‘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 , , , 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, 2126, Venezuela. 381 PAHO Bdletin 20(4), 1986 xih,

FIGURE1. Geographicdistributfon of onchocerciasisfoci, and of confirmedand suspected onchocerciasis vectors, in the AmericanTropics.

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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 1955. 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. voZvuZuslarvae 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. Ovigenesis was riae and had produced an average of 0.02 found to take 48 to 60 hours. After ovi- infective larvae. The second included position the rest of the follicular cells four people from whom feeding insects (yellow body) were found to remain visi- had taken averagesof 24.2 to 44.7 micro- ble at the end of the ovariole for about filariae and had produced an average 150 hours. of 0.12 to 0.17 infective larvae. The third Under the same laboratory group was comprised of three people conditions, Collins (20) experimentally from whom feeding insects had taken an infected S. ochraceum and S. metaZZicum average of 5 1.1 to 117.8 microfilariae with 0. VOZVUZUS.Larval development in and had produced an average of 0.5 1 to S. ochraceum was found to be synchronic 1.69 infective larvae. It appeared that the and regular, so that the filariae reached last group of persons must play the most the thoracic muscles and evolved into important role in transmission of oncho- infective larvae in close to 192 hours after cerciasis. This finding indicates that the a single ingestion of blood. In contrast, percentage of insects infected is a more their development in S. metaZZicumwas significant indicator regarding effective asynchronic and delayed. Between eight individual transmission than is the aver- and 10 days after feeding, the author ob- age number of filariae found per in- served one infective larva, together with fected insect. a few residual microfilariae and first- In the late 1970s Collins stage larvae that were atrophied and de- (18) found 0. VOZVUZUSinfectivity rates in formed. He concluded that development S. ochraceum and S. caZZidum to be of 0. VOZVUZUSin S. 0cIClraceumis com- 0.3 1% and 0.41% , respectively. When patible with the intensive transmission as- multiplied by their respective total biting sociated with human onchocerciasis(21). densities, however, the infective biting Also in the late 1970s Garms 2 density of S. ochraceum came out to be and Ochoa (22) found that an average of z 79 times that of S. caZZidum. The num- 10.2% of the parous S. ochraceum fe- ber of viable larvae that are required for males collected in endemic areas were 2 effective transmission was calculated by carrying first or second stage 0. VOZVUZUS 2 multiplying the infective biting density larvae, and that 1.7 % were carrying me- 3 by the average number of larvae per in- tacyclic forms. Outside the endemic foci Q fected insect. S. ochraceum was found to no 0. VOZVUZUSinfections of S. ocbra- have the highest infective bite density, ceum were found. By comparison, the * x and also the effective transmission capac- rates of natural 0. VOZVUZUSinfection in 8 ity associated with the human popula- S. metaZZicum and S. caZZidum were kz tion suffering from onchocerciasis. These found to be very low, both in endemic l findings showed that a high S. ochra- areas(2 .O% and 2.5 % , respectively) and k? 56 ceum bite density was required to main- a, tain the endemic at its then current t-2 \h levels. E Around the same time, Cupp 2 and Collins (19) studied the gonado- trophic cycle of S. ocbmceum. They found that a gonadotrophic harmony ex- 385 in areas without known human oncho- the dry season S. ochraceum larvae were cerciasis ( 1-l % and 1.0 % , respectively). confined to permanent streams at inter- The authors concluded that the vector mediate altitudes. During the rainy sea- capacity of S. metallicurn was extremely son, however, the immature stages low, noting that only four females spread to numerous temporary rain-fed among the 7,743 insects captured in en- creeks. At the headwaters of the two riv- demic areas (0.05 % of the total number ers the adult population was at its peak of insects biting) appeared to be in- from October to December. fected, and some of the infecting larvae As they reported in 1981, were not 0. VOZVUZUS. Monroy et al. (zr) were able to deter- Throughout 1977 Onofre mine that temperature plays a key role in Ochoa (23) investigated the natural in- experimental development of 0. voZvu- fection of vectors in the pilot study area Zus in S. ochraceum and S. metaddicum. of San Vicente Pacaya, at an altitude of Under laboratory conditions temperature 750 m. The highest rate of S. ochraceum was found to directly affect the survival infectivity observed was 1.6% (in the of both insects, there being lower sur- month of September). The annual aver- vival at higher temperatures and higher age rate of parous females found among survival at lower temperatures. Tempera- the collected S. ochraceum specimens ture was also found to affect the time re- was 42.9. A total of 46 metacyclic larvae quired for development of 0. VOZVUZUS morphologically indistinguishable from larvae. Thus, the higher the tempera- 0. VOZVUZUSwere obtained from 16 speci- ture, the shorter the time required for mens of S. ochracezlm. In contrast, the the nematode to complete its develop- rate of 0. VOZVUZUSinfection found in S. ment in the insect. In addition, the au- metallicurn and S. caZZidum was very thors found that a temperature between low; furthermore, these infections were 18°C and 30°C was required to permit not considered to be of human origin in complete development of infective larvae view of the insects’ marked zoophilic in both species of simuliid. For S. ochra- tendency and the impossibility of mak- ceum the optimum transmission temper- ing a correct identification. The authors ature was found to lie between 22 ’ C and concluded that S. ocbraceum was the 24°C because that temperature permit- sole effective vector of 0. VOZVUZUS,and ted the highest survival rate. that the status of S. metaddicum as an 0. However, other laboratory ex- voZv%Zustransmitter was still uncertain. periments carried out by Takaoka (26) To ascertain seasonal varia- and Takaoka et al. (27) have shown that WI tions of S. ochraceum populations, Ta- daily exposure to lower temperatures 3h kaoka (24) did research from August (14-18”(Z) during the night assists 0. - 1978 to January 1980 at the headwaters voZvuZ.uslarval development in S. ochra- z of two major rivers that flow through the ceum and also enhances the longevity of % endemic areas of Escuintla Department. S. ochraceum adults. These findings ..jj P, His findings showed that at the end of help to explain why transmission of on- a3 chocerciasis has continued without inter- ruption in a region of temperate climate 2 in Guatemala where there are apprecia- 3 a, ble differences between daytime and nighttime temperatures. During the late 1970s and 386 early 198Os, Tada et al. (28) and Tada (29) carried out another study of an epi- demiologic nature in San Vicente Pa- EXICO caya. Using a single skin biopsy, they ex- M amined 2,153 persons, of whom 664 In 1923 Fiilleborn (‘32) re- (30.8 % ) proved positive for 0. voZvuZus. ported seeing onchocerciasis nodules on They also found that altitude played an the head of a five-year-old Mexican child important role in the parasitosis, with who attended his clinic in Hamburg, transmission occurring mainly at alti- Germany In 1925 (33) Bustamante re- tudes between 600 and 1,300 m. Out of ported that the disease probably existed 1,2 17 persons examined by simultaneous in the Monte Cristo Valley of Chiapas biopsy and nodule palpation, 587 State. In 1926 the presence of this disease proved positive by one or both methods: was demonstrated unequivocally in both 101 nodules were detected, mostly in Chiapas and Oaxaca. children or persons who had lived in Regarding other research in areasof low endemicity. It was concluded Mexico, in 1931 Torroella (34) first ob- that both diagnostic methods needed to served microfilariae in the anterior cham- be used in order to accurately determine ber of the eye of an onchocerciasis pa- the prevalence of the disease in Guate- tient. Using wild females, Hoffmann mala. (35, 36) accomplished the first experi- Regarding areas affected by mental infections of S. metaZZicum, S. onchocerciasis in Guatemala, only seven caZZidum, and S. ochraceum with 0. of the country’s 22 departments are in- voZvuZus.Dampf (37, 38) made impor- volved. No new transmission foci have tant studies of the biology and distribu- been reported recently, and the known tion of the simuliid transmitters in en- foci appear to have grown smaller. In demic areas. In 1949 and Ruiz 1981 Garcia Manzo (30) reported that Reyes (39) reported natural infection of the endemic area included three biomes S. exzjpum (= S. gon.zaZezzj)with inter- (using Holdridge’s classification). These mediate stages of 0. VOZVUZUS.Later, were (1) the wet tropical biome, (2) the Vargas (40) added the names of two wet premontane biome, and (3) the very other possible vectors-SimuZium wet premontane biome. The very wet haematopotum (which is very trouble- premontane biome was located near the some in the states of Michoacan and Pacific, and the others were found in Guerrero) and S. veracruzanum (in the Huehuetenango Department. state of Veracruz). In addition, Vargas According to this same report and Diaz Najera (41) carried out a study (30), Robles’ disease (ocular onchocer- of Mexican simuliid morphology and sys- ciasis) is distributed in two main areas- tematics in the 1950s and Vargas (42) that occupied by the Sierra Madre moun- wrote an important monograph entitled tain range along the south coast on the “SimGZidos deZ Nuevo Mundo ” (Simu- Pacific (at an altitude of 6OO-1,200 m) Ziids of the New IKzZd) that was pub- and that of the Cuchumatanes area of lished in 1945. Huehuetenango Department (a continu- ation of the Soconusco focus in Mexico). According to Aguilar et al. (31), around 1981 the area involved covered approxi- mately 5,130 square kilometers contain- ing 343,000 inhabitants, of whom some 30,000 were infected. Regarding entomologic fac- breeding ground over which onchocer- tors that relate to interruption of oncho- ciasis could be transmitted often corre- cerciasis transmission in Mexico and sponded to the maximum flying distance Guatemala, in 1960 Vargas (43) noted of the adult simuliid. This does not im- that the risk of contracting onchocerciasis ply that a single insect would commonly for the first time depends primarily on be a transmitter, but rather that the the number of bites that a susceptible in- range of a dense population of adult si- dividual receives and on the extent to muliids capable of transmitting oncho- which the local population of female si- cerciasis would determine the size of the muliids are parasitized by infective lar- area involved. vae. This means that a high density of No current statistics are avail- biting females combined with few hu- able on the prevalence of human infec- man reservoirs would produce a very low tion with 0. vo~vvzcl7zlsin Mexico. How- rate of simuliid-transmitted infection. ever, Salazar-Mallin (4.5, 46) reported in As this implies, a given simu- 1975 and 1977 that prevalences close to liid species’ role in transmitting the dis- 70% existed in some endemic areas and ease (leaving aside factors relating to the that some purported reduction of mor- filaria worm, man, and the environ- bidity had been due to diagnostic error ment) depends on (a) the vector species’ attributable to systematic nodule re- degree of susceptibility to the parasite, moval-a practice that considerably re- (b) the number of biting females existing duced the number of people with tumors at a given moment, (c) their propensity without directly affecting parasitism by to take blood from people instead of microfrlariae in the skin. other vertebrates, (d) the number of go- Overall, it is roughly esti- nadotrophic cycles involved, and (e) the mated that some 40,000 people are in- insects’ longevity in nature. In general, a fected in Mexico, and that the affected person may receive the first and subse- regions cover an area of some 8,900 quent infective doses of 0. voZvz&~sat square kilometers. In 1962 Garcia San- intervals depending on the timing of the chez and Chavez (47) stated that the fo- initial and final stages of the seasonal cus with the largest number of infections transmission cycle. However, this only was in southern Chiapas, and that the occurs at certain altitudes (between 500 next largest was in Oaxaca. Coast erysipe- and 1,600 meters). Transmission does las of the kind described in Guatemala not occur at sea level. It has been noted has not been reported in Chiapas; how- that the areas endemic for onchocerciasis ever, notable skin discoloration has been b are located around human settlements seen, sometimes producing a greenish 3Y and near watercourses. The vectors nei- tinge, and this appears to be the source - ther rest within houses nor preferentially of the so-called “ma1 morado” (purple 52 bite people within houses. Vargas (44) sickness) applied to such alterations in G also found that the distance from a Mexico (Vargas-48). According to Bel- ..g t&r-Hern6nde.z (49), as of 1983 oncho- cerciasiswas not a public health problem in Mexico. He indicated that a quarter of the caseswere asymptomatic, that severe ocular lesions progressing toward blind- ness were unknown, and that the num- ber of people blinded by the diseasewas 388 very small. Accord&g to Salazar-Mallen As reported in 1961, the abil- (46), in the mid-1970s there were three ity of S. metuZZicum to act as a principal onchocerciasis foci in Mexico. The largest vector for onchocerciasis was demon- was in Soconusco, in the southern part of strated by Pefialver (54), who studied the state of Chiapas, located between lat- histologic sections of insects futed in for- itudes 1504’ and 15”57’ N and longi- malin and stained with hematoxylin- tudes 90”5’ and 93”7’ W with an area eosin. Of 1,226 S. metaZZiczm exam- of some 6,800 square kilometers. A sec- ined, 104 (8.5%) were found to be ond focus was also located in the state of infected; however, the highest positive Chiapas further north, this being the indices of infection were found among “chamula” focus situated between lati- females captured at endemic foci in the tudes 16”52’ and 17”7’ N and lon- states of Aragua and (this index gitudes 92 “29 ’ and 92”40 ’ W and of 12.5 % included S. metallicurn con- covering an area of some 700 square taining any of the three larval stages of kilometers. A third focus was in the state 0. VOZV~ZZCS).In addition, S. exigztmrv of Oaxaca, at a place called Alto Papa- was implicated as a second transmitter in loapan to the west of the “chamula” fo- the coastal mountain range, even though cus. between latitudes 17”25’ and this insect’s small size appeared to permit 17”48 ’ N and longitudes 96”12’ and development of only a small number of 96”40’ W and covering some 1,400 nematodes. square kilometers. During the 196Os,in response to an invitation from the Government of Venezuela, Lewis (55), an entomologist with the British Museum of Natural His- V ENEZUELA tory, studied the biology of vectors in en- demic areas of San Antonio de Maturin The first known onchocer- in eastern Venezuela. He found that S. ciasis focus in Venezuela was discovered me.tuZZiczlmpreferred to bite the lower in the eastern part of the country in the extremities of human subjects, while S. late 1940s (JO). Its discoverers (Potenza, exigzum alit indifferently on the upper Febres Cordero, and Anduze) captured and lower parts of the human body. He S. met&Z&m and S. em)pzlumin the en- also found that the immature stagesof S. demic zone but did not prove natural in- metaddiczm inhabited small streams 25 fection. In 195 1 Guerrero (51) repotted to 50 cm in width, while the larvae and finding a case in the state of Miranda pupae of S. exziuum were collected in that marked discovery of another en- rivers whose beds measured five meters demic area in central Venezuela. Arends or more across. et al. (~2) reported finding the diseasein In 1965 Rivas et al. (5G) pub- the state of Aragua in 1954, and in 1957 lished a study on the geographic distri- Garcia Ocampo et al. (53) reported see- bution of onchocerciasis in nine states ing a casewith ocular lesions originating where the overall prevalence of infection in the state of . was found to be 39.94 per thousand in- habitants examined, and where the in- fection had been diagnosed in nearly 17,000 people. The clinical part of the study detected nodules in 23% of the onchocerciasis patients studied. The commonest ocular lesion found, ac- counting for 47.59% of the total, was state of Aragua. The results showed that keratitis. In addition, microfilariae were nulliparous females (which are epidemi- found in the anterior chamber of the eye ologically harmless) were very common in 11.17% of the infected subjects. The throughout the year at the National methods used to diagnose infection with Park, and that a high percentage of mul- 0. voZvzcZzlswere the Mazzotti test and tiparous (potentially dangerous) females skin biopsy. Regarding transmission, the appeared in the endemic rural Giiiripa principal vector was found to be S. me- area in the dry season. This suggested t~ZZicum; the observed infection rate in that the dry season was the time of peak collected S. metuZZ&m specimens was transmission, although the indices of in- 2.8 infected insects per thousand exam- fection and natural infectivity were not ined. estimated at that time. As reported in 1970, Duke Ramirez Perez (3) also suc- (11) brought two Africans carrying On- ceeded in experimentally infecting S. cbocercu voZvuZtis(one native to the West metaZZ&m with 0. voZvz~Zzl.tand in de- African jungle and the other to the Suda- veloping infective forms over a period of nese savanna) to Venezuela. When S. six days and 16 hours at a temperature met~ZZiczmzand S. exz&.zcm were al- that ranged between 25 ’ C and 30” C lowed to feed on these African volun- (the relative humidity was kept at 68- teers, they ingested the African microfi- 75 “Yo).Under the same laboratory condi- lariae without difficulty, but the worms tions, digestion of blood and develop- did not develop into the infective stage. ment of the ovaries (a gonadotrophic cy- In contrast, when the two vectors were al- cle) took 48 hours. What these results in- lowed to feed on two Venezuelan carri- dicate is that if ovule development takes ers, ingested microfilariae were able to two days and the microfilariae need be- reach the infective stage. However, S. ex- tween six and seven days to become in- iguum was found to be a vector of low fective, then the insect must make two or susceptibility since most of the parasites three ovipositions in order to become a did not reach the third larval stage, their potential transmitter in nature. development halting at the “sausage” To determine the endemicity stage. By comparison, S. metadlicum of onchocerciasis in Venezuela and evalu- turned out to be four to 10 times more ate seasonal variations, Ramirez Perez et efficient as a principal vector than S. ex- al. (>9) carried out a systematic study of iguum. In this regard, it is noteworthy the natural infection index in S. metaZZi- that when S. metallicam females in- calm collected at eight localities in the @ gested an average of 10 microfilariae, the country’s central region (in the states of % latter were well tolerated, but when they Aragua, Carabobo, and Guarico) through- . ingested more than 20, many of the in- out the dry and rainy seasons of 1974. 5? sects died in the first 24 hours after their They were able to show that the rate of S. % blood meal. metaZZicz,minfection rises in the dry sea- $j u During the whole of the dry son and falls in the rainy season. The av- 2 and rainy seasonsof 1973, Ramirez Perez erage number of filariae found per in- et al. (~7) studied the age groups of fected insect (including all the stages of 2 wild female S. metuZZicum specimens 3n, captured systematically in the Henry Pit- tier National Park (a primary wet tropical forest) and in an onchocerciasis 390 focus at Giiiripa (secondary forest) in the 0. voZvtiZtis)ranged from a high of 6.2 in Parima Moutains (including the upland February to a low of 1.2 in November. savannas of Parima A and Parima B at The highest incidence was recorded in 1,050 m and 950 m, respectively), and in March in a locality (Santa Rosa in Cara- the wet forest of the Little (at bobo State) where 13 % of the collected 250 m), S. pintoi had previously been insects were infected. implicated as the principal vector. This The author also performed a finding was based on its high biting den- detailed study (60) of the microscopic sity, natural index of infection with the morphology of the S. met~ZZictim larva, three larval forms of 0. VOZVZJZ~S(an in- pupa, and adult. The resulting mono- dex reaching So/), and natural infection graph presents a thoroughgoing descrip- index with infective 0. voZvztZmlarvae tion of the insect’s digestive, circulatory, (2% in the Little Orinoco area). Also, tracheal, nervous, muscular, and repro- study of a low area (at about 100 m) in- ductive systemsand ancillary organs, giv- cluding Platanal, Boca de Ocamo, and ing particular attention to the digestive Tamatama, found metacyclic forms of 0. tract and the thoracic muscles (which are voZvzldzcsin 0.25 % of the cephalic cap- directly involved in the passage and de- sules of Simz4Zizm amazoniczcm (sensu velopment of the parasite in the vector). Rassi) females captured at Platanal. It also shows how the morphology of the A later study of simuliids in female changes at different physiologic the Federal Territory of Amazonas, de- ages and distinguishes between the in- scribed by Ramirez Perez et al. in 1982 nocuous nulliparous and potentially (6.?), identified 27 species collected as dangerous multiparous forms. Also, by pupae or with human bait. Later works analyzing the epidemiologic determi- have confirmed that the principal vector nants of 0. voZv~Zzls transmission to of onchocerciasis among the Yanomama 2 man, the author concluded that it would groups is S. piatoi, this having been E be necessary to apply larvicides to the demonstrated both in nature (64) and iz permanent creeks during the dry season experimentally (65). Sim~Zi~m yamabaZi in order to reduce the rainy season adult (GG), now synonymous with S. incrzlsta- 2 population. tarn Lutz 1910 (6i’), sustains some devel- 5 In 1975, Rassi et al. (61) dis- opment of 0. voZvzZz4smicrofilariae up covered a new onchocerciasis focus in the to the infective stage and could act as a 2 2 Federal Territory of Amazonas. More spe- secondary transmitter in the Parima cifically, the disease was found to be Mountains; but it has not been found in- 25 prevalent among the Yanomama Indians fected in the wild (64). In the depart- 3 who inhabit an area of 200,000 square ments of and Casiquiare the E kilometers on both sides of the Brazil- transmitter appears to be another black- Venezuela frontier (62). Skin biopsies fly, SimzlZimz ctiasisungzlineum (63); s and Mazzotti tests carried out in this re- this is probably the species that Rassi et 5 gion yielded positivity rates ranging from al. (61, 81) identified at first as S. ama- . 35.7 % (at the Mavaca Mission) to 88.9 % zonicum. In 1982 Godoy (68) reported 2 $6 (at the CoyowPteri Mission). In the an additional focus among the Amerin- a, dians who inhabit the Upper Caura, in ,$ the Cedeno District of Bolivar State. He E assumed that this focus was a continua- 2 tion of the Amazonas focus, in which case the vectors involved in transmission are probably the same. 391 As of 1983, there appeared to June 1974, a total of 1,628,370 persons be three onchocerciasis foci in Venezuela in these areas were tested for onchocer- (67). The first was within the Coastal ciasis, and 40,091 proved positive by the Mountain Range of the country’s north- Mazzotti test, yielding an apparent in- central zone-a mountainous area in- fection rate of 24.6 per thousand inhab- cluding portions of the states of Aragua, itants. In comparing the situation in Carabobo, , Guarico, Miranda, Venezuela with that in Guatemala and and . The second focus is located Mexico, Pefialver noted in 1963 (71) that to the northeast, in the eastern part of the cutaneous lesions so frequently seen the Coastal Mountain Range, and in- in Mexico and Guatemala were rare in cludes portions of the states of Anzoate- Venezuela, appearing in only 7.5% of gui, , and . The third fo- the positive cases. cus is located in the Upper Caura, in the The degree of susceptibility of Cedeno District of Bolivar State, in the Simulium metaddicum to infection with Parima Mountains, and from the upper Onchocerca voZvuZz~~has also been stud- Ventuari to the Upper Orinoco to the ied in Venezuela (72). The results of that east of the Federal Territory of Ama- study indicate that despite asynchronous zonas. and retarded development, many larvae The endemic Venezuelan foci can develop to the infective stage in S. are located at altitudes between 400 and metallicurn; and the possibility of infec- 1,000 meters, and from an ecologic tive larvae eventually being inoculated standpoint (G9) involve three biomes: (1) into man is high. It is suggested that the wet tropical, (2) dry premontane, and (3) susceptibility of S. metaZZicum in Vene- wet premontane, the latter typically be- zuela to the indigenous strain of 0. ing composed of coffee-growing areas. VOZVUZUSis relatively high, compared The principal vectors involved in trans- with that of the same species in Guate- mission are S. met&ZZiczcmin the Coastal mala or Colombia. Range and S. pintoi in the Parima In addition, the ingestion and Mountains within the Federal Territory of development of 0. voZvuZusin SimuZium Amazonas. The secondary vectors are S. pintoi from the Parima Mountain region ex&uum to the north and S. cuasism- of the Federal Territory of Amazonas in guineum and S. incrustatzlm to the Venezuela have been studied experimen- south. tally (73). At a temperature ranging The transmitting insects are from 16 ‘C to 24’C, the development of more widely distributed at different lati- 0. voZvuZuslarvae in S. pintoi was syn- b tudes and altitudes than is the disease. chronous and orderly; no abnormal or % For example, S. metaZZicum and S. ex- deformed larvae were observed. (This syn- . iguum are common in the three moun- chronous development contrasts markedly s? tainous states of Tachira, Merida, and with the asynchronous development of G and in State’s Serrania de 0. voZvuZzlslarvae in S. metaddicum- .g u Perija; but no onchocerciasis has been re- i’.?.) Third-stage larvae were first seen in a23 ported in any of these areas (70). The affected areas of the 2 Coastal Range are quite densely popu- 3a, lated. According to data obtained from the Institute of Biomedicine, these areas had a total population of about 1.9 mil- 392 lion inhabitants in 1974. Beginning in the heads of flies dying eight or nine days an altitude of 670 m in a wet premon- after microfilariae were ingested; 98 of tane biome. A total of 89% of the black- 100 larvae recovered on days 10 through flies previously captured with human 16 were in the third stage. In conclusion, bait by Rassi et al. (80) were S. pintoi. it is suggested that S. pintoi is an effi- New observations, reported by Moraes et cient vector of 0. VOZV~ZUSdue to its high al. (78) in 1977, indicated that only susceptibility, in spite of the high mortal- 8.6 % of the Mayongongue Indians (at ity caused by excessiveintake of microfi- the only known Maquiritare Indian vil- lariae . lage in Brazil) were infected, as com- Finally, a comparative study pared to 31.5 % of the Sanuma Indians of onchocerciasis in South and Central belonging to the Yanomama group that America has been made (74) in order to were living at the same locality along the distinguish the features of the disease Auaris River under the influence of the and its transmission patterns in Guatemala Mayongongues . from those in Venezuela. Among other The Surucucu Mission (lati- things, it was found that S. ochraceum, tude 2 o50’ N, longitude 63 “45 ’ W, alti- the Guatemalan vector, apparently dif- tude 830 m) is likewise located in a wet fers from Venezuelan S. me.taZZicumand premontane biome. Rassi et al. (SO) S. pintoi in the mortality experienced af- found that the prevalence of onchocer- ter ingesting large numbers of microfila- ciasis infection was roughly 30% (based riae and in the preference exhibited for on positive biopsies), and that the pre- biting certain portions of the upright hu- dominant anthropophilic species, ac- man body. counting for 95 % of the collected vec- tors, was SimuZium incrustatum. The Toototobi Mission (lati- tude 1’ 10’ N, longitude 63 “45 ’ W, alti- BRAZILtude 180 m, in a wet tropical biome) was found to have the highest prevalence of In 1967 Bearzoti et al. (73) re- infection of the three sites studied, Rassi ported diagnosing the first known caseof et al. (SO)reporting a positive biopsy rate onchocerciasis in Brazil, in a child three of 67.4% in persons over 15 years of age. years of age. In 1972 Moraes and Dias In addition, the Mazzotti test produced a (76) reported another two casesin mis- clearly positive response in all the sub- sionaries living near the Toototobi River jects examined. In more recent work, in the north central part of the state of Moraes et al. (79) found 91.7 % of the Amazonas. Then, in mid-1974, Moraes subjects biopsied at the shoulders and and collaborators located new casesin the buttocks to be infected. SurucucG Mountains, where the Yano- The blackflies captured at the mama Indians live in the west of the Fed- Toototobi Mission by Rassi et al. (80, 81) eral Territory of (77-79). And in were all identified as S. umazonicum 1976 Rassi et al. (62) reported finding (sense Rassi), and seven sausageforms of another focus in a new ethnic group, the Maquiritares, who live in Auaris in the extreme northwestern part of the Ro- raima Territory. The Auaris Mission (latitude 4O8’ N, longitude 64”25’ W), where the latter focus is located, is situated at 393 0. voZvz&s were found in 972 dissected tory of Amazonas, were subsequently insects. However, as Rassi himself ex- compared with the females captured by plained, he was dealing with a complex Rassi in the vicinity of the Toototobi of several species that were hard to iden- River. tify, especially since at that time the lar- vae, pupae, and males of the insects in- volved were not known. In 1976 Shelley et al. (82) questioned Rassi’s identifica- COLOMBIA tion and provisionally termed the insect The first caseof onchocerciasis Simulium specimen A. Then, in a subse- discovered in Colombia was reported in quent publication, Shelley et al. (8.3) stated with certain reservations that the 1965 by Assis-Masriand Little (89) among a group of patients suffering from oph- principal vector of 0. voZvuZus in the thalmologic complications. The focus of Toototobi area was SimuZium sangui- the infection was subsequently reported neum. However, Tidwell et al. (84, 8s) by Little and D’ Alessandro (90) as being redescribed S. sanguineurn (sensu strictz) on the banks of the San Juan de Micay from Colombian topotypes in 198 1, after River, which has its headwaters in the which Shelley et al. (86) provisionally Western Mountain Range and flows into identified the vector in question as Simu- the Pacific. The endemic area lies be- Zium minusci&m Lutz, 1910. tween the settlements of Lopez and San To resolve these difficulties, Antonio (latitude 3”N and longitude the UNDP/ World Bank/ WHO Special 77 “23 ’ W) at 90 m above sea level in Program for Research and Training in Cauca Department. The area can be re- Tropical Diseases and the Pan American garded as one of transition between a wet Health Organization assembled a group tropical biome and a very wet tropical bi- of specialists active in this field for work- ome, the annual precipitation averaging shop meetings on the taxonomy of simu- about 5 ,OOO-6,000mm. Most of the eco- liids of medical importance. These meet- nomically active population is engaged ings were held at the Oswald0 Cruz in agriculture or mining. Institute in Rio de Janeiro, Brazil, and at Little and D’ Alessandro (90) the Pilot Center, Vector Studies Section, examined 292 persons from the Micay Institute of Biomedicine in Villa de Cura, River area ( 167 males and 125 females) in Aragua, Venezuela; and their results the late 1960s. Of these people, 268 were were reported in World Health Organi- classed as blacks, 16 as whites, and eight zation documents TDRIFILI 79.1 and as . Onchocelza infections were TDR/FILISIM/ 82.3 (87, 88). The species b detected in 44 persons (22 males and 22 under discussion was finally described in 3 females), representing 15 % of the popu- - 1983 by Ramkez PErezet al. (63) and was lation studied. All but one of the resi- 5? designated S. cuasisanguineum . Typical 0 dents found to be infected were blacks. ru specimens of this insect, which could be -g The ages of the infected subjects ranged QJ found at Tamatama in the Federal Terri- % from seven to 60 years, but the infection 3 rate was found to be highest among peo- 2 ple over 30. Only five subjects were found to have microfilariae in their eyes, and none had palpable nodules. Non- palpable nodules were detected in 20 394 people, six of these being found on the thorax, three on the hips, and one on the Duke (11) has suggested that head. The average number of microfila- the contribution of S. exzguum to the riae observed was 17.4 per mg of skin, natural transmission of 0. voZvuZus in within a range of two to 64 microfilariae Venezuela is minimal, and that S. metaZ- per mg. The authors concluded that the Zicum is four to 10 times more efficient as infections existing in this Colombian fo- an experimental vector. In Colombia, cus appeared to be light. however, data indicate that S. metal’li Trapido et al. @I), by re- cum from the Cali area is even less effr- searching historical documents from the cient than S. exz&uarn in supporting the year 1717 that were in the Central Ar- development of 0. voZvvzlZtisin experi- chives of Cauca at Popayan, determined mental studies. Tidwell et al. (93) have that the surnames of 136 black slaves liv- reported that of 206 0. VOZVZJZUSlarvae in ing in the mining area of the Micay River S. metuZZicum examined on days seven agreed with names of inhabitants in through 13 after ingestion, 25 % were parts of West Africa where onchocerciasis abnormal, 69% had not developed be- foci exist at the present time. This sug- yond the first stage, and only 10% had gests that the onchocerciasis recently de- reached the third stage. Engorged flies tected in Colombia and Ecuador was were kept within a temperature range of brought over from Africa with the slave 22-27-c. trade. Preliminary entomologic research on the Colombian focus by Barreto in the 1960s (92) implicated SimzlGizm ex- igtium as the principal and sole transmit- ECUADOR ter, a finding later confirmed in a 1980 report by Tidwell et al. (93). Carvajal Huerta et al. (94) Although development of 0. and Arzube (9j) reported the existence voZvuZusto the infective stage has been of a focus of onchocerciasis in the Ecua- observed in S. exz&um from Colombia, dorean province of Esmeraldas (latitude this species does not appear to be a par- O”42’ N, longitude 78”54’ W) in 1980 ticularly efficient intermediate host un- and 1981. The endemic zone is located der experimental conditions. Results of between the settlements of Sapallo an entomologic investigation carried out Grande and San Miguel de Cayapas at by Tidwell et al. (93) indicated that ab- about 30 m above sealevel in the western normal development of the parasite was foothills of the Andes Mountains. The common and that approximately 34 % of climate is hot and humid with an average the larvae observed had not proceeded temperature of 27°C and a relative hu- beyond the first stage five days after in- midity generally ranging from 70% to gestion. However, third-stage larvae were 95 % . Annual precipitation generally recovered late on the fifth day (1.40 hours ranges between 2,500 and 4,200 mm, after ingestion), and on days six through which makes the area a wet tropical bi- 10, 27 % of the flies were found to har- ome. The population is classedas 79.4 % bor third-stage larvae in their heads. The average number of infective larvae per fly was 0.8 1, and these represented 5 1% of the third-stage larvae recovered. The highest number of third-stage larvae (nine) was found in the head of a fly dis- sected on day six. black, 14.9% Indian, and 5.7% white. to the infective stage in a short enough The main sources of employment are time to suggest they could naturally farming, hunting, fishing, and mining. transmit the parasite. S. exiguum ap- Arzube (96) reported per- peared to be a good host becauseparasite forming biopsy examinations on 87 per- development in it was synchronous and sons in 1982. 0. volv7z.lz~microfilariae rapid, and because even high rates of in- were found in 72 (83 %) of the study sub- fection had little or no effect on S. ex- jects. Of these, 62 (86%) were blacks and iguum mortality after the larvae reached 10 (14 %) were Indians belonging to the the fly’s thoracic musculature (101). Capaya group; 42 (5 8 % ) were males and Natural infection rates of S. 30 (42%) were females. Skin biopsies ex&uam and S. qzcadrivittatzlm with fi- were taken from 39 infected subjects and lariae were found to be very similar. Of weighed. It was found that in 29 (74%) 557 S. exigzlzlm dissected, 2.5% of the of these subjects the density of microfila- flies contained filarial larvae and 1.1% riae was higher at the iliac crest than at contained infective 0. vodvz~lzlslarvae. the scapula. The following clinical mani- And of 178 S. qzludrivittut~m dissected, festations were found in the positive 2.2 % contained filarial larvae and 1.1% cases:nodules in 45 subjects (63%); der- contained infective larvae (101). Also, matitis, pigment changes, and/or skin current data indicate that onchocerciasis atrophy in 31 (43 %); lymphoadeno- transmission in Ecuador is high during pathy and/ or lymphoedema of the exter- the end of the wet season at localities nal genital organs in 19 (26 % ); cornea1 along the middle reaches of the Capayas opacities in 32 (44%); and dermatitis River. and/or pruritis in 49 (68%). The paucity of data on S. The Ecuadorian onchocer- antillar~m precludes any conclusions ciasis foci are regarded by Guderian et al. about its susceptibility to filarial infec- (97-l 00) as divisible into two groups: the tion; but even if it were shown experi- main or Santiago focus encompassing mentally to be a potential vector of 0. localities on the Cayapas, Onzole, and volvulzls, this blackfly would be unlikely Santiago rivers and their tributaries, and to contribute significantly to the epide- several peripheral foci on different river miology of the diseasein the Santiago fo- systems, such as those of the Canande, cus because of its low anthropophily and Cojimies, Sucio, and Viche rivers. The human biting rates compared to the two disease has been found in over 2,000 of aforementioned species (101). the 11,000 people sampled in rural areas, indicating that it afflicts nearly 1% uco 2 of the 285,000 inhabitants of Esmeraldas . Province. SUMMARY s Of 274 simuliids captured In all, 12 fly speciesof the ge- z with human bait in the endemic zone by .j$ nus Simz&m have been implicated as 9, Arzube (96), 206 were found to be Si- * confirmed or suspected vectors of oncho- x mdium quadrivittutz4m, 59 were S. ex- cerciasis in those six countries (Brazil, igwm, and nine were S. antdawm. 2 Data presented on experimental infec- 2a, tion of these three speciesin the Santiago focus clearly showed that S. exz&zlm and S. quadnwttatzlm were capable of per- 396 mitting full development of 0. VOZV.&LS Colombia, Ecuador, Guatemala, Mrx- 40,000 people are infected in Mexico, ice, and Venezuela) with known foci in and that the endemic areas cover about the Americas. 8,900 square kilometers. Vectors impli- In Guatemala, the first focus cated or suspected of 0. VOZVZJZZLStrans- discovered (and also the first focus dis- mission in Mexico include Simudium covered in the Americas) was described ochruceum, S. metallicurn, S. cuZZLa?um, by Rodolfo Robles in 1915. At present, S. exiguum (= S. gon.zaZezzj,S. baema- ocular onchocerciasis appears distributed topotum, and S. verucmczanum. in two main areas, one in mountains In Venezuela, where over near the southern Pacific Coast and the 40,000 people were infected in the mid- other in the far west along the Mexican 197Os,there are three known focal areas. border, this latter being an extension of One is among the coastal mountains in the Soconusco focus of southern Mexico. the north-central part of the country; a The principal vector of the disease in second is to the east in the states of Anzo- Guatemala is Simdium ochruceum. ategui, Monagas, and Sucre; and the Other species implicated as secondary third is far to the south in Bolivar State vectors include S. metaZZicumand S. c&Z- and the Federal Territory of Amatonas ZidU?72. along the Brazil-Venezuela frontier. The Among other things, research principal vectors of onchocerciasis in conducted in Guatemala and Venezuela Venezuela are S. metaZZicum (in the two has shown that African and American northern foci) and S. pintoi (in the onchocerciasis differ in many respects, south). Secondary vectors include S. ex- and that the latter can be regarded as an igzlzcm in the north and S. cuasisan- indigenous disease. Additional research guineum and S. incrustatzcm in the in Guatemala has provided information south. about the vectors’ taxonomy, biology, In Brazil, where the disease 2 and ecology; has helped to define the was first reported in 1967, the focal area k! levels of natural 0. voZvz4Zz4sinfection in is located in the state of Amazonas and various vectors; and has elucidated the the Federal Territory of Roraima near the 5 key role played by temperature in the de- Venezuelan Frontier. This area, like its 5 velopment of 0. uoZv.uZz~inside the counterpart focal areas across the border 2 vector. in southern Venezuela, covers a large In Mexico there are three area sparsely populated by jungle Indi- 2 2 known foci. One, the largest, is the So- ans. Prevalences of infection at specific 5 conusco focus on the Guatemalan bor- study sites appear to range from roughly 3 der. A second, the so-called “chamula” 30% to over 90% of the human popula- g focus, is slightly further north in Chiapas tion. Initial difficulty in classifying one State. And the third, considerably to the of the responsible vectors was resolved 6 west of the “chamula” focus, is around a when this insect was designated Simu- 5 place called Alto Papaloapan in Oaxaca Zium cuasisunguineum in 1983. The vec- . N State. It has been estimated that some tors of onchocerciasis in Brazil include S. 2 cuusisanguineum, S. pintoi, and S. in- 2 cli’;s&&4.m. D In Colombia, where the first 22 known case of onchocerciasis was re- ,$ ported in 1965, the one established focus is located in the far western part of the country in a mountainous area near the 397 Pacific Coast. S. exiguum has been im- 8 Dalmat, H. T. The blackflies (Diptera, Simu- plicated as the sole transmitter. liidae) of Guatemala and their role as vectors of Onchocerciasis. Smithsonian Miscelane- In Ecuador, where the exis- ous Collections 125(1):1-425, 1955. tence of an endemic zone was reported in 1980, the focal area is located in the 9 Gibson, C. L. Experimental studies on the parasite and vectors of onchocerciasis in Gua- north, close to the Pacific Coast and the temala. Boletin Sanitaria de Guatemala Colombian Border. Confirmed or sus- 36:246-287, 1965. pected vectors include S. exziuzcm, S. 10 De Leon, J. R., and B. 0. L. Duke. Experi- quadrivittatum, and S. untillarum. mental studies on the transmission of Guate- malan and West African strains of Oncho- cerca volvu~us by Simdium ochraceum, S. metaKcum and S. cakz’um. Trans R SOGTrop Med Hyg 60(6):735-752, 1966. RxFERENCES 11 Duke, B. 0. L. Onchocerca-Simdium com- plexes: VI. Experimental studies on the trans- 1 Robles, R. Onchocercose humaine au Guate- mission of Venezuelan and West African mala produisant la &cite et I’erysipile du li- strains of Oncbocerca vol’vulus bv Simdium toral. Bull SOCPuthd Exot 12(7):442463, metallicurn and S. exiguum in’venezuela. 1919. Ann Fob Med Parasitol 64l4k421-411.\ I 1970. - 2 Calderon, V. M. Contribucidn al estudio de1 fildrido Onchocerca 9. Dr. Robles- 1915 y de 12 Figueroa Marroquin, H. Historia de la en- las enfermedades ue produce. Doctoral fermedad de Robles en America y de su des- Thesis. Sanchez an 8 De Guise. Guatemala cubrimiento en Guatemala. In: Enfermedad City, 1920. de Rob/es. Academia de Ciencias MCdicas, fisicas y Naturales, Guatemala, 1963, 90 pp. 3 Strong, R. I?, J. H. Sandground, J. C. Be- quaert, and M. N. Ochoa. Onchocerciasis, 13 Duke, B. 0. L., I?.J. Moore, and J. R. De with Special Reference to the Central Ameri- Leon. Onchocerca-Simdium complexes: V. can Form of the Disease. Contr. No. 6. De- The intake and subsequent fate of microfi- partment of Tropical Medicine and Institute laria of a Guatemalan strain of Onchocerca of Tropical Biology and Medicine. Harvard vo&ulus in forest and Sudan-savanna forms University Press, Cambridge, 1934, 234 pp. of West African Simdium damnosum. Ann pop MedParasitol61:332-337, 1967. 4 De Ledn, J. R. Preliminares para la descrip- ci6n de cinco nuevas especies de simfilidos en 14 Bain, O., M. C. Durette-Besset, and R. De Guatemala. Bol Sanit Guatemala 5 I :94-101, Leon. Onchocercose au Guatemala: L’in es- 1943. tion des microfilaires par Simuhum oc2 ra- ceum et leur passage dam I’himocele de ce De Leon, J. R. Nuevas especies de simdlidos vectour. Ann ParasitoL Hum Comp 49:467- en la region occidental de Guatemala. Bd 487. 1974. Sanit Guatemala 52~66-77, 1944. u 15 Omar, M. S., and R. Garms. The fate and 6 De Leon, J. R. Un nuevo simdido de la re- migration of microfilariae of a Guatemalan 5 gio’n occidental’ de Guatemala. Publication strain of Onchocerca vol’vdus in Simdium No. 56. Instituto de Investigaciones Cientifi- ochraceum and S. metadicum, and the role $ cas, Universidad de San Carlos, Guatemala, of the buccopharyngeal armature in the de- G 1948, 23 pp. struction of microfilariae. Tropenmed Parasi- tol26:183-190, 1975. .$j 9, 7 De Leon, J. R. Entomologia de la oncocerco- % 16 Garms. R. Observations on filarial infections a sis. In: Oncocercosis (Enfermedad de Ro- bles). Universidad de San Carlos, Guate- and parous rates of anthropophilic blackflies 2 mala, 1947, pp. 147-172. in Guatemala, with reference to the transmis- sion of Onchocerca volvulus. 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