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Table of Contents
ORIGINAL ARTICLE
Year : 2023  |  Volume : 22  |  Issue : 1  |  Page : 5-10  

Changes in opthalmic artery doppler velocimetry in women with preeclampsia in Kano, Nigeria


1 Department of Radiology, Muhammad Abdullahi Wase Teaching Hospital, Kano, Nigeria
2 Department of Radiology, Faculty of Clinical Sciences, Aminu Kano Teaching Hospital, Bayero University, Kano, Nigeria

Date of Submission27-Jan-2021
Date of Decision23-Aug-2022
Date of Acceptance14-Nov-2022
Date of Web Publication24-Jan-2023

Correspondence Address:
Mansur Yahuza Adamu
Department of Radiology, Aminu Kano Teaching Hospital, Bayero University, Kano
Nigeria
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/aam.aam_26_21

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   Abstract 


Background: Hypertensive disorders in pregnancy are among the most serious complications of pregnancy and represent important contributors to maternal and neonatal morbidity and mortality worldwide. Preeclampsia (PE)–eclampsia syndrome is the most important hypertensive gestational condition. Maternal ophthalmic artery Doppler velocimetry enables the identification of pregnant women with increased cerebral blood flow who are at risk of developing severe PE and eclampsia. Hence the need to determine the changes in ophthalmic artery Doppler velocimetric indices in PE in Kano,Nigeria becomes paramount. Materials and Methods: Ninety-six patients with the clinical diagnosis of PE and 96 normotensive pregnant controls between 20 and 40 weeks' gestational age were recruited for this study. Ophthalmic artery Doppler velocimetric indices of the two groups were measured and documented. Results: The mean velocimetric measurements in the control group were as follows: peak systolic velocity (PSV) = 38.04 ± 13.68 cm/s, End-diastolic volume (EDV) =9.14 ± 3.65 cm/s, resistivity index (RI) = 0.75 ± 0.091, pulsatility index (PI) =1.62 ± 0.55, peak mesodiastolic velocity (PMDV) = 21.02 ± 8.83 cm/s, peak ratio (PR) = 0.56 ± 0.14. The mean velocimetric indices in the PE group were PSV = 44.59 ± 11.54 cm/s, EDV = 12.23 ± 2.66 cm/s, RI = 0.71 ± 0.069, PI = 1.67 ± 0.42, PMDV = 32.27 ± 9.12 and PR = 0.72 ± 0.10. Conclusion: There is a significant difference in the ophthalmic artery Doppler velocimetric indices between women with PE and normal pregnant women. Ophthalmic artery Doppler ultrasound is a useful tool in monitoring the hemodynamic changes in cerebral circulation in PE.

   Abstract in French 

Résumé
Contexte: Les troubles hypertensifs de la grossesse font partie des complications les plus graves de la grossesse et représentent des contributeurs importants à la morbidité et à la mortalité maternelles et néonatales dans le monde. Le syndrome de pré-éclampsie-éclampsie est la condition gestationnelle hypertensive la plus importante. La vélocimétrie Doppler de l'artère ophtalmique maternelle permet d'identifier les femmes enceintes présentant un débit sanguin cérébral accru qui risquent de développer une pré-éclampsie et une éclampsie sévères. D'où la nécessité de déterminer par échographie les changements des indices vélocimétriques Doppler de l'artère ophtalmique dans la pré-éclampsie à Kano, au Nigeria. Méthodes: Quatre-vingt-seize patientes présentant un diagnostic clinique de prééclampsie et quatre-vingt-seize témoins enceintes normotendues entre 20 et 40 semaines d'âge gestationnel ont été recrutées pour cette étude. Les indices vélocimétriques Doppler de l'artère ophtalmique des deux groupes ont été mesurés et documentés. Résultats: Les mesures vélocimétriques moyennes dans le groupe témoin étaient les suivantes ; PSV (Vitesse systolique maximale) = 38,04 ± 13,68 cm / s, EDV (volume diastolique final) = 9,14 ± 3,65 cm / s, RI (indice de résistivité) = 0,75 ± 0,091, PI (indice de pulsatilité) = 1,62 ± 0,55, PMDV ( Vitesse méso diastolique maximale) = 21,02 ± 8,83 cm / s, PR (rapport maximal) = 0,56 ± 0,14. Les indices vélocimétriques moyens dans le groupe PE (PE) étaient ; PSV = 44,59 ± 11,54 cm/s, EDV = 12,23 ± 2,66 cm/s, RI = 0,71 ± 0,069, PI = 1,67 ± 0,42, PMDV = 32,27 ± 9,12 et PR = 0,72 ± 0,10. Conclusion: Il existe une différence significative dans les indices vélocimétriques Doppler de l'artère ophtalmique entre les femmes atteintes d'EP et les femmes enceintes normales. L'échographie Doppler artérielle ophtalmique est un outil utile pour surveiller les modifications hémodynamiques de la circulation cérébrale dans la prééclampsie.
Mots clés : Doppler, Hypertension, Artère ophtalmique, Prééclampsie

Keywords: Doppler, hypertension, ophthalmic artery, preeclampsia, velocimetry


How to cite this article:
Hikima MS, Adamu MY, Lawal Y, Isyaku K, Isma段l A. Changes in opthalmic artery doppler velocimetry in women with preeclampsia in Kano, Nigeria. Ann Afr Med 2023;22:5-10

How to cite this URL:
Hikima MS, Adamu MY, Lawal Y, Isyaku K, Isma段l A. Changes in opthalmic artery doppler velocimetry in women with preeclampsia in Kano, Nigeria. Ann Afr Med [serial online] 2023 [cited 2023 Jan 28];22:5-10. Available from: https://www.annalsafrmed.org/text.asp?2023/22/1/5/368413




   Introduction Top


Maternal mortality remains a burden globally, with about 810 women said to be dying every day around the world from pregnancy or childbirth-related complications.[1] About 94% of these deaths occur in low and lower-middle-income countries.[1] Hypertension is the most common disorder that complicates pregnancy worldwide.[2] The most important hypertensive condition in pregnancy is preeclampsia (PE)–eclampsia syndrome. PE occurs when blood pressure (BP) is elevated and accompanied by proteinuria (≥0.3 g of protein in a 24-h specimen or ≥1+ reading on a dipstick in a random urine sample with no evidence of urinary tract infection) after 20 weeks of pregnancy and resolves after delivery.[3],[4]

The etiology of PE is still unknown; however, abnormal placentation resulting in placental ischemia is widely considered to be the initiating event in the development of PE. This disorder represents a major cause of maternal deaths worldwide, having the highest case-fatality ratio than any of the common pregnancy-related conditions.[4],[5],[6] Several factors have been described to play a role in the pathogenesis, which include genetic, immunologic, and environmental.[7]

Severe PE is defined as the onset of PE with heavy proteinuria (3–5 g/d) or with one or more of the following adverse conditions: maternal symptoms including persistent or new/unusual headache, visual disturbance, persistent abdominal pain, severe nausea or vomiting, chest pain, or dyspnoea; maternal signs of end-organ dysfunction, including eclampsia, severe hypertension (BP ≥160/110 mm), pulmonary edema, or suspected placental abruption; abnormal maternal serum liver enzymes levels with symptoms.[8]

PE involves endothelial dysfunction along with generalized arterial constriction and decreased intravascular volume, including the ocular areas.[7],[9],[10]

The ocular circulation is an indirect reflector of the status of the hemodynamics of cerebral circulation due to its embryological, anatomical, and functional similarities of cerebral circulation. Doppler studies of the ocular vessels have been widely utilized to evaluate, treat, and manage diseases that affect cerebral vasculature, including PE.[11]

A lot of peripheral vessels, with mainly the uterine artery Doppler indices, have been investigated as potential markers of the development of PE, with ophthalmic artery Doppler gaining more acceptability and utility.[12] The advantages of ophthalmic artery Doppler are that it is easy to measure with standard ultrasound equipment, it is unaffected by adiposity, and its indices have constant reference ranges throughout pregnancy trimesters.[13] These factors make the ophthalmic artery Doppler a good candidate for use in the screening and surveillance of patients with PE in a low-resource setting with limited technical equipment and poor adherence to antenatal follow-up.


   Materials and Methods Top


This was a cross-sectional, hospital-based prospective study that recruited 192 randomly selected preeclamptic (PE) women and 96 normotensive pregnant women as controls, between 20 and 40 weeks gestational age (GA) at Aminu Kano Teaching Hospital (AKTH) and Murtala Muhammed Specialist Hospital (MMSH), Kano, North Western Nigeria, from October 2014 to September 2015. Informed consent was obtained from the participants. Approval and permission to conduct this study were sought and obtained from the ethics and research committee of AKTH and MMSH Hospital board, Kano in accordance with the Helsinki declaration.

The study participants were subgrouped based on PE status into 2: subgroup 1 (mild-to-moderate PE and subgroup 2 (severe PE). Furthermore, according to the parity of the participants, they were categorized into three groups: group 1; nulliparous, Group 2; para 1–4, Group 3; para 5 and above (grand multiparous), as shown in [Table 1] and [Figure 1]. The normal were consenting pregnant women who came to the departments for a routine obstetric ultrasound scan.
Table 1: The mean values and standard deviation of the velocimetric indices in the control and study subgroups

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Figure 1: Histogram showing the age distribution of the control and study subgroups

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All participants with the clinical diagnosis of PE at 20–40weeeks GA were included in the study. Whereas pregnant women <20 weeks and >40 weeks of gestation, nonconsenting individuals, smokers, and those with orbital pathologies and the presence of maternal diseases before pregnancy, such as chronic hypertension, diabetes, and multiple pregnancy were excluded for both groups. For the control group, all normal pregnant women between 20 and 40 weeks of normal gestation were included.

After documenting the age, parity, clinical history, and GA of the participants, BP of the participants was measured using aneroid sphygmomanometer. Urinalyses were done using Mission expert urinalysis strips, and urine protein levels were measured and documented. DC-6 mindray (Biomed electronics, Shenzhen, China, 2007) machine was used in AKTH, while a Toshiba UIDM-580A (Toshiba, Japan, 2008) was used in MMSH.

Transabdominal obstetric ultrasound scan was then done to determine the GA of the pregnancy in the participants using a 3.5MHz transducer to measure a combination of two or more of the following parameters: biparietal diameter, femur length, head circumference, and abdominal circumference.[14],[15]

For the ophthalmic artery Doppler, participants were examined using a 7.5MHz linear transducer in the supine position with the head tilted approximately 15° away from the examination side after a rest period of about 10 min. A small amount of gel was applied to the closed eyelid with the transducer positioned horizontally without applying pressure to the eye to avoid alteration of the flow velocity measurements. Color Doppler was applied, and the transducer toggled up and down until the ophthalmic artery is identified approximately 15 mm from the optic disc, on the medial aspect of the optic nerve.[13],[16],[17] The angle of insonation between the ultrasound beam and the vessel was adjusted to <20° while the size of the sample volume was adjusted to 2 mm.[13],[16] Spectral waveform was thereafter obtained by activating pulsed wave and obtaining five spectral waveforms of similar shape and size. The peak systolic velocity (PSV), end-diastolic volume (EDV), resistivity index (ri), and pulsatility index (PI) were then obtained by using auto-tracing to obtain an average measurement from the spectra obtained. Only the right eye was examined, as previous studies have shown no statistically significant difference between blood flows in each eye.[13],[16],[18] The spectral waveforms of control and PE groups are represented in [Figure 1] and [Figure 2], respectively.
Figure 2: Histogram showing the parity distribution of the groups

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Data collected were analyzed using the Statistical Package for the Social Sciences (SPSS) software, version 17.0 (SPSS Inc. IBM, Armonk, NY). The statistical association between categorical variables was assessed using the Chi-square test, while the difference in mean between qualitative variables was assessed using the Student's t-test. All tests were conducted using a 5% alpha level of significance. The results obtained were presented in tables, graphs, and charts.


   Results Top


A total of 192 participants comprising 96 normotensive pregnant and 96 patients with the clinical diagnosis of PE, were examined. The study participants were subgrouped based on PE status into 2: subgroup 1 (mild-to-moderate PE) and subgroup 2 (severe PE), as shown in [Table 2].
Table 2: The clinico-demographic characteristics of the subjects

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The mean and standard deviation of the ages were 27.29 ± 5.97 years in the control and 25.81 in the study group. The difference in age between the control and study groups showed no statistical significance (P = 0.61). The mean and standard deviation of the study subgroups were 29.1 ± 5.86 years and 24.3 ± 6.7 years for the study subgroups 1 and 2, respectively. Majority of the participants (53.6%) belonged to the age range of 20–29 years [Figure 1].

The parity of the participants ranged from 0 to 11, with a mean of 2.89 in the control group, 3.13 in the mild-moderate PE subgroup and 2.79 in the severe PE subgroup.

Majority of the participants (40.6%) belonged to Group 2 parity group, 30.2% were grand multiparous, while 29.2% were nulliparous, as shown in [Figure 2].

The GA of the participants ranged from 20 to 39 weeks. The mean and standard deviation GA of the participants in the control group was 30.6 ± 4.47 and 33.20 ± 3.74 weeks in the PE group. This difference is statistically insignificant (P = 0.71). The mean GA of the mild-moderate PE and severe PE was 30.4 ± 4.33 weeks and 34.45 ± 2.56 weeks, respectively. No statistically significant change was seen between the change in GA and all the measured Doppler parameters in the control group [Table 2].

The systolic BP of the control group ranged from 90 to 130 mmHg, with a mean of 110.15 ± 16.30 mmHg, while the diastolic BP of the control group ranged from 60 to 85 mmHg, with a mean of 71.03 ± 6.0 mmHg. The mean systolic pressure for the study group ranged from 140 to 230 mmHg with a mean of 173.54 ± 24 mmHg. The mean diastolic BP for the control group ranged from 80 to 140 mmHg with a mean of 102.81 ± 12.09 mmHg [Table 2].

The PSV of the participants ranged from 14 to 68 cm/s and 17-69cm/s in the control and preeclamptic groups respectively, while the mean values were 37.04 ± 13.68 in the controls and 44.59 ± 11.54 in the preeclamptics. The PSV of the PE group is significantly higher than that of the control group [Table 1] and [Table 3], P = 0.02].
Table 3: Comparing the mean values (standard deviation) of velocimetric indices of the control and the study groups

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The EDV ranged from 3.57 to 18.33 cm/s and 5.0–16.9 cm/s in the control and PE groups, respectively, with mean values of 9.13 ± 3.64 cm/s in control and 12.2 ± 2.66 cm/s in the preeclamptic [Table 1] and [Table 3]. The mean EDV of the study group was also found to be statistically higher than that of the control group (P = 0.04), as shown in [Table 3].

The RI also showed a variation between the groups, ranging from 0.45 to 0.91 and 0.52 to 0.88 in the control and PE groups, respectively, P = 0.001, as shown in [Table 4]. The mean RI values were 0.75 ± 0.091 in the control and 0.66 ± 0.069 in the PE group, the mean RI of the PE group was significantly lower than that of the PE group P = 0.001, as shown in Table 3.
Table 4: Change in mean velocimetric indices with the severity of preeclampsia

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The PI ranged from 0.63 to 3.23 in the controls and 0.74–2.87 in the PE groups [Table 1]. The mean values were 1.62 ± 0.54 and 1.36 ± 0.42 in the control and PE groups, respectively. Thus, significantly lower PI was recorded in the PE group (P = 0.04).

The peak ratio(PR) of the control group ranged from 0.22-0.84 with a mean value of 0.55. Whereas in the study group the PR ranged from 0.44-0.91. Thus,the PR is statistically higher in the study group than in the control group.


   Discussion Top


In this study, the ophthalmic artery Doppler velocimetric indices were studied among normotensive pregnant women and those with the clinical diagnosis of PE. The mean age of the subjects in the study group (25.81 ± 6.85 years) was similar to that reported by Yakasai and Bello[18] (26.03 years) in Kano in 2013, but lower than that reported by Adokiye et al.[19] (29.02 ± 10.34 years) in Bayelsa state and Olatunji et al.[20] in Ibadan, Southwestern Nigeria. A slightly lower mean age was recorded in the severe PE group (24.3 ± 6.78). This variation is likely due to differences in age at marriage in the Northern part of Nigeria than the Southern part of the country. It was also observed that the age group with the largest number of participants in the severe PE group was 15–19 years, having 23 participants (34.8%). This is also lower than the report of Adokiye et al.[19] where 50.53% of the participants were in the age range of 20–29 years, and Kooffreh et al.[21] who reported 42.4% in the age range of 20–25 years.

The parity of the study group portrayed that 55.4% of the PE patients were primigravidas, of which 41.1% were in the severe PE subgroup, while the remaining 14.3% were in the mild-moderate PE subgroup. This finding is consistent with other literature which reported a higher incidence of PE among primigravidas. A significant proportion of the study subjects were also found to be grand multiparous (having parity ≥5), as shown in [Table 1] above.

Majority of the patients with symptoms at presentation were also found to be in the severe PE subgroup, with only 16.7% of those with mild-moderate PE having symptoms. This finding is consistent with the documented symptoms of PE.[22]

The mean GA of the control group (30.46 ± 4.47) was smaller than that of the PE group (33.18 ± 3.71), though the difference was statistically insignificant. A small variation in the GA was also recorded among the PE subgroups, being 35.4 ± 4.33 in the mild-moderate PE subgroup and 34.45 ± 2.56 in the severe PE subgroup. The GA of severe PE patients is consistent with the finding of Yakasai and Bello[18] who reported that the GA of development of PE is about 34 weeks and Kooffreh et al.[21] who reported 34–38 weeks as the GA of presentation of PE in Calabar, Nigeria. The earlier presentation of severe PE is probably due to the presence of symptoms in this subgroup as against mild-moderate PE, which is asymptomatic.[14]

The relationship between GA and the measured velocimetric indices was also determined among the normal control group, and it was observed that no significant change was seen in all the Doppler parameters with GA. This is in concordance with previous literatures.[14],[20],[23],[24]

The mean PSV for PE patients was significantly higher than that for normotensive patients. Similarly, there is a significant increase in the mean PSV between the mild-moderate and severe PE subgroups, as shown in [Table 4] above. This finding is similar to that of Hata et al.[10] and Diniz et al.[25] and could be due to orbital hyperperfusion, which is seen in PE. However, Olatunji et al.[26] who did similar work in southwestern Nigeria found a statistically insignificant decrease in PSV in women with PE compared with normal pregnant women. The mean PSV of the normotensive group was similar to that obtained by de Oliveira et al.[13] but lower than that obtained by Baxter and Williamson[27] and higher than those obtained by Olatunji et al.[26], Mihu D et al.[11] and Carneiro et al.[23] The reason for the variation between these works is probably due to variations in the prevalence of risk factors of PE among the different study populations. de Oliveira et al.[13] also found a statistically significant increase in these parameters among pregnant women with risk factors of PE.

This study also found a significant increase in the mean EDV of the PE group compared to the normotensive group. A significant increase in mean EDV was also observed between mild-moderate PE and severe PE subgroups. This finding is in concordance with the documentation of other literatures.[13],[20],[25] There is an increase in diastolic blood flow in patients with PE compared to normal pregnancy. It is also noted that a similar increase in diastolic flow occurs in severe PE compared to mild-moderate PE.

There was a statistically significant difference between the RI of pregnant women with PE compared to those of the control group. Lower RI (0.71 vs. 0.78, P = 0.04), was recorded in patients with PE than those in the control group [Table 3]. The results obtained also showed lower RI (0.69 vs. 0.75) in severe PE compared to the mild-moderate PE subgroup. These findings are consistent with those of Olatunji et al.,[26] Diniz et al.,[25] Ohno et al.,[28] and Ayaz et al.[29] In PE, severe hypertension exceeds the limit of autoregulation, leading to vasodilatation. Moreover, endothelial dysfunction leads to increased secretion of systemic vasodilators such as nitric oxide and decreased secretion of vasoconstrictors with subsequent orbital hyperperfusion due to lower impedance to ocular blood flow.[23],[29],[30]

Comparison between the PI of PE participants with that of the normal pregnant participants also showed significantly lower PI in the PE participants with a P = 0.04. Similarly, significantly lower PI was recorded in the severe PE subgroup compared to the mild-moderate PE subgroup. This finding is in conformity with that of other authors.[13],[25]

This study also showed significantly higher PR in the PE group compared to the control group. Comparison between mild-moderate PE and severe PE subgroups also showed significantly higher PR in the latter group compared to the former. de Oliveira et al,[15] found a mean PR of 0.89 in women with severe PE. This value is slightly higher than what was observed in this subgroup of participants (0.80), probably due to the proportion of the participants in this group who had already commenced medications before the study, which may lower this parameter. However, this value is very close to the finding of Olatunji et al.[26] who found a mean PR of 0.84 in this category of patients in Southwestern Nigeria. The PR, which is the ratio of the values of for the peak diastolic velocity and the PSV, has gained popularity since its introduction 2002. Similar to increase in EDV and PSV, an increase in this parameter also suggests reduction in vascular impedance in the ophthalmic arteries, particularly associated with severe PE. Although the mechanism of elevation of PR is not clearly known, it is proposed as the most sensitive indicator of vascular changes associated with orbital overperfusion.[28],[30]


   Conclusion Top


This study has shown the value of ophthalmic artery Doppler in Patients with PE and those at risk of its development. It showed that there is an increase in the PSV, EDV and PR and a decrease in PI and RI in PE. These changes are consistent with increase in cerebral perfusion, leading to the clinical features of PE and will play a role in evaluation of patients with PE. Potentially, OA Doppler may be used to identify those at risk of PE thereby intensifying care to avert the possible complications from this disease, ultimately reducing maternal mortality.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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