Osteoporosis International

, Volume 29, Issue 10, pp 2275–2281 | Cite as

Breech presentation is associated with lower bone mass and area: findings from the Southampton Women’s Survey

  • A. Ireland
  • S. R. Crozier
  • A. E. P. Heazell
  • K. A. Ward
  • K. M. Godfrey
  • H. M. Inskip
  • C. Cooper
  • N. C. HarveyEmail author
Original Article



We compared bone outcomes in children with breech and cephalic presentation at delivery. Neonatal whole-body bone mineral content (BMC) and area were lower in children with breech presentation. At 4 years, no differences in whole-body or spine measures were found, but hip BMC and area were lower after breech presentation.


Breech presentation is associated with altered joint shape and hip dysplasias, but effects on bone mineral content (BMC), area (BA) and density (BMD) are unknown.


In the prospective Southampton Women’s Survey mother-offspring cohort, whole-body bone outcomes were measured using dual-energy X-ray absorptiometry (DXA) in 1430 offspring, as neonates (mean age 6 days, n = 965, 39 with a breech presentation at birth) and/or at age 4.1 years (n = 999, 39 breech). Hip and spine bone outcomes were also measured at age 4 years.


Neonates with breech presentation had 4.2 g lower whole-body BMC (95% CI −7.4 to − 0.9 g, P = 0.012) and 5.9 cm2 lower BA (− 10.8 to − 1.0 cm2, P = 0.019), but BMD was similar between groups (mean difference − 0.007, − 0.016 to 0.002 g/cm2, P = 0.146) adjusting for sex, maternal smoking, gestational diabetes, mode of delivery, social class, parity, ethnicity, age at scan, birthweight, gestational age and crown-heel length. There were no associations between breech presentation and whole-body outcomes at age 4 years, but, in similarly adjusted models, regional DXA (not available in infants) showed that breech presentation was associated with lower hip BMC (− 0.51, − 0.98 to − 0.04 g, P = 0.034) and BA (− 0.67, − 1.28 to − 0.07 cm2, P = 0.03) but not with BMD (− 0.009, − 0.029 to 0.012 g, P = 0.408), or spine outcomes.


These results suggest that breech presentation is associated with lower neonatal whole-body BMC and BA, which may relate to altered prenatal loading in babies occupying a breech position; these differences did not persist into later childhood. Modest differences in 4-year hip BMC and BA require further investigation.


Bone mass Epidemiology Foetal growth Osteoporosis Pregnancy 


Funding information

KMG is supported by the UK Medical Research Council (MC_UU_12011/4), the National Institute for Health Research (as an NIHR Senior Investigator (NF-SI-0515-10042) and through the NIHR Southampton Biomedical Research Centre) and the European Union’s Erasmus+ Capacity-Building ENeASEA Project. The work was supported by the European Union’s Seventh Framework Programme (FP7/2007-2013), projects EarlyNutrition and ODIN under grant agreement numbers 289346 and 613977, and the ALPHABET project [an award made through the ERA-Net on Biomarkers for Nutrition and Health (ERA HDHL)], Horizon 2020 grant agreement number 696295 (UK component: BBSRC: BB/P028179/1). HMI is supported by the UK Medical Research Council (MC_UU_12011.4). This work was supported by grants from the Medical Research Council, British Heart Foundation, Arthritis Research UK, National Institute for Health Research (NIHR) Southampton Biomedical Research Centre, University of Southampton and University Hospital Southampton NHS Foundation Trust, Nestec and NIHR Biomedical Research Centre, University of Oxford.

Compliance with ethical standards

The study was approved by Southampton and Southwest Hampshire Local Research Ethics Committee (approval numbers 267/97, 307/97, 153/99 and 005/03/t) and parental informed consent was given at both scan timepoints.

Conflicts of interest


Supplementary material

198_2018_4626_MOESM1_ESM.pptx (69 kb)
Fig. S1 (PPTX 68.7 kb)


  1. 1.
    Harvey NC, Javaid MK, Arden NK, Poole JR, Crozier SR, Robinson SM, Inskip HM, Godfrey KM, Dennison EM, Cooper C, the SWS Study Team (2010) Maternal predictors of neonatal bone size and geometry: the Southampton Women’s Survey. J Dev Orig Health Dis 1:35–41PubMedPubMedCentralCrossRefGoogle Scholar
  2. 2.
    Godfrey K, Walker-Bone K, Robinson S, Taylor P, Shore S, Wheeler T, Cooper C (2001) Neonatal bone mass: influence of parental birthweight, maternal smoking, body composition, and activity during pregnancy. J Bone Miner Res 16:1694–1703PubMedCrossRefGoogle Scholar
  3. 3.
    Holroyd CR, Osmond C, Barker DJ, Ring SM, Lawlor DA, Tobias JH, Smith GD, Cooper C, Harvey NC (2016) Placental size is associated differentially with postnatal bone size and density. J Bone Miner Res 31:1855–1864PubMedPubMedCentralCrossRefGoogle Scholar
  4. 4.
    Rogers IS, Ness AR, Steer CD, Wells JC, Emmett PM, Reilly JR, Tobias J, Smith GD (2006) Associations of size at birth and dual-energy X-ray absorptiometry measures of lean and fat mass at 9 to 10 y of age. Am J Clin Nutr 84:739–747PubMedCrossRefGoogle Scholar
  5. 5.
    Dennison EM, Syddall HE, Sayer AA, Gilbody HJ, Cooper C (2005) Birth weight and weight at 1 year are independent determinants of bone mass in the seventh decade: the Hertfordshire cohort study. Pediatr Res 57:582–586PubMedCrossRefGoogle Scholar
  6. 6.
    Hannam K, Lawlor DA, Tobias JH (2015) Maternal preeclampsia is associated with reduced adolescent offspring hip BMD in a UK population-based birth cohort. J Bone Miner Res 30:1684–1691PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    Cooper C, Westlake S, Harvey N, Javaid K, Dennison E, Hanson M (2006) Review: developmental origins of osteoporotic fracture. Osteoporos Int 17:337–347PubMedCrossRefGoogle Scholar
  8. 8.
    Ireland A, Rittweger J, Schönau E, Lamberg-Allardt C, Viljakainen H (2014) Time since onset of walking predicts tibial bone strength in early childhood. Bone 68:76–84PubMedCrossRefGoogle Scholar
  9. 9.
    Ireland A, Maden-Wilkinson T, McPhee J, Cooke K, Narici M, Degens H, Rittweger J (2013) Upper limb muscle-bone asymmetries and bone adaptation in elite youth tennis players. Med Sci Sports Exerc 45:1749–1758PubMedCrossRefGoogle Scholar
  10. 10.
    Sayers A, Deere K, Tobias JH (2015) The effect of vigorous physical activity and body composition on cortical bone mass in adolescence. J Bone Miner Res 30:584PubMedCrossRefGoogle Scholar
  11. 11.
    Ireland A, Sayers A, Deere KC, Emond A, Tobias JH (2016) Motor competence in early childhood is positively associated with bone strength in late adolescence. J Bone Miner Res 31:1089–1098PubMedPubMedCentralCrossRefGoogle Scholar
  12. 12.
    Ireland A, Muthuri S, Rittweger J, Adams JE, Ward KA, Kuh D, Cooper R (2017) Later age at onset of independent walking is associated with lower bone strength at fracture-prone sites in older men. J Bone Miner Res 32:1209–1217PubMedPubMedCentralCrossRefGoogle Scholar
  13. 13.
    Hannam K, Deere KC, Hartley A, Al-Sari UA, Clark EM, Fraser WD, Tobias JH (2017) Habitual levels of higher, but not medium or low, impact physical activity are positively related to lower limb bone strength in older women: findings from a population-based study using accelerometers to classify impact magnitude. Osteoporos Int 28:2813–2822Google Scholar
  14. 14.
    Johansson J, Nordström A, Nordström P (2015) Objectively measured physical activity is associated with parameters of bone in 70-year-old men and women. Bone 81:72–79PubMedCrossRefGoogle Scholar
  15. 15.
    Sival DA, Prechtl HF, Sonder GH, Touwen BC (1993) The effect of intra-uterine breech position on postnatal motor functions of the lower limbs. Early Hum Dev 32:161–176PubMedCrossRefGoogle Scholar
  16. 16.
    Miller E, Kouam L (1981) Zur Haufigkeit von Beckenendlagen im Verlauf Der Schwangerschaft und zum Zeitpunkt der Geburt. Zentralbl Gynakol 103:105–109PubMedGoogle Scholar
  17. 17.
    Cammu H, Dony N, Martens G, Colman R (2014) Common determinants of breech presentation at birth in singletons: a population-based study. Eur J Obstet Gynecol Reprod Biol 177:106–109PubMedCrossRefGoogle Scholar
  18. 18.
    Verbruggen SW, Kainz B, Shelmerdine SC, Hajnal JV, Rutherford MA, Arthurs OJ, Phillips AT, Nowlan NC (2018) Stresses and strains on the human fetal skeleton during development. Journal of The Royal Society InterfaceGoogle Scholar
  19. 19.
    Bartlett D, Okun N (1994) Breech presentation: a random event or an explainable phenomenon? Dev Med Child Neurol 36:833–838PubMedCrossRefGoogle Scholar
  20. 20.
    Fong BF, Savelsbergh GJ, de Vries JI (2009) Fetal leg posture in uncomplicated breech and cephalic pregnancies. Eur J Pediatr 168:443–447PubMedCrossRefGoogle Scholar
  21. 21.
    Andersen GL, Irgens LM, Skranes J, Salvesen KA, Meberg A, Vik T (2009) Is breech presentation a risk factor for cerebral palsy? A Norwegian birth cohort study. Dev Med Child Neurol 51:860–865PubMedCrossRefGoogle Scholar
  22. 22.
    Nowlan NC, Sharpe J, Roddy KA, Prendergast PJ, Murphy P (2010) Mechanobiology of embryonic skeletal development: insights from animal models. Birth Defects Res C Embryo Today 90:203–213PubMedPubMedCentralCrossRefGoogle Scholar
  23. 23.
    Giorgi M, Carriero A, Shefelbine SJ, Nowlan NC (2015) Effects of normal and abnormal loading conditions on morphogenesis of the prenatal hip joint: application to hip dysplasia. J Biomech 48:3390–3397PubMedPubMedCentralCrossRefGoogle Scholar
  24. 24.
    Chan A, McCaul KA, Cundy PJ, Haan EA, Byron-Scott R (1997) Perinatal risk factors for developmental dysplasia of the hip. Arch Dis Child Fetal Neonatal Ed 76:F94–F100Google Scholar
  25. 25.
    Hinderaker T, Uden A, Reikerås O (1994) Direct ultrasonographic measurement of femoral anteversion in newborns. Skelet Radiol 23:133–135CrossRefGoogle Scholar
  26. 26.
    Tshorny M, Mimouni FB, Littner Y, Alper A, Mandel D (2007) Decreased neonatal tibial bone ultrasound velocity in term infants born after breech presentation. J Perinatol 27:693–696PubMedCrossRefGoogle Scholar
  27. 27.
    World Health Organisation (2006) WHO child growth standards: length/height for age, weight-for-age, weight-for-length, weight-for-height and body mass index-for-age, methods and development. World Health Organization, GenevaGoogle Scholar
  28. 28.
    Hinderaker T, Daltveit AK, Irgens LM, Udén A, Reikerås O (1994) The impact of intra-uterine factors on neonatal hip instability. An analysis of 1,059,479 children in Norway. Acta Orthop Scand 65:239–242PubMedCrossRefGoogle Scholar
  29. 29.
    Luterkort M, Persson PH, Weldner BM (1984) Maternal and fetal factors in breech presentation. Obstet Gynecol 64:55–59PubMedCrossRefGoogle Scholar
  30. 30.
    Moessinger AC, Blanc WA, Marone PA, Polsen DC (1982) Umbilical cord length as an index of fetal activity: experimental study and clinical implications. Pediatr Res 16:109–112PubMedCrossRefGoogle Scholar
  31. 31.
    Wright D, Chan GM (2009) Fetal bone strength and umbilical cord length. J Perinatol 29:603–605PubMedCrossRefGoogle Scholar
  32. 32.
    Soernes T, Bakke T (1986) The length of the human umbilical cord in vertex and breech presentations. Am J Obstet Gynecol 154:1086–1087PubMedCrossRefGoogle Scholar
  33. 33.
    Hofmeyr GJ, Kulier R, West HM (2015) External cephalic version for breech presentation at term Cochrane Database Syst Rev CD000083Google Scholar
  34. 34.
    Lambeek AF, De Hundt M, Vlemmix F, Akerboom BM, Bais JM, Papatsonis DN, Mol BW, Kok M (2013) Risk of developmental dysplasia of the hip in breech presentation: the effect of successful external cephalic version. BJOG 120:607–612PubMedCrossRefGoogle Scholar
  35. 35.
    Suzuki S, Yamamuro T (1985) Fetal movement and fetal presentation. Early Hum Dev 11:255–263PubMedCrossRefGoogle Scholar
  36. 36.
    Witkop CT, Zhang J, Sun W, Troendle J (2008) Natural history of fetal position during pregnancy and risk of nonvertex delivery. Obstet Gynecol 111:875–880PubMedCrossRefGoogle Scholar
  37. 37.
    Harvey NC, Cole ZA, Crozier SR et al (2012) Physical activity, calcium intake and childhood bone mineral: a population-based cross-sectional study. Osteoporos Int 23:121–130PubMedCrossRefGoogle Scholar
  38. 38.
    Janz KF, Burns TL, Torner JC, Levy SM, Paulos R, Willing MC, Warren JJ (2001) Physical activity and bone measures in young children: the Iowa bone development study. Pediatrics 107:1387–1393PubMedCrossRefGoogle Scholar
  39. 39.
    Johannsen N, Binkley T, Englert V, Neiderauer G, Specker B (2003) Bone response to jumping is site-specific in children: a randomized trial. Bone 33:533–539PubMedCrossRefGoogle Scholar

Copyright information

© International Osteoporosis Foundation and National Osteoporosis Foundation 2018

Authors and Affiliations

  • A. Ireland
    • 1
  • S. R. Crozier
    • 2
  • A. E. P. Heazell
    • 3
  • K. A. Ward
    • 2
  • K. M. Godfrey
    • 2
    • 4
  • H. M. Inskip
    • 2
    • 4
  • C. Cooper
    • 2
    • 4
    • 5
  • N. C. Harvey
    • 2
    • 4
    Email author
  1. 1.School of Healthcare ScienceManchester Metropolitan UniversityManchesterUK
  2. 2.MRC Lifecourse Epidemiology UnitUniversity of SouthamptonSouthamptonUK
  3. 3.Division of Developmental Biology and Medicine, Faculty of Biology, Medicine and HealthUniversity of ManchesterManchesterUK
  4. 4.NIHR Southampton Biomedical Research CentreUniversity of Southampton and University Hospital Southampton NHS Foundation TrustSouthamptonUK
  5. 5.NIHR Oxford Biomedical Research CentreUniversity of OxfordOxfordUK

Personalised recommendations