Skip to main content
Top
Published in: Acta Diabetologica 5/2013

01-10-2013 | Original Article

Pre-eclampsia and pregnancy-induced hypertension are associated with severe diabetic retinopathy in type 1 diabetes later in life

Authors: Daniel Gordin, Risto Kaaja, Carol Forsblom, Vilho Hiilesmaa, Kari Teramo, Per-Henrik Groop

Published in: Acta Diabetologica | Issue 5/2013

Login to get access

Abstract

To investigate whether pre-eclampsia (PE) or pregnancy-induced hypertension (PIH) predicts the development of severe diabetic retinopathy (SDR) in type 1 diabetes. Altogether, 203 women with type 1 diabetes who were followed during pregnancy were re-examined within the Finnish Diabetic Nephropathy Study. After excluding patients with pre-pregnancy hypertension and those who had had laser treatment or whose retinopathy was graded as proliferative at the index pregnancy, 158 were prospectively studied. As a surrogate marker for SDR, retinal laser photocoagulation was used. The time from pregnancy to SDR (N = 21) or follow-up was 16 years (interquartile range, 11–19). HbA1c was repeatedly measured both during pregnancy and follow-up. Women with prior PE (26 % vs. 6 %, P = 0.003) or PIH (24 % vs. 6 %, P = 0.008) had more often incident SDR during follow-up compared to those with normotensive pregnancy. The hazard ratios (HR) remained associated with the progression to SDR after adjustment for duration of diabetes and diabetic nephropathy in a Cox regression analysis [PE: 3.5 (95 % CI 1.1–10.9); P = 0.03 and for PIH: 3.2 (1.1–9.8); P = 0.04]. The association between PIH and incident SDR did not change after inclusion of mean HbA1c, measured during pregnancy (all 3 trimesters) and serial HbA1c measurements during follow-up, 3.5 (1.1–11.8; P = 0.03). However, in a similar model, the HR for PE was no more significant 2.0 (0.6–6.8; P = NS). The results suggest that women with type 1 diabetes and a hypertensive pregnancy have an increased risk of severe diabetic retinopathy later in life.
Literature
1.
go back to reference Ewers IM, de Valk HW, Visser GHA (2004) Risk of complications of pregnancy in women with type 1 diabetes: nationwide prospective study in the Netherlands. Br Med J 328:915–921CrossRef Ewers IM, de Valk HW, Visser GHA (2004) Risk of complications of pregnancy in women with type 1 diabetes: nationwide prospective study in the Netherlands. Br Med J 328:915–921CrossRef
2.
go back to reference Hiilesmaa V, Suhonen L, Teramo K (2000) Glycaemic control is associated with pre-eclampsia but not with pregnancy-induced hypertension in women with type I diabetes mellitus. Diabetologia 43:1534–1539PubMedCrossRef Hiilesmaa V, Suhonen L, Teramo K (2000) Glycaemic control is associated with pre-eclampsia but not with pregnancy-induced hypertension in women with type I diabetes mellitus. Diabetologia 43:1534–1539PubMedCrossRef
3.
go back to reference Redman CW, Sargent IL (2005) Latest advances in understanding preeclampsia. Science 308:1592–1594PubMedCrossRef Redman CW, Sargent IL (2005) Latest advances in understanding preeclampsia. Science 308:1592–1594PubMedCrossRef
4.
go back to reference Pouta A, Hartikainen AL, Sovio U, Gissler M, Laitinen J, McCarthy MI, Ruokonen A, Elliott P, Järvelin MR (2004) Manifestations of metabolic syndrome after hypertensive pregnancy. Hypertension 43:825–831PubMedCrossRef Pouta A, Hartikainen AL, Sovio U, Gissler M, Laitinen J, McCarthy MI, Ruokonen A, Elliott P, Järvelin MR (2004) Manifestations of metabolic syndrome after hypertensive pregnancy. Hypertension 43:825–831PubMedCrossRef
5.
go back to reference Irgens HU, Reisaeter L, Irgens LM, Lie RT (2001) Long term mortality of mothers and fathers after pre-eclampsia: population based cohort study. Br Med J 323:1213–1217CrossRef Irgens HU, Reisaeter L, Irgens LM, Lie RT (2001) Long term mortality of mothers and fathers after pre-eclampsia: population based cohort study. Br Med J 323:1213–1217CrossRef
6.
go back to reference Hannaford P, Ferry S, Hirsch S (1997) Cardiovascular sequelae of toxaemia of pregnancy. Heart 77:154–158PubMed Hannaford P, Ferry S, Hirsch S (1997) Cardiovascular sequelae of toxaemia of pregnancy. Heart 77:154–158PubMed
7.
go back to reference Haukkamaa L, Salminen M, Laivuori H, Leinonen H, Hiilesmaa V, Kaaja R (2004) Risk for subsequent coronary artery disease after preeclampsia. Am J Cardiol 93:805–808PubMedCrossRef Haukkamaa L, Salminen M, Laivuori H, Leinonen H, Hiilesmaa V, Kaaja R (2004) Risk for subsequent coronary artery disease after preeclampsia. Am J Cardiol 93:805–808PubMedCrossRef
8.
go back to reference Vikse BE, Irgens LM, Leivestad T, Skjaerven R, Iversen BM (2008) Preeclampsia and the risk of end-stage renal disease. N Engl J Med 359:800–809PubMedCrossRef Vikse BE, Irgens LM, Leivestad T, Skjaerven R, Iversen BM (2008) Preeclampsia and the risk of end-stage renal disease. N Engl J Med 359:800–809PubMedCrossRef
9.
go back to reference Gordin D, Hiilesmaa V, Fagerudd J, Rönnback M, Forsblom C, Kaaja R, Teramo K, Groop PH, FinnDiane Study Group (2007) Pre-eclampsia, but not pregnancy-induced hypertension is a risk factor for diabetic nephropathy in type 1 diabetic women. Diabetologia 50:516–522PubMedCrossRef Gordin D, Hiilesmaa V, Fagerudd J, Rönnback M, Forsblom C, Kaaja R, Teramo K, Groop PH, FinnDiane Study Group (2007) Pre-eclampsia, but not pregnancy-induced hypertension is a risk factor for diabetic nephropathy in type 1 diabetic women. Diabetologia 50:516–522PubMedCrossRef
10.
go back to reference National High Blood Pressure Education Program Working Group on High Blood Pressure in Pregnancy (2000) Report of the national high blood pressure education program working group on high blood pressure in pregnancy. Am J Obst Gynecol 83:S1–S22CrossRef National High Blood Pressure Education Program Working Group on High Blood Pressure in Pregnancy (2000) Report of the national high blood pressure education program working group on high blood pressure in pregnancy. Am J Obst Gynecol 83:S1–S22CrossRef
11.
go back to reference Levine RJ, Ewell MG, Hauth JC, Curet LB, Catalano PM, Morris CD, Choudhary G, Sibai BM (2000) Should the definition of preeclampsia include a rise in diastolic blood pressure of Q15 mm Hg to a level <90 mm Hg in association with proteinuria? Am J Obst Gynecol 183:787–792CrossRef Levine RJ, Ewell MG, Hauth JC, Curet LB, Catalano PM, Morris CD, Choudhary G, Sibai BM (2000) Should the definition of preeclampsia include a rise in diastolic blood pressure of Q15 mm Hg to a level <90 mm Hg in association with proteinuria? Am J Obst Gynecol 183:787–792CrossRef
12.
go back to reference Early Treatment Diabetic Retinopathy Study Research Group (1991) Fundus photographic risk factors for progression of diabetic retinopathy. ETDRS report number 12. Ophthalmology 98:823–833 Early Treatment Diabetic Retinopathy Study Research Group (1991) Fundus photographic risk factors for progression of diabetic retinopathy. ETDRS report number 12. Ophthalmology 98:823–833
13.
go back to reference Loukovaara S, Immonen I, Koistinen R, Hiilesmaa V, Kaaja R (2005) Inflammatory markers and retinopathy in pregnancies complicated with type 1 diabetes. Eye Lond 19:422–430PubMedCrossRef Loukovaara S, Immonen I, Koistinen R, Hiilesmaa V, Kaaja R (2005) Inflammatory markers and retinopathy in pregnancies complicated with type 1 diabetes. Eye Lond 19:422–430PubMedCrossRef
14.
go back to reference Grassi MA, Mazzulla DA, Knudtson MD, Huang WW, Lee KE, Klein BE, Nicolae DL, Klein R (2009) Patient self-report of prior laser treatment reliably indicates presence of severe diabetic retinopathy. Am J Ophthalmol 147:501–504PubMedCrossRef Grassi MA, Mazzulla DA, Knudtson MD, Huang WW, Lee KE, Klein BE, Nicolae DL, Klein R (2009) Patient self-report of prior laser treatment reliably indicates presence of severe diabetic retinopathy. Am J Ophthalmol 147:501–504PubMedCrossRef
15.
go back to reference Kytö JP, Harjutsalo V, Forsblom C, Hietala K, Summanen PA, Groop PH, on behalf of the FinnDiane Study Group (2011) Decline in the cumulative incidence of severe diabetic retinopathy in patients with type 1 diabetes. Diabetes Care 3: 2005–2007 Kytö JP, Harjutsalo V, Forsblom C, Hietala K, Summanen PA, Groop PH, on behalf of the FinnDiane Study Group (2011) Decline in the cumulative incidence of severe diabetic retinopathy in patients with type 1 diabetes. Diabetes Care 3: 2005–2007
16.
go back to reference Groop PH, Thomas MC, Moran JL, Wadèn J, Thorn LM, Mäkinen VP, Rosengård-Bärlund M, Saraheimo M, Hietala K, Heikkilä O, Forsblom C, FinnDiane Study Group (2009) The presence and severity of chronic kidney disease predicts all-cause mortality in type 1 diabetes. Diabetes 58:1651–1658PubMedCrossRef Groop PH, Thomas MC, Moran JL, Wadèn J, Thorn LM, Mäkinen VP, Rosengård-Bärlund M, Saraheimo M, Hietala K, Heikkilä O, Forsblom C, FinnDiane Study Group (2009) The presence and severity of chronic kidney disease predicts all-cause mortality in type 1 diabetes. Diabetes 58:1651–1658PubMedCrossRef
17.
go back to reference Levey AS, Coresh J, Greene T, Stevens LA, Zhang YL, Hendriksen S, Kusek JW, Van Lente F, Chronic Kidney Disease Epidemiology Collaboration (2006) Using standardized serum creatinine values in the modification of diet in renal disease study equation for estimating glomerular filtration rate. Ann Intern Med 145:247–254PubMedCrossRef Levey AS, Coresh J, Greene T, Stevens LA, Zhang YL, Hendriksen S, Kusek JW, Van Lente F, Chronic Kidney Disease Epidemiology Collaboration (2006) Using standardized serum creatinine values in the modification of diet in renal disease study equation for estimating glomerular filtration rate. Ann Intern Med 145:247–254PubMedCrossRef
18.
go back to reference Klein R, Knudtson MD, Lee KE, Gagnon R, Klein BE (2008) The Wisconsin Epidemiologic Study of Diabetic Retinopathy: XXII the twenty-five-year progression of retinopathy in persons with type 1 diabetes. Ophthalmology 115:1859–1868PubMedCrossRef Klein R, Knudtson MD, Lee KE, Gagnon R, Klein BE (2008) The Wisconsin Epidemiologic Study of Diabetic Retinopathy: XXII the twenty-five-year progression of retinopathy in persons with type 1 diabetes. Ophthalmology 115:1859–1868PubMedCrossRef
19.
go back to reference Holmes VA, Young IS, Patterson CC, Pearson DW, Walker JD, Maresh MJ, McCance DR, Diabetes and Pre-eclampsia Intervention Trial Study Group (2011) Optimal glycemic control, pre-eclampsia, and gestational hypertension in women with type 1 diabetes in the diabetes and pre-eclampsia intervention trial. Diabetes Care 34:1683–1688PubMedCrossRef Holmes VA, Young IS, Patterson CC, Pearson DW, Walker JD, Maresh MJ, McCance DR, Diabetes and Pre-eclampsia Intervention Trial Study Group (2011) Optimal glycemic control, pre-eclampsia, and gestational hypertension in women with type 1 diabetes in the diabetes and pre-eclampsia intervention trial. Diabetes Care 34:1683–1688PubMedCrossRef
20.
go back to reference Lain KY, Roberts JM (2002) Contemporary concepts of the pathogenesis and management of preeclampsia. JAMA 287:3183–3186PubMedCrossRef Lain KY, Roberts JM (2002) Contemporary concepts of the pathogenesis and management of preeclampsia. JAMA 287:3183–3186PubMedCrossRef
21.
go back to reference Arngrimsson R, Bjornsson S, Gersson RT, Bjornsson II, Walker JJ, Snaedal G (1990) Genetic and familial predisposition to eclampsia and preeclampsia in a defined population. Br J Obstet Gynaecol 97:131–140 Arngrimsson R, Bjornsson S, Gersson RT, Bjornsson II, Walker JJ, Snaedal G (1990) Genetic and familial predisposition to eclampsia and preeclampsia in a defined population. Br J Obstet Gynaecol 97:131–140
22.
go back to reference Brownlee M (2001) Biochemistry and molecular cell biology of diabetic complications. Nature 414:813–820PubMedCrossRef Brownlee M (2001) Biochemistry and molecular cell biology of diabetic complications. Nature 414:813–820PubMedCrossRef
23.
go back to reference Klein BE, Moss SE, Klein R (1990) Effect of pregnancy on progression of diabetic retinopathy. Diabetes Care 13:34–40PubMedCrossRef Klein BE, Moss SE, Klein R (1990) Effect of pregnancy on progression of diabetic retinopathy. Diabetes Care 13:34–40PubMedCrossRef
24.
go back to reference Dibble CM, Kochenour NK, Worley RJ, Tyler FH, Swartz M (1982) Effect of pregnancy on diabetic retinopathy. Obstet Gynecol 59:699–704PubMed Dibble CM, Kochenour NK, Worley RJ, Tyler FH, Swartz M (1982) Effect of pregnancy on diabetic retinopathy. Obstet Gynecol 59:699–704PubMed
25.
go back to reference Chew EY, Mills JL, Metzger BE, Remaley NA, Jovanovic-Peterson L, Knopp RH, Conley M, Rand L, Simpson JL, Holmes LB (1995) Metabolic control and progression of retinopathy. The Diabetes in Early Pregnancy Study. National Institute of Child Health and Human Development Diabetes in Early Pregnancy Study. Diabetes Care 18:631–637PubMedCrossRef Chew EY, Mills JL, Metzger BE, Remaley NA, Jovanovic-Peterson L, Knopp RH, Conley M, Rand L, Simpson JL, Holmes LB (1995) Metabolic control and progression of retinopathy. The Diabetes in Early Pregnancy Study. National Institute of Child Health and Human Development Diabetes in Early Pregnancy Study. Diabetes Care 18:631–637PubMedCrossRef
26.
go back to reference Colatrella A, Loguercio V, Mattei L, Trappolini M, Festa C, Stoppo M, Napoli A (2010) Hypertension in diabetic pregnancy: impact and long-term outlook. Best Pract Res Clin Endocrinol Metab 24:635–651PubMedCrossRef Colatrella A, Loguercio V, Mattei L, Trappolini M, Festa C, Stoppo M, Napoli A (2010) Hypertension in diabetic pregnancy: impact and long-term outlook. Best Pract Res Clin Endocrinol Metab 24:635–651PubMedCrossRef
27.
go back to reference Diabetes Control and Complications Trial Research Group (2000) Effect of pregnancy on microvascular complications in the diabetes control and complications trial. The Diabetes Control and Complications Trial Research Group. Diabetes Care 23:1084–1091CrossRef Diabetes Control and Complications Trial Research Group (2000) Effect of pregnancy on microvascular complications in the diabetes control and complications trial. The Diabetes Control and Complications Trial Research Group. Diabetes Care 23:1084–1091CrossRef
28.
go back to reference Vérier-Mine O, Chaturvedi N, Webb D, Fuller JH (2005) Is pregnancy a risk factor for microvascular complications? The EURODIAB Prospective Complications Study. Diabet Med 22:1503–1509PubMedCrossRef Vérier-Mine O, Chaturvedi N, Webb D, Fuller JH (2005) Is pregnancy a risk factor for microvascular complications? The EURODIAB Prospective Complications Study. Diabet Med 22:1503–1509PubMedCrossRef
29.
go back to reference Kaaja R, Sjöberg L, Hellsted T, Immonen I, Sane T, Teramo K (1996) Long-term effects of pregnancy on diabetic complications. Diabet Med 13:165–169PubMedCrossRef Kaaja R, Sjöberg L, Hellsted T, Immonen I, Sane T, Teramo K (1996) Long-term effects of pregnancy on diabetic complications. Diabet Med 13:165–169PubMedCrossRef
30.
go back to reference Lövestam-Adrian M, Agardh CD, Aberg A, Agardh E (1997) Pre-eclampsia is a potent risk factor for deterioration of retinopathy during pregnancy in Type 1 diabetic patients. Diabet Med 14:1059–1065PubMedCrossRef Lövestam-Adrian M, Agardh CD, Aberg A, Agardh E (1997) Pre-eclampsia is a potent risk factor for deterioration of retinopathy during pregnancy in Type 1 diabetic patients. Diabet Med 14:1059–1065PubMedCrossRef
31.
go back to reference Lindheimer MD, Taler SJ, Cunningham FG (2010) Hypertension in pregnancy. J Am Soc Hypertens 4:68–78PubMedCrossRef Lindheimer MD, Taler SJ, Cunningham FG (2010) Hypertension in pregnancy. J Am Soc Hypertens 4:68–78PubMedCrossRef
Metadata
Title
Pre-eclampsia and pregnancy-induced hypertension are associated with severe diabetic retinopathy in type 1 diabetes later in life
Authors
Daniel Gordin
Risto Kaaja
Carol Forsblom
Vilho Hiilesmaa
Kari Teramo
Per-Henrik Groop
Publication date
01-10-2013
Publisher
Springer Milan
Published in
Acta Diabetologica / Issue 5/2013
Print ISSN: 0940-5429
Electronic ISSN: 1432-5233
DOI
https://doi.org/10.1007/s00592-012-0415-0

Other articles of this Issue 5/2013

Acta Diabetologica 5/2013 Go to the issue
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.