Publisher Summary Filarial nematodes are arthropod-borne parasites, which sometimes cause serious disease in man and animals. The most important filarial worms of man are Onchocerca volvulus, the cause of river-blindness and severe skin disease, and Wuchereria bancrofti, the cause of tropical elephantiasis and hydrocoel. Another serious pathogen of man is Brugia malayi (B. malayi), and its distribution is limited to Asia. There are two well-defined strains of B. malayi, which differ in their microfilarial periodicity patterns. The nocturnally subperiodic strain is found in the dense swamp forest where its mosquito vectors prefer to feed at night but also bite during the day. The nocturnally periodic strain of B. malayi is found in the open plains where the vectors feed only at night. The correlation between peak peripheral microfilaraemia and peak biting time suggests that filarial nematodes have adapted their periodicity patterns to vector periodicity patterns for facilitating their transmission by mosquitoes. Nocturnally subperiodic B. malayi is common in wild monkeys, and this led to the assumption that it is zoonotic. Mansonia mosquitoes, the vectors of subperiodic B. malayi, feed on a variety of animal hosts, including man. The chapter presents the vector-parasite and definitive host–parasite relationships.

Brugian filariasis: epidemiological and experimental studies.

Randomised community-based trial of annual single-dose diethylcarbamazine with or without ivermectin against Wuchereria bancrofti infection in human beings and mosquitoes

Quantitative understanding of the transmission dynamics of lymphatic filarial parasites is essential for the rational planning of control strategies. One of the most important determinants of transmission dynamics is the relationship between parasite yield, the success rate of ingested microfilariae (mf) becoming infective larvae in a mosquito vector, and mf density in the source of the human blood meal. Three types of relationship have been recognized in human filaria/mosquito couples--limitation, facilitation and proportionality; facilitation has hitherto been observed only in the couple Wuchereria bancrofti/Anopheles gambiae in Burkina Faso, in experimental studies on a high density mf carrier. The present paper demonstrates facilitation in W. bancrofti/An. gambiae and W. bancrofti/An. arabiensis in lower mf density carriers in The Gambia and Tanzania, and in W. bancrofti/An. funestus in Tanzania. Facilitation was not found in An. melas in The Gambia nor in An. merus in Tanzania. Analysis of published data shows limitation at low level mf densities in W. bancrofti/Culex quinquefasciatus in Sri Lanka, and in the same couple in India. Limitation also occurs in Brugia malayi/Aedes togoi in experimental cats; proportionality occurs in B. malayi/Mansonia bonneae in Malaysia. The epidemiological significance of these host/parasite relationships is discussed, and supporting evidence for its validity is presented from the published results of large-scale control programmes.

Factors affecting transmission of Wuchereria bancrofti by anopheline mosquitoes. 4. Facilitation, limitation, proportionality and their epidemiological significance

Background: Recent data from Ghana indicates that after seven rounds of annual mass drug administration (MDA) there is still sustained transmission albeit at low levels in certain areas where Anopheles melas, An. gambiae s.s., Mansonia and Culex species are the main biting mosquitoes. Anopheles gambiae s.l. and An. funestus are the known vectors in Ghana and a recent report indicated that An. melas could transmit at low level microfilaraemia. However, because An. melas is not found everywhere there was the need to determine whether any of the other culicine species could also be playing a role in the transmission of LF. Methods: Indoor mosquitoes collected once a month for three months using pyrethrum spray catches in six communities within the Kommenda-Edina-Eguafo-Abirem (KEEA) District, Central Region of Ghana were morphologically identified, dissected and examined for the presence of W. bancrofti. Additionally, stored mosquito samples collected during previous years in 8 communities from the Gomoa District also in the Central Region were similarly processed. The identities of all W. bancrofti parasites found were confirmed using an established PCR method. Results: A total of 825 indoor resting mosquitoes comprising of 501 Anopheles species, 239 Mansonia species, 84 Culex species and 1 Aedes species were dissected and examined for the presence of W. bancrofti. Mansonia africana had infection and infectivity rates of 2.5%. and 2.1% respectively. Anopheles gambiae s.l. had an infection rate of 0.4% and a similar infectivity rate. None of the Culex sp. and Aedes sp were found with infection. From the stored mosquitoes the infection and infectivity rates for M. africana were 7.6% (N=144) and 2.8% respectively whilst the corresponding rates for M. uniformis were 2.9% (N=244) and 0.8%. Conclusions: This is the first report of Mansonia species as vectors of lymphatic filariasis (LF) in Ghana and in West Africa since that of 1958 in Guinea. The revelation of a hitherto unrecognised vector which is possibly more efficient in transmission than the recognised ones has a profound implication for elimination of lymphatic filariasis programmes in the sub-region.

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Mansonia africana and Mansonia uniformis are Vectors in the transmission of Wuchereria bancrofti lymphatic filariasis in Ghana

This paper attempts to pinpoint the most original morphological anatomical features of the biology of filariae per se and those which are or could be important for triggering regulatory processes in the arthropod vector and uncontrolled pathogenic processes in the vertebrate hosts. The following stages are considered: the motile egg or newly-hatched larva, the microfilaria, in the lymphatic or blood vessels of its vertebrate host; the larva, its migrations and its intrasyncitial development in the hematophagous arthropod subverted as vector; its transfer to the vertebrate host, migratory properties through the lymphatic system, maturation, mating and, finally, egg laying in the tissues they reach. This synthesis is based on parasite morphological features and their functional interpretation, histological features in the different niches the filariae reach, and on quantitative analyses of filarial development at its different phases, as well as on the rare and valuable observations of living parasites in situ. Data have been drawn from various species of Onchocercidae from amphibians, reptiles, birds and mammals. These comparative analyses have revealed the major constraints to which the filariae, including those parasitizing humans, have been subjected during their evolution from their ancestors, the oviparous and heteroxenic spirurids. Emphasis is placed on mechanical events: resistance of the microfilariae to the currents in the blood or lymph vessels, regulatory processes induced in the vector mesenteron by the movements of the ingested microfilariae, transient disruption by the microfilarial cephalic hook of the vectors' tissues and cell membranes during microfilarial translocation, attachment of males to females during mating by means of 'non-slip' systems, etc. Like other nematodes, filariae are equipped with sensory organs and a locomotor system, composed of the muscles and of the original osmoregulatory-excretory cell. Any change in one of these elements will result in the destruction of the filaria, at some stage of its development. In the vertebrate host, the intravascular stages will no longer be able to resist being carried passively towards the organs of destruction such as the lymph nodes or the lungs.

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Behaviour of filariae: morphological and anatomical signatures of their life style within the arthropod and vertebrate hosts

Seule une fraction des microfilaires ingerees par le vecteur passe dans l’hemocele et peut se developper en stades infestants. Il existe deux types de relations numeriques entre microfilaires ingerees et microfilaires passees dans l’hemocele :1)la proportion des microfilaires passees dans l’hemocele augmente en fonction du nombre des microfilaires ingerees : c’est la facilitation, observee chez le couple Wuchereria bancrofti - Anopheles gambiae A (457 ♀ dissequees) et etudiee dans un article precedent.2)le nombre des microfilaires passees dans l’hemocele est proportionnel au nombre des microfilaires ingerees pour les faibles prises de microfilaires ; puis, quand le repas est plus riche en microfilaires, il atteint un chiffre limite : c’est la limitation, mise en evidence chez 3 couples : Wuchereria bancrofti - Aedes aegypti (100 ♀ dissequees), Setaria labiatopapillosa - A. aegypti (357 ♀ dissequees), Onchocerca volvulus - Simulium damnosum (550 ♀ dissequees).1) Interpretation du phenomene de limitation. Aucune image histologique ne permet de l’expliquer. Par contre, un ensemble de faits, issus d’analyses des resultats numeriques, conduit a une hypothese qui fait intervenir a la fois l’etat physiologique et le mode de dispersion des microfilaires chez l’hote vertebre.a)Chez les 3 couples Filaire-vecteur, presentant le phenomene de limitation, on constate que le nombre des microfilaires passees dans l’hemocele est proportionnel au nombre des microfilaires ingerees jusqu’a un nombre critique de microfilaires ingerees, que nous appelons le seuil de limitation (il est de 25 microfilaires chez Wuchereria - Aedes , 6-9 microfilaires chez Setaria - Aedes et 3 microfilaires chez Onchocerca - Simulium ) ; au-dessus de ce seuil, la proportion decroit. Tout se passe donc comme si le vecteur qui fait de petits repas de microfilaires prelevait des microfilaires physiologiquement aptes a traverser la paroi stomacale (microfilaires +) et que le vecteur qui fait des repas riches en microfilaires prelevait des microfilaires inaptes a traverser la paroi stomacale (microfilaires-).b)L’analyse de la distribution des vecteurs en fonction du nombre de microfilaires ingerees montre qu’une partie des femelles semble prelever ses repas dans un milieu ou les microfilaires ont une dispersion homogene (distribution des femelles selon une courbe de Poisson) et qu’une autre partie des femelles semble prelever des microfilaires dans un autre milieu, ou elles sont dispersees de facon anarchique et en densites plus fortes (distribution des femelles « non poissonienne »). Les deux ensembles de distributions se recouvrent legerement, a leur contact.c)Si l’on marque en abcisses sur les histogrammes de distribution des femelles le seuil de limitation, on constate qu’il correspond a la separation entre la population des femelles a distribution essentiellement poissonienne et le reste de la population, comprenant l’aire de recouvrement plus la distribution residuelle. Cette correlation (retrouvee trois fois) signifie pour nous que la population des femelles chez laquelle le pourcentage de reussite des microfilaires est eleve correspond a la population des femelles qui a une distribution poissonienne. Ainsi, les microfilaires dispersees de facon homogene semblent correspondre aux microfilaires aptes a traverser la paroi stomacale (microfilaires +).d)La possibilite, pour un meme vecteur, d’ingerer des « microfilaires + » ou des « microfilaires » semble etre etayee par la mise en evidence chez A. aegypti de deux mecanismes de piqure (Gordon et Lumsden, 1939).2) Consequences. L’etude de la distribution des vecteurs en fonction du nombre des microfilaires ingerees apparait comme un moyen de mesurer le degre de coaptation du couple Filaire-vecteur. Dans le cas d’une parfaite adaptation, seules les « microfilaires + » doivent etre ingerees, ce qui se traduira par une distribution poissonienne du vecteur. Le couple Dipetalonema perstans - Culicoides austeni semble realiser cet equilibre (chiffres publies par Nicholas et Kershaw, 1954).Au contraire, chez Onchocerca - Simulium (souche voltaique), la plupart des Simulies ingerent des microfilaires inaptes a traverser la paroi stomacale. Mais ce meme couple, en region forestiere du Cameroun ne parait pas presenter un tel degre d’inadaptation (chiffres de Duke et Lewis, 1964). L’adaptation Filaire-vecteur, qui est le resultat d’une longue suite de selections, varie d’une region geographique a l’autre.

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O. Bain

Papers

Transmission des Filarioses - Limitation des passages des microfilaires ingérées vers l’hémocèle du vecteur ; interprétation