Skip to main content

Advertisement

SpringerLink
Log in

Maternal diabetes mellitus and risk of neonatal respiratory distress syndrome: a meta-analysis

  • Review Article
  • Published:
Acta Diabetologica Aims and scope Submit manuscript

Abstract

Aim

The relationship between maternal diabetes mellitus (DM) and neonatal respiratory distress syndrome (RDS) has long been recognized, but the conclusions of this relationship were non-consistent. We conducted this meta-analysis to explore the association between maternal DM and the risk of neonatal RDS.

Methods

We searched PubMed and Web of Science databases for cohort or case–control studies related to the association of maternal DM and neonatal RDS risk up to 25 August 2018. The pooled odds ratios (ORs) with 95% confidence intervals (CIs) were estimated by the use of random effect model. Meta-regression was used to explore potential sources of between-study heterogeneity.

Results

A total of 24 studies from 23 available articles were included in this meta-analysis. For the association between maternal DM and the risk of neonatal RDS, the pooled OR was 1.47 (95% CI 1.24–1.74), especially for cohort studies (1.39, 95% CI 1.17–1.65). The pooled OR of the risk of neonatal RDS was 1.57 (95% CI 1.28–1.93) for gestational diabetes mellitus (GDM) and 2.66 (95% CI 2.06–3.44) for pre-gestational diabetes mellitus (PGDM).

Conclusions

This meta-analysis suggests that maternal DM, including GDM and PGDM, is linked to an increased risk of neonatal RDS.

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. De Luca D, van Kaam AH, Tingay DG, Courtney SE, Danhaive O, Carnielli VP et al (2017) The Montreux definition of neonatal ARDS: biological and clinical background behind the description of a new entity. Lancet Respir Med 5:657–666

    Article  PubMed  Google Scholar 

  2. Tochie JN, Choukem SP, Langmia RN, Barla E, Koki-Ndombo P (2016) Neonatal respiratory distress in a reference neonatal unit in Cameroon: an analysis of prevalence, predictors, etiologies and outcomes. Pan Afr Med J 24:152

    Article  PubMed  PubMed Central  Google Scholar 

  3. Garvey J (1975) Infant respiratory distress syndrome. Am J Nurs 75:614

    CAS  PubMed  Google Scholar 

  4. Kamper J (1978) Long term prognosis of infants with severe idiopathic respiratory distress syndrome. II. Cardio-pulmonary outcome. Acta Paediatr Scand 67:71–76

    Article  CAS  PubMed  Google Scholar 

  5. Dani C, Reali MF, Bertini G, Wiechmann L, Spagnolo A, Tangucci M et al (1999) Risk factors for the development of respiratory distress syndrome and transient tachypnoea in newborn infants. Eur Respir J 14:155–159

    Article  CAS  PubMed  Google Scholar 

  6. Reed DM, Bakketeig LS, Nugent RP (1978) The epidemiology of respiratory distress syndrome in Norway. Am J Epidemiol 107:299–310

    Article  CAS  PubMed  Google Scholar 

  7. Rehan VK, Moddemann D, Casiro OG (2002) Outcome of very-low-birth-weight (< 1,500 grams) infants born to mothers with diabetes. Clin Pediatr 41:481–491

    Article  Google Scholar 

  8. O’Sullivan JB (1961) Gestational diabetes. Unsuspected, asymptomatic diabetes in pregnancy. N Engl J Med 264:1082–1085

    Article  PubMed  Google Scholar 

  9. Hedderson MM, Darbinian JA, Ferrara A (2010) Disparities in the risk of gestational diabetes by race-ethnicity and country of birth. Paediatr Perinat Epidemiol 24:441–448

    Article  PubMed  PubMed Central  Google Scholar 

  10. Metzger BE, Gabbe SG, Persson B, Buchanan TA, Catalano PA, Damm P et al (2010) International association of diabetes and pregnancy study groups recommendations on the diagnosis and classification of hyperglycemia in pregnancy. Diabetes Care 33:676–682

    Article  PubMed  Google Scholar 

  11. Leary J, Pettitt DJ, Jovanovic L (2010) Gestational diabetes guidelines in a HAPO world. Best Pract Res Clin Endocrinol Metab 24:673–685

    Article  PubMed  Google Scholar 

  12. DeSisto CL, Kim SY, Sharma AJ (2014) Prevalence estimates of gestational diabetes mellitus in the United States, Pregnancy Risk Assessment Monitoring System (PRAMS), 2007–2010. Prev Chronic Dis 11:E104

    Article  PubMed  PubMed Central  Google Scholar 

  13. McKenzie-Sampson S, Paradis G, Healy-Profitos J, St-Pierre F, Auger N (2018) Gestational diabetes and risk of cardiovascular disease up to 25 years after pregnancy: a retrospective cohort study. Acta Diabetol 55:315–322

    Article  PubMed  Google Scholar 

  14. Leybovitz-Haleluya N, Wainstock T, Landau D, Sheiner E (2018) Maternal gestational diabetes mellitus and the risk of subsequent pediatric cardiovascular diseases of the offspring: a population-based cohort study with up to 18 years of follow up. Acta Diabetol 55:1037–1042

    Article  CAS  PubMed  Google Scholar 

  15. Murphy HR, Steel SA, Roland JM, Morris D, Ball V, Campbell PJ et al (2011) Obstetric and perinatal outcomes in pregnancies complicated by Type 1 and Type 2 diabetes: influences of glycaemic control, obesity and social disadvantage. Diabet Med 28:1060–1067

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Bellamy L, Casas JP, Hingorani AD, Williams D (2009) Type 2 diabetes mellitus after gestational diabetes: a systematic review and meta-analysis. Lancet 373:1773–1779

    Article  CAS  PubMed  Google Scholar 

  17. Balsells M, Garcia-Patterson A, Gich I, Corcoy R (2009) Maternal and fetal outcome in women with type 2 versus type 1 diabetes mellitus: a systematic review and metaanalysis. J Clin Endocrinol Metab 94:4284–4291

    Article  CAS  PubMed  Google Scholar 

  18. Michael Weindling A (2009) Offspring of diabetic pregnancy: short-term outcomes. Semin Fetal Neonatal Med 14:111–118

    Article  CAS  PubMed  Google Scholar 

  19. The HAPO Study Cooperative Research Group (2008) Hyperglycemia and adverse pregnancy outcomes: the HAPO Study Cooperative Research Group. Obstet Gynecol Surv 63:1991

    Google Scholar 

  20. Usher RH, Allen AC, McLean FH (1971) Risk of respiratory distress syndrome related to gestational age, route of delivery, and maternal diabetes. Am J Obstet Gynecol 111:826–832

  21. Robert MF, Neff RK, Hubbell JP, Taeusch HW, Avery ME (1976) Association between maternal diabetes and the respiratory-distress syndrome in the newborn. N Engl J Med 294:357–360

    Article  CAS  PubMed  Google Scholar 

  22. Stone CA, McLachlan KA, Halliday JL, Wein P, Tippett C (2002) Gestational diabetes in Victoria in 1996: incidence, risk factors and outcomes. Med J Aust 177:486–491

    PubMed  Google Scholar 

  23. Spain JE, Tuuli MG, Macones GA, Roehl KA, Odibo AO, Cahill AG (2015) Risk factors for serious morbidity in term nonanomalous neonates. Am J Obstet Gynecol 212:799.e1–799.e7

    Article  Google Scholar 

  24. Simoes T, Queiros A, Correia L, Rocha T, Dias E, Blickstein I (2011) Gestational diabetes mellitus complicating twin pregnancies. J Perinat Med 39:437–440

    PubMed  Google Scholar 

  25. Persson M, Shah PS, Rusconi F, Reichman B, Modi N, Kusuda S et al (2018) Association of maternal diabetes with neonatal outcomes of very preterm and very low-birth-weight infants: an international cohort study. JAMA Pediatr 172:867–875

    Article  PubMed  PubMed Central  Google Scholar 

  26. Mortier I, Blanc J, Tosello B, Gire C, Bretelle F, Carcopino X (2017) Is gestational diabetes an independent risk factor of neonatal severe respiratory distress syndrome after 34 weeks of gestation? A prospective study. Arch Gynecol Obstet 296:1071–1077

    Article  PubMed  Google Scholar 

  27. Lloreda-Garcia JM, Sevilla-Denia S, Rodriguez-Sanchez A, Munoz-Martinez P, Diaz-Ruiz M (2016) Perinatal outcome of macrosomic infants born to diabetic versus non-diabetic mothers. Endocrinol Nutr 63:409–413

    Article  PubMed  Google Scholar 

  28. Liu J, Yang N, Liu Y (2014) High-risk factors of respiratory distress syndrome in term neonates: a retrospective case–control study. Balkan Med J 31:64–68

    Article  PubMed  PubMed Central  Google Scholar 

  29. Kawakita T, Bowers K, Hazrati S, Zhang C, Grewal J, Chen Z et al (2017) Increased neonatal respiratory morbidity associated with gestational and pregestational diabetes: a retrospective study. Am J Perinatol 34:1160–1168

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Abolfazl M, Hamidreza TS, Narges M, Maryam Y (2008) Gestational diabetes and its association with unpleasant outcomes of pregnancy. Pak J Med Sci 24:566–570

    Google Scholar 

  31. Boghossian NS, Yeung E, Albert PS, Mendola P, Laughon SK, Hinkle SN et al (2014) Changes in diabetes status between pregnancies and impact on subsequent newborn outcomes. Am J Obstet Gynecol 210:431.e1–431.e14

    Article  Google Scholar 

  32. Anadkat JS, Kuzniewicz MW, Chaudhari BP, Cole FS, Hamvas A (2012) Increased risk for respiratory distress among white, male, late preterm and term infants. J Perinatol 32:780–785

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Abdalrahman Almarzouki A (2013) Maternal and neonatal outcome of controlled gestational diabetes mellitus versus high risk group without gestational diabetes mellitus: a comparative study. Med Glas 10:70–74

    Google Scholar 

  34. Rauh-Hain JA, Rana S, Tamez H, Wang A, Cohen B, Cohen A et al (2009) Risk for developing gestational diabetes in women with twin pregnancies. J Matern Fetal Neonatal Med 22:293–299

    Article  PubMed  Google Scholar 

  35. Le Ray C, Boithias C, Castaigne-Meary V, l’Helias LF, Vial M, Frydman R (2006) Caesarean before labour between 34 and 37 weeks: what are the risk factors of severe neonatal respiratory distress? Eur J Obstet Gynecol Reprod Biol 127:56–60

    Article  PubMed  Google Scholar 

  36. Guillen MA, Herranz L, Barquiel B, Hillman N, Burgos MA, Pallardo LF (2014) Influence of gestational diabetes mellitus on neonatal weight outcome in twin pregnancies. Diabet Med 31:1651–1656

    Article  CAS  PubMed  Google Scholar 

  37. Grandi C, Tapia JL, Cardoso VC (2015) Impact of maternal diabetes mellitus on mortality and morbidity of very low birth weight infants: a multicenter Latin America study. J Pediatr 91:234–241

    Article  Google Scholar 

  38. Fung GP, Chan LM, Ho YC, To WK, Chan HB, Lao TT (2014) Does gestational diabetes mellitus affect respiratory outcome in late-preterm infants? Early Hum Dev 90:527–530

    Article  CAS  PubMed  Google Scholar 

  39. Fadl HE, Ostlund IK, Magnuson AF, Hanson US (2010) Maternal and neonatal outcomes and time trends of gestational diabetes mellitus in Sweden from 1991 to 2003. Diabet Med 27:436–441

    Article  CAS  PubMed  Google Scholar 

  40. Bricelj K, Tul N, Lucovnik M, Kronhauser-Cerar L, Steblovnik L, Verdenik I et al (2017) Neonatal respiratory morbidity in late-preterm births in pregnancies with and without gestational diabetes mellitus. J Matern Fetal Neonatal Med 30:377–379

    Article  CAS  PubMed  Google Scholar 

  41. Bental Y, Reichman B, Shiff Y, Weisbrod M, Boyko V, Lerner-Geva L et al (2011) Impact of maternal diabetes mellitus on mortality and morbidity of preterm infants (24–33 weeks’ gestation). Pediatrics 128 E848-E55

    Article  Google Scholar 

  42. Becquet O, El Khabbaz F, Alberti C, Mohamed D, Blachier A, Biran V et al (2015) Insulin treatment of maternal diabetes mellitus and respiratory outcome in late-preterm and term singletons. BMJ Open 5:e008192

    Article  PubMed  PubMed Central  Google Scholar 

  43. Luerti M, Parazzini F, Agarossi A, Bianchi C, Rocchetti M, Bevilacqua G (1993) Risk factors for respiratory distress syndrome in the newborn. A multicenter Italian survey. Study Group for Lung Maturity of the Italian Society of Perinatal Medicine. Acta Obstet Gynecol Scand 72:359–364

    Article  CAS  PubMed  Google Scholar 

  44. Moher D, Liberati A, Tetzlaff J, Altman DG (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Intern Med 151:264–269, w64

    Article  PubMed  Google Scholar 

  45. Higgins JPT, Thompson SG (2002) Quantifying heterogeneity in a meta-analysis. Stat Med 21:1539–1558

    Article  PubMed  Google Scholar 

  46. Higgins JPT, Thompson SG, Deeks JJ, Altman DG (2003) Measuring inconsistency in meta-analyses. Br Med J 327:557–560

    Article  Google Scholar 

  47. Higgins JPT, Thompson SG (2004) Controlling the risk of spurious findings from meta-regression. Stat Med 23:1663–1682

    Article  PubMed  Google Scholar 

  48. Egger M, Davey Smith G, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315:629–634

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Piper JM (2002) Lung maturation in diabetes in pregnancy: if and when to test. Semin Perinatol 26:206–209

    Article  PubMed  Google Scholar 

  50. Leung-Pineda V, Gronowski AM (2010) Biomarker tests for fetal lung maturity. Biomark Med 4:849–857

    Article  CAS  PubMed  Google Scholar 

  51. Miakotina OL, Dekowski SA, Snyder JM (1998) Insulin inhibits surfactant protein A and B gene expression in the H441 cell line. Biochim Biophys Acta 1442:60–70

    Article  CAS  PubMed  Google Scholar 

  52. Westgate JA, Lindsay RS, Beattie J, Pattison NS, Gamble G, Mildenhall LF et al (2006) Hyperinsulinemia in cord blood in mothers with type 2 diabetes and gestational diabetes mellitus in New Zealand. Diabetes Care 29:1345–1350

    Article  PubMed  Google Scholar 

  53. Bonafe L, Rubaltelli FF (1996) The incidence of acute neonatal respiratory disorders in Padova county: an epidemiological survey. Acta Paediatr 85:1236–1240

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Author information

Authors and Affiliations

  1. Department of Epidemiology and Health Statistics, Public Health College, Qingdao University, No. 38 Dengzhou Road, Qingdao, Shandong, 266021, China

    Yan Li, Weijing Wang & Dongfeng Zhang

Authors
  1. Yan Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Weijing Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dongfeng Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Li and Zhang conceived the study, participated in its design and coordination, and were involved in drafting the manuscript. Li and Wang carried out the literature search, data extraction, and interpretation of the data. Li, Wang, and Zhang reviewed and revised the manuscript critically for important intellectual content. All authors approved the final manuscript as submitted and agreed to be accountable for all aspects of the work.

Corresponding author

Correspondence to Dongfeng Zhang.

Ethics declarations

Conflict of interest

The authors declare that they have no competing interests.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Informed consent

Not applicable.

Additional information

Managed by Antonio Secchi.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Table S1

Results of meta-regression (DOCX 17 KB)

Fig S1

Cumulative meta-analysis of maternal diabetes and the risk of neonatal respiratory distress syndrome (OR, odds ratio; CI, confidence interval; *low probability of delivery at term) (TIF 7229 KB)

Fig S2

Forest plot of pre-gestational diabetes mellitus and the risk of neonatal respiratory distress syndrome. The size of gray box is positively proportional to the weight assigned to each study, which is inversely proportional to the standard error of the OR, and horizontal lines represent the 95% Cis (OR, odds ratio; CI, confidence interval; *low probability of delivery at term) (TIF 2671 KB)

Fig S3

Funnel plot of relative risk (OR) for the analysis of the association between maternal diabetes and the risk of neonatal respiratory distress syndrome. Each dot represents a different study (SE, standard error) (TIF 2449 KB)

Fig S4

Funnel plot of relative risk (OR) for the analysis of the association between gestational diabetes mellitus and the risk of neonatal respiratory distress syndrome. Each dot represents a different study (SE, standard error) (TIF 2194 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, Y., Wang, W. & Zhang, D. Maternal diabetes mellitus and risk of neonatal respiratory distress syndrome: a meta-analysis. Acta Diabetol 56, 729–740 (2019). https://doi.org/10.1007/s00592-019-01327-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00592-019-01327-4

Keywords

Search

Navigation