Brugia pahangi (Buckley & Edeson, 1956) Buckley, 1960
ETYMOLOGY:Brugia for Dr. Brug and pahangi for Pahang, Malaysia where the worm was discovered.
HISTORY: This worm was originally described as Wuchereriapahangi from cats and dogs in Malaysia (Buckley and Edeson, 1956) and then subsequently transferred to the genus Brugia by Buckley (1960).
GEOGRAPGHIC LOCATION: Brugia pahangi has been reported from cats in Malaysia; Mak et al. (1980) reported that about 11% of cats sampled in Peninsular Malaysia were infected. In Thailand, Chungpivat and Sucharit (1993) reported that about 25% of blood samples from 83 cats living in Buddhist temples were found to be infected with Brugiapahangi in the area of Lat Krabang. About 61 of 325 cats (18.8%) in South Kalimantan, Indonesia, were found to have circulating microfilariae of Brugiapahangi (Palmieri et al., 1985).
LOCATION IN HOST: The adult worms are found in the lymphatic vessels as also are larval stages (Schacher, 1962a). However, immature and adult worms can sometimes be recovered from subcutaneous tissues and the carcasses of infected cats.
PARASITE IDENTIFICATION: The adult males of Brugiapahangi are 17.4 to 20 mm long; the adult females of Brugiapahangi are 38 to 63 mm long (Schacher, 1962a). The adults of Brugiapahangi are most easily recognized by the male spicules; those of Brugiapahangi are shortest of the Brugia spp. in cats, those of Brugiapatei are intermediate in length, and those of Brugiamalayi are the longest. The left spicule of Brugiapahangi is 200 µm to 215 µm long; the right spicule is 75 µm to 90 µm long. There is probably no good way to distinguish the females of these Brugia species.
The microfilaria of Brugiapahangi is 280 µm (274 µm to 288 µm) long when collected in 2% formalin as in the Knott’s technique, and 189 µm (186 µm to 200 µm long when examined in a thick blood film (Schacher, 1962b).
Diagnosis of infection is made by finding the microfilariae in the blood using a Knott’s technique or by direct smear (Fig. 4-49). The numbers of circulating microfilariae per milliliter of blood can often be greater than 10,000 microfilariae per milliliter; Denham et al. (1972) found in experimentally infected cats that there were around 2 to 10 microfilariae per μl of blood. It is difficult to distinguish the microfilaria of Brugiapahangi from that of Brugiamalayi. The distinction between the two species is made by the examination of the innenkorper of Giemsa stained microfilariae, the innenkorper in the microfilaria of Brugiapahangi is longer than that in Brugiamalayi (Sivanandam and Mak, 1975). Also, when the microfilariae are stained using the acid phosphatase histochemical method, the microfilaria of Brugiapahangi tend to be red throughout their length while those of Brugiamalayi are red mainly at the excretory and anal pores (Redington, 1975). An antigen detection ELISA and counter-immunoelectrophoresis have been used to detect infections of Brugiapahangi in cats (Au et al., 1981; Kumar et al., 1991), but these tests are not commercially available.
LIFE CYCLE: After a cat is inoculated with infective third-stage larvae from mosquitos, the molt from the third to fourth stage occurs about 8 or 9 days later (Schacher, 1962a). The molt from fourth-stage larvae to adults occurs about 23 days after infection in the case of male worms and about 27 days after inoculation in the case of female worms. Microfilariae appear in the blood about 60 days after infection (Edeson et al., 1960; Schacher, 1962a). The females do not reach maximal length until about 120 days after infection; the males reach maximal length about 60 days after infection. The mean prepatent period in cats is 69 days; but it may take up to 96 days before a patent infection develops (Denham, 1974). Ewert and Singh (1969) found that experimentally infected cats first became microfilaremic about 10 weeks after infection. Microfilarial count were around 3 or 4 microfilariae per microliter of blood. Adults worms are capable of living in some cats over two years.
Different cats respond to infections in different manners. Based on observations made after experimental infection, Denham et al. (1992) divided cats that had been inoculated with third-stage larvae on repeated occasions into five groups. One group represented about 70% of the infected cats, and these cats developed high levels of circulating microfilariae that persisted for over two years. Cats in this group often had large numbers of worms present in their tissues at necropsy. In Group two cats, the adult worms die after about a year of infection, and in the presence of repeated inoculations of larvae, the cats become refractory to reinfection. In Group three cats, the microfilariae disappear from the blood after about a year of infection, but serum antigen levels remain high with adults being present at necropsy. In Group four cats, there is only a transient presence of microfilariae in the blood, and adult worms are not recovered at necropsy. Cats in Group five were refractory to infection initially and never developed circulating microfilariae nor adult worms.
Microfilariae that are transfused in whole blood to naive cats are capable of being detected in the circulation for up to 136 days after injection (Ponnudurae et al., 1975). Kittens born to two queens with circulating microfilariae were found to be negative for microfilariae, although microfilariae were found in the lungs of one kitten killed two days after birth (Kimmig, 1979). The microfilariae in a transplacentally infected kitten would not grow to adults because they have not passed through a mosquito, and it also appears likely that there is little chance of kittens presenting with microfilariae acquired from the queen.
The vectors of Brugiapahangi are mosquitos of the genus Mansonia, Anopheles, and Armigeres (Edeson et al., 1960). It has been shown that although this worm is not present in the United States that species of Anopheles and Psorphora found in Louisiana are capable of transmitting the infection experimentally (Schacher, 1962b). Infective larvae are found in the mouth parts of mosquitos about 9 to 11 days after the ingestion of blood containing microfilariae.
CLINICAL PRESENTATION AND PATHOGENESIS: The clinical presentation and pathogenesis of infection in cats has been examined almost exclusively for the purpose of using cats as models of human infection. Thus, there has been very little if any work done on possible disease being seen in naturally infected cats in endemic areas. Rogers and Denham (1974) and Rogers et al. (1975) reported on the changes in the lymphatics of cats infected with 100 to 200 infective larvae in the dorsum of one hind foot and then killed from two days to five years after infection. By 14 to 15 days after infection, some of the larvae were in the lymphatic sinus while others had migrated to the afferent lymphatic just below the popliteal node. At this stage the lymphatics were slightly dilated and the valves were slightly thickened. By 6 weeks after infection, the varicosity of the lymphatics had increased enormously and pockets of worms extended from the popliteal node to the tarsal joint. By 16 weeks after infection, the lymphatics showed extensive and chronic inflammation and fibrosis, and sometimes, there was obvious thrombo-lymphangitis. Cats that had been infected for 4 to 5 years typically improved and showed less lymphatic disorganization than cats infected for a year or so. In cats that were repeatedly infected over long periods of time (100 larvae and then rechallenged with 50 larvae at 10 day intervals for various periods), the pathological manifestations were variable. Sometimes the popliteal nodes were enormously enlarged, and other times, the nodes were scarcely palpable. In these studies of repeated inoculation, secondary inguinal lymph node systems and new lymphatics developed and ran alongside the non-functional lymphatic. Also, many new or enlarged skin lymphatics were observed.
A small percentage of humans infected with the related worm, Brugiamalayi, will develope marked fibrosis of various lymphatic tissues and fibrosis and apparent swelling of associated limbs or tissues; this condition is known as elephantiasis. This tends to occur in only a small percentage of infected individuals (Partono et al., 1977). Although there have been several studies where cats have been examined for microfilariae of Brugiapahangi, there have been no reports of elephantiasis occurring naturally in cats. Rogers and Denham (1974) noted that of the cats receiving repeated infections for 3 to 5 years, the limbs of a few cats seemed to simulate cases of human elephantiasis with edema and skin thickening.
TREATMENT: Although cats have been a major experimental model for studying infections with lymphatic filariid parasites, there has been very little work on the direct treatment of cats infected with Brugiapahangi. Edeson and Laing (1959) treated experimentally infected cats with diethylcarbamazine. The activity of the drug on the microfilariae in these cats was unlike in humans where there is a rapid die off after treatment. In the cats, the microfilariae often remained at pretreatment levels, the microfilariae remained infectious to mosquitoes and from mosquitoes infectious to other cats. At the same time, the adult worms in the cats appeared to die following treatments ranging from 10 to 100 milligrams per day from several days to a week. Work in humans infected with Brugiamalayi has shown that the oral administration of either diethylcarbamazine at 6 mg/kg or ivermectin at 20 to 200 μg/kg will markedly reduce the number of circulating microfilariae for 3 to 6 months in many cases (Otteson et al., 1997). It is not known what effects these treatment have on the adults in the tissues. In the case of elephantiasis in humans, treatment is currently usually through surgical intervention.
EPIZOOTIOLOGY:Brugiapahangi is a parasite of cats that has also been reported from dogs (Mak et al., 1980). The biology of the parasite is such that there is either no periodicity associated with the appearance of microfilariae in the blood or they are present at all times and somewhat increased in numbers either at night or during the day (Chunpivat and Sucharit, 1990; and Sucharit, 1973).
HAZARDS TO OTHER ANIMALS: Infection could be transmitted from cats to dogs, but this would require the animals living together and the infection being passed to the dog through a mosquito vector. Denham and McGreevy (1977) cite the various hosts of Brugiapahangi and note that it is in only a few primates , the dusky leaf-monkey and the slow loris, but appears several other animals, mainly carnivores, e.g., various civet cats, the panther, the pangolin, the moon rat, and the giant squirrel.
HAZARD TO HUMANS: Although humans have been experimentally infected with Brugiapahangi (Edeson et al., 1960); it would appear that there have been no natural human infections with this parasite reported (Abdullah et al., 1993). The diagnosis of infection in humans is complicated because the parasite overlaps the range of Brugiamalayi which has an almost indistinguishable microfilaria that is present in the same areas often in a subperiodic form.
CONTROL/PREVENTION: More recent work using the related worm Brugiamalayi (see below) would suggest that diethylcarbamazine is more likely to be a successful preventative than ivermectin.
Abdullah WO, Oothuman P, Yunu H. 1993. Detection of circulating antigens and parasite specific antibodies in filariasis. SE Asian J Trop Med Publ Hlth.
Au ACS, Denham DA, Steward MW, Draper CC, Ismail MM, Rao CK, Mak JW. 1981. Detection of circulating antigens and immune complexes in feline and human lymphatic filariasis. SE Asian J Trop Med Publ Hlth 12:492-498.
Buckley JJC. 1960. On Brugia gen. nov for Wuchereria spp. of the “malayi” group, i.e. W. malayi (Brug, 1927), W. pahangi Buckley and Edeson, 1956, W. patei Buckley, Nelson, and Heisch, 1958. Ann Trop Med Parasitol 54:75-77.
Buckley JJC. Edeson JFB. 1956. On the adult morphology of Wuchereria sp (malayi?) from a monkey (Macacairis) and from cats in Malaya, and on Wuchereriapahangi n. sp. from a dog and a cat. J Helmintol 30:1-20.
Chungpivat S, Sucharit S. 1990. Microfilarial periodicity of Brugiapahangi in naturally infected cats in Bangkok. Thai J Vet Med 20;239-245.
Chungpivat S, Sucharit S. 1993. Microfilariae in cats in Bangkok. Thai J Vet Med. 23:76-87.
Denham DA., 1974. Studies with Brugia pahangi. 6. The susceptibility of mal and female cats to infection. J Parasitol 60:642.
Denham DA, McGreevy PB. 1977. Brugian filariasis: epidemiology and experimental studies. Adv Parasitol 15:243-309.
Denham DA, Medeiros F, Baldwin C, Kumar H, Midwinter ICT, Vbirch DW, Smail A. 1992. Repeated infection of cats with Brugiapahangi: parasitological observations.
Denham DA, Ponnudurai T, Nelson GS, Rogers R, Guy F. 1972. Studies with Brugiapahangi I. Parasitological observations on primary infections of cats (Feliscatus). Int J Parasitol 2:239-247.
Denham DA, Rogers R. 1975. Structural and functional studies on the lymphatics of cats infected with Brugia pahangi. Trans Roy Soc Trop Med Hyg 69:173-176.
Edeson JFB, Laing ABG.. 1959. Studies on filariasis in Malaya: the effects of diethylcarbamazine on Brugia malayi and B. pahangi in domestic cats. Ann Trop Med Parasitol 53:394-399.
Edeson JFB, Wharton RH, Laing ABG. 1960. A preliminary account of the transmission, maintenance and laboratory vectors of Brugiapahangi. Trans Roy Soc Trop Med Hyg 54:439-449.
Ewert A, Singh M. 1969. Microfilarial levels in cats infected with Brugiapahangi by two alternative routes. Trans Toy Soc Trop Med Hyg 63:603-607.
Gooneratne BWM. 1973. A chronological lymphographic study of cats experimentally infected with Brugia filariasis from 5 days to 5 years. Lymphology 6:127-149.
Gooneratne BWM, Nelsonn GS, Denham DA, Rurzr H, Monson E. 1971. Lytmphographic changes inh cats with filariasis. Tras Roy Soc Trop Med Hytge 65:195-198.
Kimmig P. Diaplacentare Übertragung von Mikrofilarien der Art Brugiapahangi bei der Katze. Z Parasitenk 58:181-186.
Kumar H, Baldwin C, Birch DW, Kenham DA, Medeiros FD, Midwinter ITC, Smail A. Circulating filarial antigen in cats infected with Brugiapahangi is indicative of the presence of adult worms. Parasit Immunol 13:405-412.
Mak JW, Yen PKF, Lim KC, Ramiah N. 1980. Zoonotic implications of cats and dogs in filarial transmission in Peninsular Malaysia. Trop Geogr MEd 32:259-264.
Ottesen EA; Duke BO; Karam M; Behbehani K. 1997. Strategies and tools for the control/elimination of lymphatic filariasis. Bull World Health Organ 75: 491 503.
Palmieri JR, Masbar S, Purnomo Marwoto HA, Tirtokusumo S, Darwis F. 1985. The domestic cat as a host for Brugian filariasis in South Kalimantan (Borneo), Indonesia. J Helmintol 59:277-281.
Partono F, Oemijati SH, Joesoef A, Clarke MD, Durfee PT, Irving GS, Taylor J, Cross JH. 1977. Brugia malayi in seven villages in south Kalimatnan, Indonesia. SE Asina J Trop Med Publ Hlth 8:400-407.
Ponnampalam JT. 1972. Histological changes produced in cats by the microfilariae of Brugiapahangi. SE Asian J Trop Med Publ Hlth 3:511-517.
Pondurai T, Denham DA, Rogers R. 1975. Studies on Brugiapahangi 9. The logenvity of microfilariae transfused from cat to cat. J Helminthol 49:25-30.
Redington BC, Montgomery CA, Jervis HR, Hockmeyer WT. 1975. Histochemical differentiation of the microfilariae of Brugiapahangi and sub-periodic Brugiamalayi. An Trop Med Parasitol 69:489-492.
Rogers R, Denham DA. 1974. Studies with Brugiapahangi. 7. Changes in lymphatics of injected cats. J Helminthol 48:213-219.
Rogers R, Denham DA. 1975. Studies with Brugiapahangi: 11. Measurements of lymph flow in infected cats. SE Asian J Trop Med Publ Hlth 6:199-205.
Rogers R, Denham DA, Nelson GS, Guy F, Ponnudurai T. 1975. Studies with Brugiapahangi. III. Histological changes in the affected lymph nodes of infected cats. Ann Trop Med Parasitol 69:77-84.
Sakamoto M. 1980. Changes in the lymphatic system of cats experimentally infected with Brugia. Trop Med 22:223-236.
Schacher JF., 1962a. Developmental stages of Brugiapahangi in the final host. J Parasitol 48:693-706.
Schacher JF. 1962b. Morphology of the microfilaria of Brugiapahangi and of the larval stages in the mosquito. J Parasitol 48:679-692.
Schacher JF, Sahyoun PF. 1967. A chronological study of the histopathology of filaria disease in cats and dogs caused by Brugiapahangi (Buckley & Edeson, 1956). Trans Roy Soc Trop Med Hyg 61:234-243.
Sivanandam S, Mak JW. 1975. Some problems associated with the processing and staining of blood film for filaria diagnosis. J Med Hlth Lab Tech Malaysia 2:4-6.
Sucharit S. 1973. Brugiapahangi in small laboratory animals: the microfilarial periodicity. SE Asian J Trop Med Publ Hlth 4:492-497.
Sucharit S, Harinasuta C, Viraboonchai S, Smithanonda S. 1975. The differentiation of Brugiamalayi, B. pahngi, B. tupaiae and Wuchereriabancrofti. SE Asian J Trop Med Publ Hlth 6:549-554.
Suswillo RR, Denham DA, McGreevy P. 1982. The number and distribution of Brugiapahangi in cats at different times after a primary infection. Acta Trop 39:151-156.
Figure 4-49. Brugiapahangi. Microfilaria from experimentally infected rat Giemsa stain (specimen courtesy Dr. Robin Bell).