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Microfilariae of Onchocerca cervicalis were detected in midventral skin biopsy samples in 64 of 84 (76%) mixed-breed ponies greater than 2 years old from the Gulf Coast area and in 42 of 51 (82.4%) horses from Louisiana breeding herds. The number of microfilariae per 8 mm of biopsied skin (ponies) ranged from 1 to 21,570. The number of microfilariae per 6 mm of biopsied skin (horses) ranged from 8 to 55,600.
A simple compartmental process, which is time-homogeneous and has differing transition rates between compartments, is discussed. When such a process is hierarchical, with all individuals released into the first compartment, the resulting distribution of individuals over the various compartments is multinomial. This process is applied to the migration of Onchocerca volvulus in simuliids and appears to represent successfully the early migration from the stomach through the abdomen to the thorax, provided that allowances are made for the engorgement period and the encapsulation of the blood meal by a peritrophic membrane.
To determine the susceptibility of a heterologous filarial antigen for measuring Onchocerca volvulus antibodies, worms were compared using an enzyme-linked immunosorbent assay (ELISA) test. Control serum samples from helminth-free U.S. residents and from helminth-infected but filariae-free Salvadoran residents were tested and compared with serum obtained from microfilariae-positive and -negative Guatemalan residents living in an area of endemic onchocerciasis. The results showed that none of the sera from U.S. residents had positive O. volvulus ELISA titers (greater than or equal to 1:160); however, 8.51% (4/47) had positive B. malayi ELISA titers (greater than or equal to 1:640). The geometric mean titers with the B. malayi ELISA test were higher than with the O. volvulus ELISA test--in sera from 47 U.S. residents (1:219 vs. 1:49), from 108 Salvadoran residents (1:92 vs. 1:71), and from 145 microfilariae-negative (1:539 vs. 1:167) and 303 microfilariae-positive (1:1,270 vs. 1:561) Guatemalan residents. The B. malayi ELISA test exhibited slightly less sensitivity than the homologous O. volvulus ELISA test; nevertheless, a good correlation (r = 0.74) was found between the 2 test antigens, indicating that the B. malayi antigen could be used to measure O. volvulus antibodies.
Third-stage larvae of Onchocerca volvulus and O. lienalis were observed to molt to the fourth stage in various cell-free in vitro systems. The percentage of O. lienalis completing the molt was similar in the three culture media and two gas phases tested ranging from 44.8% (1:1 IMDM:NCTC + 5% CO2: 95% N2) to 56.7% (L-15 + 5% CO2: 95% air). Percent molting in O. volvulus ranged from 0% (F12(K) + 5% CO2: 95% N2) to 33.3% (L-15 + 5% CO2: 95% N2). All media were supplemented with either 20% FCS or 20% horse serum. Molting by O. lienalis occurred on days 2-5 in culture. Molting by O. volvulus was observed as early as day 5 and as late as day 10. Incomplete casting of the third-stage cuticle was frequently observed in O. volvulus. Larvae of both species entered a lethargus 24-48 hours prior to the onset of molting. Maximum survival in culture was 42 days for O. lienalis and 25 days for O. volvulus. Significant growth of larval O. lienalis was noted early in the culture period, but neither species continued development to the fifth stage.
Simulium ornatum s.l. is a natural vector of Onchocerca lienalis in Britain. These studies investigated the role of the blood meal on the development of the parasite in the thoracic musculature. Infection was by the standard technique of intrathoracic injection, allowing precise doses of microfilariae to be administered. Prior to infection flies were fed on bovine blood through a chick skin membrane. In 3 trials the number of O. lienalis larvae developing in non-blood fed flies was between 60.2 and 68.4% lower than in blood fed insects. The mean number of eggs recovered per fly ranged from 131.7 to 187.5 in infected groups. In uninfected control groups the levels ranged from 315.4 to 378.1 per fly. This represents reductions in fecundity of between 50.4 and 51.7% in infected groups of simuliids. It appears that in order to maintain relatively high levels of transmission an intermediate blood meal, between uptake of microfilariae and release of infective stage larvae, may be important. Furthermore, great care must be taken when using fecundity to assess the age of simuliids. Levels of parasitic infection may affect egg production to a much greater extent.
Biting flies were collected from the umbilical areas of Onchocerca lienalis-infected cattle in New York (state) from June through September of 1980. Of the 766 flies collected, 705 were Simulium jenningsi. Microfilariae were detected in the midguts of 37 (50%) of 73 females dissected immediately after the flies had fed. The mean number of larvae per positive fly (fly with microfilariae) was 15.2. Third-stage larvae were recovered from 25 (21.9%) of 114 S jenningsi dissected 8 to 13 days after they had fed on the infected cattle; the mean number of 3rd-stage larvae per positive fly was 3.5. Dissections of flies performed on days 1 through 7 after feeding yielded various numbers of 1st and 2nd-stage larvae from the thoracic muscles. Ovarian dissections performed on 304 S jenningsi attacking cattle indicated an overall parous rate of 58%. Naturally occurring infections with filarial larvae indistinguishable from O lienalis were found in 7.3% of the parous females. Three of these flies, or 1.7% of the parous collection, harbored 3rd-stage larvae. The onset of naturally occurring filarial infections in the population of S jenningsi coincided with a peak in the parous rate in late June. Thereafter, filarial infections were generally detected when the parous rate was above 50%.
The macrofilaria population was analysed in a hyperendemic focus in western Upper Volta to determine the effect of eight years of Simulium control on the adult Onchocerca volvulus. During the first months of 1983 in three neighbouring villages 629 out of 786 inhabitants were examined for onchocerciasis and from 76 patients as far as possible all onchocercomata were extirpated. The macrofilariae were isolated from the nodules after collagenase digestion and examined microscopically. There were no major differences between men and women or different age groups. The average worm burden was 9.8 live macrofilariae per patient. All worms were several years old but developing sperms were found in 94% of the male and embryos in 55% of the female filariae. 36% of all worms were dead and 23% were calcified. Compared with the findings in a Liberian focus with continuous transmission it is concluded that the interruption of the transmission has lead to a reduced worm burden of entirely old worms but that a few more years of control will be needed until the production of microfitariae will end.
Forty horses having microfilariae of Onchocerca cervicalis in association with dermatitis, alopecia, and pruritus on the ventral midline were given a single IM injection of 0.2 mg of ivermectin/kg of body weight (June to August 1981). Microfilarial counts in the 40 horses ranged from 18 to 42,446 microfilariae/skin snip on the day of treatment, and histopathologic examination of these skin sections indicated a chronic eosinophilic dermatitis. Numerous microfilariae were in the dermis, but there was no consistent relationship between the presence of microfilariae and the severity of the inflammatory reaction. In all 40 horses, skin snips taken 4 to 33 days after treatment were negative for microfilariae, and a marked clinical improvement occurred 2 to 3 weeks after treatment, when the lesion was replaced by healthy skin and new hair. Twenty-four hours after treatment, an edematous reaction occurred on the lower portion of the abdomen of 4 (10%) horses and within the area of the lesion in 6 (15% horses). The reactions disappeared within 24 to 72 hours, irrespective of whether horses were treated with corticosteroids. When further skin samples were taken from 15 horses 4 to 9 months later, 9 of them were free of microfilariae and the 6 others had only low counts (17 to 97). An additional 7 infected horses, treated when there was little chance of reinfection (November to December 1981), were all free of microfilariae at 6 to 10 days and 4 to 5 months after treatment. The marked clinical improvement in all horses after disappearance of microfilariae from the dermis indicates that microfilariae are involved in the cause and pathogenesis of the dermatitis.
Two species of Simulium were used to examine the effect of experimental Onchocerca lienalis infections on their fecundity and oviposition rates. S. ornatum s.l. was chosen as a natural vector of bovine onchocerciasis in Britain, and S. lineatum was selected because of its suitability as an experimental model for oviposition studies. Infection was either by feeding with blood containing microfilariae, or by intrathoracic injection of the parasites. Using the blood feeding technique, reductions in the fecundity of S. lineatum were observed at rates of 21 to 76%, depending on the concentration of parasites. A reduction of 21% in the fecundity of S. ornatum s.l. (P less than 0.05) was achieved when flies were fed on microfilariae at 69,000 per ml. Although individual flies feeding on infected blood may take as much as those in control groups, the feeding rates were reduced in several instances. S. lineatum also showed a depression of oviposition rate when infected by O. linenalis larvae. Fecundity was also significantly reduced when the route of infection was intrathoracic. Reductions for S. lineatum depended on the inoculum, but were either 36% (10 microfilariae per fly) or 54% (50 microfilariae per fly). S. ornatum s.l. showed a 13% reduction in fecundity when given 20 microfilariae per fly. It was concluded that similar experimental studies could be usefully performed with S. damnosum s.l. infected with O. volvulus microfilariae.
The limited accessibility of specimens of Onchocerca volvulus has hampered investigations of factors that determine the clinical course of infection of man by this filarial nematode. Parasites antigenically related to O. volvulus have been variously proposed as alternative sources of test antigens. The present study has utilized serologic methods to probe the degree of identity of the antigenic constituents of O. volvulus and Dirofilaria immitis, the dog heartworm. 35S-methionine-labeled proteins of dog heartworm microfilariae (mf) were analyzed in immunoprecipitation assays by using a panel of sera drawn from humans diagnosed for onchocerciasis and from canines infected with D. immitis. Unique and common antigens detected by these sera were resolved in polyacrylamide gels. The majority of high-titered human and infected dog sera reacted with antigenic molecules estimated at 15, 16, 28, 42, 54, 66, and 100 kilodaltons. In addition, a subset of these sera detected large amounts of a 75 kilodalton antigen. Human anti-O. volvulus antibodies were found to bind to intact glutaraldehyde-fixed mf of D. immitis in immunoperoxidase assays. In enzyme-linked immunosorbent assays, the same sera reacted with extracts of three distinct developmental stages of the canine pathogen--namely, the mf, embryonated eggs, and adult worms. Preincubation of dirofilarial antigens with human anti-O. volvulus sera inhibited the binding of dog anti-heartworm serum by as much as 70%. Sera of guinea pigs hyperimmunized with mf of O. volvulus inhibited the binding of the immune dog serum to the same extent. These results represent evidence for extensive homology in the antigenic composition of O. volvulus and D. immitis.
Three species of British blackflies, Simulium ornatum s.l., S. erythrocephalum and S. lineatum, were infected with the cryopreserved microfilariae of Onchocerca volvulus obtained from human skin-snips in the Sudan. Doses of 5 or 10 microfilariae per fly were administered by intrathoracic injection into females, 1-2 days after eclosion from pupae. After 7 days at 27.5 degrees C and 85% relative humidity, microfilariae had completed development to third-stage larvae. Fly survival rates were highest for S. ornatum (96%) and lowest for S. lineatum (56%), and fell only marginally in each species when the larger dose of microfilariae was given. Infection rates ranged from 42% in S. lineatum up to 58% in S. ornatum following the lower dose of microfilariae, and 58% in S. lineatum up to 79% in S. ornatum following the higher dose. The proportion of microfilariae which completed development was relatively constant in each species of fly, ranging from 3.1-4.2% in S. lineatum to 10.5-16.8% in S. erythrocephalum. The greatest number of third-stage larvae recovered came from S. erythrocephalum at the higher dose of microfilariae, with a mean of 2.4 larvae per infected fly. As S. erythrocephalum has been successfully colonized through several generations in the laboratory, it is concluded that this is a promising species for reselection for increased susceptibility to O. volvulus.
Microfilariae of Onchocerca gutturosa were extracted from the skin of the bovine naval by teasing in saline and then suspending the skin in a gauze bag overnight in Tyrode's solution with 20% human serum. They survived for ten days in this medium, with antibiotics, in plastic microtitration plates at 11 C. After dispersal in flat containers, microfilariae slowly assumed clumped dispersion patterns. They also accumulated in glass wool, suggesting that aggregation was a tactile phenomenon. Analysis of videotapes of microfilarial movement indicated that activity, expressed as the number of undulations present on the body and the rate of knot formation (where the microfilaria held itself tightly coiled), increased up to 40 C and thereafter declined. The rate of headwave formation, however, appeared constant up to 40 C after which it declined. Where the greatest number of undulations were found on the body the wave amplitude was minimal. Because greater apparent activity was not correlated with increased forward progression, microfilariae at lower temperatures may travel farther than those at 40 C. This may relate to site preference in the host and to uptake by the vector Simulium ornatum.
The effects of temperature on the development of Onchocerca volvulus in Simulium ochraceum, and on the vector's longevity were studied under simulated environmental conditions in the laboratory. When S. ochraceum (which had fed on a person infected with O. volvulus) were maintained at different, constant temperatures (10-30 C), larvae developed to the infective stage between 20 and 28 C. The time required for development to the infective stage depended on the relationship of y = -0.3760 + 0.0222x (y = velocity in development; x = rearing temperature). However, larval development to the infective stage occurred in all groups kept at different temperatures by day and by night (25 C during the day and 10-18 C during the night), although the developmental period was prolonged (10 days in the group held at 25/18 C, and 13 days in other groups). The percentage of females harboring infective larva(e) among those maintained was highest at a constant temperature of 22 C (21.9%), followed by 15.0% at 25 C. When S. ochraceum females were held at day/night differing temperatures, much higher rates were observed at 25/16 C (30.0%) and at 25/14 C (23.0%). Our results suggest that the distribution of onchocerciasis in Guatemala may be related to ambient temperature and to day/night temperature cycles.
Two sets of controlled experiments were conducted, using 13 adult onchocerciasis patients from a village in the hyperendemic rain-forest zone of Western Nigeria, to determine the effect of the excision of one or two onchocercal nodules on the concentration of microfilariae in the skin. The results show that, in patients with established infections who are exposed to continuing reinfection, nodulectomy per se does not reduce the microfilarial density, overall or in the same anatomical region from which the nodule is excised, to any significant degree. It is therefore concluded that the indirect assessment of the activity of test drugs against the adult Onchocerca volvulus by serial estimation of microfilarial concentrations over a period of about 24 months is unlikely to be compromised by limited selective nodulectomy.
Male and female Onchocerca volvulus from Liberia, Upper Volta, Tanzania and Guatemala were examined by scanning and by transmission electron microscopy. In the cuticle of the female a basal, a median and a cortical layer can be differentiated. The outer limitation of the cuticle is an irregularly folded surface membrane. Excluding the anterior region the entire cuticle of the worm is covered by a coat. A regular fine honey-comb structure of the surface is found in the anterior region of the female. The morphology of the mouth, the amphidial openings, the papillae and the vulva, as well as the anus and the phasmidial openings, are presented. The cuticle of the male is also composed of a basal, a median and a cortical layer. The surface membrane shows a regular honey-comb pattern, which covers the entire worm with the exception of the anterior and posterior ends, but no coat was found. The cephalic region looks like that of the female. Papillae are arranged around the anus and the caudal tip. The variability of these papillae regarding their number and distribution is presented. The type of the two spicules and of the canal of the longer one is illustrated. The comparison of the worms from Liberia, Upper Volta, Tanzania and Guatemala revealed no morphological differences. Groups of males were examined statistically for differences of the distribution of the posterior papillae, but no geographical differences could be proven.
A survey revealed that Onchocerca tarsicola Bain & Schulz-Key, 1974 is a widespread parasite among reindeer in northern Finland. Of 407 animals studied from 12 reindeer herds, 124 (30.5%) were infected. There was a marked difference in infection levels between different reindeer herds and the frequency as well as the intensity of infection was highest in old animals whereas the parasites were rare in yearlings.
In Guatemala, 16 wild Simulium ochraceum were permitted to feed on a 15" x 15" grid on the back of each of 13 persons infected with Onchocerca volvulus. Based on 6 skin biopsies, the mean microfilarial density (mfd) in these study participants ranged from 1.256 mf/mg of skin to 111.824 mf/mg. The files were dissected 6 to 10 hours after feeding and the number of microfilariae in the blood meal and escaping the midgut into the thoracic musculature were counted. A nearly linear relationship was found between the mean skin mfd and the mean microfilarial uptake by S. ochraceum (rs = 0.868). An even stronger relation existed between the mean mfd and the mean number of microfilariae escaping the midgut (rs = 0.915). Because the approximate 1:1 relationship observed between the number of microfilariae escaping the midgut and the subsequent number of infective (L3) larvae has been previously demonstrated, it can be concluded that a similar linear relationship exists between microfilarial skin densities and the number of L3 larvae available for transmission of O. volvulus by the Guatemalan vector.
Two species of Nearctic black fly, Simulium decorum and S. pictipes, exhibit partial susceptibility to infection with the bovine parasite, Onchocerca lienalis, when inoculated intrathoracically with microfilariae. In addition, a proportion of S. decorum females will support the development of the human parasite, O. volvulus, to the third larvae stage. Infection rates with second- or third-stage larvae seven or more days after varied among geographic strains of S. decorum, ranging from 6.5% in a strain from northern New York State to 48.7% in a strain from Georgia. The average number of larvae per infected female ranged from 1.00 to 1.78 in the three strains examined. Partial susceptibility to O. lienalis was found to persist in colonized strains of s. decorum, and cryopreserved microfilariae of this parasite retained their infectivity. Seven or more days after inoculation with microfilariae of the Guatemalan strain of O. volvulus, 16.7% of the females of S. decorum harbored second- or third-stage larvae. Development of O. lienalis and O. volvulus proceeded normally in these black flies, and moderate increases in susceptibility rate and number of infective larvae were noted in response to increased microfilarial dosages.