Fracture Risks Related to Parity and Breastfeeding Effect in Post-Menopausal Women Aged Sixty and Over: Results from the “Quality of Bone in Lorraine” Register — Oak Academic Publishing
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Fracture Risks Related to Parity and Breastfeeding Effect in Post-Menopausal Women Aged Sixty and Over: Results from the “Quality of Bone in Lorraine” Register
Department of Endocrinology, University Hospital Center of Nancy, Lorraine, France
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Department of Epidemiology and Clinical Evaluation, University Hospital Center of Nancy, Lorraine, France
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Department of Internal Medicine II, University Hospital Center of Dakar, Cheikh Anta Diop University, Dakar, Sénégal
,
Department of Endocrinology, University Hospital Center of Nancy, Lorraine, France
,
Department of Obstetrics and Medical Gynecology, University Hospital Center of Nancy, Lorraine, France
,
Department of Internal Medicine II, University Hospital Center of Dakar, Cheikh Anta Diop University, Dakar, Sénégal
,
Department of Obstetrics and Medical Gynecology, University Hospital Center of Nancy, Lorraine, France
,
Department of Endocrinology, University Hospital Center of Nancy, Lorraine, France
1 Department of Endocrinology, University Hospital Center of Nancy, Lorraine, France
2 Department of Epidemiology and Clinical Evaluation, University Hospital Center of Nancy, Lorraine, France
3 Department of Internal Medicine II, University Hospital Center of Dakar, Cheikh Anta Diop University, Dakar, Sénégal
4 Department of Endocrinology, University Hospital Center of Nancy, Lorraine, France
5 Department of Obstetrics and Medical Gynecology, University Hospital Center of Nancy, Lorraine, France
6 Department of Internal Medicine II, University Hospital Center of Dakar, Cheikh Anta Diop University, Dakar, Sénégal
7 Department of Obstetrics and Medical Gynecology, University Hospital Center of Nancy, Lorraine, France
8 Department of Endocrinology, University Hospital Center of Nancy, Lorraine, France
Introduction: The long term effect of accumulation of genital events as repeated pregnancy and longer breastfeeding in bone heath later in women’s life is still disputed. The objective was to assess the impact of parity and cumulated duration of breastfeeding on fracture risk in post-menopausal women aged sixty an over. Patients and Methods: It was a leading study from the register “Quality of Bone in Lorraine (QBL)” achieved in the department of endocrinology and osteoporotic disease of Nancy (France). This register included all patients sent for an assessment of the bone mass density from January 1, 2006 to December 31, 2014 (9 years). It was about post-menopausal women aged sixty an over suffering or not from osteoporosis fracture or bone fragility just after the age of 45. The genital events of patients to their age (from puberty to menopause) as well as the existence of hormone replacement therapy use, parity, and breastfeeding duration were taken into account. The assessment of bone fracture was clinical, radiological or by using the vertebral fracture assessment method. Results: 861 post-menopausal women were included. In comparison to the control group, the fractured population had a mean age of (74.3 ± 9 vs. 72 ± 8 years), a family history of fracture (32.1% vs. 26%), and an average input of calcium (2.4 ± 1 vs. 2.3 ± 0 portions per day). The age at menarche was of 12.8 ± 1 years in each group, a mean genital activity duration of (36.8 ± 3 vs. 37.2 ± 3 years), a parity of (2.1 ± 1 vs. 1.8 ± 1 children), a cumulated breastfeeding duration (4.2 ± 16 vs. 3.1 ± 5 months) and an age of menopause of (48.6 ± 4 vs. 48.6 ± 4 years) were respectively found in fractured and witness population. Overall, an osteoporotic fracture has been rediscovered in 50.9%. In multivariate analysis, only a cumulative duration of breastfeeding of 6 months and over was associated with a higher fracture risk (OR = 1.5 [1.1 - 2.2]). The impact of parity was not significant (OR = 1.1 [0.7 - 1.8]). Association with obesity was quasi significant (OR = 1.3 [0.9 - 1.9]). There was no correlation between the fracture risk and the genital activity duration (OR = 0.7 [0.5 - 1.0]), hormone replacement therapy use (OR = 1.0 [0.8 - 1.4]), daily calcium input (OR = 0.8 [0.6 - 1.3]), and age of menarche (OR = 1.0 [0.9 - 1.1]). Conclusion: This work confirms a negative impact from 6 months of cumulative breastfeeding. The modest effects observed may be related to the selection of Caucasian patients who live in an economically developed country with a limited number of pregnancies and limited duration of breastfeeding.
KeywordsParityBreastfeedingFracture Risk
Melton, L.J., Chrischilles, E.A., Cooper, C., Lane, A.W. and Riggs, B.L. (1992) Perspective: How Many Women Have Osteoporosis? Journal of Bone and Mineral Research, 7, 1005-1010. https://doi.org/10.1002/jbmr.5650070902
Silva, M.J. and Gibson, L.J. (1997) Modeling the Mechanical Behavior of Vertebral Trabecular Bone: Effects of Age-Related Changes in Microstructure. Bone, 21, 191-199. https://doi.org/10.1016/S8756-3282(97)00100-2
Currey, J.D. (1999) What Determines the Bending Strength of Compact Bone? Journal of Experimental Biology, 202, 2495-2503.
Prentice, A. (2000) Calcium in Pregnancy and Lactation. Annual Review of Nutrition, 20, 249-272. https://doi.org/10.1146/annurev.nutr.20.1.249
Ensom, M.H., Liu, P.Y. and Stephenson, M.D. (2002) Effect of Pregnancy on Bone Mineral Density in Healthy Women. Obstetrical & Gynecological Survey, 57, 99-111. https://doi.org/10.1097/00006254-200202000-00022
Karlsson, M.K., Ahlborg, H.G. and Karlsson, C. (2005) Female Reproductive History and the Skeleton: A Review. BJOG: An International Journal of Obstetrics & Gynaecologyl, 112, 851-856. https://doi.org/10.1111/j.1471-0528.2005.00571.x
Bezerra, F.F., Mendonça, L.M., Lobato, E.C., O’Brien, K.O. and Donangelo, C.M. (2004) Bone Mass Is Recovered from Lactation to Post-Weaning in Adolescent Mothers with Low Calcium Intakes. The American Journal of Clinical Nutrition, 80, 1322-1326. https://doi.org/10.1093/ajcn/80.5.1322
Duan, X., Wang, J. and Jiang, X. (2016) A Meta-Analysis of Breast-feeding and Osteoporotic Fracture Risk in the Females. Osteoporosis International, 28, 495-503. https://doi.org/10.1007/s00198-016-3753-x
Wang, Q., Huang, Q., Zeng, Y., Liang, J.J., Liu, S.Y., Gu, X. and Liu, J.A. (2016) Parity and Osteoporotic Fracture Risk in Postmenopausal Women: A Dose-Response Meta-Analysis of Prospective Studies. Osteoporosis International, 27, 319-330. https://doi.org/10.1007/s00198-015-3351-3
Diédhiou, D., Weryha, G., Angelousi, A., et al. (2017) Impact of Parity on Fracture Risk after Menopause: A Systematic Review. HSOA Journal of Human Endocrinology, 2, 009. https://doi.org/10.24966/HHE-9640/10009
Kanis, J.A., Oden, A., Johnell, O., et al. (2007) The Use of Clinical Risk Factors Enhances the Performance of BMD in the Prediction of Hip and Osteoporotic Fractures in Men and Women. Osteoporosis International, 18, 1033-1046. https://doi.org/10.1007/s00198-007-0343-y
Menopause
Genant, H.K., Li, J., Wu, C.Y. and Shepherd, J.A. (2000) Vertebral Fractures in Osteoporosis: A New Method for Clinical Assessment. Journal of Clinical Densitometry, 3, 281-290. https://doi.org/10.1385/JCD:3:3:281
Riggs, B.L., Melton, L.J., Robb, R.A., et al. (2004) Population-Based Study of Age and Sex Differences in Bone Volumetric Density, Size, Geometry and Structure at Different Skeletal Sites. Journal of Bone and Mineral Research, 19, 1945-1954. https://doi.org/10.1359/jbmr.040916
Cole, T.J., Bellizzi, M.C., Flegal, M. and Dietz, W.H. (2000) Establishing a Standard Definition for Child Overweight and Obesity Worldwide: International Survey. BMJ, 320, 1240-1243. https://doi.org/10.1136/bmj.320.7244.1240
Black, A.J., Reid, R., Reid, D.M., MacDonald, A.G. and Fraser, W.D. (2003) Effect of Pregnancy on Bone Mineral Density and Biochemical Markers of Bone Turnover in a Patient with Juvenile Idiopathic Osteoporosis. Journal of Bone and Mineral Research, 18, 167-171. https://doi.org/10.1359/jbmr.2003.18.1.167
Peris, P., Guañabens, N., Monegal, A., et al. (2002) Pregnancy Associated Osteoporosis: The Familial Effect. Clinical and Experimental Rheumatology, 20, 697-700.
Anai, T., Tomiyasu, T., Arima, K. and Miyakawa, I. (1999) Pregnancy-Associated Osteoporosis with Elevated Levels of Circulating Parathyroid Hormone-Related Protein: A Report of Two Cases. Journal of Obstetrics and Gynaecology Research, 25, 63-67. https://doi.org/10.1111/j.1447-0756.1999.tb01124.x
Hwang, I.R., Choi, Y.K., Lee, W.K., et al. (2016) Association between Prolonged Breastfeeding and Bone Mineral Density and Osteoporosis in Postmenopausal Women: KNHANES 2010-2011. Osteoporosis International, 27, 257-265. https://doi.org/10.1007/s00198-015-3292-x
Ahn, S.K., Kam, S. and Chun, B.Y. (2014) Incidence of and Factors for Self-Reported Fragility Fractures among Middle-Aged and El-derly Women in Rural Korea: An 11-Year Follow-Up Study. Journal of Preventive Medicine & Public Health, 47, 289-297. https://doi.org/10.3961/jpmph.14.020
Bolzetta, F., Veronese, N., De Rui, M., et al. (2014) Duration of Breastfeeding as a Risk Factor for Vertebral Fractures. Bone, 68, 41-45. https://doi.org/10.1016/j.bone.2014.08.001
Carneiro, R.M., Prebehalla, L., Tedesco, M.B., et al. (2010) Lactation and Bone Turnover: A Conundrum of Marked Bone Loss in the Setting of Coupled Bone Turnover. The Journal of Clinical Endocrinology & Metabolism, 95, 1767-1776. https://doi.org/10.1210/jc.2009-1518
VanHouten, J.N., Dann, P., Stewart, A.F., et al. (2003) Mammary-Specific Deletion of Parathyroid Hormone-Related Protein Preserves Bone Mass during Lactation. Journal of Clinical Investigation, 112, 1429-1436. https://doi.org/10.1172/JCI200319504
VanHouten, J.N. and Wysolmerski, J.J. (2003) Low Estrogen and High Parathyroid Hormone-Related Peptide Levels Contribute to Accelerated Bone Resorption and Bone Loss in Lactating Mice. Endocrinology, 144, 5521-5529. https://doi.org/10.1210/en.2003-0892
Bjørnerem, Å., Ghasem-Zadeh, A., et al. (2016) Irreversible Deterioration of Cortical and Trabecular Microstructure Associated with Breastfeeding. Journal of Bone and Mineral Research, 32, 676-680. https://doi.org/10.1002/jbmr.3018
Dursun, N., Akin, S., Dursun, E., Sade, I. and Korkusuz, F. (2006) Influence of Duration of Total Breast-Feeding on Bone Mineral Density in a Turkish Population: Does the Priority of Risk Factors Differ from Society to Society? Osteoporosis International, 17, 651-655. https://doi.org/10.1007/s00198-005-0029-2
Chan, H.H., Lau, E.M., Woo, J., Lin, F., Sham, A. and Leung, P.C. (1996) Dietary Calcium Intake, Physical Activity and the Risk of Vertebral Fracture in Chinese. Osteoporosis International, 6, 228-232. https://doi.org/10.1007/BF01622739
Johnell, O., Gullberg, B., Kanis, J.A., et al. (1995) Risk Factors for Hip Fracture in European Women: The MEDOS Study. Mediterranean Osteoporosis Study. Journal of Bone and Mineral Research, 10, 1802-1815. https://doi.org/10.1002/jbmr.5650101125
Clark, P., DeLa Pena, F., Gomez-Garcia, F., Orozco, J.A. and Tugwell, P. (1998) Risk Factors for Osteoporotic Hip Fractures in Mexicans. Archives of Medical Research, 29, 253-257.
Michaëlsson, K., Baron, J.A., Farahmand, B.Y. and Ljunghall, S. (2001) Influence of Parity and Lactation on Hip Fracture Risk. American Journal of Epidemiology, 153, 1166-1172. https://doi.org/10.1093/aje/153.12.1166
Cure-Cure, C., Cure-Ramírez, P., Terán, E. and López-Jaramillo, P. (2002) Bone-Mass Peak in Multiparity and Reduced Risk of Bone-Fractures in Menopause. International Journal of Gynecology & Obstetrics, 76, 285-291. https://doi.org/10.1016/S0020-7292(01)00583-5
Naves, M., Diaz-Lopez, J.B., Gomez, C., Rodriguez-Rebollar, A. and Cannata-Andia, J.B. (2005) Determinants of Incidence of Osteoporotic Fractures in the Female Spanish Population Older than 50. Osteoporosis International, 16, 2013-2017. https://doi.org/10.1007/s00198-005-1983-4
Mori, T., Ishii, S., Greendale, G.A., et al. (2015) Parity, Lactation, Bone Strength, and 16-Year Fracture Risk in Adult Women: Findings from the Study of Women’s Health across the Nation (SWAN). Bone, 73, 160-166. https://doi.org/10.1016/j.bone.2014.12.013
Lambrinoudaki, I., Flokatoula, M., Armeni, E., et al. (2015) Vertebral Fracture Prevalence among Greek Healthy Middle-Aged Postmenopausal Women: Association with Demographics, Anthropometric Parameters, and Bone Mineral Density. The Spine Journal, 15, 86-94. https://doi.org/10.1016/j.spinee.2014.07.021
Hoffman, S., Grisso, J.A., Kelsey, J.L., Gammon, M.D. and O’Brien, L.A. (1993) Parity, Lactation and Hip Fracture. Osteoporosis International, 3, 171-176. https://doi.org/10.1007/BF01623672
Cumming, R.G. and Klineberg, R.J. (1993) Breastfeeding and Other Reproductive Factors and the Risk of Hip Fractures in Elderly Women. International Journal of Epidemiology, 22, 684-691. https://doi.org/10.1093/ije/22.4.684
Alderman, B.W., Weiss, N.S., Daling, J.R., Ure, C.L. and Ballard, J.H. (1986) Reproductive History and Postmenopausal Risk of Hip and Forearm Fracture. American Journal of Epidemiology, 124, 262-267. https://doi.org/10.1093/oxfordjournals.aje.a114384
Bjørnerem, A., Ahmed, L.A., Jørgensen, L., Størmer, J. and Joakimsen, R.M. (2011) Breastfeeding Protects against Hip Fracture in Postmenopausal Women: The Tromsø Study. Journal of Bone and Mineral Research, 26, 2843-2850. https://doi.org/10.1002/jbmr.496
Huo, D., Lauderdale, D.S. and Li, L. (2003) Influence of Reproductive Factors on Hip Fracture Risk in Chinese Women. Osteoporosis International, 14, 694-700. https://doi.org/10.1007/s00198-003-1429-9
Mallmin, H.S., Ljunghall, S., Persson, I. and Bergström, R. (1994) Risk Factors for Fractures of the Distal Forearm: A Population-Based Case-Control Study. Osteoporosis International, 4, 298-304. https://doi.org/10.1007/BF01622186
Wiklund, P.K., Xu, L., Wang, Q., et al. (2012) Lactation Is Associated with Greater Maternal Bone Size and Bone Strength Later in Life. Osteoporosis International, 23, 1939-1945. https://doi.org/10.1007/s00198-011-1790-z
Chapman, D.J. (2012) Longer Cumulative Breastfeeding Duration Associated with Improved Bone Strength. Journal of Human Lactation, 28, 18-19. https://doi.org/10.1177/0890334411433573
Streeten, E.A., Ryan, K.A., McBride, D.J., Pollin, T.I., Shuldiner, A.R. and Mitchell, B.D. (2005) The Relationship between Parity and Bone Mineral Density in Women Characterized by a Homogeneous Lifestyle and High Parity. The Journal of Clinical Endocrinology & Metabolism, 90, 4536-4541. https://doi.org/10.1210/jc.2004-1924
Schnatz, P.F., Marakovits, K.A. and O’Sullivan, D.M. (2010) Assessment of Postmenopausal Women and Significant Risk Factors for Osteoporosis. Obstetrical & Gynecological Survey, 65, 591-596. https://doi.org/10.1097/OGX.0b013e3181fc6d30
Seeman, E. (2002) Pathogenesis of Bone Fragility in Women and Men. The Lancet, 359, 1841-1850. https://doi.org/10.1016/S0140-6736(02)08706-8
Henderson, P.H., Sowers, M., Kutzko, K.E. and Jannausch, M.L. (2000) Bone Mineral Density in Grand Multiparous Women with Extended Lactation. American Journal of Obstetrics & Gynecology, 182, 1371-1377. https://doi.org/10.1067/mob.2000.107468
Cauley, J.A., Wu, L.L., Wampler, N.S., et al. (2007) Clinical Risk Factors for Fractures in Multi-Ethnic Women: The Women’s Health Initiative. Journal of Bone and Mineral Research, 22, 1816-1826. https://doi.org/10.1359/jbmr.070713
El-Maghraoui, A., Rezqi, A., Mounach, A., Achemlal, L., Bezza, A. and Ghozlani, I. (2013) Systematic Vertebral Fracture Assessment in Symptomatic Postmenopausal Women. Bone, 52, 176-180. https://doi.org/10.1016/j.bone.2012.09.023
Fujiwara, S., Kasagi, F., Yamada, M. and Kodama, K. (1997) Risk Factors for Hip Fracture in Japanese Cohort. Journal of Bone and Mineral Research, 12, 998-1004. https://doi.org/10.1359/jbmr.1997.12.7.998
Trémollières, F.A., Pouilles, J.M., Drewniak, N., Laparra, J., Ribot, C.A. and Dargent-Molina, P. (2010) Fracture Risk Prediction Using BMD and Clinical Risk Factors in Early Postmenopausal Women: Sensitivity of the WHO FRAX Tool. Journal of Bone and Mineral Research, 25, 1002-1009. https://doi.org/10.1002/jbmr.12
Honkanen, R.J., Honkanen, K., Kröger, H., Alhava, E., Tuppurainen, M. and Saarikoski, S. (2000) Risk Factors for Perimenopausal Distal Forearm Fracture. Osteoporosis International, 11, 265-270. https://doi.org/10.1007/s001980050291
Paganini-Hill, A., Atchison, K.A., Gornbein, J.A., Nattiv, A., Service, S.K. and White, S.C. (2005) Menstrual and Reproductive Factors and Fracture Risk: The Leisure World Cohort Study. Journal of Women’s Health (Larchmt), 14, 808-819. https://doi.org/10.1089/jwh.2005.14.808
Hillier, T.A., Rizzo, J.H., Pedula, K.L., et al. (2003) Nulliparity and Fracture Risk in Older Women: The Study of Osteoporotic Fractures. Journal of Bone and Mineral Research, 18, 893-899. https://doi.org/10.1359/jbmr.2003.18.5.893
Taylor, B.C., Schreiner, P.J., Stone, K.L., et al. (2004) Long-Term Prediction of Incident Hip Fracture Risk in Elderly White Women: Study of Osteoporotic Fractures. Journal of the American Geriatrics Society, 52, 1479-1486. https://doi.org/10.1111/j.1532-5415.2004.52410.x
Kauppi, M., Heliövaara, M., Impivaara, O., Knekt, P. and Jula, A. (2011) Parity and Risk of Hip Fracture in Postmenopausal Women. Osteoporosis International, 22, 1765-1771. https://doi.org/10.1007/s00198-010-1392-1
Nguyen, T.V., Jones, G., Sambrook, P.N., White, C.P., Kelly, P.J. and Eisman, J.A. (1995) Effects of Estrogen Exposure and Reproductive Factors on Bone Mineral Density and Osteoporotic Fractures. The Journal of Clinical Endocrinology & Metabolism, 80, 2709-2714. https://doi.org/10.1210/jcem.80.9.7673413