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Vector situation of tick-borne diseases in the Caribbean islands
veterinary parasitology ELSEVIER
Veterinary Parasitology 57 ( 1995 ) 167-176
Vector situation of tick-borne diseases in the Caribbean islands E. Camus*, N. Barre CIRAD-EMVT, B.P 1232, 97185 Pointea PitreCedex, Guadeloupe
Abstract
The most important ticks transmitting diseases to ruminants in the Caribbean islands are: Arnblyomrna variegatum, vector of cowdriosis and associated with acute dermatophilosis; Amblyomma cajennense, potential vector of cowdriosis; Boophilus rnicroplus, vector of babesiosis and anaplasmosis. At the present time, Amblyomma variegatum is widespread in the Lesser Antilles from Barbados to Puerto Rico. The intensity of the tick control program varies in the different islands and the tick infestation in each island ranges from limited foci to widespread infestations. The vector situation appeared stable since 1988 in the Lesser Antilles but the outbreak in 1992 in Puerto Rico emphasized the risk of spread to other islands and to the American mainland, particularly with cattle egrets. Cowdriosis remains apparently limited to Guadeloupe and Antigua. Amblyomrna cajennense, experimental vector of cowdriosis, is present in Cuba, Jamaica and Trinidad but also in most American countries. Boophilus rnicroplus is widespread throughout the Caribbean. Its presence and importance are often indirectly estimated by the clinical and serological diagnosis of babesiosis and anaplasmosis. There is no correlation between the intensity ofAmblyornma variegaturn control in each island of the Lesser Antilles and the effect on the Boophilus microplus population measured by the seroprevalence to babesiosis and anaplasmosis, but within the island of Martinique a regular Arnblyornrna variegaturn control decreases the seroprevalences to babesiosis and anaplasmosis.
Keywords:Amblyomma spp.; Boophilus microplus; Epidemiology-Protozoa
* Corresponding author. 0304-4017/95/$09.50 © 1995 Elsevier Science B.V. All rights reserved
SSD10304-4017(94)03118-5
168
E. Camus, N. Barre / Veterinary Parasitology 5 7 (1995) 16 7-176
1. Introduction
The objectives of the study are to present the distribution and importance in the Caribbean islands of: ( 1) Amblyomma variegatum, vector of cowdriosis and associated with acute dermatophilosis; (2) Amblyomma cajennense, potential vector of cowdriosis; (3) Boophilus microplus, vector ofbabesiosis and anaplasmosis, and to evaluate the incidence of Amblyomma variegatum control/eradication on Boophilus microplus and transmitted diseases. Following the diagnosis of cowdriosis in 1980 in Guadeloupe (Perreau et al., 1980) the research focused on the disease and its vector Amblyomma variegatum in the Caribbean. To avoid the risk of spreading to the American mainland, an eradication campaign ofAmblyomma mriegatum has been considered since 1985. However, another important vector, Boophilus microplus, is present in the Caribbean region and the epidemiological status of anaplasmosis and babesiosis can be modified by an Amblyomma variegatum eradication program (George, 1991 ).
2. Materials and methods
2.1. LesserAntilles A survey was carried out in 1992, in collaboration with all the veterinary services of the Lesser Antilles. Eleven islands were surveyed from Grenada to St. Martin. One percent of the overall ruminant population estimated at 400 000 was sampled. A cluster sample technique was applied: 1% of the animals in herds in each island were randomly selected and all animals (to a maximum of 15 ) within selected herds were sampled. In each herd, data were collected on the tick control methods. The presence of Amblyomma variegatum was recorded for each sampled animal. In addition each island was classified according to its status regarding the overall infestation by Amblyomma variegatum and Boophilus microplus. The seroprevalence of anaplasmosis (Anaplasma marginale) and babesiosis (Babesia boris and Babesia bigemina) was determined by testing the sera with a DOT-ELISA (Montenegro-James et al., 1992 ). All sera were also tested for the presence of antibodies to Cowdria ruminantium using an indirect ELISA (Camus et al., 1993; Martinez et al., 1993). The incidence of Amblyomma variegatum control on babesiosis and anaplasmosis was evaluated by comparing the seroprevalences of these diseases between islands with different intensity of tick control. This incidence was also evaluated more precisely between herds in the particular island of Martinique where three approaches were observed: tick control every week, every 2 weeks and every month or more.
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169
2.2. GreaterAntilles The ticks and disease data were collected from the scientific literature and various unpublished reports.
3. Results
3.1. Distribution, importanceand control ofAmblyomma variegatum and associated diseases These are presented in Table 1 (a) and Fig. 1. ( 1 ) Since 1988 there has been no new observation of ticks in St. Vincent. (2) The foci in Dominica and St. Lucia are under control and the tick infestation is very low: only one engorged female was observed in St. Lucia and no ticks were observed in Dominica during the survey (Benderdouche and Lunel, 1992; Camus and Lannoy, 1992). (3) The focus in Puerto Rico was eradicated but a new one appeared in another place (Bokma and Shaw, 1993). (4) Cowdriosis is suspected serologically in Martinique and Montserrat (Camus et al., 1993). (5) Acute dermatophilosis remains a major constraint in St. Martin, St. KittsNevis, Antigua and Martinique. The economic importance ofAmblyomma variegatum and associated diseases in the lesser Antilles was estimated in 1986 at $4.6 million year-l (Anonymous, 1987 ), but the incalculable losses expected from an introduction on the American mainland are also potentially important.
3.2. Distribution and importance ofAmblyomma cajennense ticks Amblyomma cajennenseis an experimental and potential vector of cowdriosis (Uilenberg, 1983 ). If the pathogenic agent is introduced in a country free of Amblyomma variegatum but infested with Amblyomma cajennense,the disease might possibly spread but the tick appears to be a poor vector (Jongejan, 1992; Uilenberg, 1983). Fig. l shows the wide distribution ofAmblyomma cajennensein the Caribbean region: Cuba, Jamaica, Trinidad, but also all the American countries bordering the Caribbean Sea and the great majority of other South American countries. Moreover, according to Barr6 et al. ( 1987 ), Amblyomma cajennensecan infest a wide range of hosts including domestic ruminants, can live in open habitats and can be disseminated by migratory birds. Beside its potential role as vector of cowdriosis, Amblyomma cajennense is considered the second most economically important tick species in Latin America (Luque, 1978; Solis, 1989 ). Presently there is no particular program to control Amblyomma cajennense.
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Table 1 Distribution of ticks and associated diseases in the Caribbean (a) Amblyomma variegatum Reported not established P. Rico St. Martin St. Kitts/Nevis Montserrat Antigua Guadeloupe Dominica Martinique St. Lucia Barbados St. Vincent Grenada
Very limited
Limited
Widespread
Control
1
1
3
2 3 3
3 5 7
7 9 10 3 3
10 3
Cowdriosis
?4 6 8 ?4
Acute dermato
2 3 3 5 7 10 3
11
Ref: 1, Bokma and Shaw, 1993; 2, Camus and Thi6bot, 1992; 3, Benderdouche and Lunel, 1992; 4, Camus et al., 1993; 5, Camus and Louvet, 1992; 6, Birnie et al., 1984; 7, Denormandie, 1991; 8, Perreau et al., 1980; 9, Camus and Lannoy, 1992; 10, EDE-DSV-IEMVT, 1989; 11, Alexander, 1988.
(b ) A mblyomma cajennense and Boophilus microplus
Cuba Jamaica Haiti Dominican Rep Puerto Rico St. Martin St. Kitts/Nevis Montserrat Antigua Guadeloupe Dominica Martinique St. Lucia Barbados Grenada Trinidad
Amblyomma cajennense
Boophilus microplus
Babesia boris
Babesia bigemina
Anaplasma marginale
Tick control
1 3
1 4 6 6 8 9 I1 11 12 13 14 15 11 11 11 7
2 5 7 7 7 10 10 10 10 10 10 10 10 10 10 7
2 5 7 7 7 10 10 10 10 10 10 10 10 10 10 7
2 5 7 7 7 10 10 10 10 10 10 10 10 10 I0 7
1
8
Ref: 1, Cordoves and Vitorte, 1989; 2, Blandino et al., 1993; 3, Bishop and Trembley, 1945; 4, Bundy and Grey, 1982; 5, Bundy et al., 1983; 6, PAHO, 1980; 7, Caraphin, 1992; 8, Crom, 1992; 9, Camus and Thi6bot, 1992; 10, Camus and Montenegro-James, 1994; 11, Benderdouche and Lunel, 1992; 12, Camus and Louver, 1992; 13, Denormandie, 1991; 14, Camus and Lannoy, 1992; 15, EDE-DSVIEMVT, 1989.
E. Camus, N. Barre / VeterinaryParasitology 57 (1995) 167-176
0
2 C O ~ N
171
- Widoeprmad l~lt~ diltzibution l~tted - r e p o r t e d not e s t a b l i s h e d A. caJeanenme -
-very
Oo
/
~ VL R
DOXINICIJ
PUgRTO RICO
~
~
Ant£g V4
Fig. 1. Geographical distribution ofAmblyomma variegatum and Amblyomma cajennensein the Caribbean region.
3.3. Distribution and importance ofBoophilus microplus and transmitted diseases in the Caribbean Boophilus microplus is widespread in all the Caribbean countries, as are the transmitted diseases. The latest available report or reference for each pathogen and each country is presented in Table 1 (b). ( 1 ) In the Lesser Antilles, babesiosis and anaplasmosis are in an unstable epidemiological situation (Camus and Montenegro-James, 1994), with clinical cases observed mainly in dairy and imported cattle. (2) In Cuba (Cordoves and Vitorte, 1989) the economic losses induced by ticks and tick-borne diseases of cattle moved from the fourth to the seventh rank thanks to the tick control, even though 80% of livestock are represented by Holstein cows. In 1987, 81% of cattle were regularly treated with organophosphate acaricides and the average tick infestation was six adults per animal. Babesiosis remains one of the main causes of mortality (Blandino et al., 1993 ). ( 3 ) In Jamaica, anaplasmosis is widely recognized by clinicians (McGinnis et al., 1989 ) and outbreaks of babesiosis are associated with the seasonal recrudescence of the tick between December and March (Bundy and Grey, 1982 ).
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Table 2 Seroprevalence to babesiosis and anaplasmosis in the Lesser Antilles related to the intensity of tick control Island
Anaplasmosis
Babesiaboris
Babesiabigemina
Tick control
Guadeloupe
2 p. 100 78 31 51 64 82 71 45 34 70 55
35 p. 100 44 29 49 62 82 33 30 38 41 72
49 p. 100 37 36 49 43 80 25 22 34 27 50
1 2 3 2 1 3 3 2 2 2 1
St. Martin
Antigua Dominica St. Lucia St. Vincent
Grenada Barbados St. Kitts/Nevis
Montserrat Martinique
Tick control: 1, regular ( 1/week or 1/ 15 days): 2, irregular; 3, absent.
Table 3
Seroprevalence to babesiosis and anaplasmosis in Martinique related to the intensity of tick control Tick control
Anaplasmosis
Babesia bovis
Babesia bigemina
1/week X2 1/ 15 days X2 1/month or less X2 1 or 2/15 days
130/271 = 0.48 1.53 NS 41/73 =0.56 4.92* 102/143 =0.71 19.09*** 171/344 = 0.50
156/271 = 0.58 4.53* 52/73=0.71 4.22* 119/143=0.83 23.73*** 208/344 = 0.60
124/271 = 0.46 2.38 NS 26/73 =0.36 10.95"** 85/143 =0.59 10.15*** 150/344 = 0.44
*P= 0.05; **P= <0.01; ***P< 0.001.
(4) In the Dominican Republic, the spread of babesiosis is illustrated by the difficulty of finding serologically negative herds for determining the cut-off point of the ELISA (J. Quirico, personal communication, 1993 ). (5) In Haiti, a survey conducted in 1978 revealed that bovine babesiosis was a major source of economic loss (Pan American Health Organization (PAHO), 1980). (6) In Trinidad, the presence of anaplasmosis and babesiosis led to the necessity of infecting and treating imported animals (Smith, 1977 ). (7) In Puerto Rico, the eradication program of Boophilus microplus began in 1979 and it is hoped that the eradication can be realized by 1998 (Crom, 1992 ). Both Anaplasma marginale and Babesia bigemina are enzootic. The economic losses attributable to the tick and the transmitted diseases on Puerto Rico has been estimated at more than $20 million dollars year- ~ (Geri et al., 1989).
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3.4. Impact ofAmblyomma variegatum control on babesiosis and anaplasmosis Table 2 presents the seroprevalence for babesiosis and anaplasmosis in every island of the Lesser Antilles together with the rhythm of tick control. There is no statistically significant correlation between the intensity of the Amblyomma variegatum control and the seroprevalence of each disease transmitted by Boophilus microplus (anaplasmosis, r= 0.34; Babesia bovis, r= 0.18; Babesia bigemina, r = 0.008 ). On the island of Martinique, a statistically significant difference (g 2 test) of seroprevalence was observed between herds according to the intensity of tick control, mainly between herds with one or two tick controls fortnightly and herds with less intensive tick control (Table 3 ).
4. Discussion
The distribution ofAmblyomma variegatum in the Lesser Antilles appears stable since 1988. Fortunately, the expectation of Alderink and McCauley (1988 ) that the tick will infest one new island per year and will need 5 years to cover each island, was not justified. The progression has been slower and has stopped at present. However, the risk of spreading is far from suppressed. ( 1 ) Three islands are widely infested and the tick can easily spread from there. (2) Cattle egrets can be infested by larvae and nymphs and can fly as far as Grenada and Florida (M. Burddge, personal communication, 1993; Corn et al., 1993). (3) The reinfestation of Puerto Rico in 1992 after the successful eradication in 1987 clearly underlines the possibility of the tick extending its range. (4) The distribution of cowdriosis in the Lesser Antilles appears to be even more stable than the distribution of its vector because only the same three islands of Guadeloupe, Marie-Galante and Antigua have been infected for decades. In the suspected islands of Martinique and Montserrat, the absence of clinical cases, the fact that seropositive reactions are limited to sheep, the very low tick infestation rate and the impossibility to demonstrate a single infected tick among 500 in Martinique, speak for the absence of cowdriosis and therefore for the occurrence of serological cross reactions. However, the risk exists that the infection spreads with infected nymphs infesting cattle egrets, with carder domestic ruminants recovered from cowdriosis, or with dogs infested by infected ticks. (5) Amblyomma cajennense is a potentially important vector because of its very wide distribution. Experimentally, it is not considered a good vector because only one attempt in eight succeeded (Uilenberg, 1983) and this has been confirmed by Jongejan ( 1992 ). However, only two tick strains were tested and the result could be different with other strains. (6) Boophilus microplus in the Caribbean is really controlled only in Puerto Rico and Cuba. The epidemiological situation is unstable for babesiosis and an-
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aplasmosis in the Lesser Antilles but, apart from clinical cases in dairy and imported cattle, the impact is not known for the local breeds. (7) If the Amblyomma variegatum control has no apparent effect on the diseases transmitted by Boophilus micropluson an island scale, regular control decreases obviously the seroprevalence of babesiosis and anaplasmosis as is observed in particular in Martinique. We can expect a more important drop of these seroprevalences after a strong 3 year eradication program. The eradication of Boophilus microplusafter the Amblyomma variegatumcampaign is unlikely when we consider the 14 years of unsuccessful campaign in Puerto Rico! However, there will be a significant drop in the number of young cattle naturally infected and immunized by babesiosis and anaplasmosis. At the end of the campaign, to avoid outbreaks of the diseases following the explosion ofBoophilus microplusit would be wise to immunize all the cattle born during the eradication campaign.
5. Conclusion The regular and frightening progression ofAmblyomma variegatumin the Lesser Antilles has apparently been stopped, probably thanks to the control programs. However, a recent new focus in Puerto Rico emphasizes that the risk of the tick spreading still exists. An eradication program is the only way to avoid this risk. Several islands have been waiting for this program to be implemented since 1985, and have difficulties in maintaining their own control program. As a result, the tick situation could rapidly become worse. If the eradication campaign begins at last, it will probably be necessary to protect all the cattle born during the campaign against babesiosis and anaplasmosis.
Acknowledgments This work was partly funded by the French Government under the contract no. Fic 91. We are grateful to all the chief veterinary officers of the Lesser Antilles for helpful collaboration and to Dr. S. Montenegro-James for providing DOT-ELISA reagents.
References Alderink, F.J. and McCauley, E.H., 1988. The probability of the spread of Amblyomma variegatum in the Caribbean. Prev. Vet. Med., 6: 285-294. Alexander, F.C.M., 1988. Amblyomma variegatum in the Eastern Caribbean. XVI Biennial Caribbean Veterinary Convention, Georgetown, Guyana, 2-23 November 1988 (CARAPHIN). Anonymous, 1987. Management of the tropical bont tick (Amblyomma variegatum ) and associated diseases in the Caribbean. A feasibility proposal. USAID/USDA/IICA/FAO, 105 pp. Barrr, N., Uilenberg, G., Morel, P.C. and Camus, E., 1987. Dangers of introducing heartwater onto the American mainland: potential role of indigenous and exotic A mblyomma ticks. Onderstepoorl J. Vet. Res., 54(3): 405-417. Benderdouche, A. and Lunel, E., 1992. Enquete srro-epidrmiologique sur les maladies transmises par
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les tiques dans les petites Antilles. Memoire de Stage DESS, CIRAD-EMVT Maisons-Alfort, 98 pp. (Unpublished.) Birnie, E.J., Burridge, M.J., Camus, E. and Barrd, N., 1984. Heartwater in the Caribbean: Isolation of Cowdria ruminantium from Antigua. Vet. Rec., 116: 121-123. Bishop, F.C. and Trembley, H.L., 1945. Distribution and hosts of certain north American ticks. J. Parasitol., 31 ( 1 ): 1-54. Blandino, T., Barrera, M., Alonso, M., Faure, M. and Rodrignez Diego, J., 1993. Diagnostic de Babesia bigemina avec le test/t rimmunoperoxydase. Rev. Elev. Mdd. Vdt. Pays. Trop., in press. Bokma, B.H. and Shaw, J.L., 1993. Detection and eradication of a new focus of Amblyomma variegatum in Puerto Rico. Rev. Elev. Mdd. Vdt. Pays. Trop.,46: 355-358. Bundy, D.A.P. and Grey, C.L., 1982. Occurrence and distribution of protozoan parasites in the Caribbean livestock--A review. Trop. Anim. Health Prod., 14:235-241. Bundy, D.A.P., Hylton, G.A. and Wagner, G.G., 1983. Bovine haemoparasitic diseases in Jamaica. Trop. Anim. Health Prod., 15: 47-48. Camus, E. and Lannoy, L., 1992. Seroepidemiological survey of tick-borne diseases of ruminants in Dominica. CIRAD-EMVT Guadeloupe, 4 pp. (Unpublished.) Camus, E. and Louvet, A., 1992. Seroepidemiological survey of tick-borne diseases of ruminants in Antigua. CIRAD-EMVT Guadeloupe, 4 pp. (Unpublished.) Camus, E. and Montenegro-James, S., 1994. Bovine anaplasmosis and babesiosis in the Lesser Antilles: Risk assessment of unstable situation. Vet. Res., 25:313-317. Camus, E. and Thidbot, B., 1992. Seroepidemiological survey of tick-borne diseases of ruminants in St. Martin and St. Maarteen. CIRAD-EMVT Guadeloupe, 3 pp. (Unpublished.) Camus, E., Martinez, D., Beauperthuy, L., Benderdouche, A., Coisne, S., Corbette, C., Denormandie, N., Game, G., Harris, E., King, T., Lannoy, L., Louvet, A., Lunel, E., Montrose, M., Nisbett, B., Nyack, R., Robinson, J., Swanston, G., Thiebot, B. and Thye, G., 1993. Heartwater in Guadeloupe and in the Caribbean. Rev. Elev. Mdd. Vdt. Pays. Trop., 46:109-114. CARAPHIN, 1992. Regional surveillance report on animal pest and diseases in the Caribbean countries. IICA, Trinidad and Tobago: Vol. I, No. 2, June 1992. (Unpublished.) Cordoves, C.O. and Vitorte, E., 1989. Historia del control y erradicacion de las garrapatas en la Republica de Cuba. Proceedings of the Expert Consultation on the Eradication of Ticks, Mexico, 2226 June 1987, FAO, Rome, pp. 60-73. Corn, J., Barrd, N., Thiebot, B., Creekmore, T.E., Garris, G.I. and Nettles, U.F., 1993. The potential role of cattle egrets, Bubulcus ibis (Ciconiformes: ardendal) in the dissemination ofA mblyomma variegatum (Acari: Ixodidae) in the Eastern Caribbean. J. Med. Entomol., 30 (6): 1029-1037. Crom, R.L., 1992. Eradication of Boophilus rnicroplus (Acari: Ixodidae) in Puerto Rico. Ann. N.Y. Acad. Sci., 653: 64-71. Denormandie, N., 1991. Enquete sdro 6piddmiologique sur la cowdriose et Arnblyomma variegatum en Guadeloupe et Marie-Galante. Mdmoire de stage DESS, IEMVT Maisons-Alfort. (Unpublished.) EDE-DSV-IEMVT, 1989. Enquete sur la tique sdndgalaise, le ddtiquage et la dermatophilose en Martinque. IEMVT-CIRAD Guadeloupe, 17 pp. (Unpublished.) George, J.E., 1991. Summing-up of strategies for the control of ticks in regions of the world other than Africa. Parasitologia, 32: 203-209. Geri, L., Vollmerhausen, F., Wilson, D., Garris, G. and Popham, T., 1989. Puerto Rico tick eradication program benefit-cost analysis. USDA, APHIS, Hyattsville, MD. Jongejan, F., 1992. Studies on the transmission of Cowdria ruminantium by African and American A mblyomma ticks. In: U.G. Mundedoh and T.J. Kurtti (Editors), Proceedings and Abstracts, 1st Int. Conf. on Tick-borne Pathogens at the Host-Vector Interface: An Agenda for Research, 15-18 September 1992, St. Paul, MN, p. 143. Luque, G., 1978. Current knowledge of tick species distribution in Latin America. In: K.C. Thomson (Editor), Proc. of a Workshop on the Ecology and Control of Ectoparasites on Bovines in Latin America, 23-27 1975, CIAT, Cali, Colombia. Martinez, D., Coisne, S. and Sheikboudo, C., 1993. Detection of antibodies to Cowdria ruminantiurn in the serum of domestic ruminants by ELISA. Rev. Elev. Mdd. Vdt. Pays Trop., 46 ( 1-2 ): 115120. McGinnis, B., Grant, G., Hugh-Jones, M. and Wagner, G., 1989. Bovine Babesia bigemina seroreactors in Jamaica. Trop. Anim. Health Prod., 21: 227-228.
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Montenegro-James, S., Guillen, T. and Toro, M., 1992. DOT ELISA para el diagnostico serologico de la anaplasmosis y babesiosis bovina. Rev. Cient. FCV de LUZ, 2(2): 23-29. Pan American Health Organization, 1980. Inter-American Study on the Animal Health Situation. Vols. I-IV. PAHO. Perreau, P., Morel, P.C., Barre, N. and Durand, P., 1980. Existence de la cowdriose (heartwater) a Cowdria ruminantiurn chez les petits ruminants des Antilles frangaise (la Guadeloupe) et des Mascareignes (la Rrunion et Ile Maurice). Rev. Elev. Mrd. Vrt. Pays. Trop., 33 (1): 21-22. Smith, M.W., 1975. Some aspects on the ecology and life cycle ofAmblyomma cajennense ( Fabricus 1787) in Trinidad and their influence on tick control measure. Ann. Trop. Med. Parasitol., 69: 121-129. Smith, M.W., 1977. A procedure for the infection of susceptible imported cattle with field strains of Babesia bigernina and Anaplasma rnarginale in Trinidad. Pest Articles News Summaries, 23( 1 ): 27-32. Solis, S., 1989. E1 efecto del programma de control de Boophilus microplus en la dinamica de poplacion de Arnblyomrna spp. en Mexico. Proc. of the Expert Consultation on the Eradication of Ticks, Mexico, 22-26 June 1987, FAO, Rome, pp. 211-216. Uilenberg, G., 1983. Acquisitions nouvelles dans la connaissance du role vecteur de tiques du genre Amblyomma (Ixodidae). Rev. Elev. Mrd. Vrt. Pays Trop., 36( 1 ): 61-66.
Veterinary Parasitology 57 ( 1995 ) 167-176
Vector situation of tick-borne diseases in the Caribbean islands E. Camus*, N. Barre CIRAD-EMVT, B.P 1232, 97185 Pointea PitreCedex, Guadeloupe
Abstract
The most important ticks transmitting diseases to ruminants in the Caribbean islands are: Arnblyomrna variegatum, vector of cowdriosis and associated with acute dermatophilosis; Amblyomma cajennense, potential vector of cowdriosis; Boophilus rnicroplus, vector of babesiosis and anaplasmosis. At the present time, Amblyomma variegatum is widespread in the Lesser Antilles from Barbados to Puerto Rico. The intensity of the tick control program varies in the different islands and the tick infestation in each island ranges from limited foci to widespread infestations. The vector situation appeared stable since 1988 in the Lesser Antilles but the outbreak in 1992 in Puerto Rico emphasized the risk of spread to other islands and to the American mainland, particularly with cattle egrets. Cowdriosis remains apparently limited to Guadeloupe and Antigua. Amblyomrna cajennense, experimental vector of cowdriosis, is present in Cuba, Jamaica and Trinidad but also in most American countries. Boophilus rnicroplus is widespread throughout the Caribbean. Its presence and importance are often indirectly estimated by the clinical and serological diagnosis of babesiosis and anaplasmosis. There is no correlation between the intensity ofAmblyornma variegaturn control in each island of the Lesser Antilles and the effect on the Boophilus microplus population measured by the seroprevalence to babesiosis and anaplasmosis, but within the island of Martinique a regular Arnblyornrna variegaturn control decreases the seroprevalences to babesiosis and anaplasmosis.
Keywords:Amblyomma spp.; Boophilus microplus; Epidemiology-Protozoa
* Corresponding author. 0304-4017/95/$09.50 © 1995 Elsevier Science B.V. All rights reserved
SSD10304-4017(94)03118-5
168
E. Camus, N. Barre / Veterinary Parasitology 5 7 (1995) 16 7-176
1. Introduction
The objectives of the study are to present the distribution and importance in the Caribbean islands of: ( 1) Amblyomma variegatum, vector of cowdriosis and associated with acute dermatophilosis; (2) Amblyomma cajennense, potential vector of cowdriosis; (3) Boophilus microplus, vector ofbabesiosis and anaplasmosis, and to evaluate the incidence of Amblyomma variegatum control/eradication on Boophilus microplus and transmitted diseases. Following the diagnosis of cowdriosis in 1980 in Guadeloupe (Perreau et al., 1980) the research focused on the disease and its vector Amblyomma variegatum in the Caribbean. To avoid the risk of spreading to the American mainland, an eradication campaign ofAmblyomma mriegatum has been considered since 1985. However, another important vector, Boophilus microplus, is present in the Caribbean region and the epidemiological status of anaplasmosis and babesiosis can be modified by an Amblyomma variegatum eradication program (George, 1991 ).
2. Materials and methods
2.1. LesserAntilles A survey was carried out in 1992, in collaboration with all the veterinary services of the Lesser Antilles. Eleven islands were surveyed from Grenada to St. Martin. One percent of the overall ruminant population estimated at 400 000 was sampled. A cluster sample technique was applied: 1% of the animals in herds in each island were randomly selected and all animals (to a maximum of 15 ) within selected herds were sampled. In each herd, data were collected on the tick control methods. The presence of Amblyomma variegatum was recorded for each sampled animal. In addition each island was classified according to its status regarding the overall infestation by Amblyomma variegatum and Boophilus microplus. The seroprevalence of anaplasmosis (Anaplasma marginale) and babesiosis (Babesia boris and Babesia bigemina) was determined by testing the sera with a DOT-ELISA (Montenegro-James et al., 1992 ). All sera were also tested for the presence of antibodies to Cowdria ruminantium using an indirect ELISA (Camus et al., 1993; Martinez et al., 1993). The incidence of Amblyomma variegatum control on babesiosis and anaplasmosis was evaluated by comparing the seroprevalences of these diseases between islands with different intensity of tick control. This incidence was also evaluated more precisely between herds in the particular island of Martinique where three approaches were observed: tick control every week, every 2 weeks and every month or more.
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2.2. GreaterAntilles The ticks and disease data were collected from the scientific literature and various unpublished reports.
3. Results
3.1. Distribution, importanceand control ofAmblyomma variegatum and associated diseases These are presented in Table 1 (a) and Fig. 1. ( 1 ) Since 1988 there has been no new observation of ticks in St. Vincent. (2) The foci in Dominica and St. Lucia are under control and the tick infestation is very low: only one engorged female was observed in St. Lucia and no ticks were observed in Dominica during the survey (Benderdouche and Lunel, 1992; Camus and Lannoy, 1992). (3) The focus in Puerto Rico was eradicated but a new one appeared in another place (Bokma and Shaw, 1993). (4) Cowdriosis is suspected serologically in Martinique and Montserrat (Camus et al., 1993). (5) Acute dermatophilosis remains a major constraint in St. Martin, St. KittsNevis, Antigua and Martinique. The economic importance ofAmblyomma variegatum and associated diseases in the lesser Antilles was estimated in 1986 at $4.6 million year-l (Anonymous, 1987 ), but the incalculable losses expected from an introduction on the American mainland are also potentially important.
3.2. Distribution and importance ofAmblyomma cajennense ticks Amblyomma cajennenseis an experimental and potential vector of cowdriosis (Uilenberg, 1983 ). If the pathogenic agent is introduced in a country free of Amblyomma variegatum but infested with Amblyomma cajennense,the disease might possibly spread but the tick appears to be a poor vector (Jongejan, 1992; Uilenberg, 1983). Fig. l shows the wide distribution ofAmblyomma cajennensein the Caribbean region: Cuba, Jamaica, Trinidad, but also all the American countries bordering the Caribbean Sea and the great majority of other South American countries. Moreover, according to Barr6 et al. ( 1987 ), Amblyomma cajennensecan infest a wide range of hosts including domestic ruminants, can live in open habitats and can be disseminated by migratory birds. Beside its potential role as vector of cowdriosis, Amblyomma cajennense is considered the second most economically important tick species in Latin America (Luque, 1978; Solis, 1989 ). Presently there is no particular program to control Amblyomma cajennense.
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Table 1 Distribution of ticks and associated diseases in the Caribbean (a) Amblyomma variegatum Reported not established P. Rico St. Martin St. Kitts/Nevis Montserrat Antigua Guadeloupe Dominica Martinique St. Lucia Barbados St. Vincent Grenada
Very limited
Limited
Widespread
Control
1
1
3
2 3 3
3 5 7
7 9 10 3 3
10 3
Cowdriosis
?4 6 8 ?4
Acute dermato
2 3 3 5 7 10 3
11
Ref: 1, Bokma and Shaw, 1993; 2, Camus and Thi6bot, 1992; 3, Benderdouche and Lunel, 1992; 4, Camus et al., 1993; 5, Camus and Louvet, 1992; 6, Birnie et al., 1984; 7, Denormandie, 1991; 8, Perreau et al., 1980; 9, Camus and Lannoy, 1992; 10, EDE-DSV-IEMVT, 1989; 11, Alexander, 1988.
(b ) A mblyomma cajennense and Boophilus microplus
Cuba Jamaica Haiti Dominican Rep Puerto Rico St. Martin St. Kitts/Nevis Montserrat Antigua Guadeloupe Dominica Martinique St. Lucia Barbados Grenada Trinidad
Amblyomma cajennense
Boophilus microplus
Babesia boris
Babesia bigemina
Anaplasma marginale
Tick control
1 3
1 4 6 6 8 9 I1 11 12 13 14 15 11 11 11 7
2 5 7 7 7 10 10 10 10 10 10 10 10 10 10 7
2 5 7 7 7 10 10 10 10 10 10 10 10 10 10 7
2 5 7 7 7 10 10 10 10 10 10 10 10 10 I0 7
1
8
Ref: 1, Cordoves and Vitorte, 1989; 2, Blandino et al., 1993; 3, Bishop and Trembley, 1945; 4, Bundy and Grey, 1982; 5, Bundy et al., 1983; 6, PAHO, 1980; 7, Caraphin, 1992; 8, Crom, 1992; 9, Camus and Thi6bot, 1992; 10, Camus and Montenegro-James, 1994; 11, Benderdouche and Lunel, 1992; 12, Camus and Louver, 1992; 13, Denormandie, 1991; 14, Camus and Lannoy, 1992; 15, EDE-DSVIEMVT, 1989.
E. Camus, N. Barre / VeterinaryParasitology 57 (1995) 167-176
0
2 C O ~ N
171
- Widoeprmad l~lt~ diltzibution l~tted - r e p o r t e d not e s t a b l i s h e d A. caJeanenme -
-very
Oo
/
~ VL R
DOXINICIJ
PUgRTO RICO
~
~
Ant£g V4
Fig. 1. Geographical distribution ofAmblyomma variegatum and Amblyomma cajennensein the Caribbean region.
3.3. Distribution and importance ofBoophilus microplus and transmitted diseases in the Caribbean Boophilus microplus is widespread in all the Caribbean countries, as are the transmitted diseases. The latest available report or reference for each pathogen and each country is presented in Table 1 (b). ( 1 ) In the Lesser Antilles, babesiosis and anaplasmosis are in an unstable epidemiological situation (Camus and Montenegro-James, 1994), with clinical cases observed mainly in dairy and imported cattle. (2) In Cuba (Cordoves and Vitorte, 1989) the economic losses induced by ticks and tick-borne diseases of cattle moved from the fourth to the seventh rank thanks to the tick control, even though 80% of livestock are represented by Holstein cows. In 1987, 81% of cattle were regularly treated with organophosphate acaricides and the average tick infestation was six adults per animal. Babesiosis remains one of the main causes of mortality (Blandino et al., 1993 ). ( 3 ) In Jamaica, anaplasmosis is widely recognized by clinicians (McGinnis et al., 1989 ) and outbreaks of babesiosis are associated with the seasonal recrudescence of the tick between December and March (Bundy and Grey, 1982 ).
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Table 2 Seroprevalence to babesiosis and anaplasmosis in the Lesser Antilles related to the intensity of tick control Island
Anaplasmosis
Babesiaboris
Babesiabigemina
Tick control
Guadeloupe
2 p. 100 78 31 51 64 82 71 45 34 70 55
35 p. 100 44 29 49 62 82 33 30 38 41 72
49 p. 100 37 36 49 43 80 25 22 34 27 50
1 2 3 2 1 3 3 2 2 2 1
St. Martin
Antigua Dominica St. Lucia St. Vincent
Grenada Barbados St. Kitts/Nevis
Montserrat Martinique
Tick control: 1, regular ( 1/week or 1/ 15 days): 2, irregular; 3, absent.
Table 3
Seroprevalence to babesiosis and anaplasmosis in Martinique related to the intensity of tick control Tick control
Anaplasmosis
Babesia bovis
Babesia bigemina
1/week X2 1/ 15 days X2 1/month or less X2 1 or 2/15 days
130/271 = 0.48 1.53 NS 41/73 =0.56 4.92* 102/143 =0.71 19.09*** 171/344 = 0.50
156/271 = 0.58 4.53* 52/73=0.71 4.22* 119/143=0.83 23.73*** 208/344 = 0.60
124/271 = 0.46 2.38 NS 26/73 =0.36 10.95"** 85/143 =0.59 10.15*** 150/344 = 0.44
*P= 0.05; **P= <0.01; ***P< 0.001.
(4) In the Dominican Republic, the spread of babesiosis is illustrated by the difficulty of finding serologically negative herds for determining the cut-off point of the ELISA (J. Quirico, personal communication, 1993 ). (5) In Haiti, a survey conducted in 1978 revealed that bovine babesiosis was a major source of economic loss (Pan American Health Organization (PAHO), 1980). (6) In Trinidad, the presence of anaplasmosis and babesiosis led to the necessity of infecting and treating imported animals (Smith, 1977 ). (7) In Puerto Rico, the eradication program of Boophilus microplus began in 1979 and it is hoped that the eradication can be realized by 1998 (Crom, 1992 ). Both Anaplasma marginale and Babesia bigemina are enzootic. The economic losses attributable to the tick and the transmitted diseases on Puerto Rico has been estimated at more than $20 million dollars year- ~ (Geri et al., 1989).
E. Camus, N. Barre / Veterinary Parasitology 5 7 (1995) 16 7-176
173
3.4. Impact ofAmblyomma variegatum control on babesiosis and anaplasmosis Table 2 presents the seroprevalence for babesiosis and anaplasmosis in every island of the Lesser Antilles together with the rhythm of tick control. There is no statistically significant correlation between the intensity of the Amblyomma variegatum control and the seroprevalence of each disease transmitted by Boophilus microplus (anaplasmosis, r= 0.34; Babesia bovis, r= 0.18; Babesia bigemina, r = 0.008 ). On the island of Martinique, a statistically significant difference (g 2 test) of seroprevalence was observed between herds according to the intensity of tick control, mainly between herds with one or two tick controls fortnightly and herds with less intensive tick control (Table 3 ).
4. Discussion
The distribution ofAmblyomma variegatum in the Lesser Antilles appears stable since 1988. Fortunately, the expectation of Alderink and McCauley (1988 ) that the tick will infest one new island per year and will need 5 years to cover each island, was not justified. The progression has been slower and has stopped at present. However, the risk of spreading is far from suppressed. ( 1 ) Three islands are widely infested and the tick can easily spread from there. (2) Cattle egrets can be infested by larvae and nymphs and can fly as far as Grenada and Florida (M. Burddge, personal communication, 1993; Corn et al., 1993). (3) The reinfestation of Puerto Rico in 1992 after the successful eradication in 1987 clearly underlines the possibility of the tick extending its range. (4) The distribution of cowdriosis in the Lesser Antilles appears to be even more stable than the distribution of its vector because only the same three islands of Guadeloupe, Marie-Galante and Antigua have been infected for decades. In the suspected islands of Martinique and Montserrat, the absence of clinical cases, the fact that seropositive reactions are limited to sheep, the very low tick infestation rate and the impossibility to demonstrate a single infected tick among 500 in Martinique, speak for the absence of cowdriosis and therefore for the occurrence of serological cross reactions. However, the risk exists that the infection spreads with infected nymphs infesting cattle egrets, with carder domestic ruminants recovered from cowdriosis, or with dogs infested by infected ticks. (5) Amblyomma cajennense is a potentially important vector because of its very wide distribution. Experimentally, it is not considered a good vector because only one attempt in eight succeeded (Uilenberg, 1983) and this has been confirmed by Jongejan ( 1992 ). However, only two tick strains were tested and the result could be different with other strains. (6) Boophilus microplus in the Caribbean is really controlled only in Puerto Rico and Cuba. The epidemiological situation is unstable for babesiosis and an-
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aplasmosis in the Lesser Antilles but, apart from clinical cases in dairy and imported cattle, the impact is not known for the local breeds. (7) If the Amblyomma variegatum control has no apparent effect on the diseases transmitted by Boophilus micropluson an island scale, regular control decreases obviously the seroprevalence of babesiosis and anaplasmosis as is observed in particular in Martinique. We can expect a more important drop of these seroprevalences after a strong 3 year eradication program. The eradication of Boophilus microplusafter the Amblyomma variegatumcampaign is unlikely when we consider the 14 years of unsuccessful campaign in Puerto Rico! However, there will be a significant drop in the number of young cattle naturally infected and immunized by babesiosis and anaplasmosis. At the end of the campaign, to avoid outbreaks of the diseases following the explosion ofBoophilus microplusit would be wise to immunize all the cattle born during the eradication campaign.
5. Conclusion The regular and frightening progression ofAmblyomma variegatumin the Lesser Antilles has apparently been stopped, probably thanks to the control programs. However, a recent new focus in Puerto Rico emphasizes that the risk of the tick spreading still exists. An eradication program is the only way to avoid this risk. Several islands have been waiting for this program to be implemented since 1985, and have difficulties in maintaining their own control program. As a result, the tick situation could rapidly become worse. If the eradication campaign begins at last, it will probably be necessary to protect all the cattle born during the campaign against babesiosis and anaplasmosis.
Acknowledgments This work was partly funded by the French Government under the contract no. Fic 91. We are grateful to all the chief veterinary officers of the Lesser Antilles for helpful collaboration and to Dr. S. Montenegro-James for providing DOT-ELISA reagents.
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