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Susceptibility of Mansonia Uniformis to Brugia Malayi Microfilariae from Infected Domestic Cat

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Susceptibility of Mansonia Uniformis to Brugia Malayi Microfilariae from Infected Domestic Cat SOUTHEAST ASIAN J TROP MED PUBLIC HEALTH SUSCEPTIBILITY OF MANSONIA UNIFORMIS TO BRUGIA MALAYI MICROFILARIAE FROM INFECTED DOMESTIC CAT Usa Lek-Uthai1 and Wanachai Tomoen2 1Department of Parasitology, Faculty of Public Health, Mahidol University, Bangkok; 2Public Health Administrative Office, Ministry of Public Health, Bangkok, Thailand Abstract. Microfilariae of Brugia malayi is transmitted to man and other susceptible hosts via mos- quito. The transmission of B. malayi from cat to man by Ma. uniformis bite has never been reported. The Ma. uniformis mosquito is the normal vector for Wuchereria bancrofti but has never been re- ported as a vector for B. malayi, or a susceptible host for the growth and development of the mi- crofilariae of B. malayi. The purpose of this study was to examine the development of B. malayi in Mansonia uniformis after feeding on the blood of an infected cat in the laboratory. The B. malayi infected cat was identified using PCR with the primers Bm-1/Bm-2 on DNA (at 10 ng/50 µl) ex- tracted from the WBC of the cat. W. bancrofti was employed as a negative control. The sensitivity of the B. malayi DNA detection by PCR was 0.0001 ng. Adult Ma. uniformis mosquitos at the ages of 5, 10, and 15 days, 100 mosquitos in each group, were fed on the infected cat blood. Recovery of third stage microfilariae was found to be the highest in the 5-day old mosquito group (48%), fol- lowed by the 10- and 15-day old mosquito groups (32% and 18 %, respectively). The mean number of B. malayi microfilariae found in thorax, head, and abdomen of the mosquitos were composed. The 5-day old (40.3%) and 10-day old (41.9%) mosquitos were significantly more susceptible to microfilariae than the 15-day old mosquitos (17.8%) (p-values using the Scheffe method: 0.027 and 0.039, respectively). There was no significant difference in the mean number of microfilariae in the thorax (p=0.482) by age, but the mean numbers of microfilariae in the heads, and abdomens were significantly different by age between the 5- and 10-, and the 15-day old mosquitos (p<0.001 and p=0.004, respectively). INTRODUCTION Province, by the Ministry of Public Health. The subjects were mostly laborers in the fisheries, Lymphatic filariasis has a broad geographic illegal floating houses, rubber plantations, and distribution. Brugia malayi, zoonotic infection is industries and house keepers. Sixty-six subjects endemic in Asia, especially in the southern part were found to be infected with nocturnally peri- of Thailand, where the microfilariae are transmit- odic Wuchereria bancrofti (Sasa, 1976; WHO, ted to man and susceptible hosts via mosquito 1995). This same survey was carried out in (mainly Mansonia bonneae). The preferred habi- Phang-Nga, Phuket, and Surat Thani. The re- tat for the Mansonia spp is in Southern Thai- sults showed that the rate of infection had in- land, specifically the species which are the vec- creased from 1% to 1.13-4.34%. Brugia and tors for B. malayi, such as Ma. bonneae, Ma. Wuchereria microfilariae usually show nocturnal dives, Ma. uniformis, Ma. indiana, Ma. annulata, periodicity in the host peripheral blood, which is and Ma. annulifera. The 1993 microfilarial blood an adaptation to the vectors that feed only at survey was carried out widely among Thai and night. There are some situations where Myanmar laborers in the border areas of Rayong subperiodic strains of these parasites have adapted to diurnally active vectors (some Man- Correspondence: Dr Usa Lek-Uthai, Department of sonia and Aedes species). Periodic strains of Parasitology, Faculty of Public Health, Mahidol Uni- Brugia spp and Wuchereria bancrofti almost versity, 420/1 Rajvithi Road, Rajthewee, Bangkok 10400, Thailand. exclusively infect man. Subperiodic strains of B. Tel: +66 (0) 2644-5130, 1806-7471; Fax: +66 (0) 2644- malayi commonly infect domestic cats and vari- 5130 ous wild carnivores, from which transmission to E-mail: [email protected] man is not unusual via diurnally active Mansonia 434 Vol 36 No. 2 March 2005 SUSCEPTIBILITY OF MA. UNIFORMIS TO B. MALAYI spp (WHO, 1984). the parasite and its vectors (Lek-Uthai et al, B. malayi occurs only in South and South- 2004). Our study divided the Ma. uniformis into east Asia, where its distribution and prevalence 3 age groups (5 days, 10 days, and 15 days) have been reduced by control of the vector, according to thier susceptibility to infective larva Mansonia spp, by the simple method of removal (L3) of B. malayi in infected cats. of the host plants from their breeding places. Subperiodic strains occur in swamp and forest MATERIALS AND METHODS habitats, transmitted mainly by Ma. bonneae in Mosquitos a zoonotic cycle. Periodic strains of B. malayi Female Ma. uniformis mosquitos from the are also transmitted by Anopheles spp, but are field (Lat Krabang, Bangkok) aged 5, 10, and usually not zoonotic (Wharton, 1962). Iyengar 15 days were prepared in a keeping room. Each (1953) first surveyed for filariasis, and found it in group comprised 100 mosquitos. The mosqui- Nakhon Si Thammarat, Phatthalung, Pattani, and tos were reared and maintained at the Faculty Surat Thani, provinces in the southern region of of Tropical Medicine, Mahidol University with a Thailand. He found B. malayi microfilariae in- 6% fructose and vitamin B complex solution fected 5.2% of human, 21% of whom were absorbed onto filter paper, and kept at 27ºC, symptomatic. Harinnasuta et al (1970a,b) and 80% relative humidity, with a photo period of Guptavanij et al (1971a,b) found nocturnally pe- 12:12 (light:dark) hours. riodic and nocturnally sub-periodic microfilaria in human blood. The nocturnally sub-periodic Extraction of microfilarial DNA from blood form of B. malayi can infect both domestic and samples wild animals (Buckley and Edeson, 1956; Microfilariae were detected by filtration of 5 Phantana et al, 1978), causing zoonotic disease ml venous cat blood, along with 15 ml of phos- (Dondero et al, 1972). B. malayi can infect both phate buffer saline (PBS), through a polycarbon- humans and animals but B. pahangi can only ate membrane millipore (0.5 µm pore size); 10 infect animals, especially domestic cats of the 65 subjects had microfilaremia (3-68 mf/ (Thammapaolo et al, 1993). The past 25 years 60 µl). One ml of their blood was then thoroughly of the filariasis control program successful re- mixed with 800 µl of phosphate buffer saline duced the mosquito vectors. In 1987, 1988, and (PBS) and centrifuged to pellet red cells and 1989, 4,745, 3,082, and 3,404 cats were sur- microfilariae. The pellets were centrifuged at veyed, respectively. The results showed that 115, 5,000 rpm for 10 minutes. After centrifugation, (2.42%), 119 (3.86%), and 140 (3.86%) cats, re- the pellet was washed in 800 ml of PBS and spectively, were infected with microfilariae of then carefully resuspended in 200 µl of DSP Brugia species. Iyengar (1953) discovered that buffer (20 mM Tris-HCl, pH 7.6, 2.5 mM MgCl2, Mansonia spp were the vectors for Malayan fi- 50 mM KCl, 0.01% proteinase K, 0.5% lariasis. A prevalence rate of 3-17% was found Tween20®). Incubation in DSP was performed by Harinnasuta et al (1970b) in Chumphon Prov- at 42ºC for 14 hours to lyse the microfilariae and ince. They found the 0.12% of Ma. uniformis and release the DNA. The proteinase K was then in- 0.04% of Ma. annulifera were vectors for filari- activated by incubating the samples at 90ºC for asis. In Thailand, during the years 1993-1994, 10 minutes. Following brief centrifugation to pel- Malayan filariasis cases were found in Surat let debris, the supernatant was kept for PCR Thani Province (Division of Filariasis, 1996). The analysis. Aliquots of each blood sample were appearance of B. malayi in cats was monitored kept frozen at -20ºC in 0.1 M EDTA until they every 2 hours, for a total of 24 hours. The high- were processed for PCR analysis. In addition, est peak in parasitemia (149 microfilaria/20 µl) W. bancrofti, D. immitis, and D. repens were was found at 12.00 hrs and the lowest (23.9 mi- used to confirm the species-specificity of the crofilaria/20 ml) at 14.00 hrs. These findings in- PCR assay. Blood was also obtained from a hu- dicate that transmission is mainly at night, which man volunteer living in a non-endemic area. is the best time for an epidemiologist to study These additional blood samples were processed Vol 36 No. 2 March 2005 435 SOUTHEAST ASIAN J TROP MED PUBLIC HEALTH and amplified by PCR exactly as described for tect B. malayi DNA 10, 1.0, 0.1, 0.01, 0.001, the cat blood samples. and 0.0001 ng. This was when less than 1 mi- PCR screening for B. malayi from infected do- crofilariae was detected (Fig 1a). The specificity mestic cat of Bm-1/Bm-2 primers for B. malayi (Fig 1b), was calculated. The PCR products were examined Infected domestic cats were obtained from for 280 bp by electrophoresis with agarose gel the Center for Vector-borne Diseases Control 45, and ethidium bromide stain. The results were Surat Thani Province, Thailand. The cats were read under ultraviolet light. The B. malayi infected tested to have Brugia spp at a concentration of cats were confirmed to have no more than 20 at least 5-microfilariae/60 µl of blood. They were microfilariae/60 µl, which is the appropriate den- maintained for 15 days in the laboratory. They sity for feeding. The cats were then sedated with were tested by polymerase chain reaction (PCR) nembutal sodium solution (50 mg/ml) 1 ml/kg to differential between Brugia malayi and B.
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