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PubMed1996

Density-dependent processes in the transmission of human onchocerciasis: relationship between microfilarial intake and mortality of the simuliid vector.

In order to construct an analytical model of onchocerciasis transmission, it is necessary to elucidate the functional relationships of the various population rate processes taking place within the human and vector hosts. Two previous papers have explored the evidence for density-dependent regulation in relation to microfilarial intake by, and larval development within, the Simulium host. This paper investigates the survivorship of wild-caught blackfly samples fed on subjects with different intensities of Onchocerca volvulus microfilarial infection. Analyses were based on data for Guatemalan S. ochraceum s.l. (possessing a well-developed cibarial armature), West African S. damnosum s.l. (forest species), and South Venezuelan S. guianense (the latter two lacking a toothed cibarium). The mean survival times of samples of the 3 species, kept under laboratory conditions, decreased as parasite intake increased, the rate of mortality being dependent on the fly's age (measured as time post-feeding) and on the worm load acquired. An empirical, time-dependent hazard function was fitted to observed death rates/fly/day which rose very shortly after engorgement, declined subsequently, and rose again throughout the extrinsic incubation period of the parasite. The parameters of this hazard model were all positively correlated with the density of microfilariae in the bloodmeal. Expressions of survivorship and life-expectancy as explicit functions of time post-feeding and mean parasite intake were derived. The average expectation of life at engorgement for uninfected flies in the laboratory was estimated to be around 1 week for both, armed and unarmed blackflies. Residual life-expectancy decreased with time post-feeding and microfilarial load in both categories of vectors. This decline (resulting from age- and parasite-dependent mortality rates) was much more pronounced in those species lacking a toothed fore-gut. Whilst a fraction of heavily infected S. ochraceum was able to survive the latent period of the parasite, being therefore potentially capable of transmitting the infection, equivalent worm loads in S. guianense resulted in a drastic reduction of the expectation of infective life. These results provide additional evidence to support the hypothesis that, in the case of intrinsically susceptible vectors, unarmed simuliids are more efficient at low microfilarial loads, when the transmission rate from human to vector host is higher, and parasite-induced fly mortality is negligible. The opposite takes place in armed flies, which perform poorly at low parasite burdens and better at heavier loads, with little parasite-induced vector death.

Animals↗
PubMed1993

The effects of vector control on the antibody response to antigens of Onchocerca volvulus.

The effects of exposure to infective larvae on the antibody response to a cocktail of specific recombinant antigens of Onchocerca volvulus and to a worm extract were evaluated by comparing the responses of individuals from a vector controlled area with those from an area of continuing transmission by ELISA. Individuals from the vector controlled areas were found to have reduced responses to both antigen preparations. A microfilerdermic (mf-) individuals from the area of vector control exhibited significantly lower total and subclass IgG responses to the worm extract. In contrast, the responses to the cocktail of specific recombinants were significantly reduced in individuals from the area of vector control who were still microfilerdermia positive (mf+). The distribution of IgG subclass specific responses was similar to both antigen preparations, both dominated by the IgG4 and IgG1 subclasses. IgG1 responses to the worm extract remained elevated in the vector controlled individuals but IgG4 was significantly reduced in the mf- individuals. Both subclasses reflected the total IgG response to the cocktail of recombinants and were significantly reduced in individuals from the vector controlled area, when compared to individuals from the hyperendemic area. IgG1 responses to the cocktail of recombinants are significantly lower than IgG4 in all individuals and virtually absent in individuals from the vector-controlled area. Measuring total IgG and IgG4 is more sensitive than IgG1 in detecting infection, 100 or 97% respectively, but they remain elevated in the individuals from the vector controlled areas even after 8-10 years interruption of transmission. These results have important implications for the serological monitoring of control programmes in individuals who have previously been infected.

Analysis of Variance↗
PubMed1994

The effects of Onchocerca lienalis infection on vitellogenesis in the British blackfly, Simulium ornatum.

We have previously described the major yolk protein, vitellin, in the British blackfly Simulium ornatum Meigen. Here we demonstrate that vitellogenin, synthesized in the fat body and secreted into the haemolymph, is composed of subunits with the same approximate molecular weight as vitellin, namely 200 and 68 kDa. Simulium ornatum is the natural vector for the cattle filarial nematode Onchocerca lienalis Stiles, which induces host fecundity depletion. A significant reduction in ovarian vitellin content was associated with infection by intrathoracic injection of 20 O. lienalis microfilariae immediately after blood-feeding. Fat body synthesis of vitellogenin was significantly reduced as early as 8 h post-infection in comparison with sham-injected flies. When total haemolymph protein from infected and sham injected flies was compared, titres were significantly depressed 6 h post-infection. However, later in the infection, titres were elevated by 30%, the major component being vitellogenin. The injection of dead microfilariae had no effect. An infection burden of a single parasite caused a significant reduction in ovarian protein content in comparison with shams, but no further significant decrease was observed as the parasite burden was increased from 5 to 20. Possible mechanisms underlying the disturbance of Simulium reproductive physiology are proposed.

Animals↗
PubMed1994

Density-dependent processes in the transmission of human onchocerciasis: intensity of microfilariae in the skin and their uptake by the simuliid host.

The transmission success of Onchocerca volvulus is thought to be influenced by a variety of regulatory or density-dependent processes that act at various points in the two-host life-cycle. This paper examines one component of the life-cycle, namely, the ingestion of microfilariae by the simuliid vector, to assess the relationship between intake of larvae and the density of parasites in the skin of the human host. Analysis is based on data from three areas in which onchocerciasis is endemic and includes published information as well as new data collected in field studies. The three areas are: Guatemala (Simulium ochraceum s.l.), West and Central Africa (savanna members of the S. damnosum complex), and South Venezuela (S. guianense). The data record experimental studies of parasite uptake by flies captured in the field and fed to repletion on locally infected subjects who harboured varying intensities of dermal microfilarial infection. Regression analyses of log transformed counts of parasite burdens ingested by the flies plotted against log transformed counts of microfilariae per mg of skin revealed little evidence for saturation in parasite uptake by the flies as the intensity in the human host increased. There was a positive and highly significant rank correlation between both variables for the three blackfly species. In an alternative analysis a model was fitted to data on prevalence of flies with ingested microfilariae (mff) versus dermal mean intensities. The model assumed an overdispersed distribution of the number of mff/fly and a given functional relationship between intake and skin load. The results of both approaches were consistent. It is concluded that parasite ingestion by the vector host is not strongly density dependent in the three geographical areas and ranges of dermal loads examined. It therefore appears that this transmission process is of reduced importance as a regulatory mechanism in the dynamics of parasite population growth.

Africa, Central↗
PubMed1995

Chemical guidance of Onchocerca lienalis microfilariae to the thorax of Simulium vittatum.

The behavioural responses of Onchocerca lienalis microfilariae (mf) to tissue factors of the surrogate black fly host, Simulium vittatum, were studied using a novel in vitro bioassay. Mf accumulated towards thoracic tissues to a density 4 times higher than towards abdominal tissues, despite the larger surface area and volume of abdominal tissues. Mf migrated toward thoracic tissues regardless of whether or not contact with thoracic tissues was possible. Therefore, mf directed themselves toward the thorax rather than arresting their movement after they make contact with thoracic tissues. Chemical cue(s) provided a principal guidance for mf to locate thoracic tissues. Mf lost their ability to differentiate thoracic and abdominal tissues following addition of thoracic attractant(s) to excised abdomens and reversed their differential response when excised thoraces were depleted of chemical cue(s). Mf did not respond to salivary gland product, but to other thoracic factor(s). Intact thorax that was connected to 1-2 abdominal segments attracted considerably less mf than excised thorax. However, intact thorax attracted more mf than excised abdomen. Abdominal tissue size did not affect thorax attractiveness. Involvement of a large molecular weight protein(s) was suggested by the high attractiveness of the 100 kDa Centricon concentrator retentate and complete precipitation of attractant(s) by ethanol.

Animals↗
PubMed1998

Parasite manipulation of insect reproduction: who benefits?

Host fertility is often curtailed as a result of parasitic infection. The hypothesis that this may confer an adaptive advantage upon the symbionts if nutrients are directed from reproduction and made available for host/parasite maintenance is explored. The suggestion is made that an understanding of the mechanisms underlying the pathophysiology of fecundity reduction may shed light upon the evolutionary implications of this strategy for both parasite and host. To illustrate this the down-regulation of egg production is explored with reference to a particular model system, the association between metacestodes of the rat tapeworm, Hymenolepis diminuta and the mealworm beetle, Tenebrio molitor. Several aspects of host reproductive behavior and physiology are affected by infection in this association, including vitellogenesis. Metacestodes directly inhibit the fat body synthesis of vitellogenin in a stage-specific, density-dependent manner. This inhibition is likely to be orchestrated by a modulator molecule, produced by the parasite. In the ovarian follicles, juvenile hormone III binding to a specific follicular membrane-binding protein is inhibited in infected beetles, resulting in the down-regulation of a cascade of events which enables vitellogenin to pass into the developing oocyte. Data to support the proposed existence of a parasite-induced antigonadotrophin, of host origin, are discussed. Evidence that similar mechanisms operate in Plasmodium-infected anopheline mosquitoes and Onchocerca-infected blackflies is presented in support of the possibility that a parasite-induced reduction in host reproductive fitness is an adaptive strategy and an assessment of who is manipulating whom is made.

Animals↗
PubMed2001

Integrin-like RGD-dependent cell adhesion mechanism is involved in the rapid killing of Onchocerca microfilariae during early infection of Simulium damnosum s.l.

Injection trials with compatible and non-compatible Onchocerca species into S. damnosum s.l., the vector of human and bovine onchocerciasis, demonstrated that the rapid killing of microfilariae within the blackfly's haemocoel is species specific. In the presence of the peptide RGDS as a blocking agent for integrin-like receptors of haemocytes, the survival of O. ochengi microfilariae in its natural intermediate host was significantly increased. This increased survival 24 h p.i. correlated with a significant decrease of apoptosis levels in the microfilariae following a 2 h exposure to the haemolymph in vivo. These findings suggest that haemocytes are directly involved in the killing of Onchocerca microfilariae in the blackfly.

Animals↗
PubMed2002

Humoral immune response of Simulium damnosum s.l. following filarial and bacterial infections.

The time-course of the humoral immune response of female blackflies after a challenge with bacteria, different Onchocerca microfilariae species, bacterial endotoxin and microfilarial extract was investigated. Strong bacteriolytic and growth inhibition activities against the Gram-positive bacterium Micrococcus luteus were induced by all agents. Specific differences were found in activity levels and time-course. Notably the endotoxin lipopolysaccharide (LPS) induced a very early, profound bacteriolytic and antibacterial response, which declined within a day after injection. In contrast, the bacteriolytic activities after Escherichia coli D31 and Onchocerca microfilariae infections were lower, but remained elevated over the observation period of 4 days. The bacteriolytic activity was correlated to a haemolymph protein with a molecular weight of around 14 kDa. Anti-Gram-positive activity in the E. coli infected group appeared within the first 6 h. However, it took 4 days in the microfilarial infected blackflies to reach significant levels. The active agent was identified to be a peptide with a molecular weight of around 4-4.5 kDa. Activity against the Gram-negative bacteria E. coli was detected in blackflies injected with E. coli D31, O. dukei microfilariae and microfilarial extract on days 1 and 4 after injection. The immune response in S. damnosum s.l. naturally infected via a bloodmeal on cattle supported the findings of the experimental infections. Similarities of the immune response kinetics between bacterial and filarial infections suggested that intracellular Wolbachia bacteria, released from microfilariae, could be responsible for the antibacterial response. This is supported by the observation that the induction of an immune response in the Drosophila melanogaster mbn-2 cell line by the filarial extract is blocked by polymyxin B, which forms inactive complexes with bacterial LPS.

Animals↗
PubMed2004

The current status of onchocerciasis in the forest/savanna transition zone of Côte d'Ivoire.

Onchocerca volvulus exists in at least two strains in West Africa, while its black-fly vectors consist of sibling species, dwelling in the savanna and forest/transition zones. In transition and degraded forest zones both parasite strains and different sibling species of the vector can be sympatric. The strain of parasite in infected humans and in vector black-flies was determined in two bioclimes along the Bandama river of Côte d'Ivoire. The upper Bandama is located in the savanna bioclime while the Middle Bandama is located in a degraded forest zone. At both sites, savanna-dwelling sibling species of the Simulium damnosum sensu lato species complex predominated. The severe-strain of O. volvulus was the predominant strain at both sites. However, severe-strain parasites represented a significantly larger proportion of those found in the vector population than in the human population in the degraded forest of the Middle Bandama. These data suggest that in degraded forest areas recently invaded by savanna-dwelling species of S. damnosunz s.l. transmission of the severe-strain of the parasite might be more efficient than transmission of the mild-strain.

Animals↗
PubMed1998

Onchocerca ochengi: epidemiological evidence of cross-protection against Onchocerca volvulus in man.

In North Cameroon, the vector of Onchocerca volvulus (causative agent of human onchocerciasis) also transmits 2 filariae of animals: O. ochengi from cattle and O. ramachandrini from wart hogs. In order to assess the qualitative and quantitative roles of these 'animal filariae' in the epidemiology of O. volvulus, the transmission of the 3 parasites was measured in 2 villages and related to the endemicity of human onchocerciasis. In Galim, a cattle-farming Guinea savanna village where wild animals are rare, the overwhelming majority of all filarial infections found in the Simulium damnosum s.l. vectors throughout the year were O. ochengi (89%). The remaining infections were mainly O. volvulus (10.5%), and a few O. ramachandrini (0.5%). In Karna, a crop-farming Sudan savanna village where cattle are rare, but wild animals common, flies were also more frequently infected with animal filariae than with the human parasite. In the dry season, when nomadic cattle are present, 54% of all infections were O. ochengi, 36% O. volvulus and 10% O. ramachindrini. In the rainy season, when the cattle move away, flies were mainly infected with O. ramachandrini (52% of all infections) and secondly with O. volvulus (48%). In Karna, the relationship between the Annual Transmission Potential (ATP) of O. volvulus and its prevalence in the human population conformed to other onchocerciasis foci, in that a moderate ATP led to hyperendemic onchocerciasis. In Galim, however, a 7-fold higher O. volvulus-ATP (caused by a very high biting rate of the flies) contrasted with a strikingly low endemicity of onchocerciasis. Since, at the same time, in Galim the transmission of O. ochengi (measured on man) was very high (15,000 L3/fly collector/year), we hypothesize that the reduced endemicity of onchocerciasis in Galim is due to 'natural heterologous vaccination' by the large annual number of O. ochengi-L3, inoculated into man by anthropo-boophilic S. damnosum s.l. The importance of micro-epidemiology for the understanding of the interlinkage of human and animal onchocerciasis is discussed.

Animals↗
PubMed1998

Onchocerca ochengi: morphological identification of the L3 in wild Simulium damnosum s.l., verified by DNA probes.

In order to assess the prevalence of the cattle filaria Onchocerca ochengi in onchocerciasis vectors (Simulium damnosum s.l.) in North Cameroon, we searched for a means to morphologically identify its developing larvae, which closely resemble those of O. volvulus. To this end microfilariae of the 2 Onchocerca species were isolated from slaughter cattle in Ngaoundéré and injected into neonate Simulium species. Whereas the early developmental stages (sausage stage, L2 and pre-infective larva) were indistinguishable, the infective larvae (L3) of O. ochengi were longer (median: 740 microns), more slender (diameter = 19.3 microns = 2.6% of body length) and had a relatively shorter tail (4.9% of body length) than those of O. volvulus (680 microns, 20.5 microns, 3.0% and 5.8% respectively). The tail of O. ochengi L3 was thick and rounded, whereas it was slightly tapering in O. volvulus L3. O. ochengi L3 produced by feeding flies on infected cattle in a different area in North Cameroon (Sora Mboum) showed the same features as intrathoracically produced O. ochengi L3 from Ngaoundéré, but were even longer (785 microns). On the basis of the differences in length, relative diameter, length of the tail and shape of the tail, a simple key for the separation of O. volvulus and O. ochengi L3 was elaborated, and 248 L3 found in wild S. damnosum s.l. were separated into 'O. ochengi' (160 L3) and 'O. volvulus' (88 L3) following this key. Sequential dot blot hybridization of each of the 248 larvae with a DNA probe which reacts with O. ochengi and O. volvulus but not with other Onchocerca species (pOo5/1) and with an O. volvulus-specific DNA probe (pOv12) revealed that the morphological identification had been correct in 86-91% of the cases. Only a small proportion (6-9%) of the dot blots did not react with either probe. Since this proportion was equal in experiments using experimentally produced L3 and in experiments using wild L3, the nonhybridization was certainly due to a loss of L3 during washing of the filters and not due to the presence of other unknown L3 species resembling O. volvulus and O. ochengi. Our study shows that in Cameroon it is possible to identify O. volvulus and O. ochengi infective larvae during routine fly dissections by morphology alone.

Animals↗
PubMed1998

Onchocerca ochengi: assessment of the Simulium vectors in north Cameroon.

In the savanna areas of tropical Africa, cattle are frequently infected with the filaria Onchocerca ochengi. This parasite is closely related to Onchocerca volvulus, the causative agent of human onchocerciasis (river blindness), and is capable of developing in the same vector, Simulium damnosum s.l. In North Cameroon, where both O. ochengi and O. volvulus are endemic, we carried out a field study (reported in this and 2 following papers) to examine to which extent the transmission of the 2 parasite species overlap and what influence this has on the epidemiology of human onchocerciasis. In this paper we report our experiments to determine which of the S. damnosum species in North Cameroon act as vectors of O. ochengi, how efficiently they do so and whether other Simulium species play a vector role. To this end, infected cattle were exposed near 5 rivers in different geographical areas. Among 14 Simulium species identified as aquatic and/or adult stages at these rivers, only 6 (S. squamosum, S. damnosum s.s., S. sirbanum, S. bovis, S. wellmanni and S. hargreavesi) were found to bite cattle in important numbers in at least 1 of the sites. The 3 species of the S. damnosum complex were all capable of ingesting microfilariae (mf) of O. ochengi and developing a proportion of them to infective larvae (L3). Whereas S. squamosum and S. damnosum s.s., the prevailing vectors in the Guinea and Sudan savanna respectively, showed a high vector competence (17% of ingested mf developed to L3), S. sirbanum, which was much rarer in both areas, appeared to have a much lower susceptibility (2%). Other boophilic Simulium species were only seen in certain sites and seasons, being either incapable of ingesting important numbers of O. ochengi mf from body regions where these mf were abundant (S. bovis, S. hargreavesi); not able to support the development of ingested mf to L3 (S. wellmanni), or bit cattle preferentially in the ears, where O. ochengi mf do not occur (S. hargreavesi). We conclude that in North Cameroon members of the S. damnosum complex are the only important vectors of O. ochengi, with S. squamosum and S. damnosum s.s. being the main vectors.

Animals↗
PubMed1999

Effects of an Onchocerca-derived cysteine protease inhibitor on microfilariae in their simuliid vector.

A recombinant cysteine protease inhibitor, onchocystatin of the parasitic nematode Onchocerca volvulus, was tested for its role in microfilarial development in the simuliid vector. Onchocystatin was found to be present in female adults and skin microfilariae of the bovine parasite O. ochengi, the closest relative of O. volvulus. In addition the inhibitor could be detected as an excretory-secretory (E-S) product of the microfilariae. Co-injection of onchocystatin and the O. ochengi microfilariae into the surrogate vector Simulium ornatum s.l. significantly enhanced the recovery rates of the parasite within 24 h into the infection (P > 0.001). The findings suggest a possible role of onchocystatin in the evasion by the parasite of the immune response of its vector.

Animals↗
PubMed1999

Detection of Onchocerca volvulus infection in Simulium ochraceum sensu lato: comparison of a PCR assay and fly dissection in a Mexican hypoendemic community.

Detection of Onchocerca volvulus larvae in vector populations is of prime importance in the assessment of the effectiveness of onchocerciasis control programmes. Traditionally, detection of larvae is attained by the dissection of flies, but this time-consuming method cannot easily discriminate between species of Onchocerca. The genome of all Onchocerca species has a unique 150 bp repeat, which can be amplified by PCR, and O. volvulus-specific DNA probes can detect these products by Southern blot (SB). This study optimizes a PCR/SB assay, and compares it with fly dissection to estimate the prevalence (p) and intensity of infection (m) in the local vector population of a Mexican community that has become hypoendemic as a result of 7 years of treatment with ivermectin and nodulectomy. The PCR detected 1 infected fly in a pool of 99 uninfected flies, but the optimal pool size was 50 flies. At the community level, 1 out of 10,550 flies was positive (p = 0.0095%, 95% confidence intervals CI = 0.00024-0.05280%; m = 0.00027 larvae/parous fly, CI = -0.00026-0.00081) by PCR, and 4 out of 10,772 flies (p = 0.0371%, CI = 0.01012-0.09505%; m = 0.00107 larvae/parous fly, 95% CI = 0.00002-0.00212) by dissection (observed m = 0.0005). Both methods produce statistically similar estimates of the prevalence and intensity, indicating that pool screening is a viable alternative for entomological surveillance in areas where the intensity of transmission is becoming extremely low as a result of control interventions.

Animals↗
PubMed2000

Onchocerca-Simulium complexes in Venezuela: can human onchocerciasis spread outside its present endemic areas?

The compatibility between sympatric and allopatric combinations of Onchocerca volvulus-anthropophilic species of Simulium was studied in the north-eastern focus of human onchocerciasis as well as in a densely populated locality of the Amazonas State in Venezuela. The objectives were to test the conjecture that local adaptation exists between the parasite and its vectors (the Onchocerca-Simulium complex hypothesis), and assess the possibility of the infection spreading from its present distributional range. For the homologous combination, O. volvulus-S. metallicum cytospecies E in Anzoátegui State (north-eastern focus), parasite yield was 45% in contrast to 1% for the heterologous, southern parasite-S. metallicum infection. This was significantly lower than the parasite yield (4-10%) expected after allowing for the effect of density-dependent limitation of infective larval output described in this paper for S. metallicum. The population of S. exiguum s.l. from southern Venezuela allowed no larval development beyond the L1 stage of either northern or southern parasites. Mechanisms for such refractoriness probably operate at the level of the thoracic muscles, not affecting microfilarial uptake or migration out of the bloodmeal. The parasite yield of southern O. volvulus in S. oyapockense s.l. flies biting man at Puerto Ayacucho (Amazonas) was about 1%, in agreement with the figures recorded for highly compatible sympatric combinations such as O. volvulus-S. ochraceum s.l. in Guatemala. No infective larval development of the northern parasite was observed in southern S. oyapockense. These results, together with considerations of typical worm burdens in the human host, presence/absence of armed cibaria in the simuliids, parasite-induced vector mortality, and fly biting rates, suggest a lower potential for onchocerciasis to spread between the northern and southern endemic areas of Venezuela than that between Amazonian hyperendemic locations and settlements outside this focus with high densities of S. oyapockense s.l.

Adult↗
PubMed2003

Larval polytene chromosomes of black flies (Simulium) from Thailand. I. Comparison among five species in the subgenus Gomphostilbia enderlein.

Larval polytene chromosome maps of Simulium (G.) asakoae and S. (G.) sp. g in the ceylonicum-group and S. (G.) angulistylum, S. (G.) decuplum and S. (G.) siamense in the batoense-group of the subgenus Gomphostilbia from Thailand are presented. These species have three pairs of chromosomes (2n = 6). Light stained centromeric bands were observed in the chromosomes of S. (G.) asakoae, S. (G.) sp. g, S. (G.) decuplum and S. (G.) siamense, whereas heavy dark centromeric bands were present in S. (G.) angulistylum. The best distinguishing character of Simulium species in the subgenus Gomphostilbia is the position of the nucleolar organizer in the short arm of chromosome I. The Ring of Balbiani and the double bubble are located in chromosome arm IIS in all species except for S. (G.) angulistylum, which showed these cytological markers in chromosome arm IIIS. A low chromosomal polymorphism was recorded in all species except for S. (G.) sp. g, which exhibited a standard polytene chromosome. Inversion polymorphisms found in this study conformed to Hardy-Weinberg equilibrium and were not associated with sex. These species have different specific markers and banding patterns although homologous banding sequences were found in chromosome arm IIS in S. (G.) asakoae, S. (G.) sp. g, S. (G.) decuplum and S. (G.) siamense and chromosome arm IIIS in S. (G.) angulistylum. Our results showed no evidence of a sibling species complex within any taxon.

Animals↗