Vitamin D Concentration during Early Pregnancy and Adverse Outcomes among HIV-Negative Women in Dar-es-Salaam, Tanzania: A Case-Control Study
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Design and Participants
2.2. Assessment of Vitamin D Status
2.3. Definition of Cases and Controls
2.4. Statistical Analysis
3. Results
3.1. Participants
3.2. The Association of Vitamin D Concentration and the Composite Adverse Pregnancy Outcomes
3.3. The Association of Vitamin D Concentration and Individual Adverse Pregnancy Outcomes
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Blencowe, H.; Cousens, S.; Jassir, F.B.; Say, L.; Chou, D.; Mathers, C.; Hogan, D.; Shiekh, S.; Qureshi, Z.U.; You, D.; et al. National, regional, and worldwide estimates of stillbirth rates in 2015, with trends from 2000: A systematic analysis. Lancet Glob. Health 2016, 4, e98–e108. [Google Scholar] [CrossRef]
- Lawn, J.E.; Blencowe, H.; Pattinson, R.; Cousens, S.; Kumar, R.; Ibiebele, I.; Gardosi, J.; Day, L.T.; Stanton, C. Lancet’s Stillbirths Series steering committee Stillbirths: Where? When? Why? How to make the data count? Lancet 2011, 377, 1448–1463. [Google Scholar] [CrossRef]
- Bickle Graz, M.; Tolsa, J.-F.; Fischer Fumeaux, C.J. Being Small for Gestational Age: Does it Matter for the Neurodevelopment of Premature Infants? A Cohort Study. PLoS ONE 2015, 10, e0125769. [Google Scholar] [CrossRef] [PubMed]
- Bianchi-Jassir, F.; Seale, A.C.; Kohli-Lynch, M.; Lawn, J.E.; Baker, C.J.; Bartlett, L.; Cutland, C.; Gravett, M.G.; Heath, P.T.; Ip, M.; et al. Preterm Birth Associated with Group B Streptococcus Maternal Colonization Worldwide: Systematic Review and Meta-analyses. Clin. Infect. Dis. 2017, 65, S133–S142. [Google Scholar] [CrossRef] [PubMed]
- Meas, T.; Deghmoun, S.; Armoogum, P.; Alberti, C.; Levy-Marchal, C. Consequences of Being Born Small for Gestational Age on Body Composition: An 8-Year Follow-Up Study. J. Clin. Endocrinol. Metab. 2008, 93, 3804–3809. [Google Scholar] [CrossRef] [PubMed]
- Mithal, A.; Kalra, S. Vitamin D supplementation in pregnancy. Indian J. Endocrinol. Metab. 2014, 18, 4. [Google Scholar]
- Miliku, K.; Vinkhuyzen, A.; Blanken, L.M.; McGrath, J.J.; Eyles, D.W.; Burne, T.H.; Hofman, A.; Tiemeier, H.; Steegers, E.A.; Gaillard, R.; et al. Maternal vitamin D concentrations during pregnancy, fetal growth patterns, and risks of adverse birth outcomes. Am. J. Clin. Nutr. 2016, 103, 1514–1522. [Google Scholar] [CrossRef] [PubMed]
- Thorne-Lyman, A.; Fawzi, W.W. Vitamin D during pregnancy and maternal, neonatal and infant health outcomes: A systematic review and meta-analysis. Paediatr. Perinat. Epidemiol. 2012, 26, 75–90. [Google Scholar] [CrossRef] [PubMed]
- Hart, P.H.; Lucas, R.M.; Walsh, J.P.; Zosky, G.R.; Whitehouse, A.J.O.; Zhu, K.; Allen, K.L.; Kusel, M.M.; Anderson, D.; Mountain, J.A. Vitamin D in Fetal Development: Findings from a Birth Cohort Study. Pediatrics 2015, 135, e167–e173. [Google Scholar] [CrossRef]
- Wang, H.; Xiao, Y.; Zhang, L.; Gao, Q. Maternal early pregnancy vitamin D status in relation to low birth weight and small-for-gestational-age offspring. J. Steroid Biochem. Mol. Biol. 2018, 175, 146–150. [Google Scholar] [CrossRef]
- Palacios, C.; Gonzalez, L. Is vitamin D deficiency a major global public health problem? J. Steroid Biochem. Mol. Biol. 2014, 144PA, 138–145. [Google Scholar] [CrossRef] [PubMed]
- Finkelstein, J.L.; Mehta, S.; Duggan, C.; Manji, K.P.; Mugusi, F.M.; Aboud, S.; Spiegelman, D.; Msamanga, G.I.; Fawzi, W.W. Maternal Vitamin D Status and Child Morbidity, Anemia, and Growth in Human Immunodeficiency Virus-Exposed Children in Tanzania. Pediatr. Infect. Dis. J. 2012, 31, 171–175. [Google Scholar] [CrossRef] [PubMed]
- Roth, D.E.; Morris, S.K.; Zlotkin, S.; Gernand, A.D.; Ahmed, T.; Shanta, S.S.; Papp, E.; Korsiak, J.; Shi, J.; Islam, M.M.; et al. Vitamin D Supplementation in Pregnancy and Lactation and Infant Growth. N. Engl. J. Med. 2018, 379, 535–546. [Google Scholar] [CrossRef] [PubMed]
- Amegah, A.K.; Klevor, M.K.; Wagner, C.L. Maternal vitamin D insufficiency and risk of adverse pregnancy and birth outcomes: A systematic review and meta-analysis of longitudinal studies. PLoS ONE 2017, 12, e0173605. [Google Scholar] [CrossRef] [PubMed]
- Ananth, C.V.; Vintzileos, A.M. Distinguishing pathological from constitutional small for gestational age births in population-based studies. Early Hum. Dev. 2009, 85, 653–658. [Google Scholar] [CrossRef]
- Chen, Y.; Zhu, B.; Wu, X.; Li, S.; Tao, F. Association between maternal vitamin D deficiency and small for gestational age: Evidence from a meta-analysis of prospective cohort studies. BMJ Open 2017, 7, e016404. [Google Scholar] [CrossRef]
- Schneuer, F.J.; Roberts, C.L.; Guilbert, C.; Simpson, J.M.; Algert, C.S.; Khambalia, A.Z.; Tasevski, V.; Ashton, A.W.; Morris, J.M.; Nassar, N. Effects of maternal serum 25-hydroxyvitamin D concentrations in the first trimester on subsequent pregnancy outcomes in an Australian population. Am. J. Clin. Nutr. 2014, 99, 287–295. [Google Scholar] [CrossRef]
- Darling, A.M.; Mugusi, F.M.; Etheredge, A.J.; Gunaratna, N.S.; Abioye, A.I.; Aboud, S.; Duggan, C.; Mongi, R.; Spiegelman, D.; Roberts, D.; et al. Vitamin A and Zinc Supplementation Among Pregnant Women to Prevent Placental Malaria: A Randomized, Double-Blind, Placebo-Controlled Trial in Tanzania. Am. J. Trop. Med. Hyg. 2017, 96, 826–834. [Google Scholar] [CrossRef]
- Holick, M.F.; Binkley, N.C.; Bischoff-Ferrari, H.A.; Gordon, C.M.; Hanley, D.A.; Heaney, R.P.; Murad, M.H.; Weaver, C.M. Endocrine Society Evaluation, treatment, and prevention of vitamin D deficiency: An Endocrine Society clinical practice guideline. J. Clin. Endocrinol. Metab. 2011, 96, 1911–1930. [Google Scholar] [CrossRef]
- Institute of Medicine (US) Committee to Review Dietary Reference Intakes for Vitamin D and Calcium. Dietary Reference Intakes for Calcium and Vitamin D. In The National Academies Collection: Reports Funded by National Institutes of Health; Ross, A.C., Taylor, C.L., Yaktine, A.L., Del Valle, H.B., Eds.; National Academies Press: Washington, DC, USA, 2011. [Google Scholar]
- Hollis, B.W.; Johnson, D.; Hulsey, T.C.; Ebeling, M.; Wagner, C.L. Vitamin D supplementation during pregnancy: Double-blind, randomized clinical trial of safety and effectiveness. J. Bone Miner. Res. 2011, 26, 2341–2357. [Google Scholar] [CrossRef]
- Weinstein, J.R.; Thompson, L.M.; Artiga, A.D.; Bryan, J.P.; Arriaga, W.E.; Omer, S.B.; McCracken, J.P. Determining gestational age and preterm birth in rural Guatemala: A comparison of methods. PLoS ONE 2018, 13, e0193666. [Google Scholar] [CrossRef] [PubMed]
- Villar, J.; Cheikh Ismail, L.; Victora, C.G.; Ohuma, E.O.; Bertino, E.; Altman, D.G.; Lambert, A.; Papageorghiou, A.T.; Carvalho, M.; Jaffer, Y.A.; et al. International standards for newborn weight, length, and head circumference by gestational age and sex: The Newborn Cross-Sectional Study of the INTERGROWTH-21st Project. Lancet 2014, 384, 857–868. [Google Scholar] [CrossRef]
- VanderWeele, T.J.; Knol, M.J. A Tutorial on Interaction. Epidemiol. Methods 2014, 3, 33–72. [Google Scholar] [CrossRef]
- McNutt, L.-A.; Wu, C.; Xue, X.; Hafner, J.P. Estimating the relative risk in cohort studies and clinical trials of common outcomes. Am. J. Epidemiol. 2003, 157, 940–943. [Google Scholar] [CrossRef] [PubMed]
- Pearce, N. Analysis of matched case-control studies. BMJ 2016, 352, i969. [Google Scholar] [CrossRef] [PubMed]
- Durrleman, S.; Simon, R. Flexible regression models with cubic splines. Stat. Med. 1989, 8, 551–561. [Google Scholar] [CrossRef]
- Saarela, O.; Kulathinal, S.; Arjas, E.; Läärä, E. Nested case-control data utilized for multiple outcomes: A likelihood approach and alternatives. Stat. Med. 2008, 27, 5991–6008. [Google Scholar] [CrossRef]
- Richardson, D.B.; Rzehak, P.; Klenk, J.; Weiland, S.K. Analyses of case-control data for additional outcomes. Epidemiology 2007, 18, 441–445. [Google Scholar] [CrossRef]
- Firth, D. Bias Reduction of Maximum Likelihood Estimates. Biometrika 1993, 80, 27–38. [Google Scholar] [CrossRef]
- Eyduran, E. Usage of Penalized Maximum Likelihood Estimation Method in Medical Research: An Alternative to Maximum Likelihood Estimation Method. J. Res. Med. Sci. 2008, 13, 325–330. [Google Scholar]
- Heinze, G.; Schemper, M. A solution to the problem of separation in logistic regression. Stat. Med. 2002, 21, 2409–2419. [Google Scholar] [CrossRef] [PubMed]
- Rubin, D.B. Multiple Imputation for Nonresponse in Surveys; John Wiley & Sons: Hoboken, NJ, USA, 2009; ISBN 978-0-470-31736-5. [Google Scholar]
- van Buuren, S. Multiple imputation of discrete and continuous data by fully conditional specification. Stat. Methods Med. Res. 2007, 16, 219–242. [Google Scholar] [CrossRef] [PubMed]
- Zhou, J.; Su, L.; Liu, M.; Liu, Y.; Cao, X.; Wang, Z.; Xiao, H. Associations between 25-hydroxyvitamin D levels and pregnancy outcomes: A prospective observational study in southern China. Eur. J. Clin. Nutr. 2014, 68, 925–930. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hollis, B.W.; Wagner, C.L. New insights into the vitamin D requirements during pregnancy. Bone Res. 2017, 5, 17030. [Google Scholar] [CrossRef] [PubMed]
- Murthi, P.; Yong, H.E.J.; Ngyuen, T.P.H.; Ellery, S.; Singh, H.; Rahman, R.; Dickinson, H.; Walker, D.W.; Davies-Tuck, M.; Wallace, E.M.; et al. Role of the Placental Vitamin D Receptor in Modulating Feto-Placental Growth in Fetal Growth Restriction and Preeclampsia-Affected Pregnancies. Front. Physiol. 2016, 7, 43. [Google Scholar] [CrossRef] [Green Version]
- Wei, S.-Q.; Qi, H.-P.; Luo, Z.-C.; Fraser, W.D. Maternal vitamin D status and adverse pregnancy outcomes: A systematic review and meta-analysis. J. Matern. Fetal. Neonatal. Med. 2013, 26, 889–899. [Google Scholar] [CrossRef]
- Bodnar, L.M.; Platt, R.W.; Simhan, H.N. Early-Pregnancy Vitamin D Deficiency and Risk of Preterm Birth Subtypes. Obstet. Gynecol. 2015, 125, 439–447. [Google Scholar] [CrossRef]
- McDonnell, S.L.; Baggerly, K.A.; Baggerly, C.A.; Aliano, J.L.; French, C.B.; Baggerly, L.L.; Ebeling, M.D.; Rittenberg, C.S.; Goodier, C.G.; Mateus Niño, J.F.; et al. Maternal 25 (OH) D concentrations ≥40 ng/mL associated with 60% lower preterm birth risk among general obstetrical patients at an urban medical center. PLoS ONE 2017, 12, e0180483. [Google Scholar] [CrossRef] [Green Version]
- Zhou, S.-S.; Tao, Y.-H.; Huang, K.; Zhu, B.-B.; Tao, F.-B. Vitamin D and risk of preterm birth: Up-to-date meta-analysis of randomized controlled trials and observational studies. J. Obstet. Gynaecol. Res. 2017, 43, 247–256. [Google Scholar] [CrossRef] [Green Version]
- Toko, E.N.; Sumba, O.P.; Daud, I.I.; Ogolla, S.; Majiwa, M.; Krisher, J.T.; Ouma, C.; Dent, A.E.; Rochford, R.; Mehta, S. Maternal Vitamin D Status and Adverse Birth Outcomes in Children from Rural Western Kenya. Nutrients 2016, 8, 794. [Google Scholar] [CrossRef]
- Katz, J.; Wu, L.A.; Mullany, L.C.; Coles, C.L.; Lee, A.C.C.; Kozuki, N.; Tielsch, J.M. Prevalence of Small-for-Gestational-Age and Its Mortality Risk Varies by Choice of Birth-Weight-for-Gestation Reference Population. PLoS ONE 2014, 9, e92074. [Google Scholar] [CrossRef] [PubMed] [Green Version]
Characteristics | Cases (Either Stillbirth 1, Premature 2 or SGA 3) | Controls |
---|---|---|
Overall, n | 310 | 321 |
Vitamin D concentration in ng/mL, mean (SD) | 42.3 (8.0) | 42.7 (8.6) |
Vitamin D concentration in ng/mL, n (%) | ||
Sufficient (≥30.0 ng/mL) | 289 (93.2) | 299 (93.2) |
Low level (<30.0 ng/mL) | 21 (6.8) | 22 (6.8) |
Vitamin D concentration in ng/mL, n (%) | ||
Sufficient (≥30.0 ng/mL) | 289 (93.2) | 299 (93.2) |
Insufficient (20.0–29.9 ng/mL) | 14 (4.5) | 17 (5.3) |
Deficient (<20.0 ng/mL) | 7 (2.3) | 5 (1.5) |
Vitamin D concentration in ng/mL, n (%) | ||
Sufficient (≥40.0 ng/mL) | 211(68.1) | 213 (66.4) |
Low level (<40.0 ng/mL) | 99 (31.9) | 108 (33.6) |
Maternal age in completed years, mean (SD) | 22.7 (4.3) | 22.4 (3.6) |
Maternal age in years, n (%) | ||
≤24 | 221 (72.0) | 252 (78.5) |
25–34 | 79 (25.7) | 66 (20.6) |
≥35 | 7 (2.3) | 3 (0.9) |
Gestational age in weeks, mean(SD) 4 | 9.9 (2.3) | 9.8 (2.4) |
Employment, n (%) | ||
Employed 5 | 85 (27.5) | 95 (29.8) |
Unemployed | 187 (60.5) | 175 (54.9) |
Other | 37 (12.0) | 49 (15.3) |
Marital status, n (%) | ||
Living single 6 | 31 (10.0) | 37 (11.5) |
Married or cohabitating | 278 (90.0) | 284 (88.5) |
Years of education, n (%) | ||
0–7 | 234 (75.5) | 225 (70.1) |
8–11 | 66 (21.3) | 78 (24.3) |
≥12 | 10 (3.2) | 18 (5.6) |
Wealth quartile, n (%) | ||
1 (Lowest) | 67 (22.6) | 71 (23.8) |
2 | 64 (21.6) | 82 (27.5) |
3 | 103 (34.8) | 89 (29.9) |
4 (Highest) | 62 (21.0) | 56 (18.8) |
Number of previous pregnancies, n (%) | ||
First | 169 (54.5) | 135 (42.1) |
Second | 141 (45.5) | 186 (57.9) |
Vitamin A supplements, n (%) | ||
Not received | 153 (49.4) | 170 (53.0) |
Received | 157 (50.6) | 151 (47.0) |
Zinc supplements, n (%) | ||
Not received | 154 (49.7) | 158 (49.2) |
Received | 156 (50.3) | 163 (50.8) |
Body mass index (kg/m2), mean (SD) | 22.4 (3.9) | 23.1 (4.4) |
Body mass index (kg/m2), n (%) | ||
Underweight | 37 (12.0) | 32 (10.0) |
Normal | 213 (69.2) | 213 (66.6) |
Overweight or obese | 58 (18.8) | 75 (23.4) |
Haemoglobin in g/dL, mean (SD) | 11.4 (1.6) | 11.5 (1.4) |
Anaemia status, n (%) | ||
Normal Hb (≥11.0 g/dL) | 199 (65.7) | 221 (70.8) |
Anaemic (˂11.0 g/dL) | 104 (34.3) | 91 (29.2) |
Exposure of Interest | Unadjusted OR 2 [95% CI 3] | p-Value | Adjusted OR 2 [95% CI 3] | p-Value |
---|---|---|---|---|
Vitamin D concentration in ng/mL | ||||
Sufficient (≥30.0 ng/mL) | Ref | Ref | ||
Low (<30.0 ng/mL) | 0.99 [0.53, 1.84] | 0.97 | 1.05 [0.55, 1.98] | 0.89 |
Vitamin D concentration in ng/mL | ||||
Sufficient (≥30.0 ng/mL) | Ref | Ref | ||
Insufficient (20.0–29.9 ng/mL) | 0.85 [0.41, 1.76] | 0.67 | 0.84 [0.39, 1.78] | 0.64 |
Deficient (<20.0 ng/mL) | 1.45 [0.46, 4.62] | 0.53 | 1.82 [0.56, 5.93] | 0.32 |
Vitamin D concentration ng/mL | ||||
Sufficient (≥40.0 ng/mL) | Ref | Ref | ||
Low (<40.0 ng/mL) | 0.93 [0.66, 1.29] | 0.65 | 0.90 [0.63, 1.27] | 0.54 |
Characteristics | Stillbirth | Controls | Small for Gestation Age among Live Births 1 | Controls | Premature (Birth before 34 Weeks) among Live Births 2 | Controls |
---|---|---|---|---|---|---|
Overall, n | 36 | 595 | 203 | 392 | 72 | 523 |
Vitamin D concentration in ng/mL, mean (SD) | 39.5 (10.0) | 42.7 (8.2) | 42.1 (8.2) | 43.0 (8.2) | 44.4 (5.6) | 42.5 (8.5) |
Vitamin D concentration in ng/mL, n (%) | ||||||
Sufficient (≥30.0 ng/mL) | 31 (86.1) | 557 (93.6) | 188 (92.6) | 369 (94.1) | 71 (98.6) | 486 (92.9) |
Low (<30.0 ng/mL) | 5 (13.9) | 38 (6.4) | 15 (7.4) | 23 (5.9) | 1 (1.4) | 37 (7.1) |
Vitamin D concentration in ng/mL, n (%) | ||||||
Sufficient (≥30.0 ng/mL) | 31 (86.1) | 557 (93.6) | 188 (92.6) | 369 (94.1) | 71 (98.6) | 486 (92.9) |
Insufficient (20.0–29.9 ng/mL) | 3 (8.3) | 28 (4.7) | 10 (4.9) | 18 (4.6) | 1 (1.4) | 27 (5.2) |
Deficient (<20.0 ng/mL) | 2 (5.6) | 10 (1.7) | 5 (2.5) | 5 (1.3) | 0 | 10 (1.9) |
Vitamin D concentration in ng/mL, n (%) | ||||||
Sufficient (≥40.0 ng/mL) | 18 (50.0) | 406 (68.2) | 137 (67.5) | 269 (68.6) | 57 (79.2) | 349 (66.7) |
Low (<40.0 ng/mL) | 18 (50.0) | 189 (31.8) | 66 (32.5) | 123 (31.4) | 15 (20.8) | 174 (33.3) |
Exposure of Interest | Unadjusted | p-Value | Adjusted | p-Value |
---|---|---|---|---|
OR 2 [95% CI 3] | OR 2 [95% CI 3] | |||
Stillbirth | ||||
Vitamin D concentration in ng/mL | ||||
Sufficient (≥30.0 ng/mL) | Ref | Ref | ||
Low (<30.0 ng/mL) | 2.27 [0.84, 6.15] | 0.11 | 3.11 [1.18, 8.23] | 0.02 |
Vitamin D concentration in ng/mL | ||||
Sufficient (≥40.0 ng/mL) | Ref | Ref | ||
Low (<40.0 ng/mL) | 2.05 [1.04, 4.03] | 0.04 | 2.53 [1.31, 4.89] | 0.01 |
Premature (birth before 34 weeks) 4 | ||||
Vitamin D concentration in ng/mL | ||||
Sufficient (≥30.0 ng/mL) | Ref | Ref | ||
Low (<30.0 ng/mL) | 0.19 [0.03, 1.40] | 0.10 | 0.29 [0.06, 1.50] | 0.14 |
Vitamin D concentration in ng/mL | ||||
Sufficient (≥40.0 ng/mL) | Ref | Ref | ||
Low (<40.0 ng/mL) | 0.52 [0.29, 0.95] | 0.03 | 0.59 [0.32, 1.07] | 0.08 |
Small for gestational age 5 | ||||
Vitamin D concentration in ng/mL | ||||
Sufficient (≥30.0 ng/mL) | Ref | Ref | ||
Low (<30.0 ng/mL) | 1.15 [0.61, 2.16] | 0.67 | 1.33 [0.69, 2.56] | 0.39 |
Vitamin D concentration in ng/mL | ||||
Sufficient (≥40.0 ng/mL) | Ref | Ref | ||
Low (<40.0 ng/mL) | 0.99 [0.70, 1.39] | 0.93 | 0.94 [0.65, 1.35] | 0.72 |
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Kalinjuma, A.V.; Darling, A.M.; Sudfeld, C.R.; Mugusi, F.; Wright, J.; Abioye, A.I.; Aboud, S.; McDonald, C.; Hertzmark, E.; Kain, K.C.; et al. Vitamin D Concentration during Early Pregnancy and Adverse Outcomes among HIV-Negative Women in Dar-es-Salaam, Tanzania: A Case-Control Study. Nutrients 2019, 11, 2906. https://doi.org/10.3390/nu11122906
Kalinjuma AV, Darling AM, Sudfeld CR, Mugusi F, Wright J, Abioye AI, Aboud S, McDonald C, Hertzmark E, Kain KC, et al. Vitamin D Concentration during Early Pregnancy and Adverse Outcomes among HIV-Negative Women in Dar-es-Salaam, Tanzania: A Case-Control Study. Nutrients. 2019; 11(12):2906. https://doi.org/10.3390/nu11122906
Chicago/Turabian StyleKalinjuma, Aneth V., Anne Marie Darling, Christopher R. Sudfeld, Ferdinand Mugusi, Julie Wright, Ajibola I. Abioye, Said Aboud, Chloe McDonald, Ellen Hertzmark, Kevin C. Kain, and et al. 2019. "Vitamin D Concentration during Early Pregnancy and Adverse Outcomes among HIV-Negative Women in Dar-es-Salaam, Tanzania: A Case-Control Study" Nutrients 11, no. 12: 2906. https://doi.org/10.3390/nu11122906