Association of preterm birth with lipid disorders in early adulthood: A Swedish cohort study

English version

Autoři: Casey Crump ^aff001; Jan Sundquist ^aff002; Kristina Sundquist ^aff002
Působiště autorů: Departments of Family Medicine and Community Health and of Population Health Science and Policy, Icahn School of Medicine at Mount Sinai, New York, New York, United States of America ^aff001; Center for Primary Health Care Research, Department of Clinical Sciences, Lund University, Malmö, Sweden ^aff002
Vyšlo v časopise: Association of preterm birth with lipid disorders in early adulthood: A Swedish cohort study. PLoS Med 16(10): e1002947. doi:10.1371/journal.pmed.1002947
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pmed.1002947

Souhrn

Background

Preterm birth has previously been linked with cardiovascular disease (CVD) in adulthood. However, associations with lipid disorders (e.g., high cholesterol or triglycerides), which are major risk factors for CVD, have seldom been examined and are conflicting. Clinicians will increasingly encounter adult survivors of preterm birth and will need to understand the long-term health sequelae. We conducted the first large population-based study to determine whether preterm birth is associated with an increased risk of lipid disorders.

Methods and findings

A retrospective national cohort study was conducted of all 2,235,012 persons born as singletons in Sweden during 1973 to 1995 (48.6% women), who were followed up for lipid disorders identified from nationwide inpatient, outpatient, and pharmacy data through 2016 (maximum age 44 years). Cox regression was used to adjust for other perinatal and maternal factors, and co-sibling analyses assessed the potential influence of unmeasured shared familial (genetic and/or environmental) factors. A total of 25,050 (1.1%) persons were identified with lipid disorders in 30.3 million person-years of follow-up. Each additional 5 weeks of gestation were associated with a 14% reduction in risk of lipid disorders (adjusted hazard ratio [HR], 0.86; 95% CI, 0.83–0.89; P < 0.001). Relative to full-term birth (gestational age 39–41 weeks), the adjusted HR associated with preterm birth (<37 weeks) was 1.23 (95% CI, 1.16–1.29; P < 0.001), and further stratified was 2.00 (1.41–2.85; P < 0.001) for extremely preterm (22–27 weeks), 1.33 (1.19–1.49; P < 0.001) for very preterm (28–33 weeks), and 1.19 (1.12–1.26; P < 0.001) for late preterm (34–36 weeks). These findings were similar in men and women (e.g., preterm versus full-term, men: HR, 1.22; 95% CI, 1.14–1.31; P < 0.001; women: HR, 1.23; 1.12–1.32; P < 0.001). Co-sibling analyses suggested that they were substantially though not completely explained by shared genetic or environmental factors in families. The main study limitation was the unavailability of laboratory data to assess specific types or severity of lipid disorders.

Conclusions

In this large national cohort, preterm birth was associated with an increased risk of lipid disorders in early- to midadulthood. Persons born prematurely may need early preventive evaluation and long-term monitoring for lipid disorders to reduce their future cardiovascular risks.

Klíčová slova:

Birth – Labor and delivery – Lipids – Cholesterol – Cardiovascular diseases – Sweden – Preterm birth – Lipid analysis

Zdroje

1. Blencowe H, Cousens S, Oestergaard MZ, Chou D, Moller AB, Narwal R, et al. National, regional, and worldwide estimates of preterm birth rates in the year 2010 with time trends since 1990 for selected countries: a systematic analysis and implications. Lancet. 2012;379(9832):2162–72. Epub 2012/06/12. doi: 10.1016/S0140-6736(12)60820-4 22682464.

2. Purisch SE, Gyamfi-Bannerman C. Epidemiology of preterm birth. Semin Perinatol. 2017;41(7):387–91. Epub 2017/09/04. doi: 10.1053/j.semperi.2017.07.009 28865982.

3. March of Dimes. PeriStats: March of Dimes; 2019. Available from: http://www.marchofdimes.com/Peristats/. [cited 2019 August 12].

4. Zeitlin J, Szamotulska K, Drewniak N, Mohangoo AD, Chalmers J, Sakkeus L, et al. Preterm birth time trends in Europe: a study of 19 countries. BJOG. 2013;120(11):1356–65. Epub 2013/05/25. doi: 10.1111/1471-0528.12281 23700966; PubMed Central PMCID: PMC4285908.

5. Crump C, Howell EA, Stroustrup A, McLaughlin MA, Sundquist J, Sundquist K. Association of Preterm Birth With Risk of Ischemic Heart Disease in Adulthood. JAMA Pediatr. 2019. Epub 2019/06/04. doi: 10.1001/jamapediatrics.2019.1327 31157896.

6. Crump C, Winkleby MA, Sundquist K, Sundquist J. Risk of hypertension among young adults who were born preterm: a Swedish national study of 636,000 births. Am J Epidemiol. 2011;173(7):797–803. doi: 10.1093/aje/kwq440 21320866; PubMed Central PMCID: PMC3105282.

7. de Jong F, Monuteaux MC, van Elburg RM, Gillman MW, Belfort MB. Systematic review and meta-analysis of preterm birth and later systolic blood pressure. Hypertension. 2012;59(2):226–34. Epub 2011/12/14. doi: 10.1161/HYPERTENSIONAHA.111.181784 22158643; PubMed Central PMCID: PMC3266458.

8. Crump C, Winkleby MA, Sundquist K, Sundquist J. Risk of diabetes among young adults born preterm in Sweden. Diabetes Care. 2011;34(5):1109–13. doi: 10.2337/dc10-2108 21411504; PubMed Central PMCID: PMC3114485.

9. Kajantie E, Strang-Karlsson S, Hovi P, Wehkalampi K, Lahti J, Kaseva N, et al. Insulin sensitivity and secretory response in adults born preterm: the Helsinki Study of Very Low Birth Weight Adults. J Clin Endocrinol Metab. 2015;100(1):244–50. Epub 2014/10/11. doi: 10.1210/jc.2014-3184 25303493.

10. Hovi P, Andersson S, Eriksson JG, Jarvenpaa AL, Strang-Karlsson S, Makitie O, et al. Glucose regulation in young adults with very low birth weight. N Engl J Med. 2007;356(20):2053–63. Epub 2007/05/18. doi: 10.1056/NEJMoa067187 17507704.

11. Hofman PL, Regan F, Jackson WE, Jefferies C, Knight DB, Robinson EM, et al. Premature birth and later insulin resistance. N Engl J Med. 2004;351(21):2179–86. Epub 2004/11/19. doi: 10.1056/NEJMoa042275 15548778.

12. Cooper R, Atherton K, Power C. Gestational age and risk factors for cardiovascular disease: evidence from the 1958 British birth cohort followed to mid-life. Int J Epidemiol. 2009;38(1):235–44. Epub 2008/07/29. doi: 10.1093/ije/dyn154 18658251; PubMed Central PMCID: PMC3481805.

13. Fagerberg B, Bondjers L, Nilsson P. Low birth weight in combination with catch-up growth predicts the occurrence of the metabolic syndrome in men at late middle age: the Atherosclerosis and Insulin Resistance study. J Intern Med. 2004;256(3):254–9. Epub 2004/08/25. doi: 10.1111/j.1365-2796.2004.01361.x 15324369.

14. Hovi P, Kajantie E, Soininen P, Kangas AJ, Jarvenpaa AL, Andersson S, et al. Lipoprotein subclass profiles in young adults born preterm at very low birth weight. Lipids Health Dis. 2013;12:57. Epub 2013/05/02. doi: 10.1186/1476-511X-12-57 23631373; PubMed Central PMCID: PMC3661387.

15. Rotteveel J, van Weissenbruch MM, Twisk JW, Delemarre-Van de Waal HA. Abnormal lipid profile and hyperinsulinaemia after a mixed meal: additional cardiovascular risk factors in young adults born preterm. Diabetologia. 2008;51(7):1269–75. Epub 2008/05/23. doi: 10.1007/s00125-008-1029-5 18496668.

16. Dalziel SR, Parag V, Rodgers A, Harding JE. Cardiovascular risk factors at age 30 following pre-term birth. Int J Epidemiol. 2007;36(4):907–15. Epub 2007/05/01. doi: 10.1093/ije/dym067 17468503.

17. Hovi P, Turanlahti M, Strang-Karlsson S, Wehkalampi K, Jarvenpaa AL, Eriksson JG, et al. Intima-media thickness and flow-mediated dilatation in the Helsinki study of very low birth weight adults. Pediatrics. 2011;127(2):e304–11. Epub 2011/01/26. doi: 10.1542/peds.2010-2199 21262880.

18. Singhal A, Kattenhorn M, Cole TJ, Deanfield J, Lucas A. Preterm birth, vascular function, and risk factors for atherosclerosis. Lancet. 2001;358(9288):1159–60. Epub 2001/10/13. doi: 10.1016/S0140-6736(01)06276-6 11597675.

19. Skilton MR, Viikari JS, Juonala M, Laitinen T, Lehtimaki T, Taittonen L, et al. Fetal growth and preterm birth influence cardiovascular risk factors and arterial health in young adults: the Cardiovascular Risk in Young Finns Study. Arterioscler Thromb Vasc Biol. 2011;31(12):2975–81. Epub 2011/09/24. doi: 10.1161/ATVBAHA.111.234757 21940950.

20. Statistics Sweden. The Swedish Medical Birth Register. Available from: https://www.socialstyrelsen.se/register/halsodataregister/medicinskafodelseregistret/inenglish. [cited 2019 August 12].

21. Crump C, Sundquist K, Winkleby MA, Sundquist J. Early-term birth (37–38 weeks) and mortality in young adulthood. Epidemiology. 2013;24(2):270–6. doi: 10.1097/EDE.0b013e318280da0f 23337240.

22. Crump C, Sundquist J, Winkleby MA, Sundquist K. Gestational age at birth and mortality from infancy into mid-adulthood: a national cohort study. Lancet Child Adolesc Health. 2019;3(6):408–17. Epub 2019/04/09. doi: 10.1016/S2352-4642(19)30108-7 30956154.

23. Ludvigsson JF, Andersson E, Ekbom A, Feychting M, Kim JL, Reuterwall C, et al. External review and validation of the Swedish national inpatient register. BMC Public Health. 2011;11:450. doi: 10.1186/1471-2458-11-450 21658213; PubMed Central PMCID: PMC3142234.

24. Rubin DB. Multiple Imputation for Nonresponse in Surveys. New York: Wiley; 1987.

25. Lahey BB, D'Onofrio BM. All in the Family: Comparing Siblings to Test Causal Hypotheses Regarding Environmental Influences on Behavior. Curr Dir Psychol Sci. 2010;19(5):319–23. Epub 2010/10/01. doi: 10.1177/0963721410383977 23645975; PubMed Central PMCID: PMC3643791.

26. Sjolander A, Frisell T, Kuja-Halkola R, Oberg S, Zetterqvist J. Carryover Effects in Sibling Comparison Designs. Epidemiology. 2016;27(6):852–8. Epub 2016/08/05. doi: 10.1097/EDE.0000000000000541 27488059.

27. D'Onofrio BM, Lahey BB, Turkheimer E, Lichtenstein P. Critical need for family-based, quasi-experimental designs in integrating genetic and social science research. Am J Public Health. 2013;103 Suppl 1:S46–55. Epub 2013/08/10. doi: 10.2105/AJPH.2013.301252 23927516; PubMed Central PMCID: PMC3778076.

28. Deeks JJ, Altman DG, Bradburn MJ. Statistical methods for examining heterogeneity and combining results from several studies in meta-analysis. In: Egger M, Smith GD, Altman DG, editors. Systematic Reviews in Health Care: Meta-Analysis in Context 2001. p. 285–321.

29. Li R, Chambless L. Test for additive interaction in proportional hazards models. Ann Epidemiol. 2007;17(3):227–36. doi: 10.1016/j.annepidem.2006.10.009 17320789.

30. VanderWeele TJ. Causal interactions in the proportional hazards model. Epidemiology. 2011;22(5):713–7. Epub 2011/05/12. doi: 10.1097/EDE.0b013e31821db503 21558856; PubMed Central PMCID: PMC3150431.

31. Henkin Y, Como JA, Oberman A. Secondary dyslipidemia. Inadvertent effects of drugs in clinical practice. JAMA. 1992;267(7):961–8. Epub 1992/02/19. doi: 10.1001/jama.267.7.961 1734110.

32. Grambsch PM. Goodness-of-fit and diagnostics for proportional hazards regression models. Cancer Treat Res. 1995;75:95–112. doi: 10.1007/978-1-4615-2009-2_5 7640169.

33. Parkinson JR, Hyde MJ, Gale C, Santhakumaran S, Modi N. Preterm birth and the metabolic syndrome in adult life: a systematic review and meta-analysis. Pediatrics. 2013;131(4):e1240–63. doi: 10.1542/peds.2012-2177 23509172.

34. Crump C, Sundquist J, Winkleby MA, Sundquist K. Preterm birth and risk of chronic kidney disease from childhood into mid-adulthood: national cohort study. BMJ. 2019;365:l1346. Epub 2019/05/03. doi: 10.1136/bmj.l1346 31043374; PubMed Central PMCID: PMC6490674.

35. Crump C, Friberg D, Li X, Sundquist J, Sundquist K. Preterm birth and risk of sleep-disordered breathing from childhood into mid-adulthood. Int J Epidemiol. 2019. Epub 2019/04/22. doi: 10.1093/ije/dyz075 31006012.

36. Clausson B, Lichtenstein P, Cnattingius S. Genetic influence on birthweight and gestational length determined by studies in offspring of twins. BJOG. 2000;107(3):375–81. Epub 2000/03/31. 10740335.

37. Wilcox AJ, Skjaerven R, Lie RT. Familial patterns of preterm delivery: maternal and fetal contributions. Am J Epidemiol. 2008;167(4):474–9. Epub 2007/12/01. doi: 10.1093/aje/kwm319 18048376.

38. Svensson AC, Sandin S, Cnattingius S, Reilly M, Pawitan Y, Hultman CM, et al. Maternal effects for preterm birth: a genetic epidemiologic study of 630,000 families. Am J Epidemiol. 2009;170(11):1365–72. Epub 2009/10/27. doi: 10.1093/aje/kwp328 19854802.

39. Heller DA, de Faire U, Pedersen NL, Dahlen G, McClearn GE. Genetic and environmental influences on serum lipid levels in twins. N Engl J Med. 1993;328(16):1150–6. Epub 1993/04/22. doi: 10.1056/NEJM199304223281603 8455681.

40. Iliadou A, Snieder H, Wang X, Treiber FA, Davis CL. Heritabilities of lipids in young European American and African American twins. Twin Res Hum Genet. 2005;8(5):492–8. Epub 2005/10/11. doi: 10.1375/183242705774310187 16212838.

41. Teslovich TM, Musunuru K, Smith AV, Edmondson AC, Stylianou IM, Koseki M, et al. Biological, clinical and population relevance of 95 loci for blood lipids. Nature. 2010;466(7307):707–13. Epub 2010/08/06. doi: 10.1038/nature09270 20686565; PubMed Central PMCID: PMC3039276.

42. Benn M, Watts GF, Tybjaerg-Hansen A, Nordestgaard BG. Mutations causative of familial hypercholesterolaemia: screening of 98 098 individuals from the Copenhagen General Population Study estimated a prevalence of 1 in 217. Eur Heart J. 2016;37(17):1384–94. Epub 2016/02/26. doi: 10.1093/eurheartj/ehw028 26908947.

43. Futema M, Whittall RA, Kiley A, Steel LK, Cooper JA, Badmus E, et al. Analysis of the frequency and spectrum of mutations recognised to cause familial hypercholesterolaemia in routine clinical practice in a UK specialist hospital lipid clinic. Atherosclerosis. 2013;229(1):161–8. Epub 2013/05/15. doi: 10.1016/j.atherosclerosis.2013.04.011 23669246; PubMed Central PMCID: PMC3701838.

44. Tuckey RC. Progesterone synthesis by the human placenta. Placenta. 2005;26(4):273–81. Epub 2005/04/13. doi: 10.1016/j.placenta.2004.06.012 15823613.

45. Catov JM, Ness RB, Wellons MF, Jacobs DR, Roberts JM, Gunderson EP. Prepregnancy lipids related to preterm birth risk: the coronary artery risk development in young adults study. J Clin Endocrinol Metab. 2010;95(8):3711–8. Epub 2010/05/27. doi: 10.1210/jc.2009-2028 20501685; PubMed Central PMCID: PMC2913035.

46. Edison RJ, Berg K, Remaley A, Kelley R, Rotimi C, Stevenson RE, et al. Adverse birth outcome among mothers with low serum cholesterol. Pediatrics. 2007;120(4):723–33. Epub 2007/10/03. doi: 10.1542/peds.2006-1939 17908758.

47. Alleman BW, Smith AR, Byers HM, Bedell B, Ryckman KK, Murray JC, et al. A proposed method to predict preterm birth using clinical data, standard maternal serum screening, and cholesterol. Am J Obstet Gynecol. 2013;208(6):472 e1-11. Epub 2013/03/19. doi: 10.1016/j.ajog.2013.03.005 23500456; PubMed Central PMCID: PMC3765002.

48. Crump C, Sundquist K, Sundquist J, Winkleby MA. Gestational age at birth and mortality in young adulthood. JAMA. 2011;306(11):1233–40. Epub 2011/09/22. doi: 10.1001/jama.2011.1331 21934056.

49. Crump C. Medical history taking in adults should include questions about preterm birth. BMJ. 2014;349:g4860. doi: 10.1136/bmj.g4860 25085466.

50. Crump C. Birth history is forever: implications for family medicine. J Am Board Fam Med. 2015;28(1):121–3. Epub 2015/01/09. doi: 10.3122/jabfm.2015.01.130317 25567832.

51. Crump C, Sundquist K, Sundquist J. Adult outcomes of preterm birth. Prev Med. 2016;91:400–1. doi: 10.1016/j.ypmed.2016.08.024 27539070.