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 Table of Contents  
ORIGINAL ARTICLE
Year : 2021  |  Volume : 33  |  Issue : 2  |  Page : 179-184

Evaluation of retinal changes in normal pregnancy and gestational hypertension – A spectral domain optical coherence tomography based study


1 Department of Ophthalmology, Jubilee Mission Medical College, Thrissur, Kerala, India
2 Department of Obstetrics and Gynaecology, Jubilee Mission Medical College, Thrissur, Kerala, India

Date of Submission07-Nov-2020
Date of Decision09-Jan-2021
Date of Acceptance13-Jan-2021
Date of Web Publication21-Aug-2021

Correspondence Address:
Dr. Niya Babu
Department of Ophthalmology, Jubilee Mission Medical College, Thrissur - 680 005, Kerala
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/kjo.kjo_179_20

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  Abstract 


Background and Objectives: Hypertensive disorders complicating pregnancy is a complication of pregnancy, which includes gestational hypertension, preeclampsia and eclampsia syndrome, preeclampsia superimposed on chronic hypertension, and chronic hypertension of any etiology. The pathogenesis of the first three and last two varies. The present study focuses on the first three categories of patients. Optical coherence tomography (OCT) is a noninvasive medical imaging modality used for in vivo visualization of retinal layers in human eyes. This study analyzed the retinal thickness changes in patients with gestational hypertension and compared it with normal pregnant study participants. Furthermore, the duration of gestational hypertension with changes in retina was compared. Materials and Methods: A comparative study was performed in 206 patients (103 normal pregnant and 103 gestational hypertensive patients). Macular thickness in nine segments and ganglion cell inner plexiform layer thickness (GC-IPL) in six sectors were assessed using cirrus high-definition OCT and compared between two groups. The study period was 18 months. Results: Among the 412 eyes in two groups, there was a statistically significant increase in macular thickness in six segments in the gestational hypertension group compared to the healthy pregnant group (P < 0.05). A statistically significant positive correlation was found between macular thickness and duration of hypertension in two segments and a negative correlation between the GC-IPL thickness in two sectors and duration of hypertension was observed (P < 0.001). Conclusion: Spectral-domain OCT can be used for detecting early retinal changes in gestational hypertension before any clinical signs appear.

Keywords: Ganglion cell inner plexiform layer, gestational hypertension, macular thickness, optical coherence tomography


How to cite this article:
Babu N, Kakkanatt AC, Menon B, Rajeev AM. Evaluation of retinal changes in normal pregnancy and gestational hypertension – A spectral domain optical coherence tomography based study. Kerala J Ophthalmol 2021;33:179-84

How to cite this URL:
Babu N, Kakkanatt AC, Menon B, Rajeev AM. Evaluation of retinal changes in normal pregnancy and gestational hypertension – A spectral domain optical coherence tomography based study. Kerala J Ophthalmol [serial online] 2021 [cited 2021 Nov 30];33:179-84. Available from: http://www.kjophthal.com/text.asp?2021/33/2/179/324221




  Introduction Top


Gestational hypertension is diagnosed when there is blood pressure >140/90 mmHg after 20 weeks of pregnancy in a previously normotensive woman.[1] The main clinical manifestations of gestational hypertension include rapid or sudden weight gain, high blood pressure, protein in the urine, swelling (hands, feet, and face).[2] Retinal vessels are the only body parts of which vascular changes can be directly observed in vivo, and fundus examination was the principal criterion to evaluate the development of the degree of gestational hypertension during the early years.[3]

Optical coherence tomography (OCT) has found wide application in ophthalmology in recent years. It is based on low coherence interferometry. With OCT, multiple thin slices of the retina can be obtained; laminar sheet structural images of morphologic changes of the retina including vitreomacular traction, diffuse thickening, intraretinal cystic changes, subretinal fluid can easily be detected.[4]

This study emphasizes on retinal thickness changes in patients with gestational hypertension and compares it with normal pregnant study participants and also compares the duration of hypertension with the OCT changes.


  Materials and Methods Top


This comparative study was conducted in the Department of Ophthalmology and Obstetrics and gynecology in a tertiary care center in Kerala from January 2019 to June 2020 and included 206 patients. Patients diagnosed with hypertension after 20 weeks of pregnancy from the Department of Obstetrics and Gynaecology were included in the study except for those patients where an OCT could not be taken, patients with other pregnancy complications that would affect the study outcome, patients on drugs that affect the retinal thickness, patients with preexisting retinal pathologies, intraocular pressure >21 mm Hg, patients with chronic hypertension and preeclampsia complicated by chronic hypertension, patients diagnosed with hypertension before 20 weeks of pregnancy and patients who had undergone previous intraocular or refractive surgeries. This was compared with normal age-matched healthy pregnant participants.

The patients were enrolled in the study after taking informed consent. Gestational hypertensives were considered as Group 1 while healthy pregnant participants as Group 2. A detailed history about any previous or existing ophthalmic diseases, surgeries, or co-existing medical or surgical conditions was taken. Ophthalmologic examination including visual acuity, slit-lamp examination, intraocular pressure (IOP) measurement and fundus evaluation was done and documented. OCT using cirrus high-definition OCT without pupillary dilatation and under the same intensity of dim room lighting was done and the following parameters evaluated:

  1. Macular thickness measured in fovea, superior inner, inferior inner, nasal inner, temporal inner, superior outer, inferior outer, nasal outer, and temporal outer fields
  2. Ganglion cell layer with inner plexiform layer thickness was measured in super nasal, infer nasal, superotemporal, inferotemporal, superior, and inferior sectors.


Values were compared with normal age-matched pregnant study participants.

Based on the mean and standard deviation of the foveal center observed in an earlier publication by “Atas et al.,”[5] with 95% confidence level and 80% power minimum, the sample size was found to be 103 in each group.

Numerical variables were expressed as either mean and standard deviation or median and IQR. Categorical variables were represented by frequency and percentage analysis. To compare retinal and ganglion cell inner plexiform layer thickness (GC-IPL) thickness between two groups Mann–Whitney U test was used. Karl Pearson's coefficient of correlation was used to find out the correlation macular and GC-IPL thickness with study variables. P value < 0.05 was considered statistically significant. Data obtained from 206 patients were coded and entered into Microsoft Excel sheet using SPSS version 25 (IBM, Armonk, NewYork, USA).


  Results Top


Age distribution

The mean age in the gestational hypertension group was 28.52 years whereas in the normal pregnant group it was 27.03 years with P = 0.068. Since P value is > 0.05 the age between the two groups are comparable. The age group of patients in both the group ranges from 18 to 45 years. The youngest patient in the study was 19 years old [Figure 1].
Figure 1: Comparison of age between gestational hypertension and normal pregnant study participants

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Retinal thickness analysis between gestational hypertension and healthy pregnant

Both macular and ganglion cell layer thickness was analyzed in 412 eyes

Macular thickness analysis

All the ETDRS segments showed an increase in macular thickness in the gestational hypertensive group compared to the healthy pregnant group.[Figure 2] A statistically significant increase in thickness was found in the foveal center, superior inner, inferior inner, inferior outer nasal outer, and temporal outer macula (P < 0.05) [Figure 3]a and [Figure 3]b.
Figure 2: Macular thickness analysis between gestational hypertension and healthy pregnant women

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Figure 3: (a) Optical coherence tomography macula of group 1 patient showing increase in thickness in foveal centre, nasal inner, nasal outer and inferior outer macula. (b) Optical coherence tomography macula of group 2 showing normal macular thickness

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Ganglion cell inner plexiform layer thickness

All the 6 sectors of GCIPL thickness showed thinning in the gestational hypertension group with the superotemporal sector showing maximum thinning in both groups. Maximum thickness was noted in the superonasal sector in the gestational hypertension group and in the inferior sector in the normal healthy pregnant group. Minimum GC-IPL thickness showed a significant thinning in the hypertensive group compared to the healthy pregnant group (P < 0.05) [Figure 4].
Figure 4: Ganglion cell inner plexiform layer thickness thickness analysis between GHTN and healthy pregnant women

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Intraocular pressure between two groups

IOP was analyzed in both groups, i.e., a total of 412 eyes. Both groups showed a normal IOP and the IOP among the healthy pregnant group was increased compared to the gestational hypertension group [Figure 5].
Figure 5: Analysis of intraocular pressure between GHTN and normal groups

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Correlation of macular and ganglion cell inner plexiform layer thickness thickness with the duration of gestational hypertension

A statistically significant positive correlation was found between the superior and temporal outer macular thickness and duration of hypertension (P < 0.001) [Table 1]. Also, a statistically significant negative correlation between the GC-IPL thickness in the superotemporal and inferonasal sector and duration of hypertension was observed (P < 0.001) [Table 2].
Table 1: Correlation of macular thickness with duration of hypertension

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Table 2: Correlation of ganglion cell inner plexiform layer thickness with duration of hypertension

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  Discussion Top


The study was a comparative study conducted in 412 eyes of 206 patients of which 103 were gestational hypertension patients and 103 were healthy pregnant women. All patients attending the Obstetrics and Gynaecology department at a tertiary care center in Kerala coming under the inclusion criteria were enrolled for the study.

Comparison of age

Patients were aged between 18and 45 years. The mean age in the gestational hypertension group was 28.52 years whereas in the normal pregnant group it was 27.03 years with P > 0.05 indicating the two groups were comparable. Statistical analysis showed that there was no significant correlation of age between the two groups. Eriksson et al.[6] conducted a study that proved that macular thickness decreases in all ETDRS segments with age. However, a study done by Xu et al.[7] proved that there was no significant change in foveal thickness with age, but the GCIPL thickness reduced with age. In this study, there was no correlation between age and macular thickness. The youngest study participant was 19 years old and the eldest 41 years.

Comparison of macular thickness

Among the 412 eyes divided between the two groups, there was an increase in macular thickness in 8 quadrants in the gestational hypertension group except in the superior outer macula which showed no change between the two groups. However statistically significant increase in macular thickness was observed in the foveal center, superior inner, inferior inner, inferior outer nasal outer, and temporal outer macula (P < 0.05) in the gestational hypertensive group.

The study conducted by Atas et al.,[5] showed that macular thickness decreased in the preeclampsia group when compared to the healthy pregnant group in all quadrants but statistically significant thinning was found only in the foveal center. This deferred from our study where it was observed that there is the increase in macular thickness in gestational hypertension when compared to healthy pregnant patients except in the superior outer macula which showed no change between the 2 groups. In a study by Demir et al.,[8] it was found that foveal and parafoveal retinal thickness were increased, particularly in the last trimester and this increase was attributed to the pregnancy-related fluid retention in the retinal tissue.

The thickness of the 9 ETDRS segments was analyzed and compared with studies conducted by Atas et al. and Demir et al. and Wu et al.[9] [Table 3].
Table 3: Comparison of macular thickness with other studies

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When macular thickness in gestational hypertension was compared between our study and other similar studies, it was found that the thickness was less in our study in all quadrants except the foveal center as compared to the study by Atas et al.[5] Whereas when compared with the study by Wu et al. thickness in all quadrants were decreased except the inferior outer macula.

Macular thickness in healthy pregnancy was compared with similar studies and it was found that retinal thickness was less on our study in all quadrants except foveal center compared to study by Atas et al. and it was less in all quadrants in our study compared to that by Demir et al.

Comparison of Ganglion cell-inner plexiform layer thickness

The GC-IPL thickness in each of the 6 sectors was compared between healthy pregnant and gestational hypertension groups and it was found that the GCIPL thickness was reduced in all sectors in patients in gestational hypertension compared to the healthy pregnant group. However, statistically significant reduction was not seen between the two groups even though the minimum GC-IPL thickness showed a statistically significant thinning in our study (P < 0.05).

A study conducted by Lee et al.[10] proved that patients with hypertension exhibited a significant reduction in GC-IPL thickness. Tok et al.[11] compared antenatal and postpartum OCT findings of ganglion cell density in preeclampsia patients and healthy pregnant women. No statistically significant difference was obtained between the groups in respect of retinal ganglion cell density.

The study by Gooding et al.[12] postulated that pregnancy itself has an up-regulated inflammatory response associated with it. In addition to this patients with hypertension in pregnancy will have an exaggerated inflammation which may lead to loss of endothelial integrity. This causes a decrease in colloid osmotic pressure and extravascular fluid retention. Retinal changes in preeclampsia may be due to a complex interaction between choroidal ischemia, due to vasoconstriction, and endothelial dysfunction with the leakage of proteins, subsequent edema, and formation of exudative retinal detachments. None of the patients showed fundus changes except one patient with eclampsia who had hypertensive retinopathy changes. Hence, it may be hypothesized that the retinal thickening may be the precursor for the hypertensive changes to occur clinically.

Intraocular pressure changes in pregnancy

Analysis of IOP recorded with Goldmann Applanation Tonometry revealed a mean IOP of 13.97 ± 2.59 in the gestational hypertension group and 14.13 ± 2.65 in the healthy pregnant group (P > 0.05). According to our study, the IOP had a small increase in the healthy pregnant group compared to hypertensive patients which were not statistically significant. Tolunay et al.[13] conducted a study on IOP changes in different trimesters of pregnancy which showed that mean IOP was 13.9 ± 1.6 mm Hg in both eyes in the third trimester. Also, a decline in the IOP was observed from 1st to 3rd trimesters in pregnancy. Midha et al. reported that mean IOP at the third trimester normotensive pregnant women (11.9 mmHg) was almost similar to that of patients of pregnancy-induced hypertension (12.1 mmHg), thereby suggesting that the factors responsible for lowering the lOP, are independent of blood pressure. No studies have compared the IOP between gestational hypertension and normal pregnancy.

IOP lowering in pregnancy is caused by placental hormones, estrogen, relaxin, and progesterone mediated vasodilatation. This results in decreased IOP with the progression of pregnancy.[14]

Correlation of macular and ganglion cell inner plexiform layer thickness thickness with the duration of gestational hypertension

A statistically significant positive correlation was found between the superior and temporal outer macular thickness and duration of hypertension (P < 0.001). However, the average macular thickness did not have any significant correlation with the duration of hypertension. There wasn't any similar study in the literature comparing the duration of hypertension and its association with OCT changes.

A statistically significant negative correlation between the GC-IPL thickness in the superotemporal and inferonasal sector and duration of hypertension was observed in our study indicating that with the increasing duration of hypertension there was a decrease in the GC-IPL thickness in the above-mentioned sectors (P < 0.001). Also, there was a decrease in average GC-IPL thickness with increasing duration even though it was not statistically significant. Tabaczi et al.[15] reported that the duration of hypertension had a weak negative correlation with GC-IPL thickness in the superotemporal, inferonasal, and inferotemporal GC-IPL in DM patients. Also, hypertension had a weak relationship with only the inferonasal sector in healthy patients.


  Conclusion Top


The study was conducted among 412 eyes of 206 patients and the results were compared between the group with gestational hypertension and the healthy pregnant group. The average age distribution in the gestational hypertensive group was 28.52 years whereas in the healthy pregnant group was 27.03 years. OCT macula showed a statistically significant increase in thickness in patients with gestational hypertension in the foveal center, superior inner, inferior inner, inferior outer nasal outer, and temporal outer macula compared to the healthy pregnant group. GC-IPL thickness was decreased in the gestational hypertension group compared to the healthy pregnant group but statistically significant thinning was not present. However, the minimum GC-IPL thickness showed statistically significant thinning in the hypertensive group. Significant positive correlation was present between the duration of hypertension and macular thickness in superior and temporal outer segments. Also, a significant negative correlation was present between GC-IPL thickness in superotemporal and inferonasal sectors and duration of gestational hypertension.

Hence, it can be concluded that spectral-domain OCT can be used as a screening tool to detect changes in the retina in gestational hypertension before the appearance of clinical signs. It can be used for detecting retinal changes in these patients before vision-threatening complications occur.

Acknowledgment

The authors would like to acknowledge the support from Jubilee Mission Medical College, Thrissur.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

1.
Angeli F, Angeli E, Verdecchia P. Novel electrocardiographic patterns for the prediction of hypertensive disorders of pregnancy-From pathophysiology to practical implications. Int J Mol Sci 2015;16:18454-73.  Back to cited text no. 1
    
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Witcher PM, Chez BF, Baird SM. Multisystem effects of hypertensive disorders of pregnancy: A comprehensive review. J Perinat Neonatal Nurs 2015;29:229-39.  Back to cited text no. 2
    
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Cunningham F Gary, Leveno KJ, Bloom SL, Dashe JS, Hoffman BL, Casey BM, et al. Williams Obstetrics. 25th ed. Mc Graw –Hill education, USA, 2018. p. 711.  Back to cited text no. 3
    
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Bhende M, Shetty S, Parthasarathy MK, Ramya S. Optical coherence tomography: A guide to interpretation of common macular diseases. Indian J Ophthalmol 2018;66:20-35.  Back to cited text no. 4
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5.
Ataş M, Açmaz G, Aksoy H, Demircan S, Ataş F, Gülhan A, et al. Evaluation of the macula, retinal nerve fiber layer and choroid in preeclampsia, healthy pregnant and healthy non-pregnant women using spectral-domain optical coherence tomography. Hypertens Pregnancy 2014;33:299-310.  Back to cited text no. 5
    
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Eriksson U, Alm A. Macular thickness decreases with age in normal eyes: A study on the macular thickness map protocol in the stratus OCT. Br J Ophthalmol 2009;93:1448-52.  Back to cited text no. 6
    
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Xu Q, Li Y, Cheng Y, Qu Y. Assessment of the effect of age on macular layer thickness in a healthy Chinese cohort using spectral-domain optical coherence tomography. BMC Ophthalmol 2018;18:169.  Back to cited text no. 7
    
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Demir M, Oba E, Can E, Odabasi M, Tiryaki S, Ozdal E, et al. Foveal and parafoveal retinal thickness in healthy pregnant women in their last trimester. Clin Ophthalmol 2011;5:1397-400.  Back to cited text no. 8
    
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Wu CY, Du WL, Zhang Y. EDI-OCT detecting retinal and choroidal thickness in patients with pregnancy induced hypertension. Int Eye Sci 2018;18:926-9.  Back to cited text no. 9
    
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Lee WH, Lee MW, Lim HB, Kim KM, Shin YI, Kim JY. Longitudinal changes in the thickness of the ganglion cell-inner plexiform layer in patients with hypertension: A 4-year prospective observational study. Acta Ophthalmol 2020;98:e479-86.  Back to cited text no. 10
    
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Tok A, Beyoğlu A. Antenatal and postpartum comparison of HD-OCT findings of macula, retinal nerve fiber layer, ganglion cell density between severe preeclampsia patients and healthy pregnant woman. Hypertens Pregnancy 2020;39:252-9.  Back to cited text no. 11
    
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Gooding C, Hall DR, Kidd M, Ziskind A. Macular thickness measured by optical coherence tomography correlates with proteinuria in pre-eclampsia. Pregnancy Hypertens 2012;2:387-92.  Back to cited text no. 12
    
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Tolunay HE, Özcan SC, Şükür YE, Özarslan Özcan D, Adıbelli FM, Hilali NG. Changes of intraocular pressure in different trimesters of pregnancy among Syrian refugees in Turkey: A cross-sectional study. Turk J Obstet Gynecol 2016;13:67-70.  Back to cited text no. 13
    
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Tabakcı BN, Demirok G, Topalak Y, Şengün A. The relationship between retinal ganglion cell damage with duration of diabetes and diabetic retinopathy status. Int J Ophthalmol Clin Res 2017;4:076.  Back to cited text no. 15
    


    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5]
 
 
    Tables

  [Table 1], [Table 2], [Table 3]



 

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