joseph E. Donnelly
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Debra K. Sullivan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jennifer R. Klemp
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Brian K. Petroff
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Teresa A. Phillips
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Trina Metheny
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Sonya Aversman
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Hung-wen Yeh
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Carola M. Zalles
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Gordon B. Mills
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Stephen D. Hursting
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Carol J. Fabian.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fabian, C.J., Kimler, B.F., Donnelly, J.E. et al. Favorable modulation of benign breast tissue and serum risk biomarkers is associated with >10 % weight loss in postmenopausal women. Breast Cancer Res Treat 142, 119–132 (2013). https://doi.org/10.1007/s10549-013-2730-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10549-013-2730-8

Keywords

Search

Navigation