Cerebral Artery Hypoplasia in a Select Adult Kenyan Population

Julius A. Ogengo; Isaac Cheruiyot; Thomas Amuti; Ibsen Ongidi; Philip Mwachaka; Beda Olabu; Peter Kitunguu; Simeon Sinkeet

doi:10.1055/s-0039-1697562

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Original Article

10 (

); 423-429

doi:

10.1055/s-0039-1697562

Cerebral Artery Hypoplasia in a Select Adult Kenyan Population

Julius A. Ogengo¹, Isaac Cheruiyot¹, Thomas Amuti¹, Ibsen Ongidi¹, Philip Mwachaka¹, Beda Olabu¹, Peter Kitunguu¹, Simeon Sinkeet¹

1Department of Human Anatomy, University of Nairobi, Nairobi, Kenya

Address for correspondence Thomas Amuti, BSc Department of Human Anatomy, University of Nairobi P.O. Box 00100, 30197, Nairobi Kenya tomamuti@gmail.com

Journal of Neurosciences in Rural Practice

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This is an open access article published by Thieme under the terms of the Creative Commons Attribution-NonDerivative-NonCommercial License, permitting copying and reproduction so long as the original work is given appropriate credit. Contents may not be used for commercial purposes, or adapted, remixed, transformed or built upon. (https://creativecommons.org/licenses/by-nc-nd/4.0/)

Disclaimer:
This article was originally published by Thieme Medical and Scientific Publishers and was migrated to Scientific Scholar after the change of Publisher.

Abstract

Background Hypoplasia of cerebral arteries predisposes to stroke and cerebral aneurysms which have an increased incidence in sub-Saharan Africa. The frequency and pattern of cerebral artery hypoplasia, however, shows population variations, and data from the African population remain scanty.

Objectives This study aimed to determine the percentage of hypoplasia in the anterior, middle, and posterior cerebral, anterior and posterior communicating, basilar, and vertebral arteries.

Materials and Methods Sections of the basilar, vertebral, posterior, and anterior communicating arteries and anterior, middle, and posterior cerebral arteries were taken, processed for histology, and examined with a light microscope at ×40. The images of the vessels were taken by a photomicroscope and circumference analyzed with the aid of Scion image analyzer. The average diameter of 10 sections was taken to be the diameter of the artery in analysis. Hypoplasia was then defined as internal diameter ≤1 mm. Photographs of representative samples of asymmetry were taken, data were analyzed using SPSS, and gender differences were analyzed using the Student's test. Results were presented in tables.

Results Two hundred and eighteen formalin-fixed brains of adult Kenyans at the Department of Human Anatomy, University of Nairobi, were studied. Of the 218, 48 brains (22%) did not have vessels with any form of hypoplasia while 170 (78%) did have vessels. Of these, anterior circulation hypoplasia (anterior cerebral artery and posterior communicating artery) was seen in 100 brains (46%) and posterior circulation hypoplasia (middle and posterior cerebral, basilar, and vertebral arteries) in 69 brains (32%).

Conclusion Cerebral arterial hypoplasia is frequent in the select adult Kenyan population.

Keywords

cerebral artery

hypoplasia

posterior

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Introduction

Hypoplasia in cerebral arteries has been shown to alter hemodynamics in the affected arteries as well as the normal arteries in the same vascular bed.1 2 It further influences the pattern of cerebral blood flow3 and predisposes to atherosclerosis of large and small cerebral arteries alike, causing stroke and transient ischemic attacks.1 2 4 Hypoplasia also causes cerebral aneurysms,5 may be associated with deformities of other intracranial arteries,6 7 and can be confused for pathological arterial occlusion.8 Cerebral hypoplasia has the potential to cause cerebral hypoperfusion and thus predisposes to cognitive dysfunction and Alzheimer's disease.9 Knowledge on cerebral hypoplasia is important during instrumentation of arteries as well as mitigating complications of endovascular treatment and prognostication of cerebrovascular disease.6 Further, it is also important to surgeons in planning shunt operations, choice of patients, and avoidance of inadvertent vascular trauma during surgery.10

Stroke, cerebrovascular disease, and cognitive decline are now recognized to be leading causes of mortality and morbidity in sub-Saharan Africa, including in Kenya.11 Since these conditions are predisposed by cerebral artery hypoplasia, and in an attempt to link their possible causation to cerebral artery hypoplasia, a study on the same in the Kenyan setting is paramount.

Hypoplasia of cerebral arteries has been shown to display ethnic variation,12 and data from the African populations are scarce. The prevalence of hypoplasia from our findings might help to explain the high prevalence of cerebrovascular disease, stroke, and cognitive impairment.13 14

This study, therefore, aimed to determine the prevalence of cerebral artery hypoplasia of several cerebral arteries in a select adult Kenyan population.

Materials and Methods

The study was done on 218 formalin-fixed brains from adult adult Kenyans (124 males; 94 females, age range: 20–79 years) obtained during autopsy at the Department of Human Anatomy, University of Nairobi, Kenya. Ethical approval was granted by the Kenyatta National Hospital/University of Nairobi Ethics and Research Committee and the Kenyan constitution. Further, consent was sought from each family member, and benefits of the study were explicitly explained to them before any dissections.

Cases of suspected cerebrovascular disease influenced by other cardiovascular risk factors and damaged arteries were excluded to minimize the potential confounding effect of these pathological conditions (such as atherosclerotic arterial narrowing). The cardiovascular risk factors excluded were alcohol (32.3%), diabetes mellitus (23.4%), cigarette smoking (20.8%), and obesity (14.5%). The study, however, included brains from causes of death such as trauma (60.1%), infections (21.4%), malignancy (13.3%), poisoning (3.5%), and drowning (1.7%). The age distribution of the cases is as shown in Table 1. The brains were divided into those of males and females.

Table 1

Age distribution of the population from which the cerebral arteries were obtained

Age range (y)	Frequency		Total (%)
Age range (y)	male	female	Total (%)
21–30	19	15	34(15.6)
31–40	24	19	43(19.7)
41–50	30	23	53(24.3)
51–60	29	22	51(23.4)
61–70	14	10	24(11)
71–80	8	5	13(6)
Total	124	94	218(100)

Arachnoid mater was gently peeled from the base of the brain to expose the basilar, vertebral, posterior, middle, and anterior cerebral arteries and the posterior and anterior communicating arteries. Two-millimeter specimens taken from each of the arteries were then fixed in 10% formalin and processed for paraffin embedding and sectioning. Ten 5-μm serial sections from each arterial site were stained with hematoxylin/eosin and examined with the help of a Leica DM3000 light microscope at ×40. The images taken by the photomicroscope were digitized. Subsequently, the internal circumference of each of the 10 sections from each site of the artery was determined using Scion image analyzer version 1.46. To do this, the image was first set to scale; then, with the help of the line tool, a line was drawn round the lumen of the artery to give a value equivalent to the circumference. Only complete sections were included. The diameter (in millimeters) was calculated from the formula D = C/π, where D is the diameter, C is the circumference, and π = 3.14. The average diameter of the 10 sections was taken to be the diameter of that artery.

Artery hypoplasia was defined as internal diameter ≤1 mm. Photographs of representative samples of asymmetry were taken using a high-resolution digital camera. Data were analyzed using Statistical Package for the Social Science (SPSS; IBM, New York, United States) for Windows. Gender differences were analyzed using the Student's test at 95% confidence intervals where value of ≤0.05 was taken as significant. Results were presented in tables.

Results

Of the 218 dissected brain specimens, 170 presented with hypoplasia. The remaining 48 did not exhibit hypoplasia. Of the 170, anterior cerebral artery hypoplasia was recorded in 13 (6%) brains with 87 (40%) showing posterior communicating artery (PCoA) hypoplasia, 26 (12%) showing posterior cerebral artery hypoplasia, 6 (3%) showing basilar artery hypoplasia, and 37 (17%) showing vertebral artery hypoplasia (VAH). All the arteries studied, except middle cerebral, displayed hypoplasia. The findings have been summarized (Tables 2 and 3 and Fig. 1 Fig.2 Fig.3 Fig.4 Fig.5).

Table 2

Frequency of hypoplasia of cerebral arteries in adult Kenyans

Artery	Frequency of hypoplasia(%)
Anterior cerebral	13(6)
Posterior communicating	87(40)
Posterior cerebral	26(12)
Vertebral	37(17
Basilar	6(3)
Total	170(78)

Table 3

Frequency of hypoplasia of the different cerebral arteries in adult Kenyans

Vascular region	Percentages
Abbreviations: BA, basilar artery; PCA, posterior cerebral artery; PCoA, posterior communicating artery; VA, vertebral artery.
Anterior circulation
Unilateral right A1 segment	3
Unilateral left A1 segment	2
Unilateral A2 segment	1
Posterior circulation
PCoA
Bilateral	23
Unilateral left	13
Unilateral right	4
PCA
Bilateral	6
Unilateral left	2
Unilateral A2 segment	2
Unilateral right	4
VA
Right	10
Left	7
BA	3

Discussion

Data from our study revealed that of all the arteries studied, the middle cerebral artery did not exhibit hypoplasia.

This finding is similar to prevailing literature from other populations.12

Cerebral artery hypoplasia was more common in the anterior circulation (46%). This is consistent with contemporary literature reports.3 15 The mechanisms by which cerebral artery hypoplasia occurs are considered to be related to hemodynamic factors. In this case, the differential growth of the various parts of the brain will continuously change the hemodynamic demands and consequently the flow patterns in the cerebral arteries.16 It is, therefore, conceivable that if a selected part of the brain does not develop, the change in the hemodynamic demand in that area will be reduced as noted by Van Overbeeke et al.17 The frequency of anterior circulation (anterior cerebral artery and PCoA) hypoplasia varied between arteries.

The frequency of A1 hypoplasia is reported to range between 1 and 15%.18 19 20 The A1 segment is the principal supplier of collateral blood flow and origin to striate arteries, which supply the hypothalamus, septum pellucidum, and corpus striatum. Hypoperfusion may, therefore, affect functioning in these areas. Further, in patients with hypoplastic A1 segments, total cerebral blood flow within the ipsilateral internal carotid is usually lower than in the contralateral internal carotid artery (ICA).14 This may cause global cerebral hypoperfusion. Accordingly, A1 hypoplasia is a risk factor for stroke-related vascular diseases,19 21 has been implicated in mild cognitive impairment,22 23 and may present with monoplegia, abulia, and urinary incontinence. It is also a risk factor for the occurrence of anterior communicating artery (ACoA) aneurysms.24 In the current study, A1 hypoplasia occurred in 6%, which was notably higher when compared with the Polish (3%),25 the Indians (4%),10 and the Sri Lankans (5%) (Table 4). It was, however, lower when compared with the Taiwanese (15%).19 The relatively higher prevalence observed among Kenyans as compared with many of the other populations may explain the high prevalence of aneurysms of ACoA.11 27 Pertinent to this suggestion is the observation that A1 hypoplasia predisposes to ACoA aneurysm.5

Table 4

Frequency of hypoplasia on anterior cerebral artery in different populations

Reference	Population	Frequency (%)
Chuang et al, 2007¹⁹	Taiwanese	15
De Silva et al, 2009²⁶	Sri Lankan	5
Klimek-Piotrowska et al, 2016¹²	Polish	1.0
Makowicz et al, 2013²⁵	Polish	3
Iqbal, 2013¹⁰	Indian	4
Current study	Kenyan	6

Posterior cerebral artery was hypoplastic in 12% of the cases. This was higher than that recorded in the Ameri-can28 (6.3%), Indian29 (5.29%), Polish12 (4%), and Pakistani30 (0%) populations (Table 5). It was notably lower when compared with the German31 (37.5%) population and other populations.32 33 The higher prevalence in the Kenyan setting as compared with most of the other populations may predispose to bilateral paramedian thalamic strokes and ischemic strokes, which have been reported to be high in Africa.

Table 5

Frequency of hypoplasia of posterior cerebral artery in various populations

Reference	Population	Frequency
Förster et al, 2014²⁹	German	37.5
Alpers et al, 1959³⁰	American	6.3
Gunnal et al, 2015³¹	Indian	5.29
Klimek-Piotrowska et al, 2016¹²	Polish	4
Siddiqi et al, 2013²⁸	Pakistani	0
Puchades-Orts et al, 1976³²		11.3
Milenković et al, 1985³³		7.68
Iqbal, 2013¹⁰	Indian	6
Current study	Kenyan	12

The 40% incidence of PCoA hypoplasia observed in the current study is lower to the 51% reported for the Sri Lankan population.26 It is, however, much higher than that noted in Korean (19.35%), Dutch (28%), Indian (23.3%), and Polish (24%) populations34 35 36 37 38 39 and previous study on the Kenyan population (Table 6). The high variability even among ethnically related Caucasian populations suggests that epigenetic factors are involved in the causation of this variation. Hypoplasia of PCoA increases the risk of atherosclerosis of large and small intracranial arteries and hence ischemic posterior circulatory strokes.1 34

Table 6

Frequency of hypoplasia of posterior communicating artery in various populations

Reference	Population	Frequency
Chuang et al, 2008³⁴	Korean	19.35
De Silva et al, 2009²⁶	Sri Lankan	51
Dzierżanowski et al, 2014³⁸	Polish	24
Krabbe-Hartkamp et al, 1998³⁶	Dutch	28
Saha et al, 2013³⁷	Indian	23.3
Siddiqi et al, 2013²⁸	Pakistani	39.5
Windle 1888³⁵	British	25
Sinkeet et al, 2010³⁹	Kenyan	25
Iqbal, 2013¹⁰	Indian	10
Current study	Kenyan	40

Basilar artery hypoplasia has been reported to be a rare occurrence frequently linked to persistent carotid-basilar communication or correlated with the presence of a large PCoA with persistent flow from the carotid to vertebrobasilar system. Cases of these variations are scarce in the literature with a case study being reported in the Italian population40 and 1 case of 62 specimens being noted in the Spanish population.32 In our setting, the basilar artery was hypoplastic in 3% of the sample population. Basilar artery hypoplasia has been shown to occur following persistent axial nonfusion of the distal basilar artery, which develops from the caudal division of the ICA to the posterior inferior cerebellar artery termination of the vertebral artery.40 Basilar artery hypoplasia has been linked to chronic brain hypoperfusion and a subsequent posterior circulation insufficiency.40

The current study revealed a 17% prevalence of VAH, higher than those reported for most Caucasian41 42 43 44 45 46 47 populations (Table 7). The variations of these vessels, similar to the above, have been shown to predispose to lacunar infarcts and strokes that have a high prevalence in our setting. This VAH-associated risk is equivalent to that of other conventional risk factors such as hypertension, diabetes, smoking, and dyslipidemia.4 Accordingly, nearly 30% of the Kenyan population may be at risk of posterior circulatory stroke and the other complications. This implies that in patients who present with vertebrobasilar insufficiency, VAH should be considered.

Table 7

Frequency of vertebral artery hypoplasia in various populations

Reference	Population	Frequency
Abbreviation: VAH, vertebral artery hypoplasia.
Chuang et al, 2008³⁴	Taiwanese	10.4
Oder et al, 1998⁴²	Austrian	10
Park et al, 2007⁴⁴	Korean	26.5
Peterson et al, 2010⁴⁵	Swizz	35.8
Thierfelder et al, 2014⁴⁶	American	15.6
Hu et al, 2013⁴⁷	Chinese	10
Current study	Kenyan	17

General Remarks

The frequency of hypoplasia varies between populations. These variations are probably genetically determined, develop early in embryonic life, and persist in postnatal life.11 It is also worth noting that in our setting, hypoplasia was predominant in the anterior circulation, specifically in the PCoA.

Conclusion

The frequency of cerebral arterial hypoplasia is high in the Kenyan population and is more common in the anterior circulation. Due care should be taken during neuroradio-logical, investigative, and interventional procedures; and patients should be followed up when presenting with cerebrovascular disease.

Acknowledgments

The authors are grateful to the staffs working in the Department of Human Anatomy for providing technical assistance and to Antonina Odock for typing the manuscript.

Conflict of Interest

None declared.

Funding None.

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Introduction

Materials and Methods

Results

Discussion

General Remarks

Conclusion

Acknowledgments

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[1] Chuang Y. M., Huang Y. C., Hu H. H., Yang C. Y., . Toward a further elucidation: role of vertebral artery hypoplasia in acute ischemic stroke. Eur Neurol. 2006;55(4):193-197.
[Google Scholar]

[2] Chen Y. Y., Chao A. C., Hsu H. Y., Chung C. P., Hu H. H., . Vertebral artery hypoplasia is associated with a decrease in net vertebral flow volume. Ultrasound Med Biol. 2010;36(1):38-43.
[Google Scholar]

[3] Pascalau R, Padurean V. A., Bartos D, Bartos A, Szabo B. A., . The geometry of the circle of Willis anatomical variants as a potential cerebrovascular risk factor. Turk Neurosurg. 2019;29(2):151-158.
[Google Scholar]

[4] Szarazova A. S., Bartels E, Turcani P, . Vertebral artery hypoplasia and the posterior circulatory stroke. Perspect Med. 2012;1:198-202.
[Google Scholar]

[5] Rinaldo L, McCutcheon B. A., Murphy M. E., Bydon M, Rabinstein A. A., Lanzino G, . Relationship of A1 segment hypoplasia to anterior communicating artery aneurysm morphology and risk factors for aneurysm formation. J Neurosurg. 2017;127(1):89-95.
[Google Scholar]

[6] Chaturvedi S, Lukovits T. G., Chen W, Gorelick P. B., . Ischemia in the territory of a hypoplastic vertebrobasilar system. Neurology. 1999;52(5):980-983.
[Google Scholar]

[7] Vilimas A, Barkauskas E, Vilionskies A, Rudzinskaite J, Moikunate R, . Vertebral artery hypoplasia: importance for stroke development, the role of posterior communicating artery, possibility for surgical and conservative treatment. Acta Med Litu. 2003;10:110-114.
[Google Scholar]

[8] Buckenham T. M., Wright I. A., . Ultrasound of the extracranial vertebral artery. Br J Radiol. 2004;77:15-20. 913
[Google Scholar]

[9] Rivera-Rivera L. A., Turski P, Johnson K. M., . 4D flow MRI for intracranial hemodynamics assessment in Alzheimer’s disease. J Cereb Blood Flow Metab. 2016;36(10):1718-1730.
[Google Scholar]

[10] Iqbal S, . A comprehensive study of the anatomical variations of the circle of Willis in adult human brains. J Clin Diagn Res. 2013;7(11):2423-2427.
[Google Scholar]

[11] Ogeng'o J. A., Olabu B, Mburu A. N., Sinkeet S. R., Ogeng'o M. N., . Ischemic cortical stroke in a Kenyan referral hospital. J Mol Biomark Diagn. 2010;5:238.
[Google Scholar]

[12] Klimek-Piotrowska W, Rybicka M, Wojnarska A, Wojtowicz A, Koziej M, Hoida M. K., . A multitude of variations in the configuration of the circle of Willis: an autopsy study. Anat Sci Int. 2016;91(4):325-333.
[Google Scholar]

[13] Tanaka H, Fujita N, Enoki T, . Relationship between variations in the circle of Willis and flow rates in internal carotid and basilar arteries determined by means of magnetic resonance imaging with semiautomated lumen segmentation: reference data from 125 healthy volunteers. AJNR Am J Neuroradiol. 2006;27(8):1770-1775.
[Google Scholar]

[14] Zarrinkoob L, Ambarki K, Wåhlin A, Birgander R, Eklund A, Malm J, . Blood flow distribution in cerebral arteries. J Cereb Blood Flow Metab. 2015;35(4):648-654.
[Google Scholar]

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Cerebral Artery Hypoplasia in a Select Adult Kenyan Population

Abstract

Abstract

Keywords

anterior

cerebral artery

hypoplasia

posterior

Introduction

Materials and Methods

Results

Discussion

General Remarks

Conclusion

Acknowledgments

Conflict of Interest

References

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