Skip to main content
Download PDF

Vitamin D deficiency and visceral adipose tissue in early pregnant women

BMC Pregnancy and Childbirth volume 21, Article number: 476 (2021) Cite this article

Abstract

Background

We aimed to assess the correlation between vitamin D serum level and visceral fat tissue during early pregnancy.

Methods

This cross-sectional study was performed in Pernambuco, Brazil. 190 low risk pregnant women (8–16 gestational weeks) were eligible. Visceral adipose tissue was measured by ultrasonography following the technique described by Armellini. The 25(OH) D in serum was determined through chemiluminescence. The Spearman correlation test was applied to evaluate the correlation between vitamin D serum level and VAT, considering p < 0.05 to be significant.

Results

Vitamin D insufficiency was present in 129 (67.8 %) of subjects. Pregnant women with or without vitamin D deficiency did not differ in age, gestational age, nutritional status and visceral adipose tissue. No correlation between visceral adipose tissue and 25(OH) D was observed: − 0.057 (p = 0.435).

Conclusions

Maternal visceral adipose tissue and vitamin D serum level are not correlated during pregnancy.

Peer Review reports

Background

Vitamin D deficiency (VDD) is a major global public health problem in all age groups, even in developed countries and regions with adequate ultraviolet radiation. Exposure to sunlight is the main source of vitamin D (VD) and factors such as season, time of day, latitude, skin phototype, sun exposure duration, type of clothing and the use of sunscreens may influence its synthesis [1,2,3]. Brazil, a tropical/subtropical country with elevated ultraviolet radiation has a very high prevalence of VDD [4]. VD has many actions in the body including the musculoskeletal system, calcium homoeostasis and immune system [5]. Recently, a link between VD and chronic non-communicable diseases has emerged including insulin resistance, diabetes and cardiovascular disease [6,7,8]. These chronic diseases are also commonly associated with obesity [9].

It is believed that VDD is associated with obesity, and adipose tissue may be responsible for its lower bioavailability. Visceral Adipose Tissue (VAT) easily absorbs VD by chemical affinity. Therefore, volumetric dilution has been proposed as the main mechanism to elucidate its low levels in obesity [10,11,12]. Two large epidemiological studies have shown that the thickness of VAT correlated inversely with the serum concentration of 25OHD in the adult population [11, 13]. Hao et al. found an inversely association between vitamin level and VAT in Chinese men [14]. Zhang et al. also reported a significant negative association between VAT and VDD in men and pre-menopausal women but not in post-menopausal women [15]. Batista et al. found that excess visceral adiposity, hypertriglyceridemia and high low-density lipoprotein cholesterol levels were strong predictors of hypovitaminosis D [16]. A meta-analysis of randomized clinical trials reported positive effects of VD supplementation on fat mass [17].

In pregnant women, VDD is also an important health problem with a prevalence ranging from 5 to 84 % [12, 18]. Besides, pregnancy is associated with a VAT increased and it has been linked to insulin resistance and hyperglycemia [19, 20]. However, we did not find in our search studies evaluating the association between VDD and VAT in pregnant women. We aimed to assess the correlation between VD serum level and VAT during early pregnancy.

Methods

This cross-sectional study was performed at the Hospital Dom Malan located in Petrolina (9°S and 40°W), Pernambuco state, Northeast of Brazil. Hospital Dom Malan registers about 6 000 births per year. This region has an average ultraviolet index of 13 during most of the year.

Pregnant women aged 13–39 years and 8–16 weeks of gestational age were eligible. Exclusion criteria were twin pregnancy, diabetes mellitus, previous gestational diabetes or preeclampsia, fetal malformations, maternal mental disease. After screening, 190 pregnant women were included. All participants answered a questionnaire regarding socio-demographic and clinical information were taken from the medical record. Weight and height were measured according to the standardized methodology. Body mass index (BMI) was calculated by the formula: weight (kg) / height (m2) and Atalah classification was used [21]. VAT was measured by ultrasonography performed by a qualified specialist. A Philips D7 ultrasound device, equipped with a 3.0 to 7.0 MHz convex transducer, multifrequency (Bothell, WA/USA), was used. VAT was determined following the technique described by Armellini [22]: the convex transducer positioned immediately above the umbilical scar, the distance in centimeters being measured between the inner edge of the rectus abdominis muscle, at the point of its insertion in the alba line, and the anterior wall of the abdominal aorta.

The 25(OH) D in serum was determined through chemiluminescence, using the Atellica EVA-Siemens device (Erlangen/Germany) with a result expressed in nanograms per Milliliter. Insufficiency and deficiency values were respectively between 20 and 30 ng/mL and < 20 ng/mL, according to the values adopted by the Endocrine Society Practice Guidelines [23].

Statistical analyses

Data were analyzed descriptively through absolute and percentage frequencies in the categorical variables and the measures: mean, standard deviation (mean ± SD), and median to numerical variables. To assess a significant association between two categorical variables, Pearson’s chi-square test including the likelihood ratio test and confidence interval (CI) was used. For the comparison between categories concerning the numerical variables, the Mann–Whitney test was used. To assess the degree of the relationship between two numerical variables, Spearman’s correlation coefficient and the specific Student’s t-test for the null correlation hypothesis were obtained.

The choice of the Mann–Whitney test and Spearman correlation was due to the absence of normality, which was verified by the Shapiro–Wilk test. The margin of error used in deciding the statistical tests was 5 and 95 % CI. The data were entered into the EXCEL spreadsheet, and the program used to obtain the statistical calculations was IMB SPSS in version 25.

Results

190 pregnant women were studied. The mean age was 26 ± 5.76 years and pregnant women were included in the study with a 12.3 ± 2.5 weeks of gestation. The BMI ranged from 16.6 to 47.0 kg/m² (25.7 ± 4.9 kg/m²); 57 (30 %) were overweight and 27 (14.2 %) obese. 129 (67.8 %) of pregnant women had vitamin D insuficiency, i.e., serum value of 25 (OH) D < 30 ng/mL. The thickness of the VAT varied between 0.9 and 6.1 cm (2.9 ± 0.9 cm). Pregnant women with or without VDD did not differ in age, gestational age, nutritional status and VAT (Table 1). The Spearman value correlation between VAT and 25(OH) D was – 0.057, (P value = 0.435). Table 2 presents Spearman correlation between VAT, 25(OH) D and age, weight and BMI.

Table 1 Characteristics of pregnant women studied according to the vitamin D status
Full size table
Table 2 Spearman correlation between visceral adipose, 25(OH) D and age, weight and body mass index
Full size table

Discussion

In the present study we did not find association between serum VD values and visceral fat in pregnant women. For the best of our knowledge, it is the first time that this association is assessed during pregnancy. Some studies have described an inverse association between VDD and visceral fat in non-pregnancy populations [24, 14]. However, among the various physiological changes that occur during pregnancy, the redistribution of adipose tissue is one of them. Although not yet properly studied, it is admitted that an increase in visceral adipose tissue occurs, but the specific function of visceral adipose in pregnancy is still unknown. Thus, it seems likely that visceral adipose tissue has somewhat distinct functions in pregnancy and our findings cannot be compared with non-pregnant populations.

Recently, Carreras-Badosa et al. found that maternal serum VD was inversely associated with visceral fat and in their offspring at the age of 5–6 years [25]. However, diet and lifestyle habits were not studied in both mothers and their children, and this, rather than maternal VD status could explain the relationship between lower maternal serum VD and offspring adiposity.

An increased risk of VDD has been described worldwide in obese individual. The underlying explanations are not clear. Receptors of VD are expressed in adipose tissue and 25(OH) D could modulate adipogenesis through VD receptors-dependent inhibition of specific components [26]. Other explanation is based on experimental findings that deficiency of VD can increases lipogenesis upregulating adipocyte calcium signaling and improving the secretion of parathyroid hormone [27]. However, the role of VD in adipogenesis or other functions of VAT during pregnancy is still unknown.

Pregnancy VDD has been described with a prevalence of 18–84 % [9]. In the present study, the prevalence of VDD was high (68 %). This value was similar to other Brazilian studies and higher than that described in countries such as Spain and United States [28]. Brazil is a tropical country with continental dimensions and abundant sunshine. The municipality of Petrolina is located at approximately − 9°, which favors the synthesis of VD. However, there is a paradox in countries with low solar incidence and with a lower frequency of VDD when compared with countries with higher solar incidence, certainly because of protection measures that prevent its synthesis and bioavailability [29].

In the multicenter HAPO study, increased maternal BMI was associated with lower maternal 25(OH) D levels [30]. However, BMI is not an accurate measure of fat tissue, especially during pregnancy. Besides, the deposition of adipose tissue preferably occurs in two distinct anatomical places, VAT and subcutaneous adipose tissue, and BMI does not differentiate them. We determine VAT through ultrasound and this method has been shown to be safe, effective, simple and reproducible [31].

Our study has some limitations. At first, a cross-sectional design was performed and we could not determine the causal relationship between VD and VAT. Second, other possible important variables confounding the VD status, like sun light exposition, dietary habits and possible seasonal variations in VD, were not evaluated in our study. However, despite these limitations our study has strengths. The present study is the first to assess the correlation of VD with VAT thickness in pregnant women. A large sample was studied and specific methods to measure VD and VAT were used.

Conclusions

Our data demonstrated that maternal visceral adiposity and low concentrations of VD were not associated during pregnancy. However, as this was the first study to assess the association between VAT and VD in pregnant women, further studies are needed to confirm these findings.

Availability of data and materials

The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.

Abbreviations

VD:

Vitamin D

VDD:

Vitamin D Deficiency

VAT:

Visceral Adipose Tissue

BMI:

Body Mass Index

References

  1. Palacios C GL. Is vitamin D deficiency a major global public health problem? Steroid Biochem Mol Biol [Internet]. 2014;144:138–45. Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4018438/pdf/nihms541186.pdf

  2. Van Schoor N, Lips P. Global Overview of Vitamin D Status. Endocrinol Metab Clin N Am. 2017;46:845–70.

    Article  Google Scholar 

  3. Correia A, do Azevedo MS, Gondim F, Bandeira F. Aspectos étnicos da defciência de vitamina D. Arq Bras Endocrinol Metabol. 2014;58(5):540–4.

    Article  Google Scholar 

  4. Eloi M, Horvath D V., Szejnfeld VL, Ortega JC, Rocha DAC, Szejnfeld J, et al. Vitamin D deficiency and seasonal variation over the years in São Paulo, Brazil. Osteoporos Int. 2016;27(12):3449–56.

    Article  CAS  Google Scholar 

  5. DeLuca HF. Vitamin D: Historical Overview. In: Vitam Horm [Internet]. 2016. p. 1–20. Available from: https://linkinghub.elsevier.com/retrieve/pii/S0083672915000655

  6. Wimalawansa SJ. Vitamin D and cardiovascular diseases: Causality. J Steroid Biochem Mol Biol. 2018;175:29–43.

    Article  CAS  Google Scholar 

  7. Berridge MJ. Vitamin D deficiency and diabetes. Biochem J. 2017;474(8):1321–32.

    Article  CAS  Google Scholar 

  8. Szymczak-Pajor I. Analysis of Association between Vitamin D Deficiency and Insulin Resistance. Nutrients. 2019;11(794):1–28.

    Google Scholar 

  9. Walsh JS, Bowles S, Evans AL. Vitamin D in obesity. Curr Opin Endocrinol Diabetes Obes. 2017;24(6):389–94.

    Article  CAS  Google Scholar 

  10. Cândido FG, Bressan J. Vitamin D: Link between osteoporosis, obesity, and diabetes? Int J Mol Sci. 2014;15(4):6569–91.

    Article  Google Scholar 

  11. Cheng S, Massaro JM, Fox CS, Larson MG, Keyes MJ, McCabe EL, et al. Adiposity, cardiometabolic risk, and vitamin D status: The framingham heart study. Diabetes. 2010;59(1):242–8.

    Article  CAS  Google Scholar 

  12. Young KA, Engelman CD, Langefeld CD, Hairston KG, Haffner SM, Bryer-Ash M, et al. Association of plasma vitamin D levels with adiposity in hispanic and African Americans. J Clin Endocrinol Metab. 2009;94(9):3306–13.

    Article  CAS  Google Scholar 

  13. Sulistyoningrum DC, Green TJ, Lear SA, Devlin AM. Ethnic-Specific Differences in Vitamin D Status Is Associated with Adiposity. PLoS One. 2012;7(8):1–6.

    Article  Google Scholar 

  14. Hao Y, Ma X, Shen Y, Ni J, Luo Y, Xiao Y, et al. Associations of serum 25-hydroxyvitamin D3 levels with visceral adipose tissue in Chinese men with normal glucose tolerance. PLoS One. 2014;9(1):3–9.

    Google Scholar 

  15. Zhang M, Li P, Zhu Y, Chang H, Wang X, Liu W, et al. Higher visceral fat area increases the risk of vitamin D insufficiency and deficiency in Chinese adults. Nutr Metab. 2015;12(1):1–14.

    Article  Google Scholar 

  16. Batista AP, Ambrosim TV, Nascimento Neto RM do, Pimenta FAP, Freitas SN de, Lauria MW, et al. Hypovitaminosis D Is Associated With Visceral Adiposity, High Levels of Low-Density Lipoprotein and Triglycerides in Alternating Shift Workers. J Endocrinol Metab. 2016;6(3):80–9.

  17. Pathak K, Soares MJ, Calton EK, Zhao Y, Hallett J. Vitamin D supplementation and body weight status: A systematic review and meta-analysis of randomized controlled trials. Obes Rev. 2014;15(6):528–37.

    Article  CAS  Google Scholar 

  18. O’Brien EC, O’Sullivan EJ, Kilbane MT, Geraghty AA, McKenna MJ, McAuliffe FM. Season and Vitamin D status are independently associated with glucose homeostasis in pregnancy. Nutr Metab. 2017;14(1):1–9.

    Article  Google Scholar 

  19. De Souza LR, Kogan E, Berger H, Alves JG, Lebovic G, Retnakaran R, et al. Abdominal adiposity and insulin resistance in early pregnancy. J Obstet Gynaecol Canada. 2014;36(11):969–75.

    Article  Google Scholar 

  20. Pontual AC, Figueiroa JN, De Souza LR, Ray JG, Alves JGB. Visceral Adiposity in the First Half of Pregnancy in Association with Glucose, Lipid and Insulin Profiles in Later Pregnancy: A Cohort Study. Matern Child Health J. 2016;20(8):1720–5.

    Article  Google Scholar 

  21. Atalah E, Castillo C, Castro R, Aldea A. [Proposal of a new standard for the nutritional assessment of pregnant women]. Rev Med Chil [Internet]. 1997 Dec;125(12):1429–36. Available from: http://www.ncbi.nlm.nih.gov/pubmed/9609018

  22. Armellini F, Zamboni M, Rigo L, Todesco T, Bosello O, Bergamo-Andreis IA, et al. The contribution of sonography to the measurement of intra‐abdominal fat J Clin Ultrasound. 1990;18(7):563–7..

  23. Holick MF, Binkley NC, Bischoff-Ferrari HA, Gordon CM, Hanley DA, Heaney RP, et al. Evaluation, treatment, and prevention of vitamin D deficiency: An endocrine society clinical practice guideline. J Clin Endocrinol Metab. 2011;96(7):1911–30.

    Article  CAS  Google Scholar 

  24. Seo JA, Cho H, Eun CR, Yoo HJ, Kim SG, Choi KM, et al. Association between visceral obesity and sarcopenia and vitamin D deficiency in older Koreans: The Ansan geriatric study. J Am Geriatr Soc. 2012;60(4):700–6.

    Article  Google Scholar 

  25. Carreras-Badosa G, Armero-Bujaldón C, Solé-Amat L, Prats-Puig A, Díaz-Roldán F, Soriano-Rodriguez P, et al. Association between maternal mid-gestation vitamin D status and neonatal abdominal adiposity. Int J Obes. 2016;42(1):40–6.

    Google Scholar 

  26. Wood RJ. Vitamin D and adipogenesis: New molecular insights. Nutr Rev. 2008;66(1):40–6.

    Article  Google Scholar 

  27. McCarty MF, Thomas CA. PTH excess may promote weight gain by impeding catecholamine-induced lipolysis-implications for the impact of calcium, vitamin D, and alcohol on body weight. Med Hypotheses. 2003;61(5–6):535–42.

    Article  CAS  Google Scholar 

  28. Figueiredo ACC, Cocate PG, Adegboye ARA, Franco-Sena AB, Farias DR, de Castro MBT, et al. Changes in plasma concentrations of 25-hydroxyvitamin D and 1,25-dihydroxyvitamin D during pregnancy: a Brazilian cohort. Eur J Nutr. 2018;57(3):1059–72.

    Article  CAS  Google Scholar 

  29. Azevedo M,Bandeira L,Luza C, Lemos A BF. Vitamin D Deficiency,Skin Phototype, Sun Index, and Metabolic Risk Among Patients with High Rates of Sun Exposure Living in the tropics. J clin Aesthet Dermatol [Internet]. 2018;11(8):15–8. Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6122513/pdf/jcad_11_8_15.pdf

  30. Josefson JL, Reisetter A, Scholtens DM, Price HE, Metzger BE, Langman CB. Maternal BMI associations with maternal and cord blood Vitamin D levels in a north American subset of hyperglycemia and adverse pregnancy outcome (HAPO) study participants. PLoS One. 2016;11(3):1–11.

    Article  Google Scholar 

  31. De Souza LR, Berger H, Retnakaran R, Maguire JL, Nathens AB, Connelly PW, et al. First-Trimester Maternal Abdominal Adiposity Predicts Dysglycemia and Gestational Diabetes Mellitus in Midpregnancy. Diabetes Care. 2016;39(1):61–4.

    Article  Google Scholar 

Download references

Acknowledgements

We would like to thank Dom Malan Hospital’s and Health Units’ employees for their help with recruitment of pregnant women.

Funding

This study was financed in part by the Coordination for the Improvement of Higher Education Personnel – Brasil (CAPES) – Finance Code 001, as a PhD Programm.

Author information

Authors and Affiliations

  1. Division of Endocrinology, University of Pernambuco Medical School, Recife, Brazil

    Rosangela Cisneiros & Francisco Bandeira

  2. Medicine School, Universidade Federal do Vale do São Francisco, Avenida José de Sá Maniçoba, s/n, Centro, 56304-917, PE, Petrolina, Brazil

    Rosangela Cisneiros

  3. Division of Endocrinology and Radiology, Universidade Federal do Vale do São Francisco, Petrolina, Brazil

    Juliana Segatto, Eloíse Paixão, Ítalo Bacellar & Álvaro Pacheco

  4. Division of Pediatrics and Radiology, Instituto de Medicina Integral Prof. Fernando Figueira, Recife, Brazil

    Marcelo Lima & João Guilherme Alves

Authors
  1. Rosangela Cisneiros
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Juliana Segatto
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Eloíse Paixão
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ítalo Bacellar
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Marcelo Lima
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Álvaro Pacheco
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. João Guilherme Alves
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Francisco Bandeira
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

RMRC— conception and design of the work, data acquisition, analysis, interpretation of data, drafting and revising of the manuscript, and final approval of the version to be published. JCMS—data acquisition, analysis and interpretation of data, drafting and revising of the manuscript, and final approval of the version to be published. EALP— data acquisition, analysis and interpretation of data, drafting and revising of the manuscript, and final approval of the version to be published. IRB— data acquisition, analysis and interpretation of data, drafting and revising of the manuscript, and final approval of the version to be published. MMSL— data acquisition, analysis and interpretation of data, drafting and revising of the manuscript, and final approval of the version to be published. AP— data acquisition, analysis and interpretation of data, drafting and revising of the manuscript, and final approval of the version to be published. JGBA— conception and design of the work, data acquisition, analysis, interpretation of data, drafting and revising of the manuscript, and final approval of the version to be published. FB— conception and design of the work, data acquisition, analysis, interpretation of data, drafting and revising of the manuscript, and final approval of the version to be published. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Rosangela Cisneiros.

Ethics declarations

Ethical approval and consent to participate

The Research Ethics Committee of the University of Pernambuco approved this project under CAAE 64806516.1.0000.5207 on February 14th 2017.All methods were carried out in accordance with relevant guidelines and regulations.All women signed previously an informed consent and if subjects were under 18, a parent and/or legal guardian has signed it.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Additional information

Publisher’s Note

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

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Cisneiros, R., Segatto, J., Paixão, E. et al. Vitamin D deficiency and visceral adipose tissue in early pregnant women. BMC Pregnancy Childbirth 21, 476 (2021). https://doi.org/10.1186/s12884-021-03888-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s12884-021-03888-1

Keywords

  • Visceral adipose tissue
  • Vitamin D
  • Pregnancy
  • Ultrasound
  • Obesity

BMC Pregnancy and Childbirth

ISSN: 1471-2393

Contact us