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. 2017 Oct 26;179(5):829–837. doi: 10.1111/bjh.14961

Association between maternal haemoglobin and stillbirth: a cohort study among a multi‐ethnic population in England

Manisha Nair 1,✉, David Churchill 2, Susan Robinson 3, Cathy Nelson‐Piercy 3,4, Simon J Stanworth 5,6,7, Marian Knight 1
PMCID: PMC5725731  PMID: 29076149

Summary

The study objectives were to examine the association of maternal haemoglobin with stillbirth and perinatal death in a multi‐ethnic population in England. We conducted a retrospective cohort analysis using anonymised maternity data from 14 001 women with singleton pregnancies ≥24 weeks’ gestation giving birth between 2013 and 2015 in two hospitals ‐ the Royal Wolverhampton NHS Trust and Guy's and St Thomas’ NHS Foundation Trust. Multivariable logistic regression analyses were undertaken to analyse the associations between maternal haemoglobin at first visit and at 28 weeks with stillbirth and perinatal death, adjusting for 11 other risk factors. Results showed that 46% of the study population had anaemia (haemoglobin <110 g/l) at some point during their pregnancy. The risk of stillbirth and perinatal death decreased linearly per unit increase in haemoglobin concentration at first visit (adjusted odds ratio [aOR] stillbirth = 0·70, 95% confidence interval [CI] 0·58–0·85, aOR perinatal death = 0·71, 95% CI 0·60–0·84) and at 28 weeks (aOR stillbirth = 0·83, 95% CI 0·66–1·04; aOR perinatal death = 0·86, 95%CI 0·67–1·12). Compared with women with haemoglobin ≥110 g/l, the risk of stillbirth and perinatal death was five‐ and three‐fold higher in women with moderate‐severe anaemia (haemoglobin <100 g/l) at first visit and 28 weeks, respectively. These findings have clinical and public health importance.

Keywords: haemoglobin concentration, pregnancy, stillbirth, perinatal death, maternal anaemia

Supporting information

Table S1. Comparison of characteristics of women giving birth in the study hospitals with that of the general population of pregnant women in England

Click here for additional data file. (50KB, doc)

Work was carried out at: National Perinatal Epidemiology Unit (NPEU), Nuffield Department of Population Health, University of Oxford; the Royal Wolverhampton NHS Trust and Guy's and St Thomas’ NHS Foundation Trust.

References

  1. Barroso, F. , Allard, S. , Kahan, B.C. , Connolly, C. , Smethurst, H. , Choo, L. , Khan, K. & Stanworth, S. (2011) Prevalence of maternal anaemia and its predictors: a multi‐centre study. European Journal of Obstetrics, Gynecology, and Reproductive Biology, 159, 99–105. [DOI] [PubMed] [Google Scholar]
  2. Di Mario, S. , Say, L. & Lincetto, O. (2007) Risk factors for stillbirth in developing countries: a systematic review of the literature. Sexually Transmitted Diseases, 34, S11–S21. [DOI] [PubMed] [Google Scholar]
  3. Flenady, V. , Koopmans, L. , Middleton, P. , Frøen, J.F. , Smith, G.C. , Gibbons, K. , Coory, M. , Gordon, A. , Ellwood, D. & Mcintyre, H.D. (2011) Major risk factors for stillbirth in high‐income countries: a systematic review and meta‐analysis. The Lancet, 377, 1331–1340. [DOI] [PubMed] [Google Scholar]
  4. Frøen, J.F. , Friberg, I.K. , Lawn, J.E. , Bhutta, Z.A. , Pattinson, R.C. , Allanson, E.R. , Flenady, V. , Mcclure, E.M. , Franco, L. & Goldenberg, R.L. (2016) Stillbirths: progress and unfinished business. The Lancet, 387, 574–586. [DOI] [PubMed] [Google Scholar]
  5. Haider, B.A. , Olofin, I. , Wang, M. , Spiegelman, D. , Ezzati, M. & Fawzi, W.W. (2013) Anaemia, prenatal iron use, and risk of adverse pregnancy outcomes: systematic review and meta‐analysis. British Medical Journal, 346, f3443. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Knight, M. , Kurinczuk, J.J. , Spark, P. & Brocklehurst, P. (2009) Inequalities in maternal health: national cohort study of ethnic variation in severe maternal morbidities. British Medical Journal, 338, b542. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Lawn, J.E. , Blencowe, H. , Pattinson, R. , Cousens, S. , Kumar, R. , Ibiebele, I. , Gardosi, J. , Day, L.T. & Stanton, C. (2011) Stillbirths: Where? When? Why? How to make the data count? The Lancet, 377, 1448–1463. [DOI] [PubMed] [Google Scholar]
  8. Lawn, J.E. , Blencowe, H. , Waiswa, P. , Amouzou, A. , Mathers, C. , Hogan, D. , Flenady, V. , Frøen, J.F. , Qureshi, Z.U. , Calderwood, C. , Shiekh, S. , Jassir, F.B. , You, D. , Mcclure, E.M. , Mathai, M. & Cousens, S. (2016) Stillbirths: rates, risk factors, and acceleration towards 2030. The Lancet, 387, 587–603. [DOI] [PubMed] [Google Scholar]
  9. Little, M.P. , Brocard, P. , Elliott, P. & Steer, P.J. (2005) Hemoglobin concentration in pregnancy and perinatal mortality: a London‐based cohort study. American Journal of Obstetrics and Gynecology, 193, 220–226. [DOI] [PubMed] [Google Scholar]
  10. Lone, F.W. , Qureshi, R.N. & Emanuel, F. (2004) Maternal anaemia and its impact on perinatal outcome. Tropical Medicine & International Health, 9, 486–490. [DOI] [PubMed] [Google Scholar]
  11. Manktelow, B. N. , Smith, L. K. , Seaton, S. E. , Hyman‐Taylor, P. , Kurinczuk, J. J. , Field, D. J. , Smith, P. W. & Draper, E. S. & On Behalf of the Mbrrace‐Uk Collaboration . (2016) MBRRACE‐UK Perinatal Mortality Surveillance Report, UK Perinatal Deaths for Births From January to December 2014, The Infant Mortality and Morbidity Studies, Department of Health Sciences, University of Leicester, Leicester. [Google Scholar]
  12. Musallam, K.M. , Tamim, H.M. , Richards, T. , Spahn, D.R. , Rosendaal, F.R. , Habbal, A. , Khreiss, M. , Dahdaleh, F.S. , Khavandi, K. , Sfeir, P.M. , Soweid, A. , Hoballah, J.J. , Taher, A.T. & Jamali, F.R. (2011) Preoperative anaemia and postoperative outcomes in non‐cardiac surgery: a retrospective cohort study. Lancet, 378, 1396–1407. [DOI] [PubMed] [Google Scholar]
  13. Nair, M. , Choudhury, M.K. , Choudhury, S.S. , Kakoty, S.D. , Webster, P. , Sarma, U.C. & Knight, M. (2016a) The association between maternal anaemia and pregnancy outcomes: a cohort study in Assam, India. BMJ Global Health, 1, e000026. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Nair, M. , Knight, M. & Kurinczuk, J.J. (2016b) Risk factors and newborn outcomes associated with maternal deaths in the UK from 2009 to 2013: a national case–control study. BJOG: An International Journal of Obstetrics & Gynaecology, 123, 1654–1662. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. NHS England . (2006). NHS Maternity Statistics England 2005‐6. Statistical Bulletin 2006/08. Information Centre for Health and Social Care, Leeds. [Google Scholar]
  16. Pavord, S. , Myers, B. , Robinson, S. , Allard, S. , Strong, J. & Oppenheimer, C. & On Behalf of the British Committee for Standards in Haematolog . (2012). UK guidelines on the management of iron deficiency in pregnancy. British Journal of Haematology, 156, 588–600. [DOI] [PubMed] [Google Scholar]
  17. Royston, P. , Ambler, G. & Sauerbrei, W. (1999) The use of fractional polynomials to model continuous risk variables in epidemiology. International Journal of Epidemiology, 28, 964–974. [DOI] [PubMed] [Google Scholar]
  18. Stephansson, O. , Dickman, P.W. , Johansson, A. & Cnattingius, S. (2000) Maternal hemoglobin concentration during pregnancy and risk of stillbirth. JAMA, 284, 2611–2617. [DOI] [PubMed] [Google Scholar]
  19. Tomashek, K.M. , Ananth, C.V. & Cogswell, M.E. (2006) Risk of stillbirth in relation to maternal haemoglobin concentration during pregnancy. Maternal & Child Nutrition, 2, 19–28. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Watson‐Jones, D. , Weiss, H.A. , Changalucha, J.M. , Todd, J. , Gumodoka, B. , Bulmer, J. , Balira, R. , Ross, D. , Mugeye, K. & Hayes, R. (2007) Adverse birth outcomes in United Republic of Tanzania: impact and prevention of maternal risk factors. Bulletin of the World Health Organization, 85, 9–18. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. WHO . (2011) Haemoglobin concentrations for the diagnosis of anaemia and assessment of severity: Vitamin and Mineral Nutrition Information System (WHO/NMH/NHD/MNM/11.1). World Health Organisation, Geneva, Switzerland. http://www.who.int/vmnis/indicators/haemoglobin. pdf (accessed 05 January 2017).
  22. Zhang, Q. , Ananth, C.V. , Rhoads, G.G. & Li, Z. (2009) The impact of maternal anemia on perinatal mortality: a population‐based, prospective cohort study in China. Annals of Epidemiology, 19, 793–799. [DOI] [PubMed] [Google Scholar]

Associated Data

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Supplementary Materials

Table S1. Comparison of characteristics of women giving birth in the study hospitals with that of the general population of pregnant women in England

Click here for additional data file. (50KB, doc)

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