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Am. J. Trop. Med. Hyg., 74(5), 2006, pp. 833-840
Copyright © 2006 by The American Society of Tropical Medicine and Hygiene

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CONSEQUENCES OF VECTOR BEHAVIOR IN EPIDEMIOLOGY OF ONCHOCERCIASIS ON THE FIRESTONE RUBBER PLANTATION IN LIBERIA

MILAN TRPIS
The W. Harry Feinstone Department of Molecular Microbiology and Immunology, Bloomberg School of Public Health, The Johns Hopkins University, Baltimore, Maryland


ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
In the current study, we have assessed the distribution of black fly vectors and the occurrence of onchocerciasis among residents of the Firestone Rubber Plantation (FRP) in Liberia. The degree of endemicity of onchocerciasis on the FRP is correlated with the breeding of Simulium yahense on the Du River and Simulium soubrense on the Farmington River, as well as with the feeding behavior of these black fly vectors. S. yahense is highly anthropophilic and highly susceptible to Onchocerca volvulus, thus, it is apparently the primary vector of O. volvulus on the plantation. S. soubrense is predominantly zoophilic; consequently, it has a low capacity for transmitting of O. volvulus to humans. The prevalence of the disease is hyperendemic in the divisional camps near the Du River, affecting 77.6% to 94.4% of males and 64.9% to 88.9% of females. In the camps along the Farmington River, the disease is hypoendemic, affecting 26.1% to 49.2% of males and 25.6% to 35.1% of females. The mean intensity of infection in the camps near the Du River was 14.1 microfilariae (mf)/mg of skin in males and 13.7 mf/mg of skin in females. The density of microfilariae in people in the camps along the Farmington River was 4.8 mf/mg of skin in males and 1.9 mf/mg of skin in females. The age-specific infection in camps along both rivers substantially increased after the ages 21–30, reaching a maximum at ages 41–50. The mean density of mf/mg of skin in three anatomic locations (calf, hip, and shoulder) was 28.0, 24.5, and 14.1 mf/mg of skin, respectively, for those living on the Du River, and 10.2, 7.6, and 5.8 mf/mg of skin, respectively, for those on the Farmington River.


INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The Firestone Rubber Plantation (FRP), established in the late 1920s at Harbel in Liberia, is a man-made biotope resulting from change of a secondary rain forest into a monoculture of Brazilian rubber trees (Hevea brasiliensis). The primary reason for choosing this area as the most suitable for development of a rubber tree plantation was the presence of a large body of water running through the area, in the form of three major rivers and several permanent creeks. Such a large source of water was required for preprocessing of latex in the production of rubber. Water was also an important commodity for a large population of plantation workers and their families residing in 45 divisional camps. However, the rivers and permanent creeks on the FRP are also active breeding places for the black flies Simulium yahense and Simulium soubrense, which are the vectors of the human filarial pathogen Onchocerca volvulus.

Workers hired by the plantation management have come from different geographic regions of Liberia, and many came from areas in which transmission of O. volvulus is active and the endemicity of onchocerciasis is high. The proximity of divisional camps to a particular river and permanent creeks at which women wash their clothes and kitchen utensils, as well as bathe their children or catch fish and crayfish to feed their families, may determine the varying degrees of prevalence and intensity of infection with O. volvulus among these groups of people.

Onchocerciasis in Liberia was first diagnosed by the Harvard Expedition to Africa in 1926–1927 and reported in 1930.1 The first study on the epidemiology of the disease on the FRP was published in 1955,2 followed by reports from several other early investigators who concentrated primarily on the clinical, pathologic aspects of human infection with O. volvulus.3–5 The most extensive field investigation of the geographic distribution of onchocerciasis in Liberia, which included samples from three divisional camps on the FRP, was published in 1975.6 In other, more recent studies of onchocerciasis on the FRP, investigators focused on various aspects of vector biology, such as identification of Simulium vectors,7,8 their distribution,9,10 population genetics,11 ecology and feeding behavior,12–14 transmission of O. volvulus,9,15–17 and epidemiology,10 all of which led to the current investigation.

The objectives of this study were to 1) elucidate the consequence of differences in breeding behavior of aquatic stages of black flies in the Du and Farmington rivers and to examine how these differences in the vector populations reflect the transmission of O. volvulus to people residing in divisional camps located on the respective rivers; 2) demonstrate differences in feeding behavior, particularly the differences in host preferences of S. yahense and S. soubrense and assess the consequences of such behavior for the epidemiology of onchocerciasis on the FRP; 3) examine correlations between prevalence and intensity of infection with O. volvulus in people living in camps along the Du and Farmington rivers.


MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Study area. The FRP is located 60 km NW of Monrovia (6°20' N, 10°25' W). It is the oldest and the largest rubber plantation in the world, having been established in 1926 on 579 km2 of a secondary rain forest rented from the Liberian government. More than 300 km2 of the total 579 km2 of the plantation area are under cultivation. The plantation management employs approximately 12,000 workers, but the resident population, including management, workers, and their families, can be as high as 100,000 people, most of them belonging to the Bassa, Kpelleh, Kisi, and Loma tribes. About 10 million Brazilian rubber trees (Hevea brasiliensis) of approximately 50 different genetic varieties are cultured on the FRP. This monoculture is now an ecologically stable biotope. Three large rivers, the Farmington, Du, and Ba, as well as several permanent creeks, run through the FRP and give the plantation a special character of suitability for cultivation of rubber trees and production and preprocessing of daily collected latex. The largest is the Farmington River (Figure 1Go), which flows in a N–SW direction and forms the western boundary of the FRP. It averages 100 m across and is in most places widely open to the sun. The Du River is a smaller sized river, averaging 50 m across. The Du River is heavily shaded with trees and bushes and has a high content of suspended detritus. The Ba River is a small-size river, 20 to 30 m wide, and it is sluggish in its flow, not attractive to Simulium damnosum s.l. to breed. The water temperature measured with a Digi-Sense Thermocouple thermometer (Cole Palmer Instrument Co., Vernon Hills, IL) in shaded and open areas in the Du River was lower (23.1°C) than in the wide open to the sun Farmington River (28.5°C). Because of the high density of suspended detritus, the pH of water measured with pH/mV Electrometer (model 245, Instrumentation Laboratory Inc., Lexington, MA) was lower in the Du River (pH 5.5) than in the Farmington River (pH 6.5).


Figure 1
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  		    FIGURE 1. Map of the Firestone Rubber Plantation at Harbel in Liberia, West Africa, showing sampling sites on the Du River (divisional camps 2, 14, 25) and on the Farmington River (divisional camps H, 41, 34). Permanent creeks are depicted as tributaries of the Du and Farmington rivers.

 
Vectors. Two species of the Simulium damnosum complex, namely Simulium yahense and Simulium soubrense, have been observed as vectors of Onchocerca volvulus on the FRP. To elucidate the differences in vectorial capacity between these two species, it is important to focus at this time on ecology and behavior of these two Simulium vectors.

S. yahense is associated with swiftly running water in the Du River and in larger, permanent creeks such as Bonee, Cement, Sia, Hunt, and Vuwe. Breeding of aquatic stages in the Du River is prolific, resulting in a high population of the biting flies. It is highly anthropophilic and highly susceptible to infection with O. volvulus. The active transmission of O. volvulus takes place in all seasons of the year. Thus, S. yahense is the most efficient vector responsible for transmission of onchocerciasis on the FRP.

S. soubrense breeds almost exclusively in the Farmington River. Human populations residing in divisional camps on the Farmington River are significantly less affected by bites of infective flies because the Farmington flies designated as S. soubrense are predominantly zoophilic.9,17 Consequently, the Farmington flies are the secondary vector of O. volvulus on the FRP. The Farmington flies lately designated as S. soubrense18,19 had been for a long time (and to some extent still remains) an enigmatic vector of O. volvulus on the plantation. It breeds almost exclusively in the Farmington River, exhibits a relatively low anthropophily, most probably feeding on wild and/or domestic birds and mammals; however, autogeny cannot be completely excluded.17 Other physiologic and behavioral phenomena associated with the Farmington adult flies result in an epidemiologic picture different from one, in which S. yahense is involved. The low anthropophily of S. soubrense results in low prevalence and intensity of infection in divisional camps located on the Farmington River.

Parasitological examination. The skin biopsies for this study were collected between March and September 1986 and in October–November 1987 from a total of 577 individuals who had given informed consent. The participation in this study was strictly voluntary. The purpose of this study was explained to interested individuals in the Bassa, Kpele, and English languages. The written protocol for our studies on the Firestone Rubber Plantation had been previously reviewed by the Committee on Human Research at Johns Hopkins School of Public Health and by the Advisory Council of the Liberian Institute for Biomedical Research. A group of 333 individuals were sampled in three divisional camps in a profile of the lower, middle, and upper parts of the Du River, and 244 people were sampled in a similar profile fashion on the Farmington River (Figure 1Go). The age and sex distribution of the persons examined is given in Tables 1Go–4GoGoGo.


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TABLE 1
Prevalence of infection with microfilariae of Onchocerca volvulus in human populations in the Firestone Rubber Plantation divisional camps on the Du River (M, male; F, female)
 

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TABLE 2
Prevalence of infection with microfilariae of Onchocerca volvulus in human populations in divisional camps on the Farmington River (M, male; F, female)
 

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TABLE 3
Intensity of infection with microfilariae of Onchocerca volvulus in human populations in divisional camps on the Du River (M, male; F, female)
 

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TABLE 4
Intensity of infection with microfilariae of Onchocerca volvulus in people by age and sex in divisional camps on the Farmington River (M, male; F, female)
 
Before the skin biopsies were obtained, the skin sampling sites were cleaned with 75% ethanol, which was then allowed to evaporate. A 1.5-mm Stortz corneal-scleral punch was used to obtain the skin biopsies. The corneal-scleral punches were kept between use for sampling in concentrated DMSO, rinsed in concentrated ETOH, which was allowed to evaporate shortly before the skin biopsies were taken. The skin abrasion was then covered with medicated antiseptic plastic patches 25 mm in diameter. Three biopsies were obtained from each individual in the same sequence: calf, hip, and shoulder, and sides of the body were altered. The parasite density was expressed as the number of microfilariae (mf)/mg of skin. Biopsy samples were placed in wells of 0.3 mL flat-bottom microtiter plates containing 0.2 mL of HEPES-buffered RPMI 1640 TC medium (pH 7.2). After all wells were filled with biopsy samples, the microtiter plates were covered with wide strips of sticky plastic to seal the wells, and the plates were placed into a cooler with ice packs to maintain the skin biopsies below ambient temperature (at 17–19°C). The microtiter plates in the cooler were then transported to the Vector Biology Laboratory at the Liberian Institute for Biologic Research. The microtiter plates were removed from the cooler and left at room temperature overnight to incubate before microfilariae counting took place. After the emergence of the microfilariae, the biopsy samples were removed from the wells, placed on filter paper to remove excess TC medium, and weighed on a Sartorius-i1800 analytical balance. Microtiter plates with microfilariae in the wells were placed on the stage of an inverted microscope and microfilariae counted at 40x magnification. The number of microfilariae emerging from each biopsy sample was calculated per milligram of skin. It is necessary to note that for the ages 1–5 years, only one or two children from three camps along the Du River were brought by their parents to be sampled, and in total two children of five sampled were infected (Table 1Go). In the three camps on the Farmington River, six children of ages 1–5 were sampled, and none of them were infected (Table 2Go).

Statistical analysis. Depending on the character of the data, the following statistical tests were performed: Fisher’s exact test, unpaired t tests, repeated measures ANOVA, and correlation coefficient values between prevalence and intensity of infection.


RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Prevalence of infection with microfilariae in the skin. Prevalence of infection by divisional camps located on the Du and Farmington rivers and the total prevalence by river. The prevalence of infection with microfilariae of O. volvulus in people living in the divisional camps 2, 14, and 25 on the Du River was hyperendemic (Table 1Go; Figure 2AGo), and the prevalence of infection in camps on the Farmington River was hypoendemic (Table 2Go; Figure 2BGo). The mean microfilariae infection by rivers was 77.4% in camps on the Du River and 35.9% in camps on the Farmington River (Figure 2CGo). The microfilariae prevalence was 2.1 times higher in camps situated on the Du River than in the camps on the Farmington River (Fisher’s two-sided exact test, P > 0.0001).


Figure 2
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  		    FIGURE 2. Prevalence of infection with microfilariae of Onchocerca volvulus in human populations on divisional camps (A) on the Du River and on divisional camps (B) on the Farmington River and the total infection by river (C).

 
Prevalence of microfilariae infection in divisional camps by sex and river and the total prevalence by sex and river. The prevalence of microfilariae infection by sex in the Du River camps 2, 14, and 25 (Figure 3AGo) and in the Farmington River camps H, 41, 34 (Figure 3BGo) was always higher in males than in females. The mean prevalence in camps on the Du River was 80.1% in males and 74.5% in females, as compared with the Farmington River where the total prevalence was 40.1% in males and 30.2% in females (Figure 3CGo). The difference in prevalence of microfilariae infection on two rivers in males was significant (unpaired two-tailed t test, P > 0.001, t = 5.3 with 4 degrees of freedom), and the same test for females shows P > 0.001, t = 6.1 with 4 degrees of freedom.


Figure 3
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  		    FIGURE 3. Prevalence of infection with microfilariae of Onchocerca volvulus in divisional camps on the Du River in Divisions 2, 14, 25 (A) and on the Farmington River in Divisions H, 41, 34, and the total prevalence by sex and river (C).

 
Prevalence by age and river. The prevalence of infection by age in people living on the Du River gradually increased, from the lowest at age 1 to 10 to the highest at age 31 to 40, then slightly decreased in those aged 41 to 50+ (Fig. 4Go). The prevalence of mf infection in people on the Farmington River in the same age groups increased from age 1 to 10 to the highest level in those aged 31 to 40, and again decreased slightly in those aged 41 to 50+ (Fig. 4Go) (unpaired two-tailed t-test with 8 degrees of freedom, P > 0.001; t = 3.4).


Figure 4
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  		    FIGURE 4. Prevalence of infection with microfilariae of Onchocerca volvulus in human populations by age and river.

 
Prevalence by age, sex, and river. The prevalence in males in the Du River camps by age increased from ages 1 to 10 to the highest prevalence at ages 31 to 40, then slightly decreased in those aged 41–50+ (Figure 5AGo). Prevalence in females on the Du River was the lowest at ages 1–10, then increased to the highest in those aged 31–40; a slight drop was observed at ages 41–50+ (Figure 5AGo). The prevalence on the Farmington River in males (Figure 5BGo) increased from ages 1 to 10 to the highest at ages 31 to 40, then slightly decreased in those aged 41–50+. The prevalence in females (Figure 5BGo) also increased gradually from the age group 1–10 years to the highest microfilariae prevalence at ages 31–40 years and then decreased in those aged 41–50+. Differences in the same sex between rivers were significant in females (unpaired two-tailed t-test with 8 degrees of freedom, P > 0.001, t = 3.85; the same test in males showed P > 0.01, t = 2.96). Differences between sexes on the same river were not significant. The mean prevalence of infection by sex on the Du River was 80.1% in males and 74.5% in females. The mean prevalence on the Farmington River was 40.1% in males and 30.2% in females (Figure 5CGo).


Figure 5
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  		    FIGURE 5. Prevalence of infection with microfilariae of Onchocerca volvulus by age, sex, and river (A, B) and the total infection by sex and river (C).

 
Intensity of infection with microfilariae in the skin. Intensity of microfilariae infection in people living in divisional camps on the Du and Farmington rivers, and the total infection by river. The intensity of microfilariae infection in people living in divisional camps 2, 14, and 25 on the Du River was higher in people in the direction of downstream camps (Figure 6AGo). However, the intensity of infection in the skin was higher in people living in divisional camps upstream of the Farmington River (Figure 6BGo). The mean microfilariae density in people living in the camps on the Du River was 13.9 mf/mg of skin and for those living in the camps along the Farmington River the density was 3.3 mf/mg of skin (Figure 6CGo). The difference in microfilariae density between camps on the Du and Farmington rivers was 4.2 times higher in camps on the Du River than in camps on the Farmington River (unpaired two-tailed t-test, 4 degrees of freedom, P > 0.0001, t = 9.99).


Figure 6
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  		    FIGURE 6. Intensity of infection with microfilariae of Onchocerca volvulus in individual camps on the Du River (A), on the Farmington River (B), and total infection by river (C).

 
Intensity of microfilariae infection in divisional camps by sex and the total intensity of infection by sex and river. The intensity of infection with microfilariae in males and females living in camps on the Du and Farmington rivers is given in Figures 7A and 7BGo. In the Du River camps, the infection in males was the highest in camps located downstream (2, 14, 25; Figure 7AGo). In two camps (14 and 25) the density of microfilariae was higher in females than in males. In the Farmington River camps, the infection in males increased in upstream camps, and in females the infection was lower and variable (Figure 7BGo) (unpaired t-test showed that differences in intensity of infection between sexes on the same river were not significant). However, differences in the same sex between rivers were significant in females (unpaired two-tailed t-test, P > 0.001) and in males (P > 0.01). The difference in mean density of microfilariae infection between males and females on the Du River was 0.4 mf/mg of skin biopsy (Figure 7CGo). On the Farmington River the mean density of infection between sexes was much higher (2.9 mf/mg of skin biopsy) than on the Du River.


Figure 7
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  		    FIGURE 7. Intensity of infection with microfilariae of Onchocerca volvulus in divisional camps by sex on the Du River (A) and Farmington River (B) and the total intensity of infection by river (C).

 
Intensity of microfilariae infection by age and river. The intensity of infection with O. volvulus in people generally increases with age. In those living on the Du River, density of infection was the lowest at ages 1–10, doubled at ages 11–20, and doubled again at ages 21–30. From age 21 to 50+, the microfiladermia remained high (Figure 8AGo). The intensity of infection in people living in camps on the Farmington River was low and variable (Figure 8BGo). The mean density of microfilariae infection in people living on the Du River was 4.2 times higher than in people living on the Farmington River (Figure 8CGo) (unpaired two-tailed t-test, 8 degrees of freedom, and P > 0.01, t = 3.08).


Figure 8
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  		    FIGURE 8. Intensity of infection with microfilariae of Onchocerca volvulus by age and river (A, B), and the total intensity of infection by river (C).

 
Intensity of microfilariae infection by age, sex, and river. The intensity of infection by age in males on the Du River in people aged 1–10 to 11–20 was low and increased sharply in people aged 21–30 to 41–50+ (Figure 9AGo). The intensity of infection in females living on the Du River was lower than in males in age groups 1–10 to 21–30. For the next two age groups (31–40 and 41–59+), the intensity of infection was higher in females than in males. In camps on the Farmington River, intensity of infection in males in all age groups was higher than in females (Figure 9BGo). Infection between sexes on the Du River was not significant by unpaired t-test; however, infection between sexes on the Farmington River was significant, P < 0.01. The mean intensity of infection in males and females was still higher for males and females in camps on both rivers (Figure 9CGo).


Figure 9
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  		    FIGURE 9. Intensity of infection with microfilariae of Onchocerca volvulus by age and sex on the Du River (A) and the Farmington River (B), and the total infection by sex and river (C).

 
Density of microfilariae in the skin at different anatomic locations. The highest density of mf/mg of skin in men and women in the Du and Farmington river camps was found at the calf location (Figures 10A and 10BGo). The microfilariae density was lower at the hip site in both sexes and was the smallest at the shoulder level. This finding may indicate that intensity of infection at the lower part of the body may be the consequence of S. yahense on the FRP feeding preferably at the lower part of the human body, particularly legs. The microfilariae density at the three body sites in both sexes living on the Du River was substantially higher than for those living on the Farmington River camps. One exception was that the density of microfilariae in females on the Farmington River was 0.9 mf/mg higher in the shoulder than in the hip location (Figure 10BGo) (repeated measures ANOVA, P > 0.001). Mean density of microfilariae at the calf, hip, and shoulder sites in people living on the Du River was 28.0, 24.5, and 14.1 mf/mg of skin, respectively (Figure 10CGo), and people living in camps on the Farmington River were infected at calf, hip, and shoulder location at 10.2, 7.6, and 5.8 mf/mg of skin, respectively (Figure 10CGo).


Figure 10
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  		    FIGURE 10. Density of microfilariae in three anatomical locations by sex in people living on the Du River (A) and the Farmington River (B), and the total density of microfilariae by body location and river (M, male; F, female).

 
Comparison of the prevalence and intensity of infection on the Du River, permanent creeks, and the Farmington River. The prevalence and intensity of infection are compared in people residing in divisional camps on the Du River, permanent creeks, and the Farmington River (Figure 11Go). The prevalence of infection with O. volvulus in divisional camps close to the permanent creeks (Divisions 9, 40, 29) was intermediate between the Du and the Farmington rivers. The intensity of infection in camps on the permanent creeks was 10.6 mf/mg of skin biopsy, which falls between the values for the camps on the Du River and the Farmington River. This graph also demonstrates a high correlation (r = 0.711) between the prevalence and intensity of infection with O. volvulus on the FRP.


Figure 11
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  		    FIGURE 11. Prevalence and intensity of infection with microfilariae of Onchocerca volvulus on the Du River, permanent creeks, and the Farmington River.

 

DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Keys for identification of Simulium sibling species based on morphologic characters20 or enzyme electrophoresis8,21 do not allow the separation of S. sanctipauli from S. soubrense. In the past, these two sibling species were separated on basis of the chromosomal inversion 2L-7, thought to be absent from S. soubrense.7 When suggesting that the inversion 2L-7 be used in separation of S. sanctipauli from S. soubrense, Vajime and Dunbar7 recognized that the inversion 2L-7 is not "strictly" diagnostic but believed that S. sanctipauli and S. soubrense are valid species. Several other investigators22–25 noticed that the inversion 2L-7 occurs as an intraspecific polymorphism. Quillévéré and others25 treated these two species as subspecies of S. sanctipauli, namely S. sanctipauli sanctipauli and S. sanctipauli soubrense.

This situation was unresolved until Post24 published 2LA as a new diagnostic inversion to differentiate S. sanctipauli s.str. from S. soubrense lacking the inversion 2L-A. He also split S. soubrense into two cytospecies, calling the new taxon S. soubrense "B," characterized by inversion 1L-A. Boakye and others26 formally named S. soubrense "B" as S. leonense sp.n. and split S. soubrense into S. konkourense sp.n., characterized by absence of inversion IIIL-24, and S. soubrense s.str., on the basis of inversions 3L-24, 1S-A, and IIIL-B. None of these three inversions individually are completely diagnostic but together evidently constitute two separate species. Boakye and others26 concluded that the two newly described species S. leonense sp.n. be identified by presence of homozygous inversion IL-A and S. konkourense sp.n. by absence of inversion IIIL-24.

According to Post’s24 reassessment of the taxonomy of the S. sanctipauli subcomplex, the flies breeding in the St. Paul and Lofa rivers are not S. sanctipauli but S. soubrense, which prompted Garms,27 Kashan and Garms,28 and Güzelhan and Garms29 to reexamine the larvae from the St. Paul, Lofa, and Farmington rivers. Because inversions 1L-A and 2L-A do not occur in flies in the Farmington River, the Farmington flies are S. soubrense. Güzelhan and Garms29 confirmed occurrence of S. soubrense in the Farmington River and also reported finding S. leonense (S. soubrense "B") there. Kashan and Garms28 have brought up other differences in inversions between populations of black flies occurring in the St. Paul, Lofa, and Farmington rivers, which necessitate further evaluative study to resolve the taxonomic status of the Farmington population.

Other factors pertinent to evolution of species, such as vector behavior, should be taken into consideration in description of Simulium vector species. Generally, S. soubrense and S. leonense are man-biting flies that are known to transmit O. volvulus to humans. The anthropophily of flies breeding in the Farmington River appears to be sporadic, comprising 1.5% of the annual human-biting in the FRP.9,17 When catching sites were located on the Farmington River (e.g., Division 40),17 the number of flies caught during the whole wet season was 394, and none of them were infected with L3 of O. volvulus. In the dry season, only 13 flies were caught in weekly biting catches on human bait, and none of them were infected with of L3 O. volvulus.17 Filarial larvae different from O. volvulus were sporadically found in the Farmington flies, therefore it is assumed that they are zoophilic.9,17 More emphasis should be given on behavior in characterization of any population of Simulium damnosum s.l. sibling species, because "behavior should be considered as the most important evolutionary determinant, particularly in the initiation of new evolutionary trends."30

The inversion 2L-D, which is almost fixed in the St. Paul River, is completely absent from the Farmington River28; and the inversion 3L-5, which is rare and autosomal in the Farmington River, is common and sex-linked in the St. Paul and Lofa rivers. Some other inversions might be present (or absent) that regard uniqueness of the Farmington flies in Liberia, distinguishing them from S. soubrense in other rivers in Liberia. The occurrence of S. leonense in the Farmington River29 is somewhat surprising. The genetic and chromosomal differences between sibling species indicate that speciation is a genetic and cytogenetic process that occurs in the ever-changing geographic and ecological environment. Possibly the Farmington flies could represent entirely new species. Differences in ecology of aquatic stages and feeding behavior of adult S. yahense, S. soubrense, and S. sanctipauli brought up here reflect the differences in epidemiology of onchocerciasis on the FRP. The two epidemiologic variants of onchocerciasis on the FRP (particularly transmission of O. volvulus by S. yahense in the Du River area and S. soubrense in the Farmington River area) may indicate which divisional camps in the FRP are safer (or more risky) for families to reside to avoid repeated infection with L3 of O. volvulus.

S. yahense flies rarely invade residential divisional camps, and the indoor biting is practically zero, but flies occurring in the rubber-tree growth 20–50 m in distance from the camps may attack people. The S. yahense flies emerging from the Du River disperse throughout the plantation area usually in a short distance from the riverbanks. Other routes of dispersal are the old, not active "dead arms" of the Du River. The standing water in these "dead arms" is overgrown with aquatic plants. Such ecosystems are used as corridors for active dispersal by S. yahense flies emerging from the main stream of the Du River. When people wash dishes and clothes and bathe their children in pools of the Du River "dead arms," they are regularly and intensely bitten by infected S. yahense. One such very active, high-transmission locality is found near the Division 19 camp.

Because the Farmington flies do not prefer to feed on humans, people residing in divisional camps on the Farmington River rarely acquire infection with L3 of O. volvulus at their camps. Such epidemiologic situation reflects the low prevalence and intensity of infection with O. volvulus in people residing in camps near the Farmington River. Their low infections might have been acquired either in their native villages prior to coming to FRP or when residing on the plantation by visiting places along the Du River and permanent creeks. Although the Du River is the primary source of breeding of S. yahense, five permanent creeks, including the Bonnee, Cement, Sia, and an unnamed creek running through Division 9, are all tributaries of the Du River, and they contribute to the size of S. yahense population on FRP. Two permanent creeks, the Vuwe and Hunt, empty into the Farmington River but support predominantly the development of S. yahense.

Received April 6, 2005. Accepted for publication November 4, 2005.

Acknowledgments: The author is grateful to Dr. Aloysius P. Hanson, Director of the Liberian Institute for Biomedical Research, for his interest and support during the course of this study, as well as for making available four laboratories and an insectary for the 14-year tenure of the Johns Hopkins University’s research projects in Liberia. Grateful appreciation is also extended to Sofi M. Ibrahim for inserting the field records into the JHU computer system. I appreciate the diligent service by the following field and laboratory technicians of the Liberian Institute for Biomedical Research: Larry Gee, Isaac Joel, and McKenzoe Kpadiu. I acknowledge the interest and support of Dr. E. Jallah, Director of the Firestone Medical Center, and Dr. Obeng, Director of the LIBR Clinic. The author thanks the Firestone Rubber Plantation management and the Government of Liberia for their interest in this research. I particularly thank Dr. R. Post for his valuable comments on this manuscript.

Financial support: This research on epidemiology of onchocerciasis on the FRP was supported by the Edna McConnell Clark Foundation, contracts 11185 and 1287, and in part by the W. Harry Feinstone Department of Molecular Microbiology and Immunology, Bloomberg School of Public Health, Johns Hopkins University, Baltimore, Maryland 21205.

Author’s address: Milan Trpis, Johns Hopkins University, Bloomberg School of Public Health, Department of Molecular Microbiology and Immunology, Baltimore, Maryland 21205, Telephone: 410-955-3475, Fax: 410-955-3475, E-mail: mtrpis{at}jhsph.edu.

Reprint requests: Milan Trpis, Ph.D., Johns Hopkins University, Bloomberg School of Public Health, Department of Molecular Microbiology and Immunology, 615 N. Wolfe Street, Baltimore, MD 21205, Telephone: 410-955-3475, Fax: 410-955-3475, E-mail: mtrpis{at}jhsph.edu.


REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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