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Amaurornis phoenicurus and Ardeola bacchus as experimental definitive hosts for Capillaria philippinensis in Thailand
Intcrnarionol Journal Prrgamon Press Ltd.
for Parnsirology Vol. 9. pp. 321 -322. 1979. Printed in Great Britain.
AMAURORNIS PHOENICURUS AND ARDEOLA BACCHUS AS EXPERIMENTAL DEFINITIVE HOSTS FOR CAPILLARIA PHILIPPINENSIS IN THAILAND Department
M. BHAIBULAYA and S. INDRA-NGARM of Helminthology, Faculty of Tropical Medicine, Mahidol University, 420/6 Rajvithi Road, Phyathai, Bangkok 4, Thailand (Received
25 September
1978)
Abstract: BHAIEIULAYA M. and INDRA-NGARM S. 1979. Amaurornisphoenicurus and Ardeola bncchus as experimental definitive hosts for CapiNaria philippinensis in Thailand. International Journal for Parasitology 9: 321-322. Two species of fish-eating bird namely, Amaurornis phoenicurus and Ardeola bncchus were fed with infective larvae of Cupilluriu philippinensis in Gambusiu holbrookii. Intestinal capillariasis was able to establish in all three A. phoenicurus and one of three A. bacchus. Prepatent period in A. phoenicurus ranged from 22 to 30 days, whereas in A. bacchus it was 16 days after infection. Auto-infection was observed in all susceptible birds and the protective immunity had developed in one of A. phoenicurus used. INDEX KEY WORDS: Capillaria auto-infection; protective immunity.
Thailand;
philippinensis;
INTRODUCTION Indra-Ngarm & Ananthaprutti (1979) demonstrated that Capillaria philippinensis possessed a low intermediate host specificity; six of nine freshwater fish species used were found susceptible. Cross, Banzon, Murrell, Watten & Dizon (1970) stated that although thousands of animal specimens consisting of a wide range of species in the Philippines were examined, the adult of C. phifippinensis was not recovered. Bhaibulaya et al. (1979) suspected that fish-eating animals, particularly fish-eating birds, would probably be the natural definitive host of C. philippinensis. Therefore, in order to provide information for further epidemiological study the present experiments were performed. BHAIBULAYA,
MATERIALS AND METHODS Three Amaurornis phoenicurus (White breasted waterhen) and three Ardeola bacchus (Chinese pond heron), obtained from the Sunday Market in Bangkok, were used in the present study. They were kept separately in a cage for stool examination after approx 14 days. None was found positive with C. philippinensis in any form. Eggs of C. philippinensis were obtained from infected Mongolian gerbils. Two weeks after incubation at room temperature the infective embryonated eggs were fed to Gambusia holbrookii which proved to be a good intermediate host (Bhaibulaya et al., 1979). Two to three weeks after infection, G. holbrookii was fed to the birds. Each bird received lo-15 infected fish per day for 2-3 days and a total of 30 fish were fed to each bird. G. holbrookii from the same aquarium was examined randomly and they were found infected with C. philippinensis larvae. The
fish-eating
birds;
definitive
host;
faecal specimens of each bird were examined daily and clinical manifestations were observed throughout the experiments. RESULTS A. phoenicurus
Eggs of C. philippinensis were recovered from the first bird on 22nd, the second bird on 26th and the third bird on 30th days after the last feeding on infected fish. Between 23 and 35 days after infection the birds were found to be less active and refused food. The stool was watery and contained mucus. Numerous adults and larvae of C. phihppinensis were found in the faecal specimens during this period. From 30 to 34 days after infection the first bird from whicheggs of C.philippinensishad been observed on the 22nd day was found to have recovered from the illness and the eggs and the worms, including adults and larvae, had disappeared. On the 35th day of infection this bird developed again the same clinical manifestations. The eggs and the worms, including adults and larvae, were found in the faeces. Finally the bird died 40 days after infection and at least 300 adults plus several hundreds of larvae were recovered from the intestinal contents. On the 41st day of infection, the second bird from which the eggs of C. philippinensis were recovered 26 days after infection was found recovered from the illness. The eggs, larvae and adults were also disappeared. Eight months later there was still no C. philippinensis in any form in the faeces of this bird, although it was fed three more times with large numbers of 321
322
M.
BHAIBULAYAand S. INDRA-NGARM
infected
fish. The third bird from which eggs of C. philippinensis had been recovered on the 30th day developed more severe symptoms. It was killed on the 46th day of infection and thousands of worms, including adults and larvae, were recovered from the intestinal contents.
A. bacchus
One of the three A. bacchus used was found susceptible. The eggs were recovered from the faeces on the 16th day of infection. Between 19 and 28 days after infection the bird refused food and had frequent watery stools with detached intestinal mucosa. Numerous adults and larvae were found in the faeces. This bird died on the 29th day of infection and approx 19,000 worms, including adults and larvae, were recovered from the intestinal contents. DISCUSSION The above results showed that A. phoenicurus was likely to be more susceptible to infection of C. phifippinensis than A. bacchus. All three A. phoenicurus, but only one of three A. bacchus could be infected. The prepatent period in A. phoenicurus ranged from 22 to 30 days, whereas in A. bacchus it was found to be 16 days after infection. Cross, Banzon & Singson (1978) found that the prepatent period in the gerbil ranged from 24 to 35 days after infection. In the monkeys, Macaca cyclopis, Macaca irus and Macaca mulatta the prepatent period ranged from 22 to 96 days after infection (Cross, Clarke, Basaca-Sevilla, Watten & Dizon, 1972). The clinical incubation period appeared between 23 and 35 days, and 19 days after infection in A. phoenicurus and A. bacchus respectively. The clinical manifestations in the two kinds of bird were similar but were more severe in A. bacchus probably because of the heavier infection. Between 30 and 34 days after infection the eggs and the worms, as well as the clinical manifestations, had disappeared from the first A. phoenicurus. It seemed that frequent defaecation considerably reduced the number of worms, particularly the full grown adults. This was probably the reason why eggs and worms were not recovered during this period. Auto-reinfection in the first A. phoenicurus probably occurred from the 35th day of infection.
I.J.P. VOL. 9. 1979
Disappearance of infection in the second A. phoenicurus may have been due to development of immunity. A. phoenicurus is a common resident, whereas A. bacchus is a common migrant to Thailand. These two kinds of fish-eating bird can be found all over the country near thick vegetation in scrub country or marshes for the former, and in open country near water for the latter (Lekagul & Cronin, 1974). The present study has indicated that A. phoenicurus, fish-eating
A. bacchus birds might
and
probably
some
serve as the reservoir
other host of
C. philippinensis in nature. Considering the wide distribution of human cases, the low intermediate host specificity (Bhaibulaya et al., 1979) and the possibility that fish-eating birds are the natural reservoir hosts. the epidemic of intestinal capillariasis in Thailand needs to be watched carefully. Acknowledgements-The
authors would like to thank Professor S. Vajrasthira, Head, Department of Helminthology, Faculty of Tropical Medicine, Mahidol University for providing facilities in this study. Thanks are also extended to Dr. J. H. Cross, the Scientilic Director and Head, Department of Medical Ecology, U.S. Naval Medical Research Unit No. 2, Taipei, Taiwan for reading and criticizing the manuscript. REFERENCES BHAIBULAYA M., INDRA-NFARM S. & ANATHAPRUTTIM. 1979. Freshwater fishes of Thailand as experimental
hosts for Capiltaria philippinensis. International Journal for Parasitology 9: 105-105.
intermediate
CROSS J. H., BANZON T., MURRELL K. D., WATTEN R. H. & DIZON J. J. 1970. A new epidemic diarrhea1 disease
by the nematode Capillaria philippinensis. Industry and Tropical Health, 7: 124-131.
caused
CROSS J. H., CLARKE M. D., BASACA-SEV[LLAV., WATTEN R. H. & DIZON J. J. 1972. Studies on the experimantal
of Capillaria philippinensis in monkeys. Transactions qf the Royal Society of Tropical Medicine and Hygiene 66 : 819-827. transmission
CROSS J. H., BANZON T. & SINGSON C. 1978. Further studies on Capillaria philippinensis: Development of
the parasite
in the
Mongolian
gerbil. Journal
oj
Parasitology 64: 208-213. LEKAGUL B. & CRONIN
Jr. E. W. 1974. Bird Guide of Ladprao, Bangkok.
Thailand, 2nd Ed. Kurusapa
for Parnsirology Vol. 9. pp. 321 -322. 1979. Printed in Great Britain.
AMAURORNIS PHOENICURUS AND ARDEOLA BACCHUS AS EXPERIMENTAL DEFINITIVE HOSTS FOR CAPILLARIA PHILIPPINENSIS IN THAILAND Department
M. BHAIBULAYA and S. INDRA-NGARM of Helminthology, Faculty of Tropical Medicine, Mahidol University, 420/6 Rajvithi Road, Phyathai, Bangkok 4, Thailand (Received
25 September
1978)
Abstract: BHAIEIULAYA M. and INDRA-NGARM S. 1979. Amaurornisphoenicurus and Ardeola bncchus as experimental definitive hosts for CapiNaria philippinensis in Thailand. International Journal for Parasitology 9: 321-322. Two species of fish-eating bird namely, Amaurornis phoenicurus and Ardeola bncchus were fed with infective larvae of Cupilluriu philippinensis in Gambusiu holbrookii. Intestinal capillariasis was able to establish in all three A. phoenicurus and one of three A. bacchus. Prepatent period in A. phoenicurus ranged from 22 to 30 days, whereas in A. bacchus it was 16 days after infection. Auto-infection was observed in all susceptible birds and the protective immunity had developed in one of A. phoenicurus used. INDEX KEY WORDS: Capillaria auto-infection; protective immunity.
Thailand;
philippinensis;
INTRODUCTION Indra-Ngarm & Ananthaprutti (1979) demonstrated that Capillaria philippinensis possessed a low intermediate host specificity; six of nine freshwater fish species used were found susceptible. Cross, Banzon, Murrell, Watten & Dizon (1970) stated that although thousands of animal specimens consisting of a wide range of species in the Philippines were examined, the adult of C. phifippinensis was not recovered. Bhaibulaya et al. (1979) suspected that fish-eating animals, particularly fish-eating birds, would probably be the natural definitive host of C. philippinensis. Therefore, in order to provide information for further epidemiological study the present experiments were performed. BHAIBULAYA,
MATERIALS AND METHODS Three Amaurornis phoenicurus (White breasted waterhen) and three Ardeola bacchus (Chinese pond heron), obtained from the Sunday Market in Bangkok, were used in the present study. They were kept separately in a cage for stool examination after approx 14 days. None was found positive with C. philippinensis in any form. Eggs of C. philippinensis were obtained from infected Mongolian gerbils. Two weeks after incubation at room temperature the infective embryonated eggs were fed to Gambusia holbrookii which proved to be a good intermediate host (Bhaibulaya et al., 1979). Two to three weeks after infection, G. holbrookii was fed to the birds. Each bird received lo-15 infected fish per day for 2-3 days and a total of 30 fish were fed to each bird. G. holbrookii from the same aquarium was examined randomly and they were found infected with C. philippinensis larvae. The
fish-eating
birds;
definitive
host;
faecal specimens of each bird were examined daily and clinical manifestations were observed throughout the experiments. RESULTS A. phoenicurus
Eggs of C. philippinensis were recovered from the first bird on 22nd, the second bird on 26th and the third bird on 30th days after the last feeding on infected fish. Between 23 and 35 days after infection the birds were found to be less active and refused food. The stool was watery and contained mucus. Numerous adults and larvae of C. phihppinensis were found in the faecal specimens during this period. From 30 to 34 days after infection the first bird from whicheggs of C.philippinensishad been observed on the 22nd day was found to have recovered from the illness and the eggs and the worms, including adults and larvae, had disappeared. On the 35th day of infection this bird developed again the same clinical manifestations. The eggs and the worms, including adults and larvae, were found in the faeces. Finally the bird died 40 days after infection and at least 300 adults plus several hundreds of larvae were recovered from the intestinal contents. On the 41st day of infection, the second bird from which the eggs of C. philippinensis were recovered 26 days after infection was found recovered from the illness. The eggs, larvae and adults were also disappeared. Eight months later there was still no C. philippinensis in any form in the faeces of this bird, although it was fed three more times with large numbers of 321
322
M.
BHAIBULAYAand S. INDRA-NGARM
infected
fish. The third bird from which eggs of C. philippinensis had been recovered on the 30th day developed more severe symptoms. It was killed on the 46th day of infection and thousands of worms, including adults and larvae, were recovered from the intestinal contents.
A. bacchus
One of the three A. bacchus used was found susceptible. The eggs were recovered from the faeces on the 16th day of infection. Between 19 and 28 days after infection the bird refused food and had frequent watery stools with detached intestinal mucosa. Numerous adults and larvae were found in the faeces. This bird died on the 29th day of infection and approx 19,000 worms, including adults and larvae, were recovered from the intestinal contents. DISCUSSION The above results showed that A. phoenicurus was likely to be more susceptible to infection of C. phifippinensis than A. bacchus. All three A. phoenicurus, but only one of three A. bacchus could be infected. The prepatent period in A. phoenicurus ranged from 22 to 30 days, whereas in A. bacchus it was found to be 16 days after infection. Cross, Banzon & Singson (1978) found that the prepatent period in the gerbil ranged from 24 to 35 days after infection. In the monkeys, Macaca cyclopis, Macaca irus and Macaca mulatta the prepatent period ranged from 22 to 96 days after infection (Cross, Clarke, Basaca-Sevilla, Watten & Dizon, 1972). The clinical incubation period appeared between 23 and 35 days, and 19 days after infection in A. phoenicurus and A. bacchus respectively. The clinical manifestations in the two kinds of bird were similar but were more severe in A. bacchus probably because of the heavier infection. Between 30 and 34 days after infection the eggs and the worms, as well as the clinical manifestations, had disappeared from the first A. phoenicurus. It seemed that frequent defaecation considerably reduced the number of worms, particularly the full grown adults. This was probably the reason why eggs and worms were not recovered during this period. Auto-reinfection in the first A. phoenicurus probably occurred from the 35th day of infection.
I.J.P. VOL. 9. 1979
Disappearance of infection in the second A. phoenicurus may have been due to development of immunity. A. phoenicurus is a common resident, whereas A. bacchus is a common migrant to Thailand. These two kinds of fish-eating bird can be found all over the country near thick vegetation in scrub country or marshes for the former, and in open country near water for the latter (Lekagul & Cronin, 1974). The present study has indicated that A. phoenicurus, fish-eating
A. bacchus birds might
and
probably
some
serve as the reservoir
other host of
C. philippinensis in nature. Considering the wide distribution of human cases, the low intermediate host specificity (Bhaibulaya et al., 1979) and the possibility that fish-eating birds are the natural reservoir hosts. the epidemic of intestinal capillariasis in Thailand needs to be watched carefully. Acknowledgements-The
authors would like to thank Professor S. Vajrasthira, Head, Department of Helminthology, Faculty of Tropical Medicine, Mahidol University for providing facilities in this study. Thanks are also extended to Dr. J. H. Cross, the Scientilic Director and Head, Department of Medical Ecology, U.S. Naval Medical Research Unit No. 2, Taipei, Taiwan for reading and criticizing the manuscript. REFERENCES BHAIBULAYA M., INDRA-NFARM S. & ANATHAPRUTTIM. 1979. Freshwater fishes of Thailand as experimental
hosts for Capiltaria philippinensis. International Journal for Parasitology 9: 105-105.
intermediate
CROSS J. H., BANZON T., MURRELL K. D., WATTEN R. H. & DIZON J. J. 1970. A new epidemic diarrhea1 disease
by the nematode Capillaria philippinensis. Industry and Tropical Health, 7: 124-131.
caused
CROSS J. H., CLARKE M. D., BASACA-SEV[LLAV., WATTEN R. H. & DIZON J. J. 1972. Studies on the experimantal
of Capillaria philippinensis in monkeys. Transactions qf the Royal Society of Tropical Medicine and Hygiene 66 : 819-827. transmission
CROSS J. H., BANZON T. & SINGSON C. 1978. Further studies on Capillaria philippinensis: Development of
the parasite
in the
Mongolian
gerbil. Journal
oj
Parasitology 64: 208-213. LEKAGUL B. & CRONIN
Jr. E. W. 1974. Bird Guide of Ladprao, Bangkok.
Thailand, 2nd Ed. Kurusapa