Skip to main content
Top
Published in: BMC Pregnancy and Childbirth 1/2019

Open Access 01-12-2019 | Systemic Lupus Erythematosus | Research article

Risk of gestational diabetes mellitus in systemic lupus erythematosus pregnancy: a systematic review and meta-analysis

Authors: Yuanyuan Dong, Ziwei Dai, Zhihui Wang, Hong Wang, Feifei Yuan, Ying Zhu, Dongqing Ye, Bin Wang

Published in: BMC Pregnancy and Childbirth | Issue 1/2019

Login to get access

Abstract

Background

It is well established that the risks of insulin resistance and diabetes mellitus are elevated in systemic lupus erythematosus (SLE) patients. However, the relationship between SLE pregnancy and gestational diabetes mellitus (GDM) is still obscure. We perform the present systematic review and meta-analysis to determine the relationship between GDM and SLE pregnancy.

Methods

According to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) statement, relevant studies were carefully retrieved through PubMed, Cochrane library and Web of Science, China National Knowledge Infrastructure, Wanfang database and China Biology Medicine database from inception till 30 August 2018. GDM risk ratio (RR) of pregnant SLE patients versus controls was calculated to evaluate the association between GDM and SLE. Pooled RRs and 95% confidence intervals (CIs) were calculated using random effects model by R software.

Results

The literature retrieval identified 339 potential studies in total, and five studies containing 3432 pregnant participants with 248 GDM events were included finally. Pooled analysis found that the risk of GDM were not significant increased in SLE patients compared to controls (RR = 1.08, 95% CI = 0.49 to 2.41, Z = 0.19 and P = 0.848). Nevertheless, meta-regression identified that glucocorticoids use and anti-double stranded DNA antibodies positive of SLE patients were positively associated with the risk of GDM.

Conclusions

Our meta-analysis demonstrated that SLE pregnancy may not increase the risk of GDM, but the steroid use during pregnancy was associated with increased risk of GDM. Further large prospective and basic immunologic studies should be implemented for exploring the mechanism underlying glucocorticoids use and GDM.
Appendix
Available only for authorised users
Literature
1.
go back to reference Nahal SK, Selmi C, Gershwin ME. Safety issues and recommendations for successful pregnancy outcome in systemic lupus erythematosus. J Autoimmun. 2018;93:16–23.CrossRef Nahal SK, Selmi C, Gershwin ME. Safety issues and recommendations for successful pregnancy outcome in systemic lupus erythematosus. J Autoimmun. 2018;93:16–23.CrossRef
2.
go back to reference Meyer O. Making pregnancy safer for patients with lupus. Joint, bone, spine. Rev Rhum. 2004;71:178–82. Meyer O. Making pregnancy safer for patients with lupus. Joint, bone, spine. Rev Rhum. 2004;71:178–82.
3.
go back to reference Jakobsen IM, Helmig RB, Stengaard-Pedersen K. Maternal and foetal outcomes in pregnant systemic lupus erythematosus patients: an incident cohort from a stable referral population followed during 1990-2010. Scand J Rheumatol. 2015;44:377–84.CrossRef Jakobsen IM, Helmig RB, Stengaard-Pedersen K. Maternal and foetal outcomes in pregnant systemic lupus erythematosus patients: an incident cohort from a stable referral population followed during 1990-2010. Scand J Rheumatol. 2015;44:377–84.CrossRef
4.
go back to reference Clowse ME, Jamison M, Myers E, James AH. A national study of the complications of lupus in pregnancy. Am J Obstet Gynecol. 2008;199:127.e121–6.CrossRef Clowse ME, Jamison M, Myers E, James AH. A national study of the complications of lupus in pregnancy. Am J Obstet Gynecol. 2008;199:127.e121–6.CrossRef
5.
go back to reference Smyth A, Oliveira GH, Lahr BD, Bailey KR, Norby SM, Garovic VD. A systematic review and meta-analysis of pregnancy outcomes in patients with systemic lupus erythematosus and lupus nephritis. Clin J Am Soc Nephrol. 2010;5:2060–8.CrossRef Smyth A, Oliveira GH, Lahr BD, Bailey KR, Norby SM, Garovic VD. A systematic review and meta-analysis of pregnancy outcomes in patients with systemic lupus erythematosus and lupus nephritis. Clin J Am Soc Nephrol. 2010;5:2060–8.CrossRef
6.
go back to reference Lateef A, Petri M. Managing lupus patients during pregnancy. Best Pract Res Clin Rheumatol. 2013;27:435–47.CrossRef Lateef A, Petri M. Managing lupus patients during pregnancy. Best Pract Res Clin Rheumatol. 2013;27:435–47.CrossRef
7.
8.
go back to reference Kc K, Shakya S, Zhang H. Gestational diabetes mellitus and macrosomia: a literature review. Ann Nutr Metab. 2015;66(Suppl 2):14–20.CrossRef Kc K, Shakya S, Zhang H. Gestational diabetes mellitus and macrosomia: a literature review. Ann Nutr Metab. 2015;66(Suppl 2):14–20.CrossRef
9.
go back to reference Wu J, Ma J, Bao C, Di W, Zhang WH. Pregnancy outcomes among Chinese women with and without systemic lupus erythematosus: a retrospective cohort study. BMJ Open. 2018;8:e020909.CrossRef Wu J, Ma J, Bao C, Di W, Zhang WH. Pregnancy outcomes among Chinese women with and without systemic lupus erythematosus: a retrospective cohort study. BMJ Open. 2018;8:e020909.CrossRef
10.
go back to reference Abdwani R, Al Shaqsi L, Al-Zakwani I. Neonatal and obstetrical outcomes of pregnancies in systemic lupus erythematosus. Oman Med J. 2018;33:15–21.CrossRef Abdwani R, Al Shaqsi L, Al-Zakwani I. Neonatal and obstetrical outcomes of pregnancies in systemic lupus erythematosus. Oman Med J. 2018;33:15–21.CrossRef
11.
go back to reference Ogurtsova K, da Rocha Fernandes JD, Huang Y, Linnenkamp U, Guariguata L, Cho NH, Cavan D, Shaw JE, Makaroff LE. IDF diabetes atlas: global estimates for the prevalence of diabetes for 2015 and 2040. Diabetes Res Clin Pract. 2017;128:40–50.CrossRef Ogurtsova K, da Rocha Fernandes JD, Huang Y, Linnenkamp U, Guariguata L, Cho NH, Cavan D, Shaw JE, Makaroff LE. IDF diabetes atlas: global estimates for the prevalence of diabetes for 2015 and 2040. Diabetes Res Clin Pract. 2017;128:40–50.CrossRef
12.
go back to reference Lapolla A, Dalfra MG, Fedele D. Diabetes related autoimmunity in gestational diabetes mellitus: is it important? Nutrition, metabolism, and cardiovascular diseases. NMCD. 2009;19:674–82.PubMed Lapolla A, Dalfra MG, Fedele D. Diabetes related autoimmunity in gestational diabetes mellitus: is it important? Nutrition, metabolism, and cardiovascular diseases. NMCD. 2009;19:674–82.PubMed
13.
go back to reference Cossu E, Incani M, Pani MG, Gattu G, Serafini C, Strazzera A, Bertoccini L, Cimini FA, Barchetta I, Cavallo MG, et al. Presence of diabetes-specific autoimmunity in women with gestational diabetes mellitus (GDM) predicts impaired glucose regulation at follow-up. J Endocrinol Investig. 2018;41:1061–8.CrossRef Cossu E, Incani M, Pani MG, Gattu G, Serafini C, Strazzera A, Bertoccini L, Cimini FA, Barchetta I, Cavallo MG, et al. Presence of diabetes-specific autoimmunity in women with gestational diabetes mellitus (GDM) predicts impaired glucose regulation at follow-up. J Endocrinol Investig. 2018;41:1061–8.CrossRef
14.
go back to reference Phansenee S, Sekararithi R, Jatavan P, Tongsong T. Pregnancy outcomes among women with systemic lupus erythematosus: a retrospective cohort study from Thailand. Lupus. 2018;27:158–64.CrossRef Phansenee S, Sekararithi R, Jatavan P, Tongsong T. Pregnancy outcomes among women with systemic lupus erythematosus: a retrospective cohort study from Thailand. Lupus. 2018;27:158–64.CrossRef
15.
go back to reference Galappatthy P, Jayasinghe JDD, Paththinige SC, Sheriff RMH, Wijayaratne LS. Pregnancy outcomes and contraceptive use in patients with systemic lupus erythematosus, rheumatoid arthritis and women without a chronic illness: a comparative study. Int J Rheum Dis. 2017;20:746–54.CrossRef Galappatthy P, Jayasinghe JDD, Paththinige SC, Sheriff RMH, Wijayaratne LS. Pregnancy outcomes and contraceptive use in patients with systemic lupus erythematosus, rheumatoid arthritis and women without a chronic illness: a comparative study. Int J Rheum Dis. 2017;20:746–54.CrossRef
16.
go back to reference Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Int J Surg. 2010;8:336–41.CrossRef Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Int J Surg. 2010;8:336–41.CrossRef
17.
go back to reference Danyliv A, Gillespie P, O'Neill C, Noctor E, O'Dea A, Tierney M, McGuire B, Glynn LG, Dunne F. Short- and long-term effects of gestational diabetes mellitus on healthcare cost: a cross-sectional comparative study in the ATLANTIC DIP cohort. Diabet Med. 2015;32:467–76.CrossRef Danyliv A, Gillespie P, O'Neill C, Noctor E, O'Dea A, Tierney M, McGuire B, Glynn LG, Dunne F. Short- and long-term effects of gestational diabetes mellitus on healthcare cost: a cross-sectional comparative study in the ATLANTIC DIP cohort. Diabet Med. 2015;32:467–76.CrossRef
18.
go back to reference Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol. 2010;25:603–5.CrossRef Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol. 2010;25:603–5.CrossRef
19.
go back to reference Higgins JP, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med. 2002;21:1539–58.CrossRef Higgins JP, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med. 2002;21:1539–58.CrossRef
20.
go back to reference Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ (Clin Res Ed). 2003;327:557–60.CrossRef Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ (Clin Res Ed). 2003;327:557–60.CrossRef
21.
go back to reference Borenstein M, Hedges LV, Higgins JP, Rothstein HR. A basic introduction to fixed-effect and random-effects models for meta-analysis. Res Synth Methods. 2010;1:97–111.CrossRef Borenstein M, Hedges LV, Higgins JP, Rothstein HR. A basic introduction to fixed-effect and random-effects models for meta-analysis. Res Synth Methods. 2010;1:97–111.CrossRef
22.
go back to reference Yan Yuen S, Krizova A, Ouimet JM, Pope JE. Pregnancy outcome in systemic lupus erythematosus (SLE) is improving: results from a case control study and literature review. Open Rheumatol J. 2008;2:89–98.CrossRef Yan Yuen S, Krizova A, Ouimet JM, Pope JE. Pregnancy outcome in systemic lupus erythematosus (SLE) is improving: results from a case control study and literature review. Open Rheumatol J. 2008;2:89–98.CrossRef
23.
go back to reference Wu J, Ma J, Zhang WH, Di W. Management and outcomes of pregnancy with or without lupus nephritis: a systematic review and meta-analysis. Ther Clin Risk Manag. 2018;14:885–901.CrossRef Wu J, Ma J, Zhang WH, Di W. Management and outcomes of pregnancy with or without lupus nephritis: a systematic review and meta-analysis. Ther Clin Risk Manag. 2018;14:885–901.CrossRef
24.
go back to reference Bundhun PK, Soogund MZ, Huang F. Impact of systemic lupus erythematosus on maternal and fetal outcomes following pregnancy: a meta-analysis of studies published between years 2001-2016. J Autoimmun. 2017;79:17–27.CrossRef Bundhun PK, Soogund MZ, Huang F. Impact of systemic lupus erythematosus on maternal and fetal outcomes following pregnancy: a meta-analysis of studies published between years 2001-2016. J Autoimmun. 2017;79:17–27.CrossRef
25.
go back to reference Wei S, Lai K, Yang Z, Zeng K. Systemic lupus erythematosus and risk of preterm birth: a systematic review and meta-analysis of observational studies. Lupus. 2017;26:563–71.CrossRef Wei S, Lai K, Yang Z, Zeng K. Systemic lupus erythematosus and risk of preterm birth: a systematic review and meta-analysis of observational studies. Lupus. 2017;26:563–71.CrossRef
26.
go back to reference Lin P, Rhew E, Ness RB, Peaceman A, Dyer A, McPherson D, Kondos GT, Edmundowicz D, Sutton-Tyrrell K, Thompson T, et al. Adverse pregnancy outcomes and subsequent risk of cardiovascular disease in women with systemic lupus erythematosus. Lupus Sci Med. 2014;1:e000024.CrossRef Lin P, Rhew E, Ness RB, Peaceman A, Dyer A, McPherson D, Kondos GT, Edmundowicz D, Sutton-Tyrrell K, Thompson T, et al. Adverse pregnancy outcomes and subsequent risk of cardiovascular disease in women with systemic lupus erythematosus. Lupus Sci Med. 2014;1:e000024.CrossRef
27.
go back to reference Yang H, Liu H, Xu D, Zhao L, Wang Q, Leng X, Zheng W, Zhang F, Tang F, Zhang X. Pregnancy-related systemic lupus erythematosus: clinical features, outcome and risk factors of disease flares--a case control study. PLoS One. 2014;9:e104375.CrossRef Yang H, Liu H, Xu D, Zhao L, Wang Q, Leng X, Zheng W, Zhang F, Tang F, Zhang X. Pregnancy-related systemic lupus erythematosus: clinical features, outcome and risk factors of disease flares--a case control study. PLoS One. 2014;9:e104375.CrossRef
28.
go back to reference Lazzaroni MG, Dall'Ara F, Fredi M, Nalli C, Reggia R, Lojacono A, Ramazzotto F, Zatti S, Andreoli L, Tincani A. A comprehensive review of the clinical approach to pregnancy and systemic lupus erythematosus. J Autoimmun. 2016;74:106–17.CrossRef Lazzaroni MG, Dall'Ara F, Fredi M, Nalli C, Reggia R, Lojacono A, Ramazzotto F, Zatti S, Andreoli L, Tincani A. A comprehensive review of the clinical approach to pregnancy and systemic lupus erythematosus. J Autoimmun. 2016;74:106–17.CrossRef
29.
go back to reference Behboudi-Gandevani S, Amiri M, Bidhendi Yarandi R, Ramezani Tehrani F. The impact of diagnostic criteria for gestational diabetes on its prevalence: a systematic review and meta-analysis. Diabetol Metab Syndr. 2019;11:11.CrossRef Behboudi-Gandevani S, Amiri M, Bidhendi Yarandi R, Ramezani Tehrani F. The impact of diagnostic criteria for gestational diabetes on its prevalence: a systematic review and meta-analysis. Diabetol Metab Syndr. 2019;11:11.CrossRef
30.
go back to reference Haller-Kikkatalo K, Uibo R. Clinical recommendations for the use of islet cell autoantibodies to distinguish autoimmune and non-autoimmune gestational diabetes. Clin Rev Allergy Immunol. 2016;50:23–33.CrossRef Haller-Kikkatalo K, Uibo R. Clinical recommendations for the use of islet cell autoantibodies to distinguish autoimmune and non-autoimmune gestational diabetes. Clin Rev Allergy Immunol. 2016;50:23–33.CrossRef
31.
go back to reference Brucato A, Doria A, Frassi M, Castellino G, Franceschini F, Faden D, Pisoni MP, Solerte L, Muscara M, Lojacono A, et al. Pregnancy outcome in 100 women with autoimmune diseases and anti-Ro/SSA antibodies: a prospective controlled study. Lupus. 2002;11:716–21.CrossRef Brucato A, Doria A, Frassi M, Castellino G, Franceschini F, Faden D, Pisoni MP, Solerte L, Muscara M, Lojacono A, et al. Pregnancy outcome in 100 women with autoimmune diseases and anti-Ro/SSA antibodies: a prospective controlled study. Lupus. 2002;11:716–21.CrossRef
32.
go back to reference Bitencourt N, Bermas BL. Pharmacological Approach to Managing Childhood-Onset Systemic Lupus Erythematosus During Conception, Pregnancy and Breastfeeding. Paediatr Drugs. 2018;20:511-21.CrossRef Bitencourt N, Bermas BL. Pharmacological Approach to Managing Childhood-Onset Systemic Lupus Erythematosus During Conception, Pregnancy and Breastfeeding. Paediatr Drugs. 2018;20:511-21.CrossRef
33.
go back to reference Chen YM, Lin CH, Lan TH, Chen HH, Chang SN, Chen YH, Wang JS, Hung WT, Lan JL, Chen DY. Hydroxychloroquine reduces risk of incident diabetes mellitus in lupus patients in a dose-dependent manner: a population-based cohort study. Rheumatology (Oxford, England). 2015;54:1244–9.CrossRef Chen YM, Lin CH, Lan TH, Chen HH, Chang SN, Chen YH, Wang JS, Hung WT, Lan JL, Chen DY. Hydroxychloroquine reduces risk of incident diabetes mellitus in lupus patients in a dose-dependent manner: a population-based cohort study. Rheumatology (Oxford, England). 2015;54:1244–9.CrossRef
34.
go back to reference Shaharir SS, Gafor AH, Said MS, Kong NC. Steroid-induced diabetes mellitus in systemic lupus erythematosus patients: analysis from a Malaysian multi-ethnic lupus cohort. Int J Rheum Dis. 2015;18:541–7.CrossRef Shaharir SS, Gafor AH, Said MS, Kong NC. Steroid-induced diabetes mellitus in systemic lupus erythematosus patients: analysis from a Malaysian multi-ethnic lupus cohort. Int J Rheum Dis. 2015;18:541–7.CrossRef
Metadata
Title
Risk of gestational diabetes mellitus in systemic lupus erythematosus pregnancy: a systematic review and meta-analysis
Authors
Yuanyuan Dong
Ziwei Dai
Zhihui Wang
Hong Wang
Feifei Yuan
Ying Zhu
Dongqing Ye
Bin Wang
Publication date
01-12-2019
Publisher
BioMed Central
Published in
BMC Pregnancy and Childbirth / Issue 1/2019
Electronic ISSN: 1471-2393
DOI
https://doi.org/10.1186/s12884-019-2329-0

Other articles of this Issue 1/2019

BMC Pregnancy and Childbirth 1/2019 Go to the issue