Comparative sonographic assessment of renal volume and arterial Doppler velocimetric indices among women with pregnancy-induced hypertension and normotensive controls in Northern Nigeria

Abstract

Introduction:

Pregnancy-induced hypertension is a global public health problem, worsening maternal morbidity and mortality. Renal complications have additional devastating consequences on maternal morbidity. Renal Doppler ultrasound is a valuable tool in the management of pregnancy-induced hypertension. It helps in the assessment of renal hemodynamics with the potential to monitor renal function and predict complications. We aimed to determine the relationship between the renal volume and arterial Doppler velocimetric indices in pregnancy-induced hypertension and matched normotensive controls.

Methods:

Following the documentation of demographic and basic obstetric characteristics of 150 women with pregnancy-induced hypertension and an equal number of their matched controls, a 3.5-MHz convex transducer was used to measure the maternal renal volumes and renal arterial Doppler velocimetric indices (peak systolic velocity, end diastolic velocity, resistive index, pulsatility index, and systolic–diastolic radio). Student’s t-test and linear regression were used to determine the differences and relationships between the quantitative variables among women with pregnancy-induced hypertension and their controls. The association chi-square test was used to determine the association between the qualitative and categorical variables. A p-value of less than 0.05 was considered significant.

Results:

The mean renal volume of pregnancy-induced hypertension patients is higher bilaterally when compared to normotensive women. The mean peak systolic velocity and resistive index in pregnancy-induced hypertension patients were significantly higher compared to normotensives (59.13 ± 13.5 vs 54.19 ± 9.8 cm/s; p < 0.001) and (0.74 ± 0.2 vs 0.68 ± 0.3).

Conclusion:

The maternal renal volume and peak systolic velocity of the renal arteries are significantly higher in women with pregnancy-induced hypertension compared to normotensives.

Keywords

Pregnancy hypertension renal artery Doppler velocimetric indices

Introduction

Pregnancy-induced hypertension (PIH) is a syndrome of hypertension with or without proteinuria and edema occurring after 20 weeks of gestation, and in some cases, convulsions occur when systolic blood pressure (BP) is greater than 140 mmHg and diastolic BP is greater than 90 mmHg.^1–3 Out of about 800 maternal deaths that occur globally, 99% are said to occur in low- and middle-income countries.^4,5 Notably, 80% of these deaths are due to four major causes: severe hemorrhage, infections, preeclampsia/eclampsia, and unsafe terminations.⁴

In northern Nigeria, pre-eclampsia/eclampsia accounts for up to 40% of maternal deaths. The incidence ranges from 3% to 9% in the north and approximately 1% to 3% in the south.⁶ Furthermore, women with PIH were at a higher risk of end-stage renal disease, compared to their normotensive counterparts.⁷ Recent studies have confirmed the relevance of maternal renal Doppler ultrasonography in the diagnostic assessment and follow-up of renal complications in patients with PIH.^8–11 Despite these advancements and the high burden of PIH in northern Nigeria, there is not enough reliable data in this environment concerning the maternal renal artery velocimetry indices in patients with hypertensive disorders of pregnancy. This study, therefore, is aimed at generating these data to fill the existing knowledge gap and assist in providing essential information about renal arterial hemodynamics and facilitating risk stratification. We hope these will ultimately contribute to improved overall maternal and fetal outcomes in patients with PIH.

Materials and methods

This case–control study was conducted at Aminu Kano Teaching Hospital (AKTH) in northern Nigeria. A total of 150 consented pregnant patients referred from the antenatal clinic and other units of AKTH, with a history of newly diagnosed PIH, were recruited into this study. An equal number of normotensive pregnant women (matched for gestational age) were recruited to the control group.

The inclusion criteria for the study group were consenting pregnant women with singleton and sonographically normal fetuses with a BP of or greater than 140/90 mmHg after 20 weeks gestation. We also included pregnant women with systolic BP exceeding 30 mmHg or diastolic BP exceeding 15 mmHg above the recorded baseline BP measurement on two occasions at least 6 hours apart after 20 weeks gestation. The control group was characteristically similar to the study group, except for their normal BP.

Pregnant women with diabetes mellitus, multiple gestations, history suggestive of urinary tract infection, congenital kidney disease, for example, ectopic kidney, and horseshoe kidney, and those with chronic hypertension predating pregnancy were excluded from the study.

Clinical evaluation

The procedure was explained to the patient and informed written consent was obtained. Information about age, parity, last menstrual period, and a detailed medical history was obtained using an interviewer-administered questionnaire, and the BP was rechecked. All medical conditions that would exclude the subjects from the study were asked about and ruled out using ultrasonography.

Techniques of renal volume and arterial Doppler measurements

Renal duplex Doppler ultrasonography was carried out to assess resistive and pulsatility indices using a 3.5-MHz transducer connected to Nortek Digital Ultrasound Imaging System (Model CS-50, Nortek Healthcare Electronics, Shenzen, China, 2015). After the application of water-soluble coupling gel to the area of interest on the maternal abdomen, following positioning in supine and in lateral or posterolateral positions on the examination table, a global examination of the kidneys was performed and the echogenicity was first assessed to establish its normality.¹² The kidneys were then scanned to rule out gross renal abnormalities in size, shape, and outline. The longitudinal (L), transverse (T), and anteroposterior (AP) diameters were measured, and renal volume (RV) was calculated using the parameters below

RV = L \times T \times AP \times 0.523 (ellipsoid volume .)

The origin of the two renal arteries was determined by the landmarks of the superior mesenteric artery and the renal vein.^13,14 The color mapping was used to demonstrate the renal blood flow as color flows toward the transducer. Doppler waveforms were obtained from the right renal artery due to the effect of the gravid uterus on the left kidney in late pregnancy, which makes the examination of the left renal artery technically difficult. Sampling of the interlobar artery was done along the border of medullary pyramids. The angle of insonation between the ultrasound beam and the vessel was adjusted to less than or equal to 60° while the spectral Doppler trace was obtained and recorded by placing a sample gate of 2 mm (adjusted when necessary) over the artery. The highest gain without obscuring background noise and the lowest possible wall filter was used. The height of the Doppler waveforms was optimized for measurements using the lowest pulse repetition frequency without aliasing to maximize waveform size.^15–18 At least three similar, sequential time-velocity waveforms of Doppler signals were obtained at each point of measurement during suspended respiration. Following the measurement of the peak systolic velocity (PSV) and end-diastolic velocity (EDV), the internal calipers and analytical software of the sonography unit, the measurement of the resistive index (RI), pulsatility index (PI), and systolic–diastolic ratio (S/D) was automatically generated by the machine.

The RI is calculated as (PSV − EDV) / PSV.

Data management

All data generated were collated and analyzed using the statistical package for social services (SPSS) version 22.0.

The continuous data were described in terms of means and standard deviation. The categorical data were described in frequencies and percentages when appropriate. Student’s t-test was used to determine the statistical difference between the means of the quantitative variables among women with PIH and their matched controls. The association chi-square test and Fisher’s exact test were used to determine the association between the qualitative and categorical variables between the PIH groups and their controls. Linear regression was used to determine the relationship between the systolic BP and diastolic BP, by the individual renal Doppler velocimetric indices (the PSV, EDV, S/D, RI, and PI). A probability value less than 0.05 was considered statistically significant at a confidence level of 95%.

Ethical considerations

The research protocol was approved by the local institutional review board (reference no. of the approval is NHREC/21/08/2008/AKTH/EC/2288). Informed written consent was obtained from the subjects involved in the study. Patients’ anonymity was protected with all identification markers removed from the images. Patients with serious abnormalities discovered during data collection were referred to the appropriate clinicians for prompt intervention and the index patients were replaced.

Results

Demographic and clinical characteristics of the study population

A total of 300 patients comprising 150 PIH and 150 gestational age-matched normotensive groups were studied. The ages of the PIH group ranged from 18 to 42 years with a mean of 30.9 ± 5.7 years, while the ages of the normotensive patients ranged from 23 to 44 years with a mean age of 29.9 ± 4.6 years.

The mean gestational age of the PIH group and that of their controls is 32.2 ± 6.1 and 31.8 ± 5.8 weeks, respectively (Tables 1 and 2). There were no statistically significant differences between the mean gestational age of the PIH and normotensive groups (p = 1.0). The parity of the PIH group ranged from 0 to 6 with 52.8% of them being primigravida, while the parity of the normotensive group also ranged from 0 to 6 with 48.7% of them being primigravida. There was no statistically significant difference between the mean parity of the PIH and normotensive group (p = 1.0) (Table 2).

Table 1.

Classification of patients according to gestational age.

Gestational age groups (weeks)	Study group		Total	p
Gestational age groups (weeks)	PIH patients, n (%)	Normotensive, n (%)	Total	p
20–24	36 (50)	36 (50)	72 (100)	1.000
25–29	28 (50)	28 (50)	56 (100)
30–34	46 (50)	46 (50)	92 (100)
35–39	40 (50)	40 (50)	80 (100)

PIH: pregnancy-induced hypertension.

Table 2.

The summary of demographic and clinical indices of PIH and normotensive patients.

Variable	Study group		p
Variable	Hypertensive	Control	p
Age (years)	30.85 ± 5.7	29.85 ± 4.6	0.096
Primigravida, n (%)	79 (52.7)	73 (48.7)	1.000
Multigravida, n (%)	71 (47.3)	77 (51.3)	1.000
Systolic BP	147.25 ± 9.0	117.27 ± 9.0	<0.001^*
Diastolic BP	94.35 ± 5.2	73.27 ± 7.9	<0.001^*
Gestational age in weeks	32.19 ± 6.1	31.8 ± 5.8	1.000
Right renal volume	154.29 ± 19.3	112.52 ± 17.1	<0.001^*
Left renal volume	170.13 ± 30.9	119.62 ± 32.4	<0.001^*

BP: blood pressure.

Significant at p ⩽ 0.05.

The systolic BP of the PIH group ranged from 140 to 180 mmHg with a mean of 147 ± 9.0 mmHg, while the systolic BP of the normotensive group ranged from 100 to 130 mmHg with a mean of 117.3 ± 9.0 mmHg. The systolic BP of the PIH group ranged from 90 to 110 mmHg with a mean of 94.4 ± 5.2 mmHg, while the diastolic BP of the normotensive group ranged from 60 to 80 mmHg with a mean of 73.3 ± 7.9 mmHg (Table 2).

The right renal volumes of the PIH group ranged from 102.01 to 176.99 cm³ with a mean of 154.29 ± 19.3 cm³, while the right renal volumes of the normotensive group ranged from 94.36 to 159.76 cm³ with a mean of 112.52 ± 17.1 cm³. There was a statistically significant difference between the mean right renal volumes of the PIH and normotensive groups (p < 0.001). There was also a statistically significant difference between the mean left renal volumes of the PIH and normotensive groups. (p < 0.001). The left renal volumes of the PIH group ranged from 110.40 to 219.48 cm³ with a mean of 170.13 ± 30.9 cm³, while the left renal volumes of the normotensive group ranged from 94.40 to 212.31 cm³ with a mean of 119.62 ± 32.4 cm³ (Table 3).

Table 3.

Mean values of Doppler velocimetric indices of PIH and normotensive patients.

Variable	Study group		p
Variable	PIH patients	Normotensive	p
PSV	59.13 ± 13.5	54.19 ± 9.8	<0.001^*
EDV	18.68 ± 6.3	18.70 ± 5.2	0.975
RI	0.74 ± 0.2	0.68 ± 0.3	0.058
S/D	3.54 ± 0.5	2.89 ± 0.7	<0.001^*
PI	1.24 ± 0.1	0.84 ± 0.3	<0.001^*

PIH: Pregnancy-induced hypertension; PSV: Peak Systolic Velocity; EDV: End Diastolic Velocity; RI: Resistive Index; S/D: systolic–diastolic radio; PI: pulsatility index.

Significant at p ⩽ 0.05.

Doppler velocimetric characteristics of subjects

The PSV of the PIH group ranged from 41.06 to 91.60 cm/s with a mean of 59.13 ± 13.5 cm/s, while the PSV of the normotensive group ranged from 43.50 to 87.35 cm/s with a mean of 54.19 ± 9.9 cm/s. There was a statistically significant difference between the mean PSV of the PIH and normotensive groups (p < 0.001) (Table 3).

As shown in Table 3, the EDV of the PIH group ranged from 11.42 to 29.52 cm/s with a mean of 18.68 ± 6.3 cm/s, while the EDV of the normotensive group ranged from 12.63 to 31.28 cm/s with a mean of 18.70 ± 5.2 cm/s. There was no statistically significant difference between the mean EDV of the PIH and normotensive groups (p = 0.008).

As illustrated in Table 3, the RI of the normotensive group ranged from 0.47 to 0.81 with a mean of 0.68 ± 0.3 while the RI of the PIH group ranged from 0.56 to 1.04 with a mean of 0.74 ± 0.2.

However, the mean RI of the PIH and normotensive groups showed no statistically significant difference (p = 0.058). The PI of the PIH group ranged from 1.02 to 1.46 with a mean of 1.24 ± 0.1, while the PI of the normotensive group ranged from 0.26 to 1.42 with a mean of 0.84 ± 0.3. There was also a statistically significant difference between the mean PI of the PIH and normotensive groups (p < 0.001).

The S/D ratio of the PIH group ranged from 2.75 to 4.20 with a mean of 3.54 ± 0.5, while the S/D ratio of the normotensive group ranged from 2.29 to 4.00 with a mean of 2.89 ± 0.7 (Table 3). There was a statistically significant difference between the mean S/D ratio of the PIH and normotensive groups (p < 0.001) (Table 4).

Table 4.

Regression statistics of indices with systolic BP among PIH patients.

Index	r	p	B
PSV	0.35	0.042^*	0.892
EDV	−0.027	0.638	−0.027
RI	0.023	0.064	0.002
S/D ratio	0.010	0.230	0.005
PI	0.29	0.049^*	0.346

PSV: Peak Systolic Velocity; EDV: End Diastolic Velocity; RI: Resistive Index; S/D: systolic–diastolic radio; PI: pulsatility index.

Significant at p ⩽ 0.05.

The PSV, RI, S/D ratio and PI showed a variable degree of positive correlations with systolic BP among PIH patients (r = 0.35, 0.023, 0.010, and 0.29, respectively). There was a statistically significant correlation between the PSV and PI with systolic BP among PIH patients. (p = 0.042, 0.014, and 0.049, respectively). EDV showed a negative correlation with systolic BP among PIH patients. (r = −0.027). However, this correlation was not statistically significant (p = 0.638) (Table 4).

Among women with PIH, the PSV, RI, and PI showed a positive correlation with diastolic BP (p = 0.370, 0.186, and 0.037). However, the correlation was not statistically significant except for PI (Figure 1). As illustrated in Table 5, there was a negative weak (but statistically not significant) correlation between the EDV and S/D ratio with diastolic BP among PIH patients (r = −0.028 and −0.003 respectively), and was not statistically significant. (p = 0.777 and p = 0.630) (Figure 2).

Figure 1.

Scatterplot showing a correlation between pulsatility index (PI1) and systolic BP (SystolicBP1).

Table 5.

Regression statistics of indices with diastolic BP among PIH patients.

Index	r	p	B
PSV	0.005	0.370	0.192
EDV	−0.028	0.777	−0.028
RI	0.012	0.186	0.003
S/D ratio	−0.003	0.630	−0.003
PI	0.29	0.037^*	0.004

PSV: Peak Systolic Velocity; EDV: End Diastolic Velocity; RI: Resistive Index; S/D: systolic–diastolic radio; PI: pulsatility index.

Significant at p ⩽ 0.05.

Figure 2.

Scatterplot showing correlation between pulsatility index (PI1) and diastolic BP (DystolicBP1).

Discussion

Hypertensive disorders account for 29.2% of all cases of medical disorders in pregnancy and 18% of all fetal deaths are associated with hypertension.^19,20 This may sometimes progress to pre-eclampsia resulting in multi-systemic dysfunction out of which the kidney bears the main brunt being a highly vascular organ.²¹

The initiating events and the factors responsible for the pathogenesis of PIH have not yet been fully elucidated despite years of continuous research.^8,21,22 However, it is believed to be related to abnormal placentation leading to endothelial dysfunction and clinical syndromes.²³ Pre-eclampsia affects the kidney both functionally and morphologically. Worsening renal hemodynamics and increasing urinary protein from glomerular lesions produce a characteristic appearance and permit differentiation of pre-eclamptic nephropathy from other glomerular alterations associated with hypertension in pregnancy.²³

Hypertensive disorders of pregnancy have been regarded as a disease of first pregnancy in the studies done by Ogunmoroti et al.⁸ in Ife western Nigeria and Miyake et al.²¹ in Japan, in which primigravidae accounted for a considerable number of women with PIH, 52% and 38%, respectively. In this study, the primigravidae with PIH (52.7%) are slightly higher than the multigravidae (47.3%). Since the difference is not much, this study has shown the need for surveillance not only for primigravidae but also for multigravidae. The possible reason for the latter may be increasing age which may predispose them to other medical conditions.

The mean age in this study among patients with PIH was 30.85 ± 5.7 years. This is similar to that observed in the studies by Ogunmoroti et al.⁸ However, the finding is slightly higher than 26.2 ± 5 years reported in the study by Julka et al.²² in India. The variation in the mean age of the study group with the one reported in the study by Julka et al.²² could be attributed to the difference in age at marriage and urbanization between Kano and India. The mean age at first marriage of women in semi-urban and rural centers of India was 18 years,²⁴ while the mean age at first marriage for urban centers of Nigeria was 21 years.²⁵

The renal volumes were significantly higher in PIH subjects than in the control groups. The right renal volume in the pregnancy-induced hypertensive group has a mean of 154.29 ± 19.3 compared to 112.52 ± 17.1 cm³ in normotensive pregnant women, respectively. The renal volume is higher in PIH than in healthy normotensive pregnant women which shows that physiological dilatation has a light effect on the increase in renal volume but the increase is actually due to intrinsic vascular and hemodynamic response to pregnancy in PIH patients, especially in the tubule–interstitial portion of the kidney. Similar studies also showed that the increase in renal volume in the PIH patient is due to active renal disease.^24,26 The renal plasma and the glomerular filtration rate increase as a result of kidney vasodilatation during a normal pregnancy. Furthermore, renal volume was found to be predominantly more in the left kidney than the right in both groups.^8,27 The possible reason for this may be due to the peculiarity of the left renal artery anatomy which is shorter and straighter than the right renal artery with associated increased blood flow. Another explanation is the discrepancy in the length of both kidneys accounting for about 1.5–2 cm in both female and male subjects.²⁸

Several investigators have attempted to evaluate renal circulation by performing Doppler sonography in PIH patients and normotensive pregnant women.^{8,9,21,22,24,27,29} However, the renal artery in PIH patients is a reflector of vascular resistance, and thus it does not assume the early systolic peak (ESP). Rather abnormal flow patterns may be seen in the form of decreased or reversed diastolic flow, round-up, or loss of ESP. The abnormal flow patterns seen in this study are round-up and loss of ESP which accounted for 28 (19%) of the PIH patients but were not statistically significant. This concurs with a study by Miyake et al.²¹ The autoregulation mechanism allows the kidney to adequately and constantly maintain the intrarenal pressure under the condition of vasospasm within the vast range of the change of systemic BP and renal resistance.^8,21 Thus, this may be the reason why emphasis by previous studies stated that abnormal renal artery Doppler velocity indices, rather than an abnormal spectral waveform, may probably be the best index to determine patients with PIH.^8,21,22

Several studies have been done to evaluate renal circulation using Doppler ultrasound in normotensive pregnant women and women with PIH.^8,30 The vessels examined in these studies were the main renal artery, segmental artery, and interlobar artery, while the parameters analyzed were restricted to the most common parameters of downstream vascular resistance, such as S/D ratio, PI, and RI. Few researchers analyzed acceleration time, systolic acceleration, and ESP. However, conflicting results have been reported across studies with some demonstrating changes and others believing that there are no effects on the renal indices.^8,21,29

The PSV is slightly higher in PIH patients compared to normotensive patients and it is statistically significant. Studies by Ogunmoroti et al.⁸ and Miyake et al.²¹ showed similar results but these were not statistically significant in the latter. The discrepancy in the sample size among normotensive and PIH patients may account for this.

The mean EDV was slightly higher in normotensive controls (18.70 ± 5.2) compared to women with PIH (18.68 ± 6.3) but this difference is not statistically significant. This is similar to the findings of Julka et al.²² and Yuan et al.²⁹ but in contrast to other studies by Miyake et al.²¹ and Ogunmoroti et al.⁸ The lower sample size used in some of these studies may explain these variations.

The mean RI is slightly higher in PIH patients (0.74 ± 0.2) compared to normotensives (0.68 ± 0.3) but not statistically significant. Similar studies confirm this result.^8,9,22 Yuan et al.²⁹ show no difference between the PIH group and the normotensive group. In contrast to the above findings, Miyake et al.²¹ show a significant increase in the RI of the normotensive renal artery (R = 0 65 ± 0.07) compared to PIH (R = 0.62 ± 0.06). However, their sample size was smaller and their study subjects were heterogeneous, thus making the findings different from those of the other researchers.

The S/D ratio is slightly higher in PIH patients with a p-value of less than 0.05 compared to normotensive patients. The increased vascular resistance among PIH patients may account for this result. The result is consistent with the findings obtained in the study by Ogunmoroti et al.⁸

The PI is generally found in a direct relationship with an increase in vascular resistance distal to the site of measurement.⁸ In this study, PI is significantly higher in PIH patients compared to normotensive pregnant with a mean of 1.24 ± 0.1 and 0.84 ± 0.3, respectively. Previous studies show similar results.^8,9 This is in contrast to the study by Yuan et al.²⁹ likely due to a smaller sample size.

Systolic BP is positively correlated with PSV, RI, S/D ratio, and PI. The PSV and PI are statistically significant while the diastolic BP is positively correlated with PSV, RI, A, and PI but statistically significant with only PI (r = 0.029 and p = 0.037) with p < 0.05. This further buttresses the reliability of PI and agrees with previous researchers who have proven that PI is a more suitable and accurate index of renal artery velocimetry indices.³⁰ These abnormal hemodynamics postulated results from the placental elaboration of vasoactive substances causing endothelial injury, vasoconstriction, and hypertension.^7,22,31

Conclusion

There is a significant difference in renal artery Doppler velocimetry indices (PSV, S/D ratio, and PI) in PIH patients compared to normotensive patients. In this study, PI was found to correlate well with renal vascular resistance.

Therefore, measuring maternal renal volume and conducting arterial Doppler velocimetry should be valuable components of antenatal care for women with PIH. These assessments help clinicians evaluate renal perfusion, direct complications early, and optimize management strategies for improved maternal outcomes.

Study limitations

A cross-sectional study like this is observational and cannot establish causality. While it can identify associations between variables, it cannot determine the direction of causality or rule out reverse causation. Despite the useful information generated by this study, it may be challenging to establish a clear temporal relationship between PIH and changes in renal volume and arterial Doppler ultrasound measurements.

Recommendations

While recommending the use of ultrasound measurement of the renal volume and renal arterial Doppler velocimetric assessment (especially the PSV, S/D, and PI) for evaluation and monitoring of patients with PIH to ascertain renal vascular hemodynamic changes, further longitudinal studies will be useful to determine the temporal relationship and outcomes, between PIH and changes in renal volume and arterial Doppler ultrasound measurements.

Footnotes

Acknowledgements

The authors thank the doctors, nurses, and record clerks of the antenatal clinic and the staff of the ultrasound unit for their kind support during the data collection process. Furthermore, the corresponding Author (Dr Anas Ismail) was partly supported by the Fogarty International Center (FIC) and the National Institute on Alcohol Abuse and Alcoholism (NIAAA) of the US National Institutes of Health (NIH) (award no. 1D43TW011544). The findings and conclusions are those of the authors and do not necessarily represent the official position of the FIC, NIAAA, NIH, the Department of Health and Human Services, or the government of the United States of America.

Contributors

Constructing an idea or hypothesis for research and/or manuscript: TIOA. Planning methodology to reach the conclusion: TNA. Organising and supervising the course of the project or the article and taking the responsibility: MAS. Providing personnel, environmental and financial support, and tools and instruments that are vital for the project: AI. Biological materials, reagents, and referred patients: MYA. Taking responsibility for the execution of the experiments, patient follow-up, data management, and reporting: TIOA, TNA and AI. Taking responsibility for logical interpretation and presentation of the results: AM. Taking responsibility for this necessary function: TIOA. Taking responsibility for the construction of the whole or body of the manuscript: AI. Reviewing the article before submission not only for spelling and grammar but also for its intellectual content.: AI.

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest concerning the research, authorship, and/or publication of this article.

Funding

The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: The management of Aminu Kano Teaching Hospital, Kano has provided part funding. In addition, the corresponding author was supported by the Fogarty International Center (FIC) and the National Institute on Alcohol Abuse and Alcoholism (NIAAA) of the US National Institutes of Health (NIH) (award no. 1D43TW011544). The findings and conclusions are those of the authors and do not necessarily represent the official position of the FIC, NIAAA, NIH, the Department of Health and Human Services, or the government of the United States of America.

Ethics approval

The research and ethics committee of Aminu Kano Teaching Hospital, Kano, Nigeria has approved the conduct of this research. The reference number of the approval is NHREC/21/08/2008/AKTH/EC/2288.

Permission from patient(s) or subject(s) obtained in writing for publishing their case report

Yes.

Permission obtained in writing from the patient or any person whose photo is included for publishing their photographs and images

Yes.

Confirm that you are aware that permission from a previous publisher for reproducing any previously published material will be required should your article be accepted for publication and that you will be responsible for obtaining that permission

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Guarantor

Anas Ismail

ORCID iD

Anas Ismail

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