THE DIFFERENT AETIOLOGIES OF FILARIOSIS IN DOMESTIC CARNIVORES IN AFRICA

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Chapter 2 LITERATURE REVIEW OF THE DIFFERENT AETIOLOGIES OF FILARIOSIS IN DOMESTIC CARNIVORES IN AFRICA

A total of ten confirmed filarial species has been reported worldwide in domestic carnivores (Table 2.1). As regards Africa and its islands, there are published reports of autochthonous cases of filarial infections in dogs and cats involving six of these species (Nelson, Heisch & Furlong 1962; Laub 1988).
Of these the species D. immitis, Dirofilaria repens, Acanthocheilonema reconditum reconditum, Acanthocheilonema dracunculoides and Brugia patei, that all belong to the family Onchocercidae of the superfamily Filarioidea, form the subjects of this study.

Dirofilaria immitis

Taxonomy

Dirofilaria immitis (Leidy, 1856), commonly known as heartworm or canine heartworm, belongs to the subfamily Dirofilariinae and was first described as Filaria canis cordis in 1850 by Leidy in Philadelphia. In 1856 the worm was renamed Filaria immitis by Leidy. Railliet & Henry (1911a) erected the genus Dirofilaria and designated Filaria immitis as its type species. As a result of subsequent descriptions by various authors the helminth figures in the literature under the following synonyms: Filaria canis cordis (Leidy, 1850), Filaria papillosa haematica canis-domestica (Gruly & Delafond, 1852), Filaria immitis (Leidy, 1856), Filaria papillosa haematica (Schneider, 1866), Filaria spirocauda (Leidy, 1858), Filaria cordis phocae (Joly, 1858), Filaria haematica (Leuckart, 1867), Filaria sanguinis (Cobbold, 1869), Filaria hebetata (Cobbold, 1873), Filaria spirocauda (Cobbold, 1879), Filaria sp. (Horst, 1889); Microfilaria immitis (Neumann & Mayer,1914), Dirofilaria nasuae (Mazza, 1926), Dirofilaria pongoi (Vogel & Vogelsang, 1930), Dirofilaria indica (Chakravarty, 1936), Filaria magalhaesi (Blanchard, 1895), Dirofilaria magalhaesi (Blanchard, 1895), Dirofilaria fausti (Skrjabin & Schikhobalova, 1948) and Dirofilaria louisianensis (Faust, Thomas & Jones, 1941) (Anderson 1952; Sonin 1985).
Faust (1937) proposed that the genus Dirofilaria be split into the subgenera Dirofilaria and Nochtiella. Species whose predilection site is the cardiovascular system were allocated to the subgenus Dirofilaria, whereas the subgenus Nochtiella contains those whose predilection site is the subcutaneous connective tissue.

Morphology

The morphological features that characterize the genus have been described by Railliet Henry (1911a), Vogel (1927), Lent & Freitas (1937) and Sonin (1985). A detailed description of the adult stages of immitis is given by Fülleborn (1912) and Vogel (1927). According to these authors, females are 21-31 cm long and 1-1.3 mm wide whereas males are 12-20 cm long and 0.6-0.9 mm wide. The left spicule is 300-355 µm long, and the right spicule 175- 226 µm.
The microfilariae are unsheathed, and a detailed description was given by Fülleborn (1912) and Taylor (1960a). The cephalic end is conical and the posterior end is acute with the nuclear column (i.e. the cells that constitute the body of the microfilaria) not extending to the end of the body. The tail in unfixed and unstained microfilariae is straight (Marconcini, Magi, Macchioni & Sassetti 1996). Minimum and maximum measurements regarding length and width range from 180-340 µm and 5-7 µm respectively (Table 2.2).
The infective filarial larva in mosquitoes has been originally described by Nelson (1959) with additional information being provided by Taylor (1960b), Orihel (1961), Lichtenfels, Pilitt, Kotani & Powers (1985) and Bain & Chabaud (1986).

Life cycle

Dirofilaria immitis females produce microfilariae which are found in the blood of the definitive host. They are also capable of passing through the placenta and infect foetuses in utero (Mantovani & Jackson 1966; Atwell 1981; Todd & Howland 1983), and microfilariae have been found in urine (Kaewthamasorn, Assarasakorn & Niwetpathomwat 2008) and synovial fluid (Hodges & Rishniw 2008). The appearance of microfilariae in dogs in the peripheral blood is nocturnal subperiodic, with maximum levels of microfilaraemia being attained during late afternoon and at night with some geographical variation (Kosuge 1924; Schnelle & Young 1944; Euzéby & Lainé 1951; Webber & Hawking 1955; Newton & Wright 1956; Tongson & Romero 1962). Apart from the daily periodicity, there is also a seasonal periodicity with microfilariae being more abundant in the peripheral blood during spring and summer (Newton 1968; Kume 1975; Sawyer 1975). There exists a coincidence between the time microfilariae are most abundant in the peripheral blood and the time mosquito vectors obtain blood meals, a circumstance which is regarded as an evolutionary adaptation (Abraham 1988). Microfilariaemia in cats is only seen in less than 20 % of cases, and is inconsistent and transient when present (Cusick, Todd, Blake & Daly 1976). In cats the microfilaraemia is also nocturnal subperiodic (Nogami, Marasugi, Shimazaki, Maeda, Harasawa & Nakagaki 2000).
Mosquitoes act as intermediate hosts. Microfilariae develop into 3^rd stage infective larvae in the mosquito and their development has been described by Taylor (1960b), Christensen (1977) and Bradley, Sauerman & Nayar (1984). The incubation period in mosquito vectors is largely temperature-dependent and may take as little as 14-17 days in Aedes aegypti (Taylor 1960b). While feeding, infective larvae emerge from the tips of the labella together with a drop of haemolymph onto the surface of the host’s skin (Lavoipierre 1958). The haemolymph pool provides a medium in which the larvae can maintain their motility to search for and penetrate the puncture wound remaining after the withdrawal of the mosquito fascicle (Zielke 1973). The developing larvae are also pathogenic for the vector itself, which results in an increased mortality (Kartmann 1953; Galliard 1957; Christensen 1977; Hamilton & Bradley 1979).
In the definitive host the infective larvae undergo an extensive somatic migration to so-called intermediate locations, which are the submuscular membrane, subcutaneous tissue, adipose tissue, subserosa and muscles of the upper abdomen, thorax, head, neck and forelimb regions (Kume & Itagaki 1955). During this migration they moult to the L4-stage and then into young adults which finally enter veins to reach their predilection sites, the right ventricle, right auricle and pulmonary artery (Nelson 1966; Kotani & Powers 1982; Orihel 1961). Worms are found in the heart as early as day 67 after infection (Kume & Itagaki 1955) and the migration is always completed by day 90 (Orihel 1961). There are many reports of D. immitis found in aberrant sites (Otto 1975) which is more common in cats than in dogs (Dillon 1988). The prepatent period is 6-9 months in dogs (Bancroft 1904; Webber & Hawking 1955; Orihel 1961; Newton 1968; Kotani & Powers 1982) and 8 months in cats (Donahue 1975). The patent period is up to 7½ years in dogs (Newton 1968) and only about 2 years in cats (Donahue 1975;Wong, Pedersen & Cullen 1983). The maximum life expectancy of microfilariae in the blood of dogs is 2½ years (Underwood & Harwood 1939).

Host range

Domestic dogs act as the preferential and principal definitive host (Abraham 1988). Cats are less prone to develop a patent infection and thus regarded as insignificant reservoirs of infection (Donahue 1975; Dillon 1988; Wong et al. 1983). Apart from these hosts, some wild canids, felids, other mammals, including man, and the Humboldt penguin (Sphenicus humboldti) have been found to be infected with adult D. immitis (Campbell & Blair 1978; Abraham 1988; Starr & Mulley 1988; Vellayan, Omar, Oothuman, Jefferey, Zahedi, Mathew & Krishnasamy 1989; Canestri Trotti, Pampiglione Rivasi 1997; Sano, Aoki, Takahashi, Miura, Komatsu, Abe, Kakino & Itagaki 2005). In the majority of these hosts the adult worms are found in aberrant locations and do not produce microfilariae (Abraham 1988).

Vectors

About 70 anopheline and culicine mosquitoes throughout the world, that belong to the genera Aedes, Anopheles, Coquillettidia, Culex, Culiseta, Mansonia and Psorophora have been identified as potential intermediate hosts (Bemrick & Sandholm 1966; Ludlam, Jachowski & Otto 1970; Lok 1988). However, innate susceptibility is only a component of true vector competence, which is determined by the demonstration of infective larvae in field-captured mosquitoes (Lok 1988). As regards Africa there are very few references to natural infections of mosquitoes with animal filariae. Because infective larvae of D. immitis are practically indistinguishable on morphological criteria from those of D. repens, available records from Africa that specifically refer to D. immitis (Table 2.3) are therefore of only limited value (Nelson et al. 1962).
Geographical strains of mosquito species from Africa that have been found to be susceptible after experimental infections and might therefore act as natural vectors, are Anopheles pembaensis from Kenya (Nelson et al. 1962), Aedes aegypti from Kenya (Nelson et al. 1962) and Tanzania (Roubaud 1937) as well as Culex pipiens fatigans from Kenya (Heisch, Nelson & Furlong 1959; Nelson et al. 1962).

Laboratory diagnosis in live animals

The laboratory diagnosis in live animals can be attained by the demonstration and identification of microfilariae, by serology and by molecular techniques. Various methods have been described for the detection of microfilariae in the blood of animals and humans. The preparation of wet blood films, thin and thick blood films stained with Romanovsky-type stains as well as the capillary haematocrit tube method are appropriate if high levels of microfilaraemia prevail (Schalm & Lain 1966; Collins 1971; Kelly 1973; Bailey 1987). Standardized concentration techniques allow detection of low microfilaraemia levels and make it possible to quantify microfilaria densities. In the classical modified Knott’s technique haemolysed blood is centrifuged and the sediment screened microscopically for microfilariae (Knott 1939; Newton & Wright 1956). Variations of this technique have been reviewed by Ho Thi Sang & Petithory (1963). In the membrane filtration technique 1 ml of blood treated with an anticoagulant is forced through a 3.0 µm polycarbonate membrane filter which is stained with Giemsa and examined microscopically (Bell 1967; Chularerk & Desowitz 1970; Dennis & Kean 1971; Chlebowsby & Zielke 1977). The membrane filtration technique is more sensitive than the Knott’s technique in cases where the microfilaria density is low (100-50 microfilariae/ml blood) (Bell 1967; Watson, Testoni & Porges 1973; Southgate 1974; Feldmeier, Bienzle, Schuh, Geister & Guggenmoos-Holzmann 1986; Beugnet, Bima-Blum & Chardonnet 1993a; Martini, Capelli, Poglayen, Bertotti & Turilli 1996).

ACKNOWLEDGEMENTS 
TABLE OF CONTENTS
LIST OF FIGURES
LIST OF TABLES
SUMMARY
CHAPTER 1 INTRODUCTION
CHAPTER 2 LITERATURE REVIEW OF THE DIFFERENT AETIOLOGIES OF FILARIOSIS IN DOMESTIC CARNIVORES IN AFRICA
2.1 Dirofilaria immitis
2.1.1 Taxonomy
2.1.2 Morphology
2.1.3 Life cycle
2.1.4 Host range
2.1.5 Vectors
2.1.6 Laboratory diagnosis in live animals
2.1.7 Veterinary and medical importance
2.1.8 Distribution on the African continent and its islands.
2.2 Dirofilaria repens
2.2.1 Taxonomy
2.2.2 Morphology
2.2.3 Life cycle
2.2.4 Host range
2.2.5 Vectors
2.2.6 Laboratory diagnosis in live animals
2.2.7 Veterinary and medical importance
2.2.8 Distribution on the African continent
2.3 Acanthocheilonema reconditum
2.3.1 Taxonomy
2.3.2 Morphology
2.3.3 Life cycle
2.3.4 Host range
2.3.5 Laboratory diagnosis in live animals
2.3.6 Veterinary and medical importance
2.3.7 Distribution on the African continent
2.4 Acanthocheilonema dracunculoides
2.4.1 Taxonomy
2.4.2 Morphology
2.4.3 Life cycle
2.4.4 Host range
2.4.5 Laboratory diagnosis in live animals
2.4.6 Veterinary and medical importance
2.4.7 Distribution on the African continent
2.5 Cercopithifilaria grassii
2.6 Brugia patei
2.7 Other reported species
CHAPTER 3 MATERIALS AND METHODS
3.1 Survey on the occurrence and prevalence of filarial helminths of domestic dogs in Gauteng, KwaZulu-Natal and Mpumalanga provinces, South Africa, and Maputo province, Mozambique
3.2 Survey on the occurrence and prevalence of filarial helminths of cats in KwaZulu-Natal province
3.3 Routine examinations for filarial infections of dogs and cats from South Africa between 1994 and 2008
3.4 Routine examinations for filarial infections of dogs and cats imported from African countries between 1992 and 2008
CHAPTER 4 RESULTS
4.1 Survey on the occurrence and prevalence of filarial helminths of domestic dogs in Gauteng, KwaZulu-Natal and Mpumalanga provinces, South Africa, and Maputo province, Mozambique
4.2 Survey on the occurrence and prevalence of filarial helminths of cats in KwaZulu-Natal province
4.3 Routine examinations for filarial infections of dogs and cats from South Africa between 1994 and 2008
4.4 Routine examinations for filarial infections of dogs and cats imported from African countries between 1992 and 2008
4.5 Literature review on filariosis of dogs and cats in Africa
CHAPTER 5 DISCUSSION
5.1 Dirofilaria immitis
5.2 Dirofilaria repens
5.3 Acanthocheilonema reconditum
5.4 Acanthocheilonema dracunculoides
5.5 Brugia patei
CHAPTER 6 REFERENCES
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