Association between breastfeeding and osteoporotic hip fracture in women:
Osteoporotic fracture has become a common healthproblem all over the world due to the aging of the popu-lation . More than one third of 50-year-old womenwill suffer from serious osteoporotic fractures in theirremaining lifetimes , and every 3 s one osteoporoticfracture occurs somewhere in the world. Hip fracture isalso known as the last fracture in their remainder life-times and is considered the most serious type of osteo-porotic fractures due to high morbidity and mortality.The previous study demonstrated that an approximated20 to 40% of patients with hip fracture will suffer fromdeath in 1 year, and only one in three of these patientscan recover their previous functional status .Breastfeeding is an essential reproductive functionamong females, provides approximately 300 mg of cal-cium a day into infants to maintain the physical develop-ment of infants , and results in 5 to 10% bone loss inwomen during breastfeedingBesides, they need toprovide large amounts of calcium for mineralization of thefetal and neonatal skeleton . Therefore, bone loss inwomenstartsearlierthaninmen and this may be onereason why osteoporosis occurs in older women far morethan in men. Women with severe osteoporosis may sufferfrom a fragility fracture . However, it is controversialwhether breastfeeding can increase the risk of osteoporotichip fractures, and the possible mechanism is considerablycomplicated. Some studies demonstrated breastfeeding maycontribute to protection against osteoporotic hip fractures, and the risk will decrease with the extent of breast-feeding . However, some studies indicated thatprolonged breastfeeding time can decrease bone mineraldensity . Whereas others indicated that breastfeed-ing was unrelated to osteoporotic hip fracture or bonedensity in postmenopausal women . What is more,there is insufficient evidence in individual studies to showthe relationship between them and express conflictingconclusions.Therefore, we performed this dose-response meta-analysis to investigate the association between breast-feeding and osteoporotic hip fracture in women, hy-pothesizing that breastfeeding is associated with lowerosteoporotic hip fracture, and to provide a better guidistrategy for clinicians.
The association between breastfeeding and bone min-eral density (BMD) in older women is complicated; studiesin different regions have yielded different conclusions. In anationwide survey in Korea by Hwang et al., the outcomesindicated that breastfeeding for more than 37 months candecrease the BMD in postmenopausal women . Foxet al. pointed out there was no significant difference in theradius BMD between the women who was breastfeedingwith those who were not . Murphy et al. reported thatthere was no association between BMD and breastfeedingin the hip and spine which is similar to the outcomesof Crandall et al. . The study of Bjørnerem et al. dem-onstrated that the level of BMD of female breastfeedingfor about 20 months or more were similar to those whodid not breastfeed at the distal forearm and hip [9].Besides, both Zhang et al. and Lenora et al. reported thatbreastfeeding does not significantly reduce BMD
What is more, the study of Melton et al. demonstratedthat breastfeeding for more than 8 months was associatedwith higher BMD at the femur and spine . Chantryet al. point out that compared to women who are notbreastfeeding, lactation among adolescent mothers had ahigher hip BMD at 20 to 25 years old.It is controversial whether breastfeeding impacts onfractures due to inconsistent breastfeeding time. Bolzettaet al. found that breastfeeding more than 18 months sig-nificantly increases the risk of spinal fractures in meno-pausal women , similar to the study of Dursun et al.. But Chan et al. considered that breastfeeding for24 months or more was protective against vertebral frac-ture . Bjørnerem et al. point out that there was nosignificant difference in wrist fracture between thebreastfeeding groups and the non-breastfeeding group. Whereas the study of Mallmin et al. demonstratedthat the ever breastfeeding group has a lower risk of fac-tors than the never breastfeeding group at the distalforearm. The study of Hwang et al. suggested thatprolonged breastfeeding has no significant effect on theincidence of osteoporotic hip fractures . However,Bjørneremet al. indicated that breastfeeding has nolong-term deleterious effect on bone fragility and frac-tures, even reduced risk for hip fracture in menopausalwomen . The outcomes of our meta-analysis demon-strated that breastfeeding within 25 months contributeto a reduced risk for osteoporotic hip fractures, whenbreastfeeding is longer than 25 months, there is no sig-nificant relationship between them
Hao JG, Zeng XT, Wang J, Liu L. Association between calcium or vitamin Dsupplementation and fracture incidence in community-dwelling olderadults: a systematic review and meta-analysis. JAMA. 2017;318(24):2466–82.2.
Saei Ghare Naz M, Ozgoli G, Aghdashi MA, Salmani F. Prevalence and riskfactors of osteoporosis in women referring to the bone densitometryacademic center in Urmia, Iran. Glob J Health Sci. 2015;8(7):135–45.3.
Guzon-Illescas O, Perez Fernandez E, Crespi Villarias N, Quiros Donate FJ,Pena M, Alonso-Blas C, Garcia-Vadillo A, Mazzucchelli R. Mortality afterosteoporotic hip fracture: incidence, trends, and associated factors. J OrthopSurg Res. 2019;14(1):203.4.
Kovacs CS. Calcium and bone metabolism disorders during pregnancy andlactation. Endocrinol Metab Clin North Am. 2011;40(4):795–826.5.
Kalkwarf HJ. Hormonal and dietary regulation of changes in bone densityduring lactation and after weaning in women. J Mammary Gland BiolNeoplasia. 1999;4(3):319–29.6. Kovacs CS. Calcium and bone metabolism during pregnancy and lactation.J Mammary Gland Biol Neoplasia. 2005;10(2):105–18.7.
Bjørnerem A, Ahmed LA, Joakimsen RM, Berntsen GK, Fonnebo V, JorgensenL, Oian P, Seeman E, Straume B. A prospective study of sex steroids, sexhormone-binding globulin, and non-vertebral fractures in women and men:the Trømso Study. Eur J Endocrinol. 2007;157(1):119–25.8.
Miyamoto T, Miyakoshi K, Sato Y, Kasuga Y, Ikenoue S, Miyamoto K,Nishiwaki Y, Tanaka M, Nakamura M, Matsumoto M. Changes in bonemetabolic profile associated with pregnancy or lactation. Sci Rep. 2019;9(1):6787.9.
Bjørnerem A, Ahmed LA, Jorgensen L, Stormer J, Joakimsen RM.Breastfeeding protects against hip fracture in postmenopausal women: theTrømso study. J Bone Miner Res. 2011;26(12):2843–50.10.
Huo D, Lauderdale DS, Li L. Influence of reproductive factors on hip fracturerisk in Chinese women. Osteoporos Int. 2003;14(8):694–700.11.
Michaelsson K, Baron JA, Farahmand BY, Ljunghall S. Influence of parity andlactation on hip fracture risk. Am J Epidemiol. 2001;153(12):1166–72.12.
Cumming RG, Klineberg RJ. Breastfeeding and other reproductive factorsand the risk of hip fractures in elderly women. Int J Epidemiol. 1993;22(4):684–91.13. Tsvetov G, Levy S, Benbassat C, Shraga-Slutzky I, Hirsch D. Influence ofnumber of deliveries and total breast-feeding time on bone mineral densityin premenopausal and young postmenopausal women. Maturitas. 2014;77(3):249–54.14.
Hwang IR, Choi YK, Lee WK, Kim JG, Lee IK, Kim SW, Park KG. Associationbetween prolonged breastfeeding and bone mineral density andosteoporosis in postmenopausal women: KNHANES 2010-2011. OsteoporosInt. 2016;27(1):257–65.15.
Crandall CJ, Liu J, Cauley J, Newcomb PA, Manson JE, Vitolins MZ, JacobsonLT, Rykman KK, Stefanick ML. Associations of parity, breastfeeding, andfractures in the Women’s Health Observational Study. Obstet Gynecol. 2017;130(1):171–80.16. Hoffman S, Grisso JA, Kelsey JL, Gammon MD, O'Brien LA. Parity, lactationand hip fracture. Osteoporos Int. 1993;3(4):171–6.17.
Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items forsystematic reviews and meta-analyses: the PRISMA statement. Int J Surg.2010;8(5):336–41.18.
Slim K, Nini E, Forestier D, Kwiatkowski F, Panis Y, Chipponi J.Methodological index for non-randomized studies (minors): developmentand validation of a new instrument. ANZ J Surg. 2003;73(9):712–6.19.
Greenland S, Longnecker MP. Methods for trend estimation fromsummarized dose-response data, with applications to meta-analysis. Am JEpidemiol. 1992;135(11):1301–9.20.
Shao C, Tang H, Zhao W, He J. Nut intake and stroke risk: a dose-responsemeta-analysis of prospective cohort studies. Sci Rep. 2016;6:30394.21.
Orsini N, Li R, Wolk A, Khudyakov P, Spiegelman D. Meta-analysis for linearand nonlinear dose-response relations: examples, an evaluation ofapproximations, and software. Am J Epidemiol. 2012;175(1):66–73.Xiaoet al. Journal of Orthopaedic Surgery and Research (2020) 15:15 Page 6 of 7
The association between breastfeeding and bone min-eral density (BMD) in older women is complicated; studiesin different regions have yielded different conclusions. In anationwide survey in Korea by Hwang et al., the outcomesindicated that breastfeeding for more than 37 months candecrease the BMD in postmenopausal women . Foxet al. pointed out there was no significant difference in theradius BMD between the women who was breastfeedingwith those who were not . Murphy et al. reported thatthere was no association between BMD and breastfeedingin the hip and spine which is similar to the outcomesof Crandall et al. . The study of Bjørnerem et al. dem-onstrated that the level of BMD of female breastfeedingfor about 20 months or more were similar to those whodid not breastfeed at the distal forearm and hip [9].Besides, both Zhang et al. and Lenora et al. reported thatbreastfeeding does not significantly reduce BMD
What is more, the study of Melton et al. demonstratedthat breastfeeding for more than 8 months was associatedwith higher BMD at the femur and spine . Chantryet al. point out that compared to women who are notbreastfeeding, lactation among adolescent mothers had ahigher hip BMD at 20 to 25 years old.It is controversial whether breastfeeding impacts onfractures due to inconsistent breastfeeding time. Bolzettaet al. found that breastfeeding more than 18 months sig-nificantly increases the risk of spinal fractures in meno-pausal women , similar to the study of Dursun et al.. But Chan et al. considered that breastfeeding for24 months or more was protective against vertebral frac-ture . Bjørnerem et al. point out that there was nosignificant difference in wrist fracture between thebreastfeeding groups and the non-breastfeeding group. Whereas the study of Mallmin et al. demonstratedthat the ever breastfeeding group has a lower risk of fac-tors than the never breastfeeding group at the distalforearm. The study of Hwang et al. suggested thatprolonged breastfeeding has no significant effect on theincidence of osteoporotic hip fractures . However,Bjørneremet al. indicated that breastfeeding has nolong-term deleterious effect on bone fragility and frac-tures, even reduced risk for hip fracture in menopausalwomen . The outcomes of our meta-analysis demon-strated that breastfeeding within 25 months contributeto a reduced risk for osteoporotic hip fractures, whenbreastfeeding is longer than 25 months, there is no sig-nificant relationship between them
Hao JG, Zeng XT, Wang J, Liu L. Association between calcium or vitamin Dsupplementation and fracture incidence in community-dwelling olderadults: a systematic review and meta-analysis. JAMA. 2017;318(24):2466–82.2.
Saei Ghare Naz M, Ozgoli G, Aghdashi MA, Salmani F. Prevalence and riskfactors of osteoporosis in women referring to the bone densitometryacademic center in Urmia, Iran. Glob J Health Sci. 2015;8(7):135–45.3.
Guzon-Illescas O, Perez Fernandez E, Crespi Villarias N, Quiros Donate FJ,Pena M, Alonso-Blas C, Garcia-Vadillo A, Mazzucchelli R. Mortality afterosteoporotic hip fracture: incidence, trends, and associated factors. J OrthopSurg Res. 2019;14(1):203.4.
Kovacs CS. Calcium and bone metabolism disorders during pregnancy andlactation. Endocrinol Metab Clin North Am. 2011;40(4):795–826.5.
Kalkwarf HJ. Hormonal and dietary regulation of changes in bone densityduring lactation and after weaning in women. J Mammary Gland BiolNeoplasia. 1999;4(3):319–29.6. Kovacs CS. Calcium and bone metabolism during pregnancy and lactation.J Mammary Gland Biol Neoplasia. 2005;10(2):105–18.7.
Bjørnerem A, Ahmed LA, Joakimsen RM, Berntsen GK, Fonnebo V, JorgensenL, Oian P, Seeman E, Straume B. A prospective study of sex steroids, sexhormone-binding globulin, and non-vertebral fractures in women and men:the Trømso Study. Eur J Endocrinol. 2007;157(1):119–25.8.
Miyamoto T, Miyakoshi K, Sato Y, Kasuga Y, Ikenoue S, Miyamoto K,Nishiwaki Y, Tanaka M, Nakamura M, Matsumoto M. Changes in bonemetabolic profile associated with pregnancy or lactation. Sci Rep. 2019;9(1):6787.9.
Bjørnerem A, Ahmed LA, Jorgensen L, Stormer J, Joakimsen RM.Breastfeeding protects against hip fracture in postmenopausal women: theTrømso study. J Bone Miner Res. 2011;26(12):2843–50.10.
Huo D, Lauderdale DS, Li L. Influence of reproductive factors on hip fracturerisk in Chinese women. Osteoporos Int. 2003;14(8):694–700.11.
Michaelsson K, Baron JA, Farahmand BY, Ljunghall S. Influence of parity andlactation on hip fracture risk. Am J Epidemiol. 2001;153(12):1166–72.12.
Cumming RG, Klineberg RJ. Breastfeeding and other reproductive factorsand the risk of hip fractures in elderly women. Int J Epidemiol. 1993;22(4):684–91.13. Tsvetov G, Levy S, Benbassat C, Shraga-Slutzky I, Hirsch D. Influence ofnumber of deliveries and total breast-feeding time on bone mineral densityin premenopausal and young postmenopausal women. Maturitas. 2014;77(3):249–54.14.
Hwang IR, Choi YK, Lee WK, Kim JG, Lee IK, Kim SW, Park KG. Associationbetween prolonged breastfeeding and bone mineral density andosteoporosis in postmenopausal women: KNHANES 2010-2011. OsteoporosInt. 2016;27(1):257–65.15.
Crandall CJ, Liu J, Cauley J, Newcomb PA, Manson JE, Vitolins MZ, JacobsonLT, Rykman KK, Stefanick ML. Associations of parity, breastfeeding, andfractures in the Women’s Health Observational Study. Obstet Gynecol. 2017;130(1):171–80.16. Hoffman S, Grisso JA, Kelsey JL, Gammon MD, O'Brien LA. Parity, lactationand hip fracture. Osteoporos Int. 1993;3(4):171–6.17.
Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items forsystematic reviews and meta-analyses: the PRISMA statement. Int J Surg.2010;8(5):336–41.18.
Slim K, Nini E, Forestier D, Kwiatkowski F, Panis Y, Chipponi J.Methodological index for non-randomized studies (minors): developmentand validation of a new instrument. ANZ J Surg. 2003;73(9):712–6.19.
Greenland S, Longnecker MP. Methods for trend estimation fromsummarized dose-response data, with applications to meta-analysis. Am JEpidemiol. 1992;135(11):1301–9.20.
Shao C, Tang H, Zhao W, He J. Nut intake and stroke risk: a dose-responsemeta-analysis of prospective cohort studies. Sci Rep. 2016;6:30394.21.
Orsini N, Li R, Wolk A, Khudyakov P, Spiegelman D. Meta-analysis for linearand nonlinear dose-response relations: examples, an evaluation ofapproximations, and software. Am J Epidemiol. 2012;175(1):66–73.Xiaoet al. Journal of Orthopaedic Surgery and Research (2020) 15:15 Page 6 of 7
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