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‘H UMAN ONCHOCERCIASIS FOCI AND VECTORS IN THE AMERICAN TROPICS AND SUBTROPICS1 Jaime RamCez P&e2 I NTRODUCTION skin areas where they are sometimes in- gested by man-biting flies of the genus Onchocerciasis (river blind- Simzldizlm. They then seek to penetrate ness) is an essentially rural parasitosis en- the thoracic musculature of these inter- demic to the valleys and foothills of mediate hosts, and after six or seven mountainous areas along streams where days, without undergoing multiplica- the vectors breed. The etiologic agent is tion, develop into an infective form the filaria worm Onchocerca voZvvuZzls about 700 microns long that is motile that lives as an adult in subcutaneous and has a fully developed digestive tract. nodules within its human host. Ocular The infective form then migrates to the lesions usually arise between five and six fly’s proboscis, from where it can enter years after infection. another human when the insect bites The worms are white and fila- again. The most suitable time for Simu- mentous. Adult males are relatively lizlm flies to introduce 0. vo~vz&.s into a small, some 2-4 cm long, while the fe- human host is on hot days, when the per- males attain a length of 40-50 cm. The son’s skin is moist with sweat and the females are viviparous and discharge mi- pores are open. crofilariae 200-300 microns long. These The account presented here microfilariae can live in the skin of their describes the ecologic characteristics of host for up to 30 months, and fertile fe- onchocerciasis foci in the Americas and males have a life-span of up to 15 years. the Simzlliam vectors implicated up to m About a year after infection the present time (see Figure 1). The de- 2~ microfilariae can be found around the scription deals with each of the affected - adult worms’ subcutaneous nodules. countries in turn (Guatemala, Mexico, SC 8 These microfilariae migrate to nearby Venezuela, Brazil, Colombia, and Ecua- .fii dor), considering first those where the u disease was discovered earliest. ’ This article has previously been published in Spanish in the BoZetirt de La Oficina Sanda+ Panamericana, vol. 98, no. 2, 1985. pp. 117-135. z Coordinator of the Vector Studies Section and PAHO/ WHO Adviser, Instituto de Biomedicina, Centro Pi- loto, Apartado No. 357, Villa de Cura, Aragua 2126, Venezuela. 381 PAHO Bdletin 20(4), 1986 xih, FIGURE1. Geographicdistributfon of onchocerciasisfoci, and of confirmedand suspected onchocerciasis vectors, in the AmericanTropics. CARIBBEAN larvae, pupae, and adults of both sexes. He also described the geographic distri- UATEMALA b bution of the vectors in detail and re- Onchocerciasis was discovered ported that both S. metaZZiczlmand S. in America in 1915 by the Guatemalan callidum bred in watercourses ranging scientist Rodolfo Robles, who with great from small creeks to major rivers, had skill described the parasite and clinical zoophilic habits, and became agitated picture, reported ocular lesions for the when fed on human bait. first time, and implicated insects of the Largely because of its strictly genus Simdium (the “blackfly” Simu- anthropophilic habits, Dalmat con- Zium metaZZicum and the “alazan” Si- cluded that the principal vector of m&urn ochraceam) as vectors of this onchocerciasis in Guatemala was S. new American disease (1). Credit for im- ochracezlm. This insect, which feeds portant early work is also due Victor Ma- intermittently on human bait without nuel Calderdn, who in 1920 reported ob- appearing attracted to other animals, has serving the intermediate stages of 0. immature stages that are found in small VOZV~ZBJin the thoracic muscles of Gua- creeks at altitudes ranging from 900 to temalan blackflies (2). 1,500 meters. It was suggested that the Subsequently, in 1934, a insect’s low rate of natural infection with group of Harvard University researchers 0. VOZVZJZ~Jcould be attributable to led by Richard Strong (3) demonstrated deaths resulting when large numbers of that S. ochracezlm, S. metaldicam, and microfilariae were ingested. The author SimuZium caZZidumwere seriously impli- indicated that in areas where S. ochra- cated in the transmission of 0. VOZV~ZXS cezm was rare or absent, SimuZium c7 to man. In 1935 the Ministry of Public haematopotum, S. veracrmzanum, and 3 Health of Guatemala began a campaign S. exz@um (= S. gon.zaZezz)could be b against onchocerciasis. And between the principal transmitting agents. 2 1943 and 1948 De Leon (4-7) carried out Also, De Ledn (7) found that a series on entomologic research projects 1.86 % of 63 1 S. metaZZicumfemales and 2 designed to establish the taxonomy of 0.89% of 433 S. ochraceum females cap- 5 the vectors that also produced descrip- tured in endemic areas of Guatemala tions of seven new species of the family were naturally infected by microfilariae g Simuliidae in Guatemala. that he classified as 0. voZvuZzs. Simi- s A major study by Dalmat (8) larly, Gibson (9) reported in 1965 that 5 on the taxonomy, biology, and ecology of over a period of a year he found 1.04 % 3 both the immature stages and the adults of 1,734 S. metal’dcum, 0.38% of 1,839 g of Guatemalan simuliids was published S. ochraceum, and 0.62 % of 162 S. caZZi- in 195 5. Dalmat devoted half his work to dzlm to be naturally infected. s redescribing 41 species (three belonging In 1966 De Leon and Duke 5 to the genus Cnephia, two to the genus (10) reported results obtained with two l Gigantodax, and 36 to the genus Simu- volunteer carriers of 0. VOZVUZUS,natives D 16 Zium) and providing keys for identifying of the West African forest and the Sudan R, savanna, who, together with two Mayan D Indians, let themselves be bitten by local k Guatemalan vectors. When S. ochra- ,$ ceum bit the Mayan Indians it ingested an average of 390 Guatemalan microfila- riae but produced only 2.5 metacyclic 383 forms-indicating that on the average were destroyed immediately after inges- 0.65 % of the microfilariae ingested de- tion. Along this same line, Omar and veloped into infective forms under ex- Garms (1.5) reported the following year perimental conditions, while the rest of that numerous chitinous teeth in the the microfilariae were apparently de- buccopharynx of S. ochraceum destroy stroyed by the insect. When the same large numbers of microfilariae, allowing vector ingested an average of 14 West Af- only some 2.6 % through to enter the rican forest microfilariae per bite, it pro- thoracic musculature. In contrast, the duced an average of 0.25 metacyclic buccopharynx of S. metaZZz&m is tooth- forms, yielding an average survival rate less, and although the insect tends to in- of 1.8 % . Ingestion of microfilariae from gest relatively few microfilariae, most the Sudan savanna did not lead to devel- (some 74.5 %) of those ingested succeed opment of the infective form in S. ochra- in migrating to the insect’s thorax. ceum, S. metaZZicum, or S. caZZidum. In 1975 Garms (16) reported The authors also established that simu- natural vector infection rates on five liids can be used for xenodiagnosis of Guatemalan coffee plantations where American onchocerciasis, since insects re- onchocerciasis was endemic to be 0.3 % cently fed on infected subjects yielded a in S. me.taZZicum,0.2% in S. caZZidum, higher concentration of microfilariae 1.3 % in S. gonzalezi, and 1.9% in S. than insects from the same regions be- ochaceum. This last species had a lower fore feeding. 0. VOZVUZUJinfection index than did the These experiments, together local human populations affected by on- with others carried out by Duke (II) in chocerciasis. It was also found that only Venezuela, demonstrated that African three S. ochraceum females were parasi- and American onchocerciasis differ in tized by third stage 0. voZvuZus larvae many respects, and that (as indicated out of a total of 3,513 insects examined, previously by Figueroa Marroquin-12) and that only two out of 3,121 S. metaZ- the latter can be regarded as an indige- Zicum examined were found to contain nous disease. The arguments in favor of filariae morphologically distinct from 0. this theory were confirmed by Duke et vozvuzus. al. (13) in 1967, after they succeeded in Around the same time, Collins infecting a chimpanzee from Cameroon et al. (17) determined the level of infec- with Guatemalan metacyclic forms of 0. tion of S. ochraceum exposed to 10 vol- VOZVUZUJ.These 0. voZvuZzlswere taken unteers with very low and average num- to Africa in specimens of S. ochraceum bers of microfilariae in the skin. This was that had previously bitten volunteers done both qualitatively (by finding the mcg Ym harboring large parasite loads. When mi- percentage of insects infected) and quan- . crofilariae appeared in the chimpanzee’s titatively (by finding the average number 55 skin, the animal was exposed to the bites of infective larvae in each insect), with % of S. damnosum, but at the end of seven the object of ascertaining S. ochracesm ‘s .g P) days the American strain had not devel- effectiveness as a reservoir of 0. VOZVUZUS 3 oped into the infective stage in the prin- infection. Q cipal African vector. Bain et al. (14) reported in 2n, 1974 that only 1 to 2% of all the microfi- lariae ingested by S. ochraceum were able to evolve in the insect’s muscula- 384 ture, and that 98 % of the microfilariae The volunteers were divided ists-i.e., that after a single ingestion of into three groups. The first consisted of blood it is possible to observe complete three people from whom feeding insects development of the follicles in all the had taken an average of 12.5 microfila- ovarioles simultaneously.