Maternal ophthalmic artery Doppler velocimetry in type 1 diabetes during pregnancy

Toshiyuki Hata1, Toshihiro Yanagihara, Hirokazu Tanaka, Chizu Yamashiro and Kenji Kanenishi

Department of Perinatology, Kagawa Medical University, 1750-1 Ikenobe, Miki, Kagawa 761-0793, Japan


    Abstract
 Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 References
 
Our purpose was to evaluate whether maternal ophthalmic artery pulsatility index (PI) in normotensive pregnancies with type 1 diabetes is different from that in normal normotensive pregnancies. The ophthalmic artery in 15 normal normotensive pregnant women, and 13 normotensive pregnant women with type 1 diabetes was studied once with colour Doppler flow imaging and pulsed Doppler ultrasonography after 16 weeks gestation. The heart rate, mean arterial blood pressure, and ophthalmic artery PI were calculated in each group. The PI (1.94 ± 0.45) in normotensive pregnant women with type 1 diabetes was significantly lower than that (2.73 ± 0.32) in normal normotensive pregnant women (P < 0.0001). There was no significant difference in maternal heart rate or mean arterial blood pressure between the two groups. These results suggest that vascular resistance in the maternal orbital circulation is reduced in pregnancies with type 1 diabetes that are normotensive. The lower PI in pregnant women with type 1 diabetes should be interpreted as orbital vascular vasodilatation, indicating orbital hyperperfusion or hyperaemia.

Key words: Doppler ultrasound/ophthalmic artery/pulsatility index/type 1 diabetes


    Introduction
 Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 References
 
Diabetes and pregnancy interact significantly such that maternal welfare can be seriously jeopardized (Cunningham et al., 1997Go). Maternal deaths have become rare in women with diabetes, although mortality is increased 10-fold, most often as a result of ketoacidosis, underlying hypertension, pre-eclampsia, and pyelonephritis. Generalized vasodilatation is observed from diagnosis in type 1 diabetes (Stehouwer and Schaper, 1996Go). This vasodilatation is more evident in the afferent arteriole, and it is believed to lead to capillary hypertension, thus contributing to the development of micro-angiopathy (Stehouwer and Schaper, 1996Go). Ophthalmic artery flow velocity waveforms can be easily depicted during pregnancy with colour Doppler imaging (Hata et al., 1992Go), and we found a decrease in orbital vascular resistance and an increase in orbital perfusion in pre-eclampsia (Hata et al., 1997Go). In this study, we evaluated whether flow velocity waveforms in the maternal ophthalmic artery in pregnant patients with type 1 diabetes are different from those in normal pregnant women.


    Materials and methods
 Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 References
 
The ophthalmic artery in 15 normal normotensive pregnant women and 11 normotensive pregnant women with type 1 diabetes was examined once with colour and pulsed Doppler ultrasonography after 16 weeks gestation. Diagnosis of type 1 diabetes was established by onset of the diabetes at <30 years, and insulin dependency from diagnosis (Garcia-Unzueta et al., 1998Go). These women were non-smokers, with no indication of maternal complications or incidence of drug administration. Those subjects with multiple pregnancies, fetal hydrops, previous pregnancy with pre-eclampsia or molar pregnancies were excluded from the study. These diabetic patients had micro-albuminuria but normal serum creatinine concentrations, and were without any kind of vascular complications, retinopathy, and renal insufficiency. Gestational age was estimated from the first day of the last menstrual period and confirmed by first-trimester and early second-trimester ultrasound measurement of crown–rump length, biparietal diameter and femur length. The study was approved by the local ethical committee of Kagawa Medical University, Japan, and standardized informed consent was obtained from each patient.

As described previously (Hata et al., 1992Go, 1997Go), maternal ophthalmic artery blood flow velocity waveforms were recorded with colour and pulsed Doppler ultrasonography (Aloka SSD-1700, Tokyo, Japan). The pulsatility index (PI), i.e. peak systolic velocity – end-diastolic velocity/time-averaged mean peak velocity, was averaged for each side. For statistical analysis, the mean PI was evaluated by averaging the values obtained from the right and left sides. All Doppler examinations were done by one examiner (T.H.). The intra-observer coefficient of variation for the measurement of PI was determined by performing five consecutive examinations on 10 patients within 30 min, and the result was 5.5% (Hata and Miyazaki, 1998Go). The maternal heart rate and mean arterial blood pressure were measured in each woman.

Statistical analysis
An unpaired t-test was used to compare gestational age at examination, maternal heart rate, mean blood pressure, and ophthalmic artery PI between normotensive pregnant women with type 1 diabetes and normal normotensive pregnant women. For comparison of maternal age and parity between the two groups, the Mann–Whitney test was used. P < 0.05 was considered to be significant.


    Results
 Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 References
 
There were no significant differences in maternal age (30.6 ± 4.2 versus 30.5 ± 3.4 years), parity (1.1 ± 0.9 versus 1.0 ± 0.9), gestational age at examination (29.8 ± 8.6 versus 30.9 ± 8.1 weeks), maternal heart rate (89 ± 5 versus 87 ± 6 beats/min), and mean blood pressure (86.8 ± 8.1 versus 82.5 ± 9.1 mmHg) respectively between normotensive pregnant women with type 1 diabetes and normal normotensive pregnant women. The PI (1.94 ± 0.45) in normotensive pregnant women with type 1 diabetes was significantly lower than that (2.73 ± 0.32) in normal normotensive pregnant women (P < 0.0001) (Figure 1Go).



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Figure 1. Maternal ophthalmic artery pulsatility index in normal pregnancies (n = 15; normal) and pregnancies with type 1 diabetes (n = 11; diabetes). Horizontal bars = mean values.

 

    Discussion
 Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 References
 
Generalized vasodilatation is observed from diagnosis in type 1 diabetes (Stehouwer et al., 1997Go). This vasodilatation is more evident in the afferent arteriole, and leads to capillary hypertension, thus contributing to the development of micro-angiopathy (Stehouwer and Schaper, 1996Go). In this study, the lower ophthalmic artery PI in pregnant women with type 1 diabetes should be interpreted as orbital vascular vasodilatation, indicating orbital hyperperfusion or hyperaemia. These results suggest that vascular resistance in the maternal orbital circulation is reduced in pregnancies with type 1 diabetes that are normotensive. The decrease in cerebral and renal vascular resistance and increase in perfusion have been noted in pre-eclampsia (Kuo et al., 1993Go; Zunker et al., 1995Go). We have also previously found that pre-eclampsia is associated with a significant decrease in ophthalmic artery vascular resistance (Hata et al., 1995Go, 1997Go). These findings suggest that there is a vasodilatation in pregnant women with type 1 diabetes, probably due to passive overdistension of arterioles of general organs and vasogenic oedema. Therefore, endothelial dysfunction may precede the occurrence of even early diabetic micro-angiopathy in type 1 diabetic pregnant women without complications. We believe that the lower PI in the ophthalmic artery may represent a compensation phase that exists before the development of clinically identifiable diabetic angiopathy in pregnant women with type 1 diabetes.


    Notes
 
1 To whom correspondence should be addressed Back


    References
 Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 References
 
Cunningham, F.G., MacDonald, P.C., Gant, N.F. et al. (1997) Williams Obstetrics. 20th edn. Appleton & Lange, Stamford, USA, pp. 1203–1221.

Garcia-Unzueta, M.T., Berrazueta, J.R., Montalban, C. et al. (1998) Plasma adrenomedullin levels in type 1 diabetes: relationship with clinical parameters. Diabetes Care, 21, 999–1003.[Abstract]

Hata, T. and Miyazaki, K. (1998) Maternal ophthalmic artery Doppler velocimetry in normotensive pregnancies with small-for-gestational-age infants. Ultrasound Obstet. Gynecol., 11, 328–331.[ISI][Medline]

Hata, T., Senoh, D., Hata, K. and Kitao, M. (1992) Ophthalmic artery velocimetry in pregnant women. Lancet, 340, 182–183.

Hata, T., Senoh, D., Hata, K. and Kitao, M. (1995) Ophthalmic artery velocimetry in preeclampsia. Gynecol. Obstet. Invest., 40, 32–35.[ISI][Medline]

Hata, T., Hata, K. and Moritake, K. (1997) Maternal ophthalmic artery Doppler velocimetry in normotensive pregnancies and pregnancies complicated by hypertensive disorders. Am. J. Obstet. Gynecol., 177, 174–178.[ISI][Medline]

Kuo, D.M., Chiu, T.H. and Hsieh, T.T. (1993) Maternal renal artery Doppler flow-velocity waveform in preeclampsia: a preliminary report. J. Reprod. Med., 38, 189–192.[ISI][Medline]

Stehouwer, C.D. and Schaper, N.C. (1996) The pathogenesis of vascular complications of diabetes mellitus: one voice or many? Eur. J. Clin. Invest., 26, 535–543.[ISI][Medline]

Stehouwer, C.D., Lambert, J., Donker, A.J. and van Hinsbergh, V.W. (1997) Endothelial dysfunction and pathogenesis of diabetic angiopathy. Cardiovasc. Res., 34, 55–68.[ISI][Medline]

Zunker, P., Ley-Pozo, J., Louwen, F. et al. (1995) Cerebral hemodynamics in pre-eclampsia/eclampsia syndrome. Ultrasound Obstet. Gynecol., 6, 411–415.[ISI][Medline]

Submitted on June 7, 1999; accepted on October 18, 1999.





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