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Twins in Guinea-Bissau have a ‘thin-fat’ body composition compared to singletons

Published online by Cambridge University Press:  04 April 2022

Rucha Wagh
Affiliation:
Diabetes Unit, King Edward Memorial Hospital and Research Centre, Pune, Maharashtra, India
Morten Bjerregaard-Andersen*
Affiliation:
2Bandim Health Project, INDEPTH Network, Bissau Codex, Guinea-Bissau Department of Endocrinology, Hospital of Southwest Jutland, Esbjerg, Denmark Steno Diabetes Center Odense, Odense University Hospital, Odense, Denmark Department of Regional Health Research, University of Southern Denmark, Odense, Denmark
Souvik Bandyopadhyay
Affiliation:
Strategic Consultant, Cytel, Inc., Bangalore, India
Pranav Yajnik
Affiliation:
Cytel, Inc., Cambridge, MA, USA
Rashmi B. Prasad
Affiliation:
Lund University Diabetes Centre, Department of Clinical Sciences Malmö, Lund University, Malmö, Sweden
Suhas Otiv
Affiliation:
Diabetes Unit, King Edward Memorial Hospital and Research Centre, Pune, Maharashtra, India
Stine Byberg
Affiliation:
2Bandim Health Project, INDEPTH Network, Bissau Codex, Guinea-Bissau Steno Diabetes Center Copenhagen, Gentofte, Denmark
Ditte Egegaard Hennild
Affiliation:
2Bandim Health Project, INDEPTH Network, Bissau Codex, Guinea-Bissau
Gabriel Marciano Gomes
Affiliation:
2Bandim Health Project, INDEPTH Network, Bissau Codex, Guinea-Bissau
Kaare Christensen
Affiliation:
The Danish Twin Registry, Epidemiology, Institute of Public Health, University of Southern Denmark, Odense, Denmark Department of Clinical Genetics, Odense University Hospital, Odense, Denmark Department of Clinical Biochemistry and Pharmacology, Odense University Hospital, Odense, Denmark
Morten Sodemann
Affiliation:
2Bandim Health Project, INDEPTH Network, Bissau Codex, Guinea-Bissau Department of Infectious Diseases, Odense University Hospital, Odense, Denmark
Dorte Møller Jensen
Affiliation:
Steno Diabetes Center Odense, Odense University Hospital, Odense, Denmark Department of Gynaecology and Obstetrics, Odense University Hospital, Odense, Denmark Department of Clinical Research, Faculty of Health Sciences, University of Southern Denmark, Odense, Denmark
Chittaranjan S. Yajnik*
Affiliation:
Diabetes Unit, King Edward Memorial Hospital and Research Centre, Pune, Maharashtra, India
*
Address for correspondence: Morten Bjerregaard-Andersen, Department of Endocrinology, Hospital of Southwest Jutland, Haraldsgade 7, 6700, Esbjerg, Denmark. E-mail: Morten.Bjerregaard-Andersen2@rsyd.dk; Chittaranjan S. Yajnik, Diabetes Unit, KEM Hospital Research Centre, Pune, India, Email: csyajnik@gmail.com
Address for correspondence: Morten Bjerregaard-Andersen, Department of Endocrinology, Hospital of Southwest Jutland, Haraldsgade 7, 6700, Esbjerg, Denmark. E-mail: Morten.Bjerregaard-Andersen2@rsyd.dk; Chittaranjan S. Yajnik, Diabetes Unit, KEM Hospital Research Centre, Pune, India, Email: csyajnik@gmail.com

Abstract

The ‘thrifty phenotype’ hypothesis proposed that fetal undernutrition increases risk of diabetes in later life. Undernourished low birthweight Indian babies are paradoxically more adipose compared to well-nourished European babies, and are at higher risk of diabetes in later life. Twin pregnancies are an example of in utero growth restrictive environment due to shared maternal nutrition. There are few studies of body composition in twins. We performed secondary analysis of anthropometric body composition of twins and singletons in Guinea-Bissau, an economically deprived African country.

Anthropometric data were available on 7–34 year-old twins (n = 209, 97 males) and singletons (n = 182, 86 males) in the Guinea-Bissau Twin Registry at the Bandim Health Project. Twins had lower birthweight (2420 vs 3100 g, p < 0.001); and at follow-up, lower height (HAZ mean Z-score difference, −0.21, p = 0.055), weight (WAZ −0.73, p = 0.024) and BMI (BAZ −0.22, p = 0.079) compared to singletons but higher adiposity (skinfolds: +0.33 SD, p = 0.001). Twins also had higher fasting (+0.38 SD, p < 0.001) and 2-hour OGTT glucose concentrations (+0.29 SD, p < 0.05). Linear mixed-effect model accounting for intrapair correlations and interactions confirmed that twins were thinner but fatter across the age range. Data on maternal morbidity and prematurity were not available in this cohort.

African populations are known to have a muscular (less adipose) body composition. Demonstration of a thin-fat phenotype in twins in a low socio-economic African country supports the thesis that it could be a manifestation of early life undernutrition and not exclusive to Indians. This phenotype could increase risk of diabetes and related conditions.

Type
Original Article
Copyright
© The Author(s), 2022. Published by Cambridge University Press in association with International Society for Developmental Origins of Health and Disease

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References

Hales, CN, Barker, DJ. Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia. 1992; 35(7), 595601. DOI 10.1007/BF00400248.CrossRefGoogle ScholarPubMed
Hales, CN, Barker, DJ, Clark, PM, et al. Fetal and infant growth and impaired glucose tolerance at age 64. BMJ. 1991; 303(6809), 10191022. DOI 10.1136/bmj.303.6809.1019.CrossRefGoogle ScholarPubMed
Whincup, PH, Kaye, SJ, Owen, CG, et al. Birth weight and risk of type 2 diabetes: a systematic review. JAMA. 2008; 300(24), 28862897. DOI 10.1001/jama.2008.886.Google ScholarPubMed
Fall, CH. Non-industrialised countries and affluence. Br Med Bull. 2001; 60(1), 3350. DOI 10.1093/bmb/60.1.33.CrossRefGoogle ScholarPubMed
Yajnik, CS, Fall, CH, Coyaji, KJ, et al. Neonatal anthropometry: the thin-fat Indian baby. The Pune Maternal Nutrition Study. Int J Obes Relat Metab Disord. 2003; 27(2), 173180. DOI 10.1038/sj.ijo.802219.CrossRefGoogle ScholarPubMed
Yajnik, CS, Lubree, HG, Rege, SS, et al. Adiposity and hyperinsulinemia in Indians are present at birth. J Clin Endocrinol Metab. 2002; 87(12), 55755580. DOI 10.1210/jc.2002-020434.CrossRefGoogle ScholarPubMed
Modi, N, Thomas, EL, Uthaya, SN, Umranikar, S, Bell, JD, Yajnik, C. Whole body magnetic resonance imaging of healthy newborn infants demonstrates increased central adiposity in Asian Indians. Pediatr Res. 2009; 65(5), 584587. DOI 10.1203/pdr.0b013e31819d98be.CrossRefGoogle ScholarPubMed
Yajnik, C. The story of the hungry Indian foetus. NFI Bulletin. 2019; 40(3), 18.Google Scholar
Yajnik, CS, Yudkin, JS. The Y-Y paradox. Lancet. 2004; 363(9403), 163. DOI 10.1016/S0140-6736(03)15269-5.CrossRefGoogle ScholarPubMed
Lakshmi, S, Metcalf, B, Joglekar, C, Yajnik, CS, Fall, CH, Wilkin, TJ. Differences in body composition and metabolic status between white U.K. and Asian Indian children (EarlyBird 24 and the Pune Maternal Nutrition Study). Pediatr Obes. 2012; 7(5), 347354. DOI 10.1111/j.2047-6310.2012.00063.x.CrossRefGoogle Scholar
D'Angelo, S, Yajnik, CS, Kumaran, K, et al. Body size and body composition: a comparison of children in India and the UK through infancy and early childhood. J Epidemiol Community Health. 2015; 69(12), 11471153. DOI 10.1136/jech-2014-204998.CrossRefGoogle ScholarPubMed
van Steijn, L, Karamali, NS, Kanhai, HH, et al. Neonatal anthropometry: thin-fat phenotype in fourth to fifth generation South Asian neonates in Surinam. Int J Obes (Lond). 2009; 33(11), 13261329. DOI 10.1038/ijo.2009.154.CrossRefGoogle ScholarPubMed
Deurenberg-Yap, M, Schmidt, G, van Staveren, WA, Deurenberg, P. The paradox of low body mass index and high body fat percentage among Chinese, Malays and Indians in Singapore. Int J Obes Relat Metab Disord. 2000; 24(8), 10111017. DOI 10.1038/sj.ijo.0801353.CrossRefGoogle Scholar
Poulsen, P, Vaag, AA, Kyvik, KO, Møller Jensen, D, Beck-Nielsen, H. Low birth weight is associated with NIDDM in discordant monozygotic and dizygotic twin pairs. Diabetologia. 1997; 40(4), 439446. DOI 10.1007/s001250050698.CrossRefGoogle ScholarPubMed
Phillips, DI, Davies, MJ, Robinson, JS. Fetal growth and the fetal origins hypothesis in twins--problems and perspectives. Twin Res. 2001; 4(5), 327331. DOI 10.1375/1369052012669.CrossRefGoogle Scholar
Hall, JG. Twinning. Lancet. 2003; 362(9385), 735743. DOI 10.1016/S0140-6736(03)14237-7.CrossRefGoogle ScholarPubMed
Smits, J, Monden, C. Twinning across the developing world. PLoS One. 2011; 6(9), e25239. DOI 10.1371/journal.pone.0025239.CrossRefGoogle ScholarPubMed
Bjerregaard-Andersen, M, Lund, N, Jepsen, FS, et al. A prospective study of twinning and perinatal mortality in urban Guinea-Bissau. BMC Pregnancy Childbirth. 2012; 12(1), 140. DOI 10.1186/1471-2393-12-140.CrossRefGoogle ScholarPubMed
Bjerregaard-Andersen, M, Gomes, GM, Hennild, DE, et al. The Guinea-Bissau twin registry update: a platform for studying twin mortality and metabolic disease. Twin Res Hum Genet. 2019; 22(6), 554560.CrossRefGoogle ScholarPubMed
Hennild, DE, Bjerregaard-Andersen, M, Joaquim, LC, et al. Prevalence of impaired glucose tolerance and other types of dysglycaemia among young twins and singletons in Guinea-Bissau. BMC Endocr Disord. 2016; 16(1), 46.CrossRefGoogle ScholarPubMed
Bjerregaard-Andersen, M, Hansen, L, da Silva, LI, et al. Risk of metabolic syndrome and diabetes among young twins and singletons in Guinea-Bissau. Diabetes care. 2013; 36(11), 35493556.CrossRefGoogle ScholarPubMed
Rabe-Hesketh, S, Skrondal, A, Gjessing, HK. Biometrical modeling of twin and family data using standard mixed model software. Biometrics. 2008; 64(1), 280288. DOI 10.1111/j.1541-0420.2007.00803.x.CrossRefGoogle ScholarPubMed
R Core Team. R: A language and environment for statistical computing, 2020. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/ Google Scholar
Yajnik, CS. The insulin resistance epidemic in India: fetal origins, later lifestyle, or both? Nutr Rev. 2001; 59(1 Pt 1), 19. DOI 10.1111/j.1753-4887.2001.tb01898.x.CrossRefGoogle ScholarPubMed
Yajnik, CS, Yajnik, PC. Fetal adiposity epidemic in the modern world: a thrifty phenotype aggravated by maternal obesity and diabetes. Am J Clin Nutr. 2020; 112(1), 810. DOI 10.1093/ajcn/nqaa122.CrossRefGoogle ScholarPubMed
NCD Risk Factor Collaboration (NCD-RisC). A century of trends in adult human height. eLife. 2016; 5, e13410.CrossRefGoogle Scholar
Anand, SS, Gupta, MK, Schulze, KM, et al. What accounts for ethnic differences in newborn skinfold thickness comparing South Asians and White Caucasians? Findings from the START and FAMILY Birth Cohorts. Int J Obes (Lond). 2016; 40(2), 239244. DOI 10.1038/ijo.2015.171.CrossRefGoogle ScholarPubMed
Joglekar, CV, Fall, CH, Deshpande, VU, et al. Newborn size, infant and childhood growth, and body composition and cardiovascular disease risk factors at the age of 6 years: the Pune Maternal Nutrition Study. Int J Obes (Lond). 2007; 31(10), 15341544. DOI 10.1038/sj.ijo.0803679.CrossRefGoogle ScholarPubMed
Bavdekar, A, Yajnik, CS, Fall, CH, et al. Insulin resistance syndrome in 8-year-old Indian children: small at birth, big at 8 years, or both? Diabetes. 1999; 48(12), 24222429. DOI 10.2337/diabetes.48.12.2422.CrossRefGoogle Scholar
Abdul-Ghani, MA, DeFronzo, RA. Pathogenesis of insulin resistance in skeletal muscle. J Biomed Biotechnol. 2010; 2010, 476279. DOI 10.1155/2010/476279.CrossRefGoogle ScholarPubMed
Wells, JC, Pomeroy, E, Walimbe, SR, Popkin, BM, Yajnik, CS. The elevated susceptibility to diabetes in India: an evolutionary perspective. Front Public Health. 2016; 4(9859), 145. DOI 10.3389/fpubh.2016.00145.CrossRefGoogle Scholar
Staimez, LR, Weber, MB, Ranjani, H, et al. Evidence of reduced β-cell function in Asian Indians with mild dysglycemia. Diabetes Care. 2013; 36(9), 27722778. DOI 10.2337/dc12-2290.CrossRefGoogle ScholarPubMed
Yajnik, CS, Bandopadhyay, S, Bhalerao, A, et al. Poor in utero growth, and reduced β-cell compensation and high fasting glucose from childhood, are harbingers of glucose intolerance in young Indians. Diabetes Care. 2021; 44(12), 27472757. DOI 10.2337/dc20-3026.CrossRefGoogle ScholarPubMed
Poulsen, P, Grunnet, LG, Pilgaard, K, et al. Increased risk of type 2 diabetes in elderly twins. Diabetes. 2009; 58(6), 13501355. DOI 10.2337/db08-1714.CrossRefGoogle ScholarPubMed
Malis, C, Rasmussen, EL, Poulsen, P, et al. Total and regional fat distribution is strongly influenced by genetic factors in young and elderly twins. Obes Res. 2005; 13(12), 21392145. DOI 10.1038/oby.2005.265.CrossRefGoogle Scholar
Petersen, I, Nielsen, MM, Beck-Nielsen, H, Christensen, K. No evidence of a higher 10 year period prevalence of diabetes among 77,885 twins compared with 215,264 singletons from the Danish birth cohorts 1910-1989. Diabetologia. 2011; 54(8), 20162024. DOI 10.1007/s00125-011-2128-2.CrossRefGoogle ScholarPubMed
ConceiçaÌ o Pedro, 2019. Human development report 2019: Beyond income, beyond averages, beyond today: Inequalities in human development in the 21st Century, New York, NY: United Nations Development Programme.Google Scholar
Alessia Vittorangeli. WFP Guinea-Bissau Country Brief July and August 2021. www.wfp.org/countries/guinea-bissau, last accessed Feb 2022.CrossRefGoogle Scholar
Wagner, DR, Heyward, VH. Measures of body composition in blacks and whites: a comparative review. Am J Clin Nutr. 2000; 71(6), 13921402. DOI 10.1093/ajcn/71.6.1392.CrossRefGoogle ScholarPubMed
Silva, AM, Shen, W, Heo, M, et al. Ethnicity-related skeletal muscle differences across the lifespan. Am J Hum Biol. 2010; 22(1), 7682. DOI 10.1002/ajhb.20956.CrossRefGoogle ScholarPubMed
Hardikar, AA, Satoor, SN, Karandikar, MS, et al. Multigenerational undernutrition increases susceptibility to obesity and diabetes that is not reversed after dietary recuperation. Cell Metab. 2015; 22(2), 312319. DOI 10.1016/j.cmet.2015.06.008.CrossRefGoogle Scholar
Muhlhausler, BS, Hancock, SN, Bloomfield, FH, Harding, R. Are twins growth restricted? Pediatr Res. 2011; 70(2), 117122. DOI 10.1203/PDR.0b013e31821f6cfd.CrossRefGoogle ScholarPubMed
Hiersch, L, Okby, R, Freeman, H, et al. Differences in fetal growth patterns between twins and singletons. J Matern Fetal Neonatal Med. 2020; 33(15), 25462555. DOI 10.1080/14767058.2018.1555705.CrossRefGoogle ScholarPubMed
Poissonnet, CM, Burdi, AR, Bookstein, FL. Growth and development of human adipose tissue during early gestation. Early Hum Dev. 1983; 8(1), 111. DOI 10.1016/0378-3782(83)90028-2.Google ScholarPubMed
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