Neurosurg. Rev.
C.N.S.
Tumors in Eastern S a u d i Arabia
15 (1992) 295-302
Abdel Wahab M. Ibrahim D e p a r t m e n t o f Neurosurgery, College of Medicine and Medical Sciences, K i n g Faisal University, D a m m a m , Saudi A r a b i a
Abstract In Saudi Arabia, there were no attempts previously to describe a population based frequency or incidence, particularly so the age adjusted incidence of various CNS tumors. This paper presents the primary CNS tumors from a population based tumor registry over two years period, from January 1987 till December 1988. There was a total of 85 cases representing 5.4% of the total captured cases (1,568 cases of malignant tumors at all sites). The population of the Eastern Province is estimated to be 1.37 million, the Saudis forming 80% of the total population. Out of the 85 cases captured over two years, there were 64 cases diagnosed in indigenous Saudi population forming 75%. The remaining occurred in non-Saudi residents. The male/female ratio in Saudis was 1 : 1.1 with a slight predominance of the female, while the reverse is true in the non-Saudis (2 : 1). The total captured cases per annum is 43, making the incidence of primary CNS neoplasms in the Eastern Province of Saudi Arabia 3.1/100,000 of all the population and 29/100,000 in Saudi nationals. Comparing this incidence to the international figure, it was clear that it is far less than the incidence reported from North America and Europe, particularly in the Caucasian population, but similar to incidences reported in the Chinese, black Americans, Romanians and Yugoslavians, but certainly less than the Ashkenazi or Safari Jews, and slightly higher than the incidence reported in Japan and Southeast Asia. Malignant brain tumors of various types dominated the primary CNS neoplasms reported over these two years forming 69% of the cases and 52% of the primary brain tumors.
Keywords: Brain tumors, CNS tumors, epidemiology CNS rumors.
1 Introduction Until recently, reports dealing with frequency o f p r i m a r y neoplasm o f the central nervous system in Saudi A r a b i a were based on experience o f individual clinicians or institutions [2, 10, 15]. While providing variable descriptions o f the clinical lea9 1992 by Walter de Gruyter & Co. Berlin 9New York
tures, p a t h o l o g y and treatment o f these tumors, these earlier reports had no information on the incidence o f brain tumors in a well defined p o p ulation group. Moreover, such reports inevitably reflected a selection bias inherent in a clinic or hospital series. The following is a description o f the central nervous system (CNS) tumors from a p o p u l a t i o n based t u m o r registry in the Eastern Province (EP) over two year period, from January 1987 until December 1988. The d a t a represent an accurate reflection o f the true incidence of various C N S tumors in the Eastern Province. However, generalized influences extending to the whole p o p u l a t i o n of the K i n g d o m o f Saudi A r a b i a (KSA) must be viewed with great caution due to regional variations o f geographical, environmental, and ethnic factors. N e o p l a s m s of the nervous system are u n c o m m o n and unless observations are m a d e on large p o p u lations o f the order of several millions [3], individual rates m a y be liable to fluctuations due to chance alone. The figures however provide an insight to the p r o b l e m and m a y be a basis for future coverage o f the whole p o p u l a t i o n o f Saudi Arabia.
2 Material and method The Tumor Registry was established in the Eastern Province through a research grant from K i n g Abdulaziz City for Science and Technology ( K A C S T ) in 1985. Over the subsequent two years coverage was extended to involve the whole p o p u l a t i o n residing and present in the region. Only d a t a o f the cases registered since the registry became fully o p e r a t i o n a l was chosen for analysis. F r o m January 1987 to December 1988 (2 year period), there were 1568 cases o f cancer conforming with a well defined and internationally accepted r e p o r t a b l e
296
Ibrahim, C.N.S. Tumors in Eastern Saudi Arabia
list for tumors. The estimated total p o p u l a t i o n of the Eastern Province in the same period was 1,374,984. Breakdown by nationality, gender and age was obtained. A total of 85 p r i m a r y C N S tumors (brain ICD-0-191 and other C N S ICD-0192) were recorded. Analysis o f these cases and c o m p a r i s o n with other m a j o r epidemiological studies are presented here.
3
Results
A total o f 85 C N S tumors were registered over two years (Table I). This figure represents 5.4% o f 1568 tumors registered during the same period. The crude annual frequency rate is 2.7%. Out o f 85 cases, there were 64 tumors diagnosed in indig-
Table
enous Saudi p o p u l a t i o n forming 75%, the remaning occurred in n o n - S a u d i residents. P r i m a r y C N S (brain ICD-0-191) tumors accounted for 67 %. The incidence o f p r i m a r y brain t u m o r in Saudi p o p u lation o f the Eastern Province is: Saudi Males Saudi Females
1.99/100,000 2.0 /100,000
Incidence rate o f all central nervous system t u m o r s in Saudis is 2.9/100,000/year. The incidence rate o f brain t u m o r s (ICD-0-191) for various age groups is shown in table II a n d figure 1. The mean age is 33.3 (_+ 30 years) and the overall male-tofemale ratio is 1 : 1.07. The male-to-female ratio in Saudis is 1 : 1.1 and is non-significant while the reverse is true in the non-Saudis with p r e d o m i nance o f males affected 2 : I (P = 0.001).
I. Distrubition of brain tumors in the Eastern Province of Saudi Arabia over two years 1987-1988
I. Primary brain tumors ICD-0-191 (n = 57) Histological description
Saudi M
1. Gliomas: Astrocytoma GI-III Glioblastoma Oligodendroglioma 2. Medulloblastoma 3. Ependymoma 4. Ependymoblastoma 5. Haemangioma 6. Choroid plexus papilloma 7. Malignant lymph0ma 8. Neurofibrosarcoma 9. Undifferentiated malignant tumors Total
Total F
Non-Saudis
Total
M
F
4 6 2 3 1 1 1 0 2 0 2
8 5 1 3 1 0 0 2 0 1 1
12 11 3 6 2 1 1 2 2 1 3
5 2 2 1 0 0 1 0 0 0 0
0 1 1 0 0 0 0 0 0 0 0
5 3 3 1 0 0 1 0 0 0 0
22
22
44
11
2
13
Total
Non-Saudis
II. Other CNS tumors ICD-0-192 (n = 28) Histological description
Saudi M
1. Meningioma NOS Psammomatous meningioma Meningothelial meningioma Transitional meningioma Haemangiomatous meningioma 2. Neuroblastoma 3. Neurolemmoma Total
3 0 2
F
Total
M
F
8 0 3
11 0 5
2 1 0
3 1 0
1
1
0
1
1
0
1
0
0
-
l
0
1
0
0
-
1
0
1
0
0
-
8
12
20
3
5
-
5 2 1
8
Neurosurg. Rev. 15 (1992)
Ibrahim, C.N.S. Tumors in Eastern Saudi Arabia
297
Table II. Incidence of primary brain tumors ICD-0-191 in Saudis of Eastern Province Age group
Frequency
Population
Incidence rate
0- 5 5-i5 Total
Male
4 5 9
117512 151973 269485
1.70 1.64 1.67
0- 5 6-15 Total
Female
5 3 8
116837 149023 265860
2.13 1.00 1.50
0- 5 6-15 Total
Male & Female
9 8 17
234349 300996 535345
1.92 1.32 1.58
ICD-0-191 in Saudis 4 6 - 65 > 65 Total
Male
6 2 8
40010 16087 56097
7.49 6.21 7.13
4 6 - 65 > 65 Total
Female
1 0 1
36449 11324 47773
1.37 0.00 1.04
46-65 > 65 Total
Male & Female
7 2 9
76459 27411 103870
4.57 3.64 4.33
700
Population (Thousands)
600
400
5o8
Brain Tumors Case: 30 25 20
',2T26~5// .qa~.~
i!
15
~12
10 200 100
10
-'"
0 0 - 5 years "
129115~
Population
"--..~ 5 28525-5~'~ 0
r
I
~
6-15 years
16-45 years
4 6 - 6 5 years
- - I - Brain Tumor Cases
> 65
rears
Age Strata
Figure 1. Frequency of brain tumors as a function of the population of each age strata
In Saudis, neuroepithelial tumors (gliomas) were found to be the most c o m m o n tumors forming 52% o f the primary brain tumor. Forty-six percent of the gliomas were encountered in the 1 6 - 45 age Neurosurg. Rev. 15 (1992)
group and 32% presented after the age o f 46. The remaining 22% were diagnosed in the young > 15 years o f age (Table Ill).
298
Ibrahim, C.N.S. Tumors in Eastern Saudi Arabia
Table lII. Morphology of primary brain tumors (ICD-0-191) in Saudis from the Eastern Province 1987--1988 No.
Description
Morphology code
Frequency in age strata 0-5
6--15
1 6 - 4 5 46--65
>65
Total
1
Astrocytoma NOS Astrocytoma Anaplastic Total
94003 94013
2 0 2
0 0 0
11 0 11
4 I 5
0 0 0
17 1 18
2
Glioblastoma NOS Total
94403
0 0
2 2
2 2
5 5
0 0
9 9
3
Medulloblastoma NOS Desmoplastic medulloblastoma Total
94703 94713
3 1 4
3 0 3
0 0 0
0 0 0
0 0 0
6 1 7
4
Oligodendroglioma NOS Anaplastic oligodendroglioma Total
94503 94513
1 0 1
I 0 1
3 0 3
0 0 0
0 1 1
5 1 6
5
Glioma malignant Mixed glioma Total
93803 93823
1 0 1
1 0 1
1 1 2
0 0 0
0 0 0
3 1 4
6 7
Hemangioma NOS Choroid plexus papilloma NOS Choroid plexus papilloma malignant Ependymoma Neoplasm NOS Neoplasm malignant Malignant lymphoma Malignant ependymoma Neurofibrosarcoma
91200 93900 93903
0
I
0
1
0
2
1
0
1
0
0
2
93913 80001 80003 95903 93941 95403
1 0 0 0 0 0
0 1 0 1 0 0
1 1 0 1 1 1
0 0 0 0 0 0
0 0 1 0 0 0
2 2 1 2 1 1
10
10
24
11
2
57
8 9 10 11 12 13
Total
Meningiomas were second in frequency forming 28 % o f the C N S tumors. All o f the meningiomas presented after the age of 15 years. Fifty eight percent occurred in the age group 1 6 - 4 5 . The remaining 42% were in patients above 45 years (Table IV). 64% of all the meningioma were diagnosed in Saudis. Predominance o f females were noted in the entire affected sample with the maleto-female ratio 1 : 1.6 in non-Saudis rising up to 1 : 2 in Saudis [6, 7, 8, 9]. Incidence rate o f meningiomas/100,000 in: 1. Saudi (1.63) 2. N o n - S a u d i (2.9)
Male Female Male Female
1.08 2.18 1.67 5.21
9 M e d u l l o b l a s t o m a constituted 12% o f all brain tumors and was the c o m m o n e s t t u m o r diagnosed in children below the age o f 15 (31.8%). The
m a j o r i t y (85%) o f the m e d u l l o b l a s t o m a s occurred in Saudi children with a mean age o f 6 ( + 4) and a M : F ratio o f i : 1.
4 Discussion A c o m p a r i s o n to other annual age adjusted incidence rates of brain tumors in various geographical, environmental, and racial groups is shown in table V, which includes our figures for the Eastern Province o f Saudi A r a b i a [6, 7, 8, 9]. The populations, listed in alphabetical order for easy reference, are g r o u p e d according to m a j o r geographical regions a n d / o r racial similarities for a wide range o f distinct p o p u l a t i o n groups worldwide for 1958 to 1978. The corresponding p o p u lations at risk and the n u m b e r o f cases diagnosed during the study periods are also shown. The m a j o r i t y o f these p o p u l a t i o n groups h a d over one Neurosurg. Rev. 15 (1992)
Ibrahim, C.N.S. Tumors in Eastern Saudi Arabia
299
Table IV. Morphology of tumors (other nervous system ICD-0-192) in Saudis from the Eastern Province in 1987-- 1988 No.
1 2 3 4 5 6 7
Description
Meningioma NOS Psammomatous meningioma Meningotheliomatous meningioma Hemangioblastic meningioma Transitional meningioma Neuroblastoma Neurilemmoma
Morphology code 95300 95330 95310 95350 95370 95003 95600
Total
millic, n persons similar to the catchment population of the Eastern Province of Saudi Arabia. The incidence rate of primary nervous system tumors in Saudi Arabian indigenous population of the Eastern Province is 2.9/100,000/year close to the incidence reported in the Japanese Americans living in Hawaii, to the Hungarians populating the area of Miskolo, to the Hongkong population and to the Japanese in the Osaka district. It is quite close to the incidence in Czechoslovakians inhabiting Western Slovakia (2.8/100,000). Further comparison of this incidence in Saudis to the reported international figures, it shows that it is far less than the high incidence reported from Sweden (10/100,000), and Jews in Israel (8.5/100,000). The Caucasian Americans (LA 5.2/100,000), and Europeans (U. K.-Thames 6.6/100,000; Denmark 6.4/ 100,000; Finland 6.6/100,000; Germany-Saarland 6.5/100,000) occupy an intermedial group. The incidence gradually decreases in Chinese (Shanghai 3.8/100,000), Columbias (Cali 3.2/10,000), American blacks (LA 3.3/100,000) and American Chinese (LA 3/100,000). The incidence is lowest in Indians (Bombay 1.2/100,000; Singapore 1.7/ 100,000; Nigerians-Ibadan 1/100,000; South African blacks-Natal Province 1.6/100,000. It would appear that the incidence of primary nervous system tumors in Saudis is similar to the most developed countries of the Southeast Asia, Japan and certainly double that in African blacks but less than half the incidence in Europeans, white Americans and Jews. It is one-third to one-fourth the incidence in Askenazi Jews and Swedish who have the highest reported incidence of primary brain tumors in the world. It is worth noting that the U.S. whites had rates similar to those of the Canadians but the U.S. blacks and other racial Neurosurg. Rev. 15 (1992)
Frequency in age strata 0-5
6-15
16-45 46--65 >65
Total
0 0 0 0 0 1 0
0 0 0 0 0 0 1
11 2 0 0 2 0 0
4 0 4 1 0 0 0
1 0 1 0 0 0 0
16 2 5 1 2 1 1
1
1
15
9
2
28
groups in the USA had rates which were less than those of their white countrymen (different ethnic groups in the same geographic and environmental location) (Table V). Primary tumors of the nervous system ranked 9th of the top 10 sites of tumors affecting the population of the Eastern Province. It ranked even higher (7th) in Saudis only with slight predominance in Saudi females (rank 7 compared to rank 11 in Saudi males). The overall male to female ratio in Saudi population is 0.9, slightly different from the generally reported male dominated ratio when all primary tumors of the nervous system were considered regardless of the histological type. The geographical, ethnic and racial variations as well as the relative consistency of predominance in males persisted. Not only is there a marked geographical and racial variation in the incidence of primary malignant tumors of the nervous system but there are also intra-regional variations. Various ethnic or racial groups living in the same region had markedly different incidence rates. This is best illustrated by population groups in USA-Hawaii. There are also striking differences between three population groups (Jews born in Europe or America, all Jews and Jews born in Israel) who have the highest rates for primary malignant tumors of the nervous system in the world, 14.3, 10.7 and 9.5 per 100,000/ year respectively. In general, rates for most American whites and Canadians were similar to those for the UK, France, Germany, Australia and New Zealand. Incidence rates in the Nordic countries (Finland, Denmark, and Norway) were intermediate between the Askenazi Jews and the American whites but slightly higher than the rest of the
300
Ibrahim, C.N.S. Tumors in Eastern Saudi Arabia
Table V. Annual age adjusted incidence rate/100,000/year of primary CNS tumors in various geographical regions and racial groups (in alphabetical order) Country
Australia Canada China Columbia Czechoslovakia Denmark England Finland France Germany Hongkong Hungary India Israel
Japan Nigeria Norway Poland Saudi Arabia Singapore South Africa Sweden USA
Region
South Australia Alberta Shanghai Cali Western Slovakia Denmark Thames Finland Bas-Rhin Saarland Hongkong County Miskolc Bombay All Jews Born in Europe or America Born in Israel Osaka Ibadan Norway Cracow Eastern Province Chinese Notal (African) Sweden Hawaii (Japanese) LA (Blacks) LA (Chinese) LA (Japanese) LA (Spanish) LA (White)
Time period
No. of cases
Population in millions
Incidence rate
M :F Ratio
Male
Female Total
1977 1973-1977 1975 1972-1977 1973-1977 1973-1977 1973-1977 1971 - 1976 1975-- 1977 1973 - 1977 1974-1977 1962-1966 1964-1966 1972-1976 1960-1966
91 433 183 108 284 1434 2580 2053 118 385 414 24 136 1300 891
1.28 1.78 5.6 0.92 1.98 5.05 6.46 4.67 0.88 1.1 4.37 0.17 4.61 2.87 0.70
9.0 6.6 3.8 3.5 3.4 7.3 7.2 7.2 5.2 7.1 2.8 2.8 1.4 9.6 14.4
5.0 4.2 3.3 3.0 2.2 5.6 6.1 6.1 3.9 5.9 2.4 2.5 1.0 8.5 13.8
7.0 5.4 3.8 3.2 2.8 6.4 6.6 6.6 4.5 6.5 2.6 2.7 1.2 9.1 14.3
1:8 1:6 1:2 1:2 1:5 1:3 1:2 1:2 1:3 1:2 1:2 1:1 1 4 1 1 1 0
1960-1966 1973 - 1977 1960-1965 1973 - 1977 1973 - 1977 1987-1988 1973-1977 1964-1966 1971 - 1975 1973 - 1977 1972-1977 1972-1977 1972-1977 1972-1977 1972-1977
260 999 21 1747 264 85 125 16 4943 27 148 10 13 218 1641
0.83 8.28 0.63 4.00 0.68 1.09 1.68 0.4 8.14 0.24 0.91 0.07 0.12 1.13 4.94
8.3 2.9 1.1 8.6 8.1 1.99 1.6 1.9 10 2.1 4.1 3.8 2.7 4.1 6.1
10.6 2.4 0.8 7.3 7.8 2.0 1.7 1.3 9.9 2.2 2.8 2.4 1.4 3.6 4.4
9.5 2.7 1.0 7.9 7.8 2.0 1.7 1.6 10 2.1 3.3 3 2.1 3.8 5.2
0 8
European Caucasians. Most Asians residing in their homelands, US blacks, some Central European groups and South Americans had similar rates which were modestly higher than those for I n d i a n and African populations. The last groups had the lowest rates in the world. Of some curiosity is the finding that the incidence of brain tumors was similar in migrant and nonmigrant members of three racial groups for whom data were available. F o r example, most Japanese, Chinese, Indians residing outside their native countries had incidence rates close to these observed for the indigenous populations of Japan, China and India respectively. The incidence rates for US black living in different areas of the U S A
I I 1 1
2 4 2 0
0 9 0 9 1 I I 1 1 1
5 0 0 5 6 9
1 1 1 4
were generally lower than those for their white counterparts residing in the same region. N o analogy could be d r a w n from the incidence in nonSaudi p o p u l a t i o n in our Tumor Registry due to rapid m o v e m e n t and changes in the composition of this mixed ethnic groups and lack of accurate break down of ethnic origins. Nevertheless the comparison of our figures to those of the available international data does show that the inhabitants of the eastern part of the A r a b i a n Peninsula has relatively low incidence rates for primary tumors of the nervous system. I n general, the more socio-economically developed countries had higher average a n n u a l age adjusted incidence rates for both sexes than the less develNeurosurg. Rev. 15 (1992)
Ibrahim, C.N.S. Tumors in Eastern Saudi Arabia oped nations. Ethnic origin seems to be a major determining factor. Saudi Arabs have an incidence similar to the Japanese, H o n g k o n g Chinese and Central European ethnic groups but slightly higher than Africans, black Americans and lower than N o r t h Europeans, white Americans and considerably lower than the Askenazi Jews and Swedish. These findings, however, should be interpreted with caution in view of the small size of the studied population of the Eastern Province and the different durations of the study periods. Geographical variations in the incidence of primary CNS tumors may be a reflection o f differences, in the quality o f medical practice including the availability of medical facilities. Where good, well established medical facilities exist, e.g. Western countries, the incidence rates were not only higher than elsewhere but remained relatively stable or changed only little over the years. It is also well recognized that such countries have better organized registries for data collection and coding. These factors as well as possibly a higher autopsy rate accounts for the observed high incidence. Also high socio-economic levels invariably increase the elderly population with concomittent rise in neoplastic diseases. However, it is possible that genetic and environmental factors, including various occupational hazards may also contribute to the geographical variations in the incidence of primary tumors of the nervous system. That the Japanese, Chinese and Indians living outside their countries have similar incidence rates to those of their compatriots living in their home countries support the genetic hypothesis.
301 FAN et al in 1987 [5] analysed 16311 cases of confirmed C N S tumors from the Armed Forces Institute of Pathology and showed that gliomas were significantly more frequent in Caucasians than in blacks. In the same series, meningiomas and nerve sheath tumors were significally more frequent in blacks. Similar findings were reported from South Africa and Nigeria [11, 13]. The difference in the incidence rates between the two sexes in the specific cases of meningioma suggest that hormonal factors m a y be important in the etiology of at least some primary CNS tumors. Meningiomas have been reported also to enlarge during pregnancy [t2] and in some cases to be associated with breast Ca [14]. Estrogen receptors were even reported in some cases of intracranial meningioma [4]. This further strengthens the hormonal hypothesis. Whether or not there are any other specific hormonal abnormalities associated with other types of primary CNS tumors is still unknown. In conclusion, a low rate of primary CNS tumors is observed in the Arabs inhabiting the Eastern Province of Saudi Arabia. It is slightly higher than that reported for the Indian and African race but significantly lower than that o f the European and N o r t h American Caucasians. It is one-quarter to one-third of the incidence in Swedish or Jews. The observed differences in the incidence rates of primary CNS tumors among various population groups, races, and sexes may not be completely coincidental or a chance finding: they may suggest a possible role of environmental, genetic, and hormonal factors in the eiotology of these tumors.
References
[1] BAHEMUKAM: Worldwide incidence of primary [2]
[3]
[4] [5]
nervous system neoplasms. Brain 111 (1988) 737755 CHOWDHARYUM, AW IBRAHIM,M SOHIBANI,DH BOEHME:Experience with brain tumours in the Eastern Province of Saudi Arabia. Annals of Saudi Medicine 7 (1987) 166 DOL R, P COOKE: Summarising indices for comparison of cancer incidence data. International Journal of Cancer 2 (1967) 269-279 DONNELLMS, GA MYER,WL DONEGAN:Estrogenreceptors protein in intracranial meningiomas. Journal of Cancer 2 (1979) 269-279 FAN KJ, J KOVI,KM EARLS:The ethnic distribution of primary CNS tumors. Armed Forces Institute of Pathology 1958-1970. Journal of Neuropathology and Experimental Neurology 36 (1977) 4 1 - 4 9
Neurosurg. Rev. 15 (1992)
[6] International Union Against Cancer: Cancer Incidence in Five Continents, Volume i, A Technical Report. DOLL R, P PAYNE, J WATERHOUSE(eds), Berlin, Springer, 1966 [7] International Union Against Cancer: Cancer Incidence in Five Continents, Volume 2. DOLL R, C MUIR, JAH WATERHOUSE(eds), Geneva: UICC (International Union Against Cancer) 1970 [8] International Agency for Research on Cancer: Cancer Incidence in Five Continents, Volume 3. IARC Scientific Publications No. 15. WATERHOUSEJ, C MUIR, P CORREA,J POWELL(eds), Lyon, IARC 1975 [9] International Agency for Research on Cancer: Cancer Incidence in Five Continents, Volume 4. IARC Scientific Publication No. 42. WATERHOUSEJ, C MUIR, K SHANMUGARATNAM,J POWELL(eds), Lyon, IARC 1982
302 [10] JAMJOOMZ, T MALABAREY, S SADIQ et al: Intracranial meningiomas: Analysis of 53 consecutive cases. Annals of Saudi Medicine 10 (1990) 3012 [11] LEIBOWlTZU, M YABLONSKI,M ALTER: Tumours of the nervous system - Incidence and population selectivity. J Chronic Diseases 4 (1971) 3 9 3 - 397 [12] MITCHELSENJJ, PFJ NEW: Brain tumours and pregnancy. J Neurology, Neurosurgery & Psychiatry 32 (1969) 3 0 5 - 307 [13] ODEKU EL, A ADELOYE,BO OSUNTOKUN et al: Intracranial tumour pattern in Abadan, Nigeria. African Journal of Medical Sciences 4 (1973) 1 3 7 141
Ibrahim, C.N.S. Tumors in Eastern Saudi Arabia [14] SCHOENBERG BS, CHRISTINE BW, WHISNANT JP: Nervous system neoplasms and primary malignancies of other sites - The unique association between meningiomas and breast cancer. Neurology Minneapolis 25 (1975) 705-712 [15] SlQUEIRAE: Neurosurgical diseases at King Faisal Specialist Hospital and Research Center. Annals of Saudi Medicine 8 (1988) 153-154 Submitted August 9, 1991. Accepted October 23, 1991. Dr. Abdel Wahab M. Ibrahim Associate Professor Department of Neurosurgery College of Medicine and Medical Sciences King Faisal University R O. Box 2114 Dammam 31451 Saudi Arabia
Neurosurg. Rev. 15 (1992)
C.N.S.
Tumors in Eastern S a u d i Arabia
15 (1992) 295-302
Abdel Wahab M. Ibrahim D e p a r t m e n t o f Neurosurgery, College of Medicine and Medical Sciences, K i n g Faisal University, D a m m a m , Saudi A r a b i a
Abstract In Saudi Arabia, there were no attempts previously to describe a population based frequency or incidence, particularly so the age adjusted incidence of various CNS tumors. This paper presents the primary CNS tumors from a population based tumor registry over two years period, from January 1987 till December 1988. There was a total of 85 cases representing 5.4% of the total captured cases (1,568 cases of malignant tumors at all sites). The population of the Eastern Province is estimated to be 1.37 million, the Saudis forming 80% of the total population. Out of the 85 cases captured over two years, there were 64 cases diagnosed in indigenous Saudi population forming 75%. The remaining occurred in non-Saudi residents. The male/female ratio in Saudis was 1 : 1.1 with a slight predominance of the female, while the reverse is true in the non-Saudis (2 : 1). The total captured cases per annum is 43, making the incidence of primary CNS neoplasms in the Eastern Province of Saudi Arabia 3.1/100,000 of all the population and 29/100,000 in Saudi nationals. Comparing this incidence to the international figure, it was clear that it is far less than the incidence reported from North America and Europe, particularly in the Caucasian population, but similar to incidences reported in the Chinese, black Americans, Romanians and Yugoslavians, but certainly less than the Ashkenazi or Safari Jews, and slightly higher than the incidence reported in Japan and Southeast Asia. Malignant brain tumors of various types dominated the primary CNS neoplasms reported over these two years forming 69% of the cases and 52% of the primary brain tumors.
Keywords: Brain tumors, CNS tumors, epidemiology CNS rumors.
1 Introduction Until recently, reports dealing with frequency o f p r i m a r y neoplasm o f the central nervous system in Saudi A r a b i a were based on experience o f individual clinicians or institutions [2, 10, 15]. While providing variable descriptions o f the clinical lea9 1992 by Walter de Gruyter & Co. Berlin 9New York
tures, p a t h o l o g y and treatment o f these tumors, these earlier reports had no information on the incidence o f brain tumors in a well defined p o p ulation group. Moreover, such reports inevitably reflected a selection bias inherent in a clinic or hospital series. The following is a description o f the central nervous system (CNS) tumors from a p o p u l a t i o n based t u m o r registry in the Eastern Province (EP) over two year period, from January 1987 until December 1988. The d a t a represent an accurate reflection o f the true incidence of various C N S tumors in the Eastern Province. However, generalized influences extending to the whole p o p u l a t i o n of the K i n g d o m o f Saudi A r a b i a (KSA) must be viewed with great caution due to regional variations o f geographical, environmental, and ethnic factors. N e o p l a s m s of the nervous system are u n c o m m o n and unless observations are m a d e on large p o p u lations o f the order of several millions [3], individual rates m a y be liable to fluctuations due to chance alone. The figures however provide an insight to the p r o b l e m and m a y be a basis for future coverage o f the whole p o p u l a t i o n o f Saudi Arabia.
2 Material and method The Tumor Registry was established in the Eastern Province through a research grant from K i n g Abdulaziz City for Science and Technology ( K A C S T ) in 1985. Over the subsequent two years coverage was extended to involve the whole p o p u l a t i o n residing and present in the region. Only d a t a o f the cases registered since the registry became fully o p e r a t i o n a l was chosen for analysis. F r o m January 1987 to December 1988 (2 year period), there were 1568 cases o f cancer conforming with a well defined and internationally accepted r e p o r t a b l e
296
Ibrahim, C.N.S. Tumors in Eastern Saudi Arabia
list for tumors. The estimated total p o p u l a t i o n of the Eastern Province in the same period was 1,374,984. Breakdown by nationality, gender and age was obtained. A total of 85 p r i m a r y C N S tumors (brain ICD-0-191 and other C N S ICD-0192) were recorded. Analysis o f these cases and c o m p a r i s o n with other m a j o r epidemiological studies are presented here.
3
Results
A total o f 85 C N S tumors were registered over two years (Table I). This figure represents 5.4% o f 1568 tumors registered during the same period. The crude annual frequency rate is 2.7%. Out o f 85 cases, there were 64 tumors diagnosed in indig-
Table
enous Saudi p o p u l a t i o n forming 75%, the remaning occurred in n o n - S a u d i residents. P r i m a r y C N S (brain ICD-0-191) tumors accounted for 67 %. The incidence o f p r i m a r y brain t u m o r in Saudi p o p u lation o f the Eastern Province is: Saudi Males Saudi Females
1.99/100,000 2.0 /100,000
Incidence rate o f all central nervous system t u m o r s in Saudis is 2.9/100,000/year. The incidence rate o f brain t u m o r s (ICD-0-191) for various age groups is shown in table II a n d figure 1. The mean age is 33.3 (_+ 30 years) and the overall male-tofemale ratio is 1 : 1.07. The male-to-female ratio in Saudis is 1 : 1.1 and is non-significant while the reverse is true in the non-Saudis with p r e d o m i nance o f males affected 2 : I (P = 0.001).
I. Distrubition of brain tumors in the Eastern Province of Saudi Arabia over two years 1987-1988
I. Primary brain tumors ICD-0-191 (n = 57) Histological description
Saudi M
1. Gliomas: Astrocytoma GI-III Glioblastoma Oligodendroglioma 2. Medulloblastoma 3. Ependymoma 4. Ependymoblastoma 5. Haemangioma 6. Choroid plexus papilloma 7. Malignant lymph0ma 8. Neurofibrosarcoma 9. Undifferentiated malignant tumors Total
Total F
Non-Saudis
Total
M
F
4 6 2 3 1 1 1 0 2 0 2
8 5 1 3 1 0 0 2 0 1 1
12 11 3 6 2 1 1 2 2 1 3
5 2 2 1 0 0 1 0 0 0 0
0 1 1 0 0 0 0 0 0 0 0
5 3 3 1 0 0 1 0 0 0 0
22
22
44
11
2
13
Total
Non-Saudis
II. Other CNS tumors ICD-0-192 (n = 28) Histological description
Saudi M
1. Meningioma NOS Psammomatous meningioma Meningothelial meningioma Transitional meningioma Haemangiomatous meningioma 2. Neuroblastoma 3. Neurolemmoma Total
3 0 2
F
Total
M
F
8 0 3
11 0 5
2 1 0
3 1 0
1
1
0
1
1
0
1
0
0
-
l
0
1
0
0
-
1
0
1
0
0
-
8
12
20
3
5
-
5 2 1
8
Neurosurg. Rev. 15 (1992)
Ibrahim, C.N.S. Tumors in Eastern Saudi Arabia
297
Table II. Incidence of primary brain tumors ICD-0-191 in Saudis of Eastern Province Age group
Frequency
Population
Incidence rate
0- 5 5-i5 Total
Male
4 5 9
117512 151973 269485
1.70 1.64 1.67
0- 5 6-15 Total
Female
5 3 8
116837 149023 265860
2.13 1.00 1.50
0- 5 6-15 Total
Male & Female
9 8 17
234349 300996 535345
1.92 1.32 1.58
ICD-0-191 in Saudis 4 6 - 65 > 65 Total
Male
6 2 8
40010 16087 56097
7.49 6.21 7.13
4 6 - 65 > 65 Total
Female
1 0 1
36449 11324 47773
1.37 0.00 1.04
46-65 > 65 Total
Male & Female
7 2 9
76459 27411 103870
4.57 3.64 4.33
700
Population (Thousands)
600
400
5o8
Brain Tumors Case: 30 25 20
',2T26~5// .qa~.~
i!
15
~12
10 200 100
10
-'"
0 0 - 5 years "
129115~
Population
"--..~ 5 28525-5~'~ 0
r
I
~
6-15 years
16-45 years
4 6 - 6 5 years
- - I - Brain Tumor Cases
> 65
rears
Age Strata
Figure 1. Frequency of brain tumors as a function of the population of each age strata
In Saudis, neuroepithelial tumors (gliomas) were found to be the most c o m m o n tumors forming 52% o f the primary brain tumor. Forty-six percent of the gliomas were encountered in the 1 6 - 45 age Neurosurg. Rev. 15 (1992)
group and 32% presented after the age o f 46. The remaining 22% were diagnosed in the young > 15 years o f age (Table Ill).
298
Ibrahim, C.N.S. Tumors in Eastern Saudi Arabia
Table lII. Morphology of primary brain tumors (ICD-0-191) in Saudis from the Eastern Province 1987--1988 No.
Description
Morphology code
Frequency in age strata 0-5
6--15
1 6 - 4 5 46--65
>65
Total
1
Astrocytoma NOS Astrocytoma Anaplastic Total
94003 94013
2 0 2
0 0 0
11 0 11
4 I 5
0 0 0
17 1 18
2
Glioblastoma NOS Total
94403
0 0
2 2
2 2
5 5
0 0
9 9
3
Medulloblastoma NOS Desmoplastic medulloblastoma Total
94703 94713
3 1 4
3 0 3
0 0 0
0 0 0
0 0 0
6 1 7
4
Oligodendroglioma NOS Anaplastic oligodendroglioma Total
94503 94513
1 0 1
I 0 1
3 0 3
0 0 0
0 1 1
5 1 6
5
Glioma malignant Mixed glioma Total
93803 93823
1 0 1
1 0 1
1 1 2
0 0 0
0 0 0
3 1 4
6 7
Hemangioma NOS Choroid plexus papilloma NOS Choroid plexus papilloma malignant Ependymoma Neoplasm NOS Neoplasm malignant Malignant lymphoma Malignant ependymoma Neurofibrosarcoma
91200 93900 93903
0
I
0
1
0
2
1
0
1
0
0
2
93913 80001 80003 95903 93941 95403
1 0 0 0 0 0
0 1 0 1 0 0
1 1 0 1 1 1
0 0 0 0 0 0
0 0 1 0 0 0
2 2 1 2 1 1
10
10
24
11
2
57
8 9 10 11 12 13
Total
Meningiomas were second in frequency forming 28 % o f the C N S tumors. All o f the meningiomas presented after the age of 15 years. Fifty eight percent occurred in the age group 1 6 - 4 5 . The remaining 42% were in patients above 45 years (Table IV). 64% of all the meningioma were diagnosed in Saudis. Predominance o f females were noted in the entire affected sample with the maleto-female ratio 1 : 1.6 in non-Saudis rising up to 1 : 2 in Saudis [6, 7, 8, 9]. Incidence rate o f meningiomas/100,000 in: 1. Saudi (1.63) 2. N o n - S a u d i (2.9)
Male Female Male Female
1.08 2.18 1.67 5.21
9 M e d u l l o b l a s t o m a constituted 12% o f all brain tumors and was the c o m m o n e s t t u m o r diagnosed in children below the age o f 15 (31.8%). The
m a j o r i t y (85%) o f the m e d u l l o b l a s t o m a s occurred in Saudi children with a mean age o f 6 ( + 4) and a M : F ratio o f i : 1.
4 Discussion A c o m p a r i s o n to other annual age adjusted incidence rates of brain tumors in various geographical, environmental, and racial groups is shown in table V, which includes our figures for the Eastern Province o f Saudi A r a b i a [6, 7, 8, 9]. The populations, listed in alphabetical order for easy reference, are g r o u p e d according to m a j o r geographical regions a n d / o r racial similarities for a wide range o f distinct p o p u l a t i o n groups worldwide for 1958 to 1978. The corresponding p o p u lations at risk and the n u m b e r o f cases diagnosed during the study periods are also shown. The m a j o r i t y o f these p o p u l a t i o n groups h a d over one Neurosurg. Rev. 15 (1992)
Ibrahim, C.N.S. Tumors in Eastern Saudi Arabia
299
Table IV. Morphology of tumors (other nervous system ICD-0-192) in Saudis from the Eastern Province in 1987-- 1988 No.
1 2 3 4 5 6 7
Description
Meningioma NOS Psammomatous meningioma Meningotheliomatous meningioma Hemangioblastic meningioma Transitional meningioma Neuroblastoma Neurilemmoma
Morphology code 95300 95330 95310 95350 95370 95003 95600
Total
millic, n persons similar to the catchment population of the Eastern Province of Saudi Arabia. The incidence rate of primary nervous system tumors in Saudi Arabian indigenous population of the Eastern Province is 2.9/100,000/year close to the incidence reported in the Japanese Americans living in Hawaii, to the Hungarians populating the area of Miskolo, to the Hongkong population and to the Japanese in the Osaka district. It is quite close to the incidence in Czechoslovakians inhabiting Western Slovakia (2.8/100,000). Further comparison of this incidence in Saudis to the reported international figures, it shows that it is far less than the high incidence reported from Sweden (10/100,000), and Jews in Israel (8.5/100,000). The Caucasian Americans (LA 5.2/100,000), and Europeans (U. K.-Thames 6.6/100,000; Denmark 6.4/ 100,000; Finland 6.6/100,000; Germany-Saarland 6.5/100,000) occupy an intermedial group. The incidence gradually decreases in Chinese (Shanghai 3.8/100,000), Columbias (Cali 3.2/10,000), American blacks (LA 3.3/100,000) and American Chinese (LA 3/100,000). The incidence is lowest in Indians (Bombay 1.2/100,000; Singapore 1.7/ 100,000; Nigerians-Ibadan 1/100,000; South African blacks-Natal Province 1.6/100,000. It would appear that the incidence of primary nervous system tumors in Saudis is similar to the most developed countries of the Southeast Asia, Japan and certainly double that in African blacks but less than half the incidence in Europeans, white Americans and Jews. It is one-third to one-fourth the incidence in Askenazi Jews and Swedish who have the highest reported incidence of primary brain tumors in the world. It is worth noting that the U.S. whites had rates similar to those of the Canadians but the U.S. blacks and other racial Neurosurg. Rev. 15 (1992)
Frequency in age strata 0-5
6-15
16-45 46--65 >65
Total
0 0 0 0 0 1 0
0 0 0 0 0 0 1
11 2 0 0 2 0 0
4 0 4 1 0 0 0
1 0 1 0 0 0 0
16 2 5 1 2 1 1
1
1
15
9
2
28
groups in the USA had rates which were less than those of their white countrymen (different ethnic groups in the same geographic and environmental location) (Table V). Primary tumors of the nervous system ranked 9th of the top 10 sites of tumors affecting the population of the Eastern Province. It ranked even higher (7th) in Saudis only with slight predominance in Saudi females (rank 7 compared to rank 11 in Saudi males). The overall male to female ratio in Saudi population is 0.9, slightly different from the generally reported male dominated ratio when all primary tumors of the nervous system were considered regardless of the histological type. The geographical, ethnic and racial variations as well as the relative consistency of predominance in males persisted. Not only is there a marked geographical and racial variation in the incidence of primary malignant tumors of the nervous system but there are also intra-regional variations. Various ethnic or racial groups living in the same region had markedly different incidence rates. This is best illustrated by population groups in USA-Hawaii. There are also striking differences between three population groups (Jews born in Europe or America, all Jews and Jews born in Israel) who have the highest rates for primary malignant tumors of the nervous system in the world, 14.3, 10.7 and 9.5 per 100,000/ year respectively. In general, rates for most American whites and Canadians were similar to those for the UK, France, Germany, Australia and New Zealand. Incidence rates in the Nordic countries (Finland, Denmark, and Norway) were intermediate between the Askenazi Jews and the American whites but slightly higher than the rest of the
300
Ibrahim, C.N.S. Tumors in Eastern Saudi Arabia
Table V. Annual age adjusted incidence rate/100,000/year of primary CNS tumors in various geographical regions and racial groups (in alphabetical order) Country
Australia Canada China Columbia Czechoslovakia Denmark England Finland France Germany Hongkong Hungary India Israel
Japan Nigeria Norway Poland Saudi Arabia Singapore South Africa Sweden USA
Region
South Australia Alberta Shanghai Cali Western Slovakia Denmark Thames Finland Bas-Rhin Saarland Hongkong County Miskolc Bombay All Jews Born in Europe or America Born in Israel Osaka Ibadan Norway Cracow Eastern Province Chinese Notal (African) Sweden Hawaii (Japanese) LA (Blacks) LA (Chinese) LA (Japanese) LA (Spanish) LA (White)
Time period
No. of cases
Population in millions
Incidence rate
M :F Ratio
Male
Female Total
1977 1973-1977 1975 1972-1977 1973-1977 1973-1977 1973-1977 1971 - 1976 1975-- 1977 1973 - 1977 1974-1977 1962-1966 1964-1966 1972-1976 1960-1966
91 433 183 108 284 1434 2580 2053 118 385 414 24 136 1300 891
1.28 1.78 5.6 0.92 1.98 5.05 6.46 4.67 0.88 1.1 4.37 0.17 4.61 2.87 0.70
9.0 6.6 3.8 3.5 3.4 7.3 7.2 7.2 5.2 7.1 2.8 2.8 1.4 9.6 14.4
5.0 4.2 3.3 3.0 2.2 5.6 6.1 6.1 3.9 5.9 2.4 2.5 1.0 8.5 13.8
7.0 5.4 3.8 3.2 2.8 6.4 6.6 6.6 4.5 6.5 2.6 2.7 1.2 9.1 14.3
1:8 1:6 1:2 1:2 1:5 1:3 1:2 1:2 1:3 1:2 1:2 1:1 1 4 1 1 1 0
1960-1966 1973 - 1977 1960-1965 1973 - 1977 1973 - 1977 1987-1988 1973-1977 1964-1966 1971 - 1975 1973 - 1977 1972-1977 1972-1977 1972-1977 1972-1977 1972-1977
260 999 21 1747 264 85 125 16 4943 27 148 10 13 218 1641
0.83 8.28 0.63 4.00 0.68 1.09 1.68 0.4 8.14 0.24 0.91 0.07 0.12 1.13 4.94
8.3 2.9 1.1 8.6 8.1 1.99 1.6 1.9 10 2.1 4.1 3.8 2.7 4.1 6.1
10.6 2.4 0.8 7.3 7.8 2.0 1.7 1.3 9.9 2.2 2.8 2.4 1.4 3.6 4.4
9.5 2.7 1.0 7.9 7.8 2.0 1.7 1.6 10 2.1 3.3 3 2.1 3.8 5.2
0 8
European Caucasians. Most Asians residing in their homelands, US blacks, some Central European groups and South Americans had similar rates which were modestly higher than those for I n d i a n and African populations. The last groups had the lowest rates in the world. Of some curiosity is the finding that the incidence of brain tumors was similar in migrant and nonmigrant members of three racial groups for whom data were available. F o r example, most Japanese, Chinese, Indians residing outside their native countries had incidence rates close to these observed for the indigenous populations of Japan, China and India respectively. The incidence rates for US black living in different areas of the U S A
I I 1 1
2 4 2 0
0 9 0 9 1 I I 1 1 1
5 0 0 5 6 9
1 1 1 4
were generally lower than those for their white counterparts residing in the same region. N o analogy could be d r a w n from the incidence in nonSaudi p o p u l a t i o n in our Tumor Registry due to rapid m o v e m e n t and changes in the composition of this mixed ethnic groups and lack of accurate break down of ethnic origins. Nevertheless the comparison of our figures to those of the available international data does show that the inhabitants of the eastern part of the A r a b i a n Peninsula has relatively low incidence rates for primary tumors of the nervous system. I n general, the more socio-economically developed countries had higher average a n n u a l age adjusted incidence rates for both sexes than the less develNeurosurg. Rev. 15 (1992)
Ibrahim, C.N.S. Tumors in Eastern Saudi Arabia oped nations. Ethnic origin seems to be a major determining factor. Saudi Arabs have an incidence similar to the Japanese, H o n g k o n g Chinese and Central European ethnic groups but slightly higher than Africans, black Americans and lower than N o r t h Europeans, white Americans and considerably lower than the Askenazi Jews and Swedish. These findings, however, should be interpreted with caution in view of the small size of the studied population of the Eastern Province and the different durations of the study periods. Geographical variations in the incidence of primary CNS tumors may be a reflection o f differences, in the quality o f medical practice including the availability of medical facilities. Where good, well established medical facilities exist, e.g. Western countries, the incidence rates were not only higher than elsewhere but remained relatively stable or changed only little over the years. It is also well recognized that such countries have better organized registries for data collection and coding. These factors as well as possibly a higher autopsy rate accounts for the observed high incidence. Also high socio-economic levels invariably increase the elderly population with concomittent rise in neoplastic diseases. However, it is possible that genetic and environmental factors, including various occupational hazards may also contribute to the geographical variations in the incidence of primary tumors of the nervous system. That the Japanese, Chinese and Indians living outside their countries have similar incidence rates to those of their compatriots living in their home countries support the genetic hypothesis.
301 FAN et al in 1987 [5] analysed 16311 cases of confirmed C N S tumors from the Armed Forces Institute of Pathology and showed that gliomas were significantly more frequent in Caucasians than in blacks. In the same series, meningiomas and nerve sheath tumors were significally more frequent in blacks. Similar findings were reported from South Africa and Nigeria [11, 13]. The difference in the incidence rates between the two sexes in the specific cases of meningioma suggest that hormonal factors m a y be important in the etiology of at least some primary CNS tumors. Meningiomas have been reported also to enlarge during pregnancy [t2] and in some cases to be associated with breast Ca [14]. Estrogen receptors were even reported in some cases of intracranial meningioma [4]. This further strengthens the hormonal hypothesis. Whether or not there are any other specific hormonal abnormalities associated with other types of primary CNS tumors is still unknown. In conclusion, a low rate of primary CNS tumors is observed in the Arabs inhabiting the Eastern Province of Saudi Arabia. It is slightly higher than that reported for the Indian and African race but significantly lower than that o f the European and N o r t h American Caucasians. It is one-quarter to one-third of the incidence in Swedish or Jews. The observed differences in the incidence rates of primary CNS tumors among various population groups, races, and sexes may not be completely coincidental or a chance finding: they may suggest a possible role of environmental, genetic, and hormonal factors in the eiotology of these tumors.
References
[1] BAHEMUKAM: Worldwide incidence of primary [2]
[3]
[4] [5]
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Neurosurg. Rev. 15 (1992)
[6] International Union Against Cancer: Cancer Incidence in Five Continents, Volume i, A Technical Report. DOLL R, P PAYNE, J WATERHOUSE(eds), Berlin, Springer, 1966 [7] International Union Against Cancer: Cancer Incidence in Five Continents, Volume 2. DOLL R, C MUIR, JAH WATERHOUSE(eds), Geneva: UICC (International Union Against Cancer) 1970 [8] International Agency for Research on Cancer: Cancer Incidence in Five Continents, Volume 3. IARC Scientific Publications No. 15. WATERHOUSEJ, C MUIR, P CORREA,J POWELL(eds), Lyon, IARC 1975 [9] International Agency for Research on Cancer: Cancer Incidence in Five Continents, Volume 4. IARC Scientific Publication No. 42. WATERHOUSEJ, C MUIR, K SHANMUGARATNAM,J POWELL(eds), Lyon, IARC 1982
302 [10] JAMJOOMZ, T MALABAREY, S SADIQ et al: Intracranial meningiomas: Analysis of 53 consecutive cases. Annals of Saudi Medicine 10 (1990) 3012 [11] LEIBOWlTZU, M YABLONSKI,M ALTER: Tumours of the nervous system - Incidence and population selectivity. J Chronic Diseases 4 (1971) 3 9 3 - 397 [12] MITCHELSENJJ, PFJ NEW: Brain tumours and pregnancy. J Neurology, Neurosurgery & Psychiatry 32 (1969) 3 0 5 - 307 [13] ODEKU EL, A ADELOYE,BO OSUNTOKUN et al: Intracranial tumour pattern in Abadan, Nigeria. African Journal of Medical Sciences 4 (1973) 1 3 7 141
Ibrahim, C.N.S. Tumors in Eastern Saudi Arabia [14] SCHOENBERG BS, CHRISTINE BW, WHISNANT JP: Nervous system neoplasms and primary malignancies of other sites - The unique association between meningiomas and breast cancer. Neurology Minneapolis 25 (1975) 705-712 [15] SlQUEIRAE: Neurosurgical diseases at King Faisal Specialist Hospital and Research Center. Annals of Saudi Medicine 8 (1988) 153-154 Submitted August 9, 1991. Accepted October 23, 1991. Dr. Abdel Wahab M. Ibrahim Associate Professor Department of Neurosurgery College of Medicine and Medical Sciences King Faisal University R O. Box 2114 Dammam 31451 Saudi Arabia
Neurosurg. Rev. 15 (1992)
