- Email: [email protected]
Microfilaruria in an Area of Nigeria with Hyperendemic Onchocerciasis
Zbl. Bakt. 285, 86-91 (1995) © Gustav Fischer Verlag, Stuttgart· Jena . New York
Microfilaruria in an Area of Nigeria with Hyperendemic Onchocerciasis O.B. AKOGUN 1 and K. TEMB0 2 1 Parasite
and Tropical Health Research, Department of Biological Sciences, Federal University of Technology, Yola, Nigeria 2 Public Health Program, Polytechnic University of Malawi, Blantyre, Malawi
Received April 28, 1995 . Revision received August 11, 1995 . Accepted October 5, 1995
Summary Urine samples collected from sixty-four Nigerians living in a community which is hyperendemic for onchocerciasis were examined for microfilaria. Each urine donor was examined for the physical symptoms of long-standing onchocerciasis. The microfilaruria rate was 23.4%. Males had a higher rate of microfilaruria (27.5%) than females (16.7%). The prevalence rates of leopard skin and nodules were 18.8% and 46.9%, respectively. Thirteen persons had microfilaruria and had nodules. Seventeen showed no microfilaruria but had nodules. Only two of those without nodules were without microfilaruria. A very strong association was found between nodule-possession, nodule-load and microfilaruria (coefficient of association 0.85). Nodule load seemed to be the major factor in having microfilaria in urine. Microfilaruria is not common in Nigeria and the present finding is the first report of microfilaruria in the Taraba river valley which is a continuous onchocerciasis zone with the Western Cameroun - Southern Chad focus of transmission where microfilaruria has been reported. This paper discusses the implications of the results of this investigation with respect to monitoring the impact of ivermectin distribution in the Taraba river valley of Nigeria.
Introduction There are sporadic reports of the occurrence of microfilaruria in many parts of the world where onchocerciasis is endemic (Dyce-Sharp, 1926; Mazzotti and Ososrio 1949; Buck et ai., 1969; 1971; Buck, 1973; Fazen et ai.; Fazen et ai., 1975). By far the most comprehensive of these studies is probably that carried out by Anderson et al. (1974) in parts of the Adamaoua Plateau of Cameroun which is an onchocerciasis focus continuous with the Taraba-Dakka-Ganye-Chad Republic zone. Buck et al. (1971) recorded an 11.4% microfilaruria rate when 386 persons were examined in Ouli Bangala, Chad Republic while Anderson et al. (1974) recorded 4.7% in Baoussi, Cameroun Republic. These studies reported an association between the community microfilaruria rate and most of the typical onchocerciasis symptoms, espe-
Microfilaruria in an Area of Nigeria with Hyperendemic Onchocerciasis
87
cially micro filariae in skin, nodules and leopard skin, irrespective of age and sex. The two reports firmly established that the presence and number of microfilaruria cases is a reflection of the intensity of the community microfilaria load. Akogun and Onwuliri (1991) reported that the previously unprospected Taraba river valley could be one of the most important onchocerciasis foci in West Africa, with very severe ocular problems among the infected population. There are many similarities in the epidemiology of onchocerciasis in Southern Chad, the Adamoua Plateau of Cameroun and the Taraba river valley of Nigeria. Important differences may also exist as a result of variations in the local strain Onchocerca volvulus or the vector species or the biting behaviour of the latter. It could be interesting to find out if the presence of microfilaruria could be used for monitoring the effectiveness of ivermectin. The present study is a preliminary baseline investigation of the pretreatment occurrence or absence of microfilaruria in an area with hyperendemic onchocerciasis. Materials and Methods Two clusters which constitute the Nyubango and Agbakom communities in the Gayam area of Gashaka district (11 °30'-11°43'E; 70 10'-8°15'N) of the Taraba river valley were studied. The Gayam area is reported to be a hyperendemic area with about 80% 0 volvulus positivity rate among 426 persons aged 5 years and older (Akogun and Onwuliri, 1991). The households were randomly selected (six from Nyubango and four from Agbakom) and a census of the number of residents in each household taken. No member of these isolated communities had ever taken either ivermectin, diethlyl-carbamazine (DEC), or suramin sodium. One container was given to each family member with instructions to bring a sample of urine when reporting for physical examination. The individuals were examined for physical onchocerciasis symptoms. The name, age, sex and urine specimen number were recorded on a specially designed epidemiological form. The results of the physical examination were also recorded against the individual's name. Particular attention was given to the presence and number of nodules, leopard skin and lizard skin. Urine samples were preserved in methioate formalin in the field. In the laboratory, 10 mL volumes of urine each were centrifuged at 1500 rpm for fifteen minutes to obtain a sediment which was examined for microfilaria under a microscope with an x40 objective. The length of each microfilaria specimen was measured, and the head and tail and examined for enlargement and nuclei respectively. Microfilaria of o. volvulus were longer than 240 [!m, had an enlarged head end and had no nuclei at the tail end. 0
Results Sixty-four individuals (40 males and 24 females) were examined. The rate of microfilaruria was 23.4% (27.5% in males and 16.7% in females). The prevalence of nodules, leopard and lizard skin was 46.9%, 18.8% and 29.7%, respectively (Table 1). The prevalence of Schistosoma haematobium was low (7, 8). There were no cases of microfilaruria in individuals below 20 years of age. However, the prevalence of microfilaria-positive urine was similar in all age groups between 20 and 49 years (28.6% to 33.3 %) but dropped to a low level (20.0%) in persons that were 50 years or older. Microfilaruria was recorded only in females between 20-29 years (50.0%) and 30-39 years (33.35%). In males, the rate of microfilaruria increased with age from 20 years (20.0%) until 49 years (60.0%) when it dropped to 28.6%
O. B. Akogun and K. Tembo
88
Table 1. Age-specific prevalence of microfilaruria and physical symptoms of onchocerciasis Male Age (Years)
No. Exam.
< 10
4 3 5 16 5 7
0 0 1 5 2 2
0 2 2 1 2 2
0 0 2 5 2 2
0 0 2 6 2 2
0 1 1 2 0 0
40
11
19
9
12
4
3 3 2 9 4 3
0 0 1 3 0 0
0 1 2 4 1 3
0 0 0 2 1 0
0 0 1 3 3 0
0 0 0 1 0 0
24
4
11
3
7
1
7 6 7 25 9 10
0 0 2 8 3 2
0 3 4 15 3 5
0 0 0 7 3 2
0 0 3 9 5 2
0 1 1 3 0 0
64
15
30
12
19
5
:2:
10-19 20-29 30-39 40-49 50
Total
Mf+ Urine
Nod. + ve
Leopard Skin
Lizard Skin
S. haem.
Female
< 10
:2:
10-19 20-29 30-29 40-49 50
Total Total
< 10
:2:
10-19 20-29 30-39 40-49 50
Total
Mf + =Microfilaria positive, Nod. + ve matobium.
=Nodules positive, S. haem. =Schistosoma hae-
among males that were 50 years or older. Both leopard skin and lizard skin increased in prevalence with increase in age. The intensity of microfilaruria and nodule load in each age group is shown in Table 2. The nodule carrier rate and the nodule load in each age group showed a pattern similar to the microfilaruria rate. As the nodule carrier rate increases, the microfilaria rate does likewise (p < 0.01). However, the closest association was that between the mean number of microfilaria in 10 ml urine and the mean nodule load (r =0.8, p < 0.05). Individuals with a large number of nodules also had a large number of microfilaria in urine. Thirteen (86.7%) of the fifteen individuals with microfilaruria also had nodules (TabId). Only 17 (34.0%) out ofthe 50 persons with nodules did not have microfilaruria.
Microfilaruria in an Area of Nigeria with Hyperendemic Onchocerciasis
89
Table 2. Intensity of Microfilaruria and Nodules load by age Age (Years)
No. Exam.
< 10 10-19 20-29 30-39 40-49 ;;:: 50
7 6 7 25 9 10
Total
64
No. of Mf in 10 ml of Urine" 0
1
2
3
4
5
7 6 5 17 6 8
0 0 1 7 0 0
0 0 1 0 1 1
0 0 0 0 1 1
0 0 0 0 1 0
0 0 0 1 0 0
MeanMfd in Urine"
Mean Nodule Load
0 0
0 1.3 1.8 1.2 2.7
1.5
1.5 5.0 2.5 2.3
Mf =Microfilaria, ..
1.5 1.5
=No. Mf of o. volvulusl10 mL urine.
Table 3. Number of Microfilaruria persons with and without nodules Mf+ Nodule +
MfNocule +
MfNoduel-
Age (Years)
Mf+ Nodules -
<10 10-19 20-29 30-39 40-49 50
0 0 0 1 1 0
0 0 2 7 2 2
0 3 2 8 1 3
7 3 3 9 5 5
7 6 7 25 9 10
Total
2
13
17
32
64
Coefficient of association C =0.85, between mf urine nodules Mf =Microfilaria.
Total
= (13 x 32) -
(17 x 2) (13 x 32) + (17 x 2),
Discussion The high rate of microfilaruria that was recorded in a small sample taken from this area is probably an indication of a rather high rate of microfilaria in the Taraba river valley which has been reported earlier (Akogun & Onwuliri, 1991). Studies carried out by Buck et al. (1969, 1971) showed an increase from 20.0% in 1967 to 34.1 % in 1971 in Ouli Bangala, a village in Southern Chad. In 1971, the average microfilaria load in urine was 10.21100 mL urine, with a minimum of 1.51100 mL urine and a maximum of 30.61100mL. Although the microfilaruria rate recorded in this study has been lower than that recorded in Chad, the average microfilaria load in urine (2.3/ 10 mL) is similar to that reported in Chad. The lower rate of microfilaruria in this investigation may be due to the use of a smaller sample size than that used by Buck et al. (1971) which involved 79 males and 74 females. The present findings are much
90
O. B. Akogun and K. Tembo
higher, however, than the 4.7% microfilaruria rate that was recorded in Baoussi, Adamaoua Plateau of Cameroun (Anderson et al. 1974). Viewed together, these results suggest that the aetiology, prevalence and intenstiy of onchocerciasis transmission in the mid-Taraba river valley is similar to that of Western Cameroun and Southern Chad. This implies that a coordinated control effort is necessary in the three zones if an effective disease management is envisaged. It also suggests the need for a multinational management strategy such as joint and well-sustained ivermectin distribution in the entire area. Anderson et al. (1974) have shown that there is a close association between the density of microfilaria in skin and the density of microfilaria in urine. Our findings have revealed a strong association between nodule load, nodule carrier rate and microfilaruria rate. Thus, the microfilaruria rate in a community may be used as an index for estimating the rate of onchocerciasis in that community. This will make unnecessary the taking of skin snips in order to confirm that microfilaria exists in a community. The taking of skin snips is costly in monetary terms and exposes the individual whose skin is taken to secondary bacterial infections or to the HIV or infective hepatitis when no sterilizing procedures are used and body fluids may be contaminated. The detection of microfilaria in urine has the advantage of revealing the parasite and can be used to confirm observations made using the rapid assessment method of nodule carrier rates in selecting communities for ivermectin delivery. Further studies of the epidemiology of microfilaruria in the Taraba river valley will establish the usefulness of microfilaruria in monitoring and evaluating the effectiveness of ivermectin on the load of microfilaria. The microfilaria rate in a community could also be used to determine the community's need for ivermectin.
Acknowledgements. We are grateful to the individuals and the village heads of Nyubango-Agbakom who took part in this study, and to Africare Organisation, USA which provided logistic support.
References
1. Akogun, o. B. and C. o. E. Onwuliri: Hyperendemic onchocerciasis in the Taraba river valley of Gongola State (Old Adamawa Province), Nigeria. Annales de Parasitologies Humaine et Compare 66, (1991) 22-26 2. Anderson, R. I., D. B. Thomas, A. A. Macrae, and A. A. Buck: Onchocerciasis Prevalence of Microfilaria and other manifestations in a village of Cameroun. American Journal of Tropical Medicine and Hygiene 74, (1), (1974) 66-70 3. Buck, A. A., R. I. Anderson, K. Kawata, and J. C. Hitchcock Jr.: Onchocerciasis: Some new epidemiologic and clinical findings. Results of an epidemiologic study in the Republic of Chad. American Journal of Tropical Medicine and Hygiene 18, (1969) 217230 4. Buck, A. A., R. I. Anderson, J. A. C. Colston Jr., c. K. Wallace, D. H. Connor, L. E. Harman Jr., M. W. Donner, and J. P. Ganley: Microfilaruria in Onchocerciasis: A clinical and epidemiological follow-up study in the Republic of Chad. Bull W.H.O. 45 (1971) 353369 5. Buck, A. A.: Microfilaruria in Onchocerciasis in Africans. Review and rewatch recommendations Z. Tropenmed Parasitol. 24 (1973) 336-338 6. Dyce-Sharp, N. A.: Contribution to the study of Onchocerca volvulus Leuckart with some observations on its prevalence in Nigeria. Transactions of the Royal Society for Tropical Medicine and Hygiene 19 (1926) 373-388
Microfilaruria in an Area of Nigeria with Hyperendemic Onchocerciasis
91
7. Fazen, L. E., R. I. Anderson, M. H. Figuerora, E G. Arthes, and A. A. Buck: Onchocerciasis in Guatemala I. Epidemiological Studies of Microfilaruria. Journal of Tropical Medicine and Hygiene 24 (1975) 52-57 8. Mazzotti, L. and M. T. Ososrio: Sobre la Presencia de Microfilarias de Onchocerca volulus en la sangre y en la orina de pacientes afectados por esta filaria. Rev. Inst. Salbur. Enferm. Trop. 10 (1949) 269-275 O. B. Akogun, Department of Biological Sciences Federal University of Technology, Yola, Nigeria
Microfilaruria in an Area of Nigeria with Hyperendemic Onchocerciasis O.B. AKOGUN 1 and K. TEMB0 2 1 Parasite
and Tropical Health Research, Department of Biological Sciences, Federal University of Technology, Yola, Nigeria 2 Public Health Program, Polytechnic University of Malawi, Blantyre, Malawi
Received April 28, 1995 . Revision received August 11, 1995 . Accepted October 5, 1995
Summary Urine samples collected from sixty-four Nigerians living in a community which is hyperendemic for onchocerciasis were examined for microfilaria. Each urine donor was examined for the physical symptoms of long-standing onchocerciasis. The microfilaruria rate was 23.4%. Males had a higher rate of microfilaruria (27.5%) than females (16.7%). The prevalence rates of leopard skin and nodules were 18.8% and 46.9%, respectively. Thirteen persons had microfilaruria and had nodules. Seventeen showed no microfilaruria but had nodules. Only two of those without nodules were without microfilaruria. A very strong association was found between nodule-possession, nodule-load and microfilaruria (coefficient of association 0.85). Nodule load seemed to be the major factor in having microfilaria in urine. Microfilaruria is not common in Nigeria and the present finding is the first report of microfilaruria in the Taraba river valley which is a continuous onchocerciasis zone with the Western Cameroun - Southern Chad focus of transmission where microfilaruria has been reported. This paper discusses the implications of the results of this investigation with respect to monitoring the impact of ivermectin distribution in the Taraba river valley of Nigeria.
Introduction There are sporadic reports of the occurrence of microfilaruria in many parts of the world where onchocerciasis is endemic (Dyce-Sharp, 1926; Mazzotti and Ososrio 1949; Buck et ai., 1969; 1971; Buck, 1973; Fazen et ai.; Fazen et ai., 1975). By far the most comprehensive of these studies is probably that carried out by Anderson et al. (1974) in parts of the Adamaoua Plateau of Cameroun which is an onchocerciasis focus continuous with the Taraba-Dakka-Ganye-Chad Republic zone. Buck et al. (1971) recorded an 11.4% microfilaruria rate when 386 persons were examined in Ouli Bangala, Chad Republic while Anderson et al. (1974) recorded 4.7% in Baoussi, Cameroun Republic. These studies reported an association between the community microfilaruria rate and most of the typical onchocerciasis symptoms, espe-
Microfilaruria in an Area of Nigeria with Hyperendemic Onchocerciasis
87
cially micro filariae in skin, nodules and leopard skin, irrespective of age and sex. The two reports firmly established that the presence and number of microfilaruria cases is a reflection of the intensity of the community microfilaria load. Akogun and Onwuliri (1991) reported that the previously unprospected Taraba river valley could be one of the most important onchocerciasis foci in West Africa, with very severe ocular problems among the infected population. There are many similarities in the epidemiology of onchocerciasis in Southern Chad, the Adamoua Plateau of Cameroun and the Taraba river valley of Nigeria. Important differences may also exist as a result of variations in the local strain Onchocerca volvulus or the vector species or the biting behaviour of the latter. It could be interesting to find out if the presence of microfilaruria could be used for monitoring the effectiveness of ivermectin. The present study is a preliminary baseline investigation of the pretreatment occurrence or absence of microfilaruria in an area with hyperendemic onchocerciasis. Materials and Methods Two clusters which constitute the Nyubango and Agbakom communities in the Gayam area of Gashaka district (11 °30'-11°43'E; 70 10'-8°15'N) of the Taraba river valley were studied. The Gayam area is reported to be a hyperendemic area with about 80% 0 volvulus positivity rate among 426 persons aged 5 years and older (Akogun and Onwuliri, 1991). The households were randomly selected (six from Nyubango and four from Agbakom) and a census of the number of residents in each household taken. No member of these isolated communities had ever taken either ivermectin, diethlyl-carbamazine (DEC), or suramin sodium. One container was given to each family member with instructions to bring a sample of urine when reporting for physical examination. The individuals were examined for physical onchocerciasis symptoms. The name, age, sex and urine specimen number were recorded on a specially designed epidemiological form. The results of the physical examination were also recorded against the individual's name. Particular attention was given to the presence and number of nodules, leopard skin and lizard skin. Urine samples were preserved in methioate formalin in the field. In the laboratory, 10 mL volumes of urine each were centrifuged at 1500 rpm for fifteen minutes to obtain a sediment which was examined for microfilaria under a microscope with an x40 objective. The length of each microfilaria specimen was measured, and the head and tail and examined for enlargement and nuclei respectively. Microfilaria of o. volvulus were longer than 240 [!m, had an enlarged head end and had no nuclei at the tail end. 0
Results Sixty-four individuals (40 males and 24 females) were examined. The rate of microfilaruria was 23.4% (27.5% in males and 16.7% in females). The prevalence of nodules, leopard and lizard skin was 46.9%, 18.8% and 29.7%, respectively (Table 1). The prevalence of Schistosoma haematobium was low (7, 8). There were no cases of microfilaruria in individuals below 20 years of age. However, the prevalence of microfilaria-positive urine was similar in all age groups between 20 and 49 years (28.6% to 33.3 %) but dropped to a low level (20.0%) in persons that were 50 years or older. Microfilaruria was recorded only in females between 20-29 years (50.0%) and 30-39 years (33.35%). In males, the rate of microfilaruria increased with age from 20 years (20.0%) until 49 years (60.0%) when it dropped to 28.6%
O. B. Akogun and K. Tembo
88
Table 1. Age-specific prevalence of microfilaruria and physical symptoms of onchocerciasis Male Age (Years)
No. Exam.
< 10
4 3 5 16 5 7
0 0 1 5 2 2
0 2 2 1 2 2
0 0 2 5 2 2
0 0 2 6 2 2
0 1 1 2 0 0
40
11
19
9
12
4
3 3 2 9 4 3
0 0 1 3 0 0
0 1 2 4 1 3
0 0 0 2 1 0
0 0 1 3 3 0
0 0 0 1 0 0
24
4
11
3
7
1
7 6 7 25 9 10
0 0 2 8 3 2
0 3 4 15 3 5
0 0 0 7 3 2
0 0 3 9 5 2
0 1 1 3 0 0
64
15
30
12
19
5
:2:
10-19 20-29 30-39 40-49 50
Total
Mf+ Urine
Nod. + ve
Leopard Skin
Lizard Skin
S. haem.
Female
< 10
:2:
10-19 20-29 30-29 40-49 50
Total Total
< 10
:2:
10-19 20-29 30-39 40-49 50
Total
Mf + =Microfilaria positive, Nod. + ve matobium.
=Nodules positive, S. haem. =Schistosoma hae-
among males that were 50 years or older. Both leopard skin and lizard skin increased in prevalence with increase in age. The intensity of microfilaruria and nodule load in each age group is shown in Table 2. The nodule carrier rate and the nodule load in each age group showed a pattern similar to the microfilaruria rate. As the nodule carrier rate increases, the microfilaria rate does likewise (p < 0.01). However, the closest association was that between the mean number of microfilaria in 10 ml urine and the mean nodule load (r =0.8, p < 0.05). Individuals with a large number of nodules also had a large number of microfilaria in urine. Thirteen (86.7%) of the fifteen individuals with microfilaruria also had nodules (TabId). Only 17 (34.0%) out ofthe 50 persons with nodules did not have microfilaruria.
Microfilaruria in an Area of Nigeria with Hyperendemic Onchocerciasis
89
Table 2. Intensity of Microfilaruria and Nodules load by age Age (Years)
No. Exam.
< 10 10-19 20-29 30-39 40-49 ;;:: 50
7 6 7 25 9 10
Total
64
No. of Mf in 10 ml of Urine" 0
1
2
3
4
5
7 6 5 17 6 8
0 0 1 7 0 0
0 0 1 0 1 1
0 0 0 0 1 1
0 0 0 0 1 0
0 0 0 1 0 0
MeanMfd in Urine"
Mean Nodule Load
0 0
0 1.3 1.8 1.2 2.7
1.5
1.5 5.0 2.5 2.3
Mf =Microfilaria, ..
1.5 1.5
=No. Mf of o. volvulusl10 mL urine.
Table 3. Number of Microfilaruria persons with and without nodules Mf+ Nodule +
MfNocule +
MfNoduel-
Age (Years)
Mf+ Nodules -
<10 10-19 20-29 30-39 40-49 50
0 0 0 1 1 0
0 0 2 7 2 2
0 3 2 8 1 3
7 3 3 9 5 5
7 6 7 25 9 10
Total
2
13
17
32
64
Coefficient of association C =0.85, between mf urine nodules Mf =Microfilaria.
Total
= (13 x 32) -
(17 x 2) (13 x 32) + (17 x 2),
Discussion The high rate of microfilaruria that was recorded in a small sample taken from this area is probably an indication of a rather high rate of microfilaria in the Taraba river valley which has been reported earlier (Akogun & Onwuliri, 1991). Studies carried out by Buck et al. (1969, 1971) showed an increase from 20.0% in 1967 to 34.1 % in 1971 in Ouli Bangala, a village in Southern Chad. In 1971, the average microfilaria load in urine was 10.21100 mL urine, with a minimum of 1.51100 mL urine and a maximum of 30.61100mL. Although the microfilaruria rate recorded in this study has been lower than that recorded in Chad, the average microfilaria load in urine (2.3/ 10 mL) is similar to that reported in Chad. The lower rate of microfilaruria in this investigation may be due to the use of a smaller sample size than that used by Buck et al. (1971) which involved 79 males and 74 females. The present findings are much
90
O. B. Akogun and K. Tembo
higher, however, than the 4.7% microfilaruria rate that was recorded in Baoussi, Adamaoua Plateau of Cameroun (Anderson et al. 1974). Viewed together, these results suggest that the aetiology, prevalence and intenstiy of onchocerciasis transmission in the mid-Taraba river valley is similar to that of Western Cameroun and Southern Chad. This implies that a coordinated control effort is necessary in the three zones if an effective disease management is envisaged. It also suggests the need for a multinational management strategy such as joint and well-sustained ivermectin distribution in the entire area. Anderson et al. (1974) have shown that there is a close association between the density of microfilaria in skin and the density of microfilaria in urine. Our findings have revealed a strong association between nodule load, nodule carrier rate and microfilaruria rate. Thus, the microfilaruria rate in a community may be used as an index for estimating the rate of onchocerciasis in that community. This will make unnecessary the taking of skin snips in order to confirm that microfilaria exists in a community. The taking of skin snips is costly in monetary terms and exposes the individual whose skin is taken to secondary bacterial infections or to the HIV or infective hepatitis when no sterilizing procedures are used and body fluids may be contaminated. The detection of microfilaria in urine has the advantage of revealing the parasite and can be used to confirm observations made using the rapid assessment method of nodule carrier rates in selecting communities for ivermectin delivery. Further studies of the epidemiology of microfilaruria in the Taraba river valley will establish the usefulness of microfilaruria in monitoring and evaluating the effectiveness of ivermectin on the load of microfilaria. The microfilaria rate in a community could also be used to determine the community's need for ivermectin.
Acknowledgements. We are grateful to the individuals and the village heads of Nyubango-Agbakom who took part in this study, and to Africare Organisation, USA which provided logistic support.
References
1. Akogun, o. B. and C. o. E. Onwuliri: Hyperendemic onchocerciasis in the Taraba river valley of Gongola State (Old Adamawa Province), Nigeria. Annales de Parasitologies Humaine et Compare 66, (1991) 22-26 2. Anderson, R. I., D. B. Thomas, A. A. Macrae, and A. A. Buck: Onchocerciasis Prevalence of Microfilaria and other manifestations in a village of Cameroun. American Journal of Tropical Medicine and Hygiene 74, (1), (1974) 66-70 3. Buck, A. A., R. I. Anderson, K. Kawata, and J. C. Hitchcock Jr.: Onchocerciasis: Some new epidemiologic and clinical findings. Results of an epidemiologic study in the Republic of Chad. American Journal of Tropical Medicine and Hygiene 18, (1969) 217230 4. Buck, A. A., R. I. Anderson, J. A. C. Colston Jr., c. K. Wallace, D. H. Connor, L. E. Harman Jr., M. W. Donner, and J. P. Ganley: Microfilaruria in Onchocerciasis: A clinical and epidemiological follow-up study in the Republic of Chad. Bull W.H.O. 45 (1971) 353369 5. Buck, A. A.: Microfilaruria in Onchocerciasis in Africans. Review and rewatch recommendations Z. Tropenmed Parasitol. 24 (1973) 336-338 6. Dyce-Sharp, N. A.: Contribution to the study of Onchocerca volvulus Leuckart with some observations on its prevalence in Nigeria. Transactions of the Royal Society for Tropical Medicine and Hygiene 19 (1926) 373-388
Microfilaruria in an Area of Nigeria with Hyperendemic Onchocerciasis
91
7. Fazen, L. E., R. I. Anderson, M. H. Figuerora, E G. Arthes, and A. A. Buck: Onchocerciasis in Guatemala I. Epidemiological Studies of Microfilaruria. Journal of Tropical Medicine and Hygiene 24 (1975) 52-57 8. Mazzotti, L. and M. T. Ososrio: Sobre la Presencia de Microfilarias de Onchocerca volulus en la sangre y en la orina de pacientes afectados por esta filaria. Rev. Inst. Salbur. Enferm. Trop. 10 (1949) 269-275 O. B. Akogun, Department of Biological Sciences Federal University of Technology, Yola, Nigeria