Bovine anaplasmosis and babesiosis in the Lesser Antilles: risk assessment of an unstable epidemiologic situation

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Bovine anaplasmosis and babesiosis in the Lesser Antilles: risk assessment of an unstable epidemiologic situation E Camus, S Montenegro-James To cite this version: E Camus, S Montenegro-James. Bovine anaplasmosis and babesiosis in the Lesser Antilles: risk assessment of an unstable epidemiologic situation. Veterinary Research, BioMed Central, 1994, 25 (2-3), pp.313-317. <hal-00902216> HAL Id: hal-00902216 https://hal.archives-ouvertes.fr/hal-00902216 Submitted on 1 Jan 1994 HAL is a multi-disciplinary open access archive for the deposit and dissemination of scientific research documents, whether they are published or not. The documents may come from teaching and research institutions in France or abroad, or from public or private research centers. L archive ouverte pluridisciplinaire HAL, est destinée au dépôt et à la diffusion de documents scientifiques de niveau recherche, publiés ou non, émanant des établissements d enseignement et de recherche français ou étrangers, des laboratoires publics ou privés.

Bovine anaplasmosis and babesiosis in the Lesser Antilles: risk assessment of an unstable epidemiologic situation E Camus S Montenegro-James 1 CIRAD-EMVT, BP 1232, 97185 Pointe-à-Pitre Cedex, France; 2Tulane University, Tropical Medicine, 1501 Canal Street, New Orleans, LA 70112, USA Summary &horbar; A seroepidemiological survey on tick-borne diseases of ruminants was carried out on 11 islands of the Lesser Antilles from Grenada to St Martin. A total of 1 795 cattle were randomly sampled and sera tested for antibodies to anaplasmosis (Anaplasma marginale) and babesiosis (Babesia bovis and B bigemina) using a dot-elisa test. Except for anaplasmosis, which was virtually absent from Guadeloupe, the seroprevalence of the 3 tick-borne diseases ranged from 18 to 71%. The epidemiologic situation was considered to be unstable in all of the study sites. The risk of clinical outbreaks was high in all the islands except for B bigemina in Montserrat and St Lucia and B bovis in St Lucia. The practical consequences in terms of tick eradication, tick control, and vaccination are discussed. Anaplasma marginale / Babesia bovis I Babesia bigemina / seroepidemiological survey I unstable situation / Lesser Antilles / Dot-ELISA Résumé &horbar; Anapiasmoses et babésioses bovines dans les Petites Antilles : évaluation du risque d instabilité. Une enquête séroépidémiologique sur les maladies transmises par les tiques a été réalisée dans 11 1 îles des Petites Antilles, de Grenade à Saint-Martin. 1 795 sérums bovins ont été prélevés au hasard et analysés pour rechercher l anaplasmose (Anaplasma marginale) et les babésioses (Babesia bovis et B bigemina) avec un test Dot-Elisa. La séroprévalence des 3 maladies variait de 18% à 71%, à l exception de la Guadeloupe où l anaplasmose semblait absente. La situation épidémiologique des 3 maladies était partout instable. Les risques de cas cliniques étaient élevés dans toutes les îles excepté la babésiose à B bovis à Montserrat et Sainte- Lucie et la babésiose à B bigemia à Sainte-Lucie. Les conséquences pratiques en termes d éradication ou de contrôle des tiques ainsi que de vaccination sont discutées. Anaplasma marginale / Babesia bovis / B bigemina / enquête séroépidémiologique / instabilité / Petites Antilles / Dot-Elisa * Correspondence and reprints

INTRODUCTION Inoculation rate Since the diagnosis of cowdriosis in Guadeloupe in 1980 (Perreau et al, 1980), investigations have focused on cowdriosis, its tick vector Amblyomma variegatum and the organization of an eradication campaign in the Lesser Antilles. The A variegatum eradication program will also have an influence upon the other major livestock tick, Boophilus microplus, and on the transmitted diseases, bovine babesiosis and anaplasmosis. The epidemiologic situation for these diseases has been only partially investigated in the Lesser Antilles. A seroepidemiological survey was organized in 1992 to assess the epidemiologic situation of bovine anaplasmosis (Anaplasma marginale) and babesiosis (Babesia bovis and B bigemina) and to draw practical conclusions. MATERIALS AND METHODS Experimental design The survey was carried out between February and September 1992 in collaboration with the Veterinary Services. of the Lesser Antilles. Eleven islands were surveyed from St Martin to Grenada; 1 % of the cattle population estimated at 200 000 heads was sampled. The islands are divided into districts, parishes or municipalities; a cluster sampling technique was applied: 1 % of herds in each area was randomly selected and almost all animals within these herds were sampled. However, 6- to 12-month-old calves were more represented in the sample in order to calculate the inoculation rate (see below). Serological test All sera were tested for the presence of antibodies to Anaplasma marginale, Babesia bovis and B bigemina using a dot-elisa (Montenegro- James et al, 1990, 1992). Mahoney and Ross (1972) developed a mathematical model to assess the enzootic stability/instability of babesiosis in Australia: 1= 11 - e! where I is the proportion of animals infected, h the daily probability of infection (inoculation rate) and tthe mean age of calves. The critical age for calves is between 6 and 12 months, when the colostral antibodies have disappeared and before the waning of natural resistance. The inoculation rate was calculated for each island and respective infection with the confidence interval calculated according to the sample size. RESULTS A total of 1 795 sera were collected from the cattle of the 11 islands, and tested for the presence of antibodies to anaplasmosis and babesiosis. On 8 islands, the age of the sampled animals was obtained: 576 6-12-month-old calves were examined. The seroprevalence and inoculation rates are presented in table I. For the 3 islands of St Kitts and Nevis, Barbados and Grenada, the age of the animals was not determined. To calculate the inoculation rates, it was assumed that the mean age was the same as the mean age for the other 8 islands. These inoculation rates with their confidence intervals are pre- 1 for each island and each sented in figure disease, and the risk areas determined according to Mahoney (1977). DISCUSSION Except for anaplasmosis in Guadeloupe (probably absent), the seroprevalence of the 3 tick-borne diseases ranged from 18 to 71% on the different islands in 6-12-

month-old calves. Even when the inoculation rates were calculated from the confidence intervals of the seroprevalence rates, the great majority of h values fell within the area of instability with maximum risk. No value reached the typical value of enzootic stability. Few of the diseases were in an unstable situation, but with a low risk of clinical cases: B bigemina in Montserrat and St Lucia; and B bovis in St Lucia. The unstable situation with maximum risk should be manifested by numerous outbreaks of anaplasmosis and babesiosis. In Guadeloupe between 1988 and 1993, 19 cases of B bovis and 1 case of B bigemina were diagnosed on Holstein, Limousin and Charolais but not a single case in Zebu Creole cattle which represents 95% of the cattle population (E Camus, personal communication). In Martinique (Alonso et al, 1992), between 1983 and 1992, 9 cases of B bovis in Holstein and 4 cases of anaplasmosis in Limousin, Holstein and Brahman were reported.

In Nevis (Hadrill et al, 1990) not a single case of babesiosis was observed during a 4-yr observation period. In St Lucia (Knowles etal, 1982), an outbreak of anaplasmosis and babesiosis was observed in imported Holstein but not in native cattle. Only rare cases were recorded in imported animals and mainly in dairy cattle. In Guadeloupe, the local creole cattle are naturally resistant to cowdriosis, babesiosis and anaplasmosis (Camus, 1989). In Martinique, there is a great majority of Brahman zebus, and the Bos indicus are more resistant to babesiosis. Is there a possibility that the Australian model is not applicable to other countries? The model was used in Brazil and Uruguay (Smith et al, 1984) for babesiosis, and in Australia and Indonesia for anaplasmosis (Wilson and Ronohardjo, 1984). What could be the impact of a 3-yr A variegatum eradication campaign on B microplus and transmitted diseases? Considering the 20-yr eradication campaign of B microplus in Puerto Rico (Crom, 1992) when the foci of A variegatum were rapidly controlled, the eradication campaign will probably reduce the population of B microplus and the seroprevalence rates of babesiosis and anaplasmosis, but it is unlikely to eradicate B microplus. In Martinique (Camus and Barr6, 1994), a strong A variegatum tick control program resulted in a decrease in the seroprevalence rates from 71 to 50% for anaplasmosis, from 83 to 60% for B bovis and 59 to 44% for B bigemina. In the Lesser Antilles, the eradication campaign will reduce the percentage of immune animals and, after the 3-yr acaricide treatment, the non-immune animals will face contacts with a growing number of infected B microplus. This phenomenon will be particularly critical for imported cattle. The epidemiologic situation for bovine babesiosis and anaplasmosis is unstable in all the islands of the Lesser Antilles, but clinical cases are only recorded on imported breeds, which represent less than 5% of the cattle population. The native cattle population reacts as if it were naturally resistant. If and when an A variegatum tick eradication campaign initiates, it will be necessary, by the end of the acaricide treatment regimen, to immunize all the imported cattle born during that period, or even, all of the seronegative imported cattle. ACKNOWLEDGMENTS Parts of this study were supported by a grant from the French Government (FIC - Fonds de Cooperation Regionale Carafbes-Guyane). We wish to thank for their collaboration to the survey: L Beauperthuy, A Benderdouche, C Corbette, N Denormandie, G Garris, E Harris, T King, L Lannoy, A Louvet, E Lunel, M Montrose, B Nisbett, B Nyack, J Robinson, P Rouchosse, B Thiebot, GD Thye. REFERENCES Alonso M, Camus E, Rodriguez Diego J, Bertaudiere L, Tatareau JC, Liabeuf JM (1992) Hémoparasitoses bovines en Martinique. Étude préliminaire. Rev Med Vet Pays Trop XLV (11), 9-14 Camus E (1989) Etude épidémiologique de la cowdriose à Cowdria ruminantium en Guadeloupe. Etudes et Syntheses de l lnstitut d Elevage et de Médecine Vétérinaire des Pays Tropicaux, Maisons-Alfort, 152 p Camus E, Barré N (1994) Vector situation of tickborne diseases in the Carribbean. Vet Parasitol (in press) Crom RL (1992) Eradication of Boophilus microplus (Acari: Ixodidae) in Puerto-Rico. Ann NY Acad Sci 653, 64-7 1 Hadrill DJ, Boid R, Jones TW, Bell-Sakyu L (1990) Bovine babesiosis on Nevis. Implications for tick control. Vet Rec 126, 403-404 Knowles RT, Montrose M, Craig TM, Wagner GG, Long RF (1982) Clinical and serological

evidence of bovine babesiosis and anaplasmosis in St Lucia. V2t Parasitol 10, 307-31 1 Mahoney DF (1977) Babesia of Domestic Animals. In: Parasitic Protozoa (JP Kreier, ed) IV, 1-52 Mahoney DF, Ross DR (1972) Epizootiological factors in the control of bovine babesiosis. Aust Vet J 48, 292-298 Montenegro-James S, Guillen AT, Tapang P, Abdel-Gawad A, Toro M, Ristic M (1990) Use of the dot enzyme-linked immunosorbent assay with isolated Anaplasma marginale initial bodies for serodiagnosis in cattle. Am J Vet Res 51, 1518-1521 Montenegro-James S, Guillen T, Toro M (1992) Dot Elisa para el diagnostico serologico de la anaplasmosis y babesiosis bovina. Rev Cientifica FCV de Luz II, 23-29 Perreau P, Morel PC, Barr6 N, Durand P (1980) Existence de la cowdriose (Heartwater) à Cowdria ruminantium chez les petits ruminants des Antilles françaises (La Guadeloupe) et des Mascareignes (la Reunion et Ile Maurice). Rev Elev Med Vet Pays Trop 33, 21-22 Smith RD, Madruga CR, Kessler RH etal (1984) Field validation of a computer simulation model of bovine babesiosis. In: Proc 2nd Symp Comp Appl Vet Med, Am Vet Comparative Soc, College Vet Med, Mississipi State Univ, 341-345 Wilson AJ, Ronohardjo P (1984) Some factors affecting the control of Bovine anaplasmosis with special reference to Australia and Indonesia. Prev Vet Med 2, 121-134 Vet Res (1994) 25, 317-32 1 Elsevier/INRA Dynamic stochastic simulation as a tool for studying bovine virus diarrhoea virus infections at the herd level JT Sørensen C Enevoldsen National Institute of Animal Science, PO Box 39, DK-8830 Tjele, Denmark Summary &horbar; Infectious diseases, such as bovine virus diarrhoea (BVD) virus infections in cattle, are often studied by Markov chain models. However, it is difficult to simulate dynamic interactions between production of a reproductive herd and the disease by this type of model. As an alternative, a dynamic stochastic model simulating the herd production was suggested. A dynamic stochastic model simulating the effect of BVD virus infection in a dairy cattle herd was used to exemplify how this type of model could be applied in research. The simulation example demonstrated that the effect of a BVD virus infection depended on the characteristics of the individual herd. dynamic stochastic simulation / bovine virus diarrhoea I dairy cattle herd * Correspondence and reprints