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 Table of Contents  
ORIGINAL ARTICLES
Year : 2021  |  Volume : 8  |  Issue : 4  |  Page : 403-409

Ocular manifestation of pregnancy-induced hypertension


1 Department of Ophthalmology, Dr. N.D. Desai Faculty of Medical Sciences and Research Centre, Dr. Dharmsinh Desai University, Nadiad, Gujarat, India
2 Department of Ophthalmology, Chief of VitreoRetina, Minto Ophthalmic Hospital – Regional Institute of Ophthalmology, Bengaluru, Karnataka, India

Date of Submission28-Jul-2021
Date of Acceptance24-Nov-2021
Date of Web Publication22-Dec-2021

Correspondence Address:
Dr. Snehal Himmatlal Shah
Department of Ophthalmology, Dr. N.D. Desai Faculty of Medical Sciences and Research Centre, Dr. Dharmsinh Desai University, Nadiad 387001, Gujarat.
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/mgmj.mgmj_56_21

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  Abstract 

Background and Objectives: Pregnancy-induced hypertension (PIH) is a challenging obstetric condition that can result in grave complications. The retina is a unique site where the vasculature in the human body is visualized directly with the help of an ophthalmoscope. Progression of retinal changes generally correlates with the progression of PIH. The purpose of this study was to determine the prevalence and association of retinal changes with the progression of PIH. Materials and Methods: This is a hospital-based, prospective, observational study. A total of 100 admitted cases diagnosed with PIH was included in the study. Ocular and systemic history, age, blood pressure, and proteinuria were noted. A dilated indirect ophthalmic examination was done at the bedside of the patient. Results: A total of 100 patients with PIH were examined. The mean age of the patients was 24.8 years; the mean gestational age was 36.5 weeks. Out of the total 100 patients with PIH who were examined, retinal changes were noted in 43 patients. The prevalence of retinopathy changes was more pronounced among patients with severe preeclampsia (76.5%) and eclampsia (88.9%). As the severity of the PIH increased, the odds of women developing retinopathy also increased substantially and this association between the severity of PIH and the development of retinopathy changes was found to be statistically significant. A significant correlation was also seen between albuminuria and the severity of retinopathy. Conclusion: Cases of severe preeclampsia and eclampsia showed higher grades of retinal changes. Thus fundus examination plays an important role in assessing the severity of PIH.

Keywords: Retinal changes, pregnancy-induced hypertension, fundoscopy


How to cite this article:
Devaru S, Nagaraj KB, Shah SH. Ocular manifestation of pregnancy-induced hypertension. MGM J Med Sci 2021;8:403-9

How to cite this URL:
Devaru S, Nagaraj KB, Shah SH. Ocular manifestation of pregnancy-induced hypertension. MGM J Med Sci [serial online] 2021 [cited 2022 Jan 18];8:403-9. Available from: http://www.mgmjms.com/text.asp?2021/8/4/403/333321




  Introduction Top


Pregnancy causes tremendous systemic and ocular changes among women: Such changes are observed in the physiological, cardiovascular, hormonal, metabolic, and immunologic systems. Hormonal changes are among the most prominent systemic changes in pregnant women. High hormone activity during pregnancy is induced due to the combination of the placenta, maternal endocrine gland, and fetal adrenal glands. With the aid of some of these mechanisms, pregnancy causes ocular changes, which may be physiological or pathological or may be modifications of preexisting conditions.[1]

This article has been presented out of a thesis submitted at Rajiv Gandhi University of Health Sciences, Bengaluru, Karnataka, India by Dr. Sheetal Devaru, one of the authors for the award of MS (Ophthalmology). It is certified that the thesis has not been published in any format anywhere to date nor it will be published in the future. Permission has been obtained from the university for the publication of the manuscript prepared out of the thesis in the proposed journal.

PIH is a clinical syndrome that afflicts 3%–5% of all pregnancies and is a leading cause of maternal mortality, especially in developing countries.[1],[2] It is a multisystem hypertensive disorder, with the clinical spectrum including preeclampsia; eclampsia; hemolysis, elevated liver enzymes, and low platelet (HELLP) syndrome; and HELLP syndrome with eclampsia.

Hypertension occurs in approximately 10% of first pregnancies and 8% of all pregnancies.[3] The incidence of eclampsia in the developed countries is about 1 in 2000 deliveries as compared with developing countries, where it varies from 1 in 100 to 1 in 1700. The average incidence of PIH in India is 15.2% and it is fourfold higher among primipara than multipara women.[4]

Visual disturbances may occur in 40% of patients with preeclampsia–eclampsia syndrome, and, on rare occasions, maybe the initial symptom. The visual system may be affected in 30% to 100% of patients with preeclampsia–eclampsia.[5],[6]

Retinal vascular changes occur in 40% to 100% of cases and are the most common abnormality seen in preeclampsia–eclampsia syndrome.[7],[8] No significant retinal changes occur in most normal pregnancies. However, pregnancy can be associated with the development of new ocular conditions such as serous retinal detachment related to preeclampsia, or with an exacerbation of preexisting disease processes such as diabetic retinopathy. These ocular changes are usually transient but occasionally cause permanent visual disability.

With this background present, the study was undertaken to study the retinal manifestation in PIH and the importance of fundus examination, progress, and management in patients with PIH. The study also assesses the association of retinal changes with blood pressure, proteinuria, and the severity of PIH.


  Materials and methods Top


This was an observational study carried out during 2015–2017 at Minto ophthalmic hospital, a regional institute of ophthalmology, and Vani Vilas Hospital attached to Bangalore Medical College and Research Institute. Data were collected from patients fulfilling the inclusion criteria admitted at Vani Vilas Hospital, diagnosed with PIH. Prior approval for the study protocol was obtained from the institutional ethical committee of Bangalore Medical College and Research Institute Ref No. BOME/IEC/32. After explaining the need for relevant investigations, and their role in further management, patients were included in the study. Informed written consent was obtained from the patient or a responsible attendant before including the patient in the study.

The study was carried out in 100 patients admitted in the obstetric ward who were diagnosed with PIH, except those under exclusion criteria. Age, race, gravida, gestational period, blood pressure, and proteinuria were noted. The fundus examination was done irrespective of visual complaints after dilating the pupils with eye drops, 1% tropicamide topical agent, with an indirect ophthalmoscope in the ward, at the patient’s bedside. The patients were followed up two days after the termination of pregnancy, and dilated fundoscopy was done in the same fashion. Informed consent was taken from the patient. Data were obtained by using a predesigned, pretested questionnaire. Fundoscopy (indirect) fundus photography (wherever possible) was carried out among patients.

Inclusion criteria were: Pregnant women fulfilling the criteria of PIH and willing to participate. Exclusion criteria were: patients with preexisting diabetes, hypertension, or renal disease, preexisting retinal pathologies, and with hazy media unfavorable for fundus examination.

Proportions were compared by using the Chi-square test of significance; the Student’s t test was used to determine the statistical difference between the groups in terms of the parameters measured. The association between MPV and the severe clinical variable was evaluated through Pearson’s correlation; multiple linear regression analysis was performed to assess independent relationships. In all the tests cited earlier, the “p” value of less than 0.05 was accepted as indicating statistical significance. Data were analyzed by using SPSS package version 10.


  Results Top


The mean age in our study group was 24.8 years; the majority of the subjects were in the age group of 20–25 years (53%). The mean age of the patients with significant fundus changes and normal fundus was 24.16 years and 24.78 years, respectively. Gestational age was divided into four groups: The highest number of patients were from the group of >36 weeks (60%), and only 2% were from the group of 24–28 weeks, with a mean gestational age of 36.5 weeks. Most of the subjects in our study population were primigravida (54%), whereas 46% were multigravida [Figure 1].
Figure 1: Distribution of stages of retinal changes among study population

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In our study, most of the subjects had mild and severe preeclampsia (37% and 34%, respectively). The least was gestational hypertension (11%). Out of the 100 patients with PIH, the prevalence of retinal changes (hypertensive retinopathy changes) was noted in 43 patients (43%). Among them, 15 had grade I hypertensive retinopathy followed by 11 individuals who had grade IV retinopathy, and then grade II and III. Grade I was the most common type of change seen overall [Figure 2].
Figure 2: Distribution of type of PIH according to stage of retinal changes

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The majority of patients were of the mild PIH group (n = 37), followed by severe PIH (n = 34), eclampsia (n = 18), and gestational hypertension (n = 11). The prevalence of retinopathy changes was more among patients with severe PIH (76.5%) and eclampsia (88.9%). The increase in severity of the PIH odds of developing retinopathy also increased substantially from OR: 117; 95% CI: 13.8–993.65 in severe PIH to OR: 288; 95% CI: 24.32–3410.56 in eclampsia, an association was found between the severity of PIH and the development of retinopathy, and changes were found to be statistically significant (P = <0.001) [Table 1].
Table 1: Prevalence of retinal changes based on PIH type

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A significant increase in the mean systolic and diastolic blood pressure was seen with an increase in the severity of retinopathy among the study groups [grade I164/110.4 (SBP/DBP) and grade IV 175.45/115 (SBP/DBP)]. A significant increase in urine albumin was seen with an increase in the severity of retinopathy [Table 2]. The photographs of the fundus observations showed various stages of changes [Figure 3].
Table 2: Association of systolic and diastolic blood pressure with grades of retinopathy

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Figure 3: Fundus photographs. Color plate 1: BE macular serous retinal detachment with Elschnig’s spots. Color plate 2: BE Grade III hypertensive retinopathy. Color plate 3: Exudative retinal detachment. Color plate 4: BE central retinal artery occlusion

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Among the 43 cases with significant findings, labor was induced in 30 cases (69.8%), emergency LSCS was done in 11 cases (25.6%), spontaneous labor occurred in two cases (4.7%) and elective LSCS was done in none. This shows that immediate termination of pregnancy was opted for in a total of 95.4% of subjects, with significant fundus changes. Among the 57 cases with no significant changes, labor was induced in 24 cases (42.1%), emergency LSCS was done in 10 cases (17.5%), spontaneous labor was allowed in 21 cases (36.8%), and elective LSCS was done in two cases (3.5%).

Grade I retinal changes were the most common among all the groups of PIH. All grades of retinal changes were observed in patients with severe PIH and eclampsia. This difference in the distribution of retinal changes among women with different stages of PIH was found to be statistically significant. All grades of retinopathy changes were observed more among women in the younger age group between 20 and 25 years compared with other age groups. Primigravida presented with all grades of retinopathy as compared with multigravida. A statistically significant association was seen between albuminuria and the severity of retinopathy.


  Discussion Top


PIH is a multiorgan hypertensive disorder that is one of the leading causes of maternal mortality, particularly in developing countries. Increasing awareness of its complications among both the medical fraternity and the general population has helped in reducing both morbidity and mortality. The ocular system is one of the main organs to be affected, and the severity of the retinal changes increases with the severity of PIH. A detailed indirect ophthalmic examination of the retina will give us an insight into the ischemic changes elsewhere in the body, especially the placenta, as retinal vasculature changes reflect the vascular changes of the brain, placenta, and other organs. Thus, this study was undertaken to prove the correlation between blood pressure and retinal changes and its importance in decision making to reduce both maternal and fetal mortality.

In a similar hospital-based, prospective study conducted by Bhandari et al.,[9] the mean age in patients with fundus changes was 23.85 years. In another study conducted by Karki et al.,[10] it was found that the mean age group of patients with retinal changes was 23.86 ± 5.51 years and without retinal changes it was 24.36 ± 5.65 years. A prospective study conducted among 20 cases of preeclampsia and eclampsia showed 70% retinal changes among different age groups.[11] In their study, 60% of cases were aged <25 years. The mean age group of patients in this study matches with the studies by Bhandari et al.,[9] Karki et al.,[10] and Shukla and Prasad.[11]

The literature has described that the ocular system may be affected in 30% to 100% of patients. By far, the most common abnormality seen in the fundus is attenuation of retinal arterioles.[12],[13] It is derived that arteriolar attenuation is the major retinal change seen in PIH. The percentage of occurrence of arteriolar attenuation in this study is in synchrony with the other studies.

The various other changes that have been observed in PIH in the literature are retinal hemorrhages, exudates, cotton wool spots, papillophlebitis, Elschnig’s spots, macular edema, RPE lesions, localized serous retinal detachment, bilateral exudative retinal detachment, retinal artery, and vein occlusion, optic neuritis, optic atrophy and isolated cases of acute ischemic optic neuropathy, and transient cortical blindness.[14] In our present study, various findings were observed in most patients with significant changes. In the study by Bhandari et al.,[9] hemorrhages were seen in 8% of severe preeclampsia and 11% of eclampsia; and cotton wool spots were seen in 6% of severe preeclampsia and 11% of eclampsia. When compared, there was a slight discrepancy with this study, showing a higher prevalence.

In the study conducted by Bhandari et al.,[9] macular edema was seen in 12% cases and retinal detachment was seen in 7%. In comparison to this study, the prevalence of retinal detachment is lesser in our study. However, in various other studies, Varija et al.,[4] Reddy et al.,[15] and Bhupally et al.,[14] the prevalence of retinal detachment is less than 1%.

A rare presentation has to be noted here, wherein a case with eclampsia presented with bilateral central retinal arterial obstruction (CRAO). None of the other similar studies have had such a presentation. However, there have been a few case reports with CRAO in one or both eyes in patients with preeclampsia/eclampsia.[2],[16]

In the study conducted by Bhandari et al.,[9] grades I, II, III, and IV(including complications) were seen in 65.9%,11.3%, 6.8%, and 15.9%, respectively. In the study conducted by Bhupally et al.,[14] in patients with significant changes, grades I, II, III, and IV were 45.2%, 45.2%, 0, and 9.52%, respectively. The study conducted by Varija et al. showed 42.8% cases to be having significant changes, of whom grades I, II, III, and IV were 75.2%,9.9%,4.97%, and 9.9%, respectively. Though there is a discrepancy in the prevalence of changes when various studies are compared, the most common change is a grade I in all the studies [Table 3].
Table 3: Distribution of the grades of retinal changes in various studies

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Our study revealed a statistically significant association (P < 0.001) between severity of PIH and development of retinopathy changes. An increase in blood pressure and proteinuria indicates an increase in the severity of PIH. A statistically significant association was found between the increase in blood pressure and proteinuria with the occurrence of retinal changes.

A significant increase in the mean systolic and diastolic blood pressure was seen with the increase in severity of retinopathy among the study subjects. The mean blood pressure noted in cases with grade III hypertensive retinopathy was 164/110.4 (SBP/DBP), and the mean blood pressure noted in cases with grade IV hypertensive retinopathy was 175.45/115 (SBP/DBP).

A significant increase in urine albumin was noted with an increase in the severity of PIH. Thus, an association between proteinuria and the severity of PIH is statistically significant (P = <0.001). We also observed and compared the mode of termination of pregnancy in cases with retinal changes and cases without retinal changes. The decision of induction or LSCS was taken for various obstetric indications and uncontrolled hypertension and worsening PIH signs. This shows that immediate termination of pregnancy was opted for in a total of 95.4% of subjects with significant fundus changes. In subjects without significant fundus changes, it was observed that immediate termination of pregnancy was opted for in only 59.6% of the patients, and the rest had spontaneous labor elective LSCS.

Vasospastic manifestations are reversible, and the retinal vessels rapidly return to normal after delivery. When the literature is reviewed, most patients with hypertensive retinopathy with visual symptoms regain lost vision. Spastic changes revert to normal. Most features, including exudative RD, resolve postpartum within a few weeks and most patients regain near-normal vision. However, However, it is observed that patients with serous retinal detachment with macular involvement showed resolving subretinal fluid with scarring of the macula. Certain patients with papilledema may end up in opticatrophy.[2],[16]

The follow-up on all the cases on day 2 post-termination of pregnancy revealed that the subjects with grades I, II, and III fundus changes did not show any improvement. However, the subjects with macular SRF and exudative RD had a resolving picture with improved visual acuity after post-termination of pregnancy. The subjects with a normal fundus remained normal.


  Conclusion Top


This study demonstrated that there is a greater chance of developing retinopathy with the increase in blood pressure, proteinuria, and the severity of PIH in cases of PIH. Retinal changes were observed more in the primigravida PIH patients compared with multigravida patients. Cases of severe preeclampsia and eclampsia showed higher grades of retinal changes. Thus, fundus examination is of paramount importance in patients with PIH and it can also be considered as an indirect marker for the severity of PIH and its prognosis.

Ethical policy and institutional review board statement

The study protocol was obtained from the Institutional Ethics Committee, Bangalore Medical College and Research Institute: An Autonomous Institute of Government of Karnataka, India vide their letter no. BOME/PGs/159/2015–16 dated November 17, 2017.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

1.
Garg P, Aggarwal P. Ocular changes in pregnancy. Nepal J Ophthalmol 2012;4:150-61.  Back to cited text no. 1
    
2.
Ober RR. Pregnancy-induced hypertension (pre-eclampsia eclampsia). In: Ryan-Retina SJ, editor. Retina Specialists; How We Think. vol. 2, Chapter 73, 4th ed. St. Louis, MO: CV Mosby; 2006. p. 1367-76.  Back to cited text no. 2
    
3.
Kaplan NM, Victor RG, Flynn JT. Kaplan’s Clinical Hypertension. 11th ed. Philadelphia, PA: Wolters Kluwer; 2015.  Back to cited text no. 3
    
4.
Varija T, Vanaja D, Sindhura , Raghavenda B. A study of prevalence and association of fundus changes in pregnancy-induced hypertension. Int J Reprod Contracept Obstet Gynecol 2016;5: 1375-9.  Back to cited text no. 4
    
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Dieckman WJ. The Toxemias of Pregnancy. 2nd ed. St. Louis, MO: CV Mosby; 1952. p. 240-9.  Back to cited text no. 5
    
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Wagener HP. Arterioles of the retina in toxemia of pregnancy. JAMA 1933;101:1380-4.  Back to cited text no. 7
    
8.
Thadhani R, Ecker JL, Kettyle E, Sandler L, Frigoletto FD. Pulse pressure and risk of preeclampsia: A prospective Study. Obstet Gynecol 2001;97:515-20.  Back to cited text no. 8
    
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Bhandari AJ, Bangal SV, Gogri PY. Ocular fundus changes in pre-eclampsia and eclampsia in a rural set-up. J Clin Ophthalmol Res 2015;3: 139-42.  Back to cited text no. 9
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10.
Karki P, Malla P, Das H, Uprety DK. Association between pregnancy-induced hypertensive fundus changes and fetal outcomes. Nepal J Ophthalmol 2010;2:26-30.  Back to cited text no. 10
    
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Shukla BK, Prasad GN. Retinal changes in eclampsia and preeclampsia. J Indian Med Assoc 1976;66:8-10.  Back to cited text no. 11
    
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So K-Y, Oh S-Y, Yang S-Y. Permanent bilateral vision loss in eclamptic posterior reversible encephalopathy syndrome. Neuroophthalmology 2015;39:243-7.  Back to cited text no. 12
    
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Bembalgi S, Kamate V, Shruthi KR. A study of eclampsia cases associated with posterior reversible encephalopathy syndrome. J Clin Diagn Res 2015;9:QC05-7.  Back to cited text no. 13
    
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Bhupally AK, Sulekha S, Rama Devi E, Swathi M, Rohini M, Shruthi T. Prevalence of hypertensive retinopathy changes in pregnancy-induced hypertension. Int J Intg Med Sci 2015;2:182-5.  Back to cited text no. 14
    
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Reddy SC, Sivalingam N, Sheila Rani KG, Tham SW. Fundus changes in pregnancy-induced hypertension. Int J Ophthal 2012;5:694-7.  Back to cited text no. 15
    
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Gass JDM, Pautler SE. Toxemia of pregnancy: Pigment epitheliopathy masquerading as a heredomacular dystrophy. Trans Am Ophthalmol Soc 1985;83:114-30.  Back to cited text no. 16
    


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    Tables

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