Rickettsia africae in the West Indies
http://www.100md.com
《传染病的形成》
Ross University School of Veterinary Medicine, Basseterre, Saint Kitts and Nevis, West Indies
Rickettsia africae is the agent of African tick-bite fever, a mild but common disease of local persons and tourists in Africa. The major vector of this spotted fever group rickettsia is most likely Amblyomma variegatum, the tropical bont tick, which has become widely distributed through the West Indies in the last 30 years. This report reviews all available information on R. africae in the West Indies.
Rickettsia africae is a recently described spotted fever group (SFG) rickettsia that is the agent of African tick-bite fever (ATBF), a mild but common tickborne disease of local persons and tourists, in particular, in sub-Saharan Africa. The clinical and laboratory features of ATBF have recently been reviewed (1), as has the diagnosis of the disease (2). In Africa, the tropical bont tick, Amblyomma variegatum, is commonly infected with R. africae and is likely the major vector of the organism (3). This tick was introduced from Africa (Senegal) into the West Indies (Guadeloupe) in the early 1800s but has only spread widely and become endemic on many islands in the last 30 years (4). This spread was probably due to an increase in the between-island movement of livestock, major hosts of A. variegatum (5), and the introduction and spread of the cattle egret (Bubulcus ibis), a host of the immature stages of A. variegatum (5). Recent studies have demonstrated R. africae infections in A. variegatum, persons, and animals in the West Indies. In this report, the available information on R. africae in the region is reviewed.
Epidemiology of R. africae
Early studies in southern Africa showed the bont tick, A. hebraeum, was commonly infected with R. africae (6). In feeding experiments, R. africae was maintained transtadially and transovarially in A. hebraeum, and the tick transmitted the organism at each feeding stage (7). Cattle and goats are common hosts of A. hebraeum and, when infected with R. africae, show no clinical or laboratory signs of disease. They are, however, intermittently rickettsemic and may then be sources of infection for ticks (8,9). While A. hebraeum is the most common vector of R. africae in southern Africa, epidemiologic evidence indicates that A. variegatum is the predominant vector in the rest of sub-Saharan Africa. This tick readily feeds on people (10,11) and is commonly infected with R. africae (16%–75%) in widely separated areas in Africa (6,12–14).
Although R. africae is widely distributed in Africa, and serosurveys have shown infections are extremely common in humans (up to 100%) (1), reports of ATBF in indigenous people are unexpectedly rare. This finding could be because they are generally infected at a young age, when the disease might be very mild or subclinical, and medical attention is not sought. Also, inoculation eschars are difficult to see in pigmented skin, and definitive diagnosis of ATBF requires sophisticated diagnostic tests not available in developing countries. The disease, however, is quite common in international travelers; up to 11% of visitors to disease-endemic areas have evidence of infection (15,16).
R. africae in the West Indies
The first suspected cases of human spotted fever were reported from Guadeloupe in the 1960s (1). The patients had a history of tick bites and antibodies against SFG rickettsiae. Although rickettsiae were isolated from A. variegatum on the island, they were never definitively identified, and samples have been lost (17).
In 1998, Parola et al. (18) described a French woman who was bitten on the foot by a tick while visiting Guadeloupe. An erythematous nodule subsequently developed at the site as well as fever, elevated liver enzyme levels, and leukopenia. Serologic and adsorption studies suggested that she had been infected with R. africae. She recovered slowly when she was treated with doxycycline for 3 weeks. Subsequently, further human infections were documented on the island (19), and R. africae was detected in 27% of A. variegatum used for isolation experiments or polymerase chain reaction (PCR) analysis with rOmpA primers (20).
In 2002, Robinson et al. (21) used PCR with rOmpA and gltA primers to show that 84% of 75 A. variegatum collected from cattle in Antigua contained DNA of R. africae. In 2003, Kelly et al. (22) found 41% of A. variegatum from Saint Kitts and Nevis were positive for DNA of R. africae in PCRs in which rOmpA primers were used for the SFG rickettsiae. Positive ticks were found at 7 of 8 sites sampled, with prevalences varying from 14% to 71%. In the same year, Parola et al. (23) reported finding DNA of the ompA gene of R. africae in 7 (56%) of 12 A. variegatum tested from Martinique.
Although Rhipicephalus (Boophilus) microplus, the tropical/southern cattle tick, and Rhipicephalus sanguineus, the brown dog tick, are widespread in the Caribbean (24), they have not been implicated as vectors of R. africae. PCR with rOmpA primers of 52 R. sanguineus and 16 R. microplus from Saint Kitts and Nevis did not show DNA of SFG rickettsiae (unpub. data). Similarly, SFG rickettsial DNA was not identified in 6 R. microplus and 11 R. sanguineus from Martinique (23) or in 6 R. microplus from Antigua (21).
The studies described show that A. variegatum is commonly infected with R. africae in the West Indies. In the only published serosurvey conducted in the region (20), high prevalences of antibodies to R. africae were found in Guadeloupean cattle (81%) and goats (87%), which are common hosts of A. variegatum (24). Antibodies to R. africae were also highly prevalent (49%) in local people from Guadeloupe. The prevalence in men was significantly higher than in women, possibly because men were more likely to be exposed while working outdoors. The West Indian population, then, appears to be commonly exposed to A. variegatum that transmits R. africae. As is the case in Africa, however, clinical cases of ATBF in local persons are unexpectedly rare; the only reported cases of ATBF contracted in the region have been in tourists (18,19).
Recently, programs have been introduced to eradicate A. variegatum from the Caribbean (25–27). The principal justification for the projects has been the economic loses to island economies caused by animal diseases associated with A. variegatum, mainly heartwater and dermatophilosis. Also of great concern have been the huge economic loses that would be anticipated if the tick and its animal diseases were introduced into South, Central, and North America (28,29). The programs have met with mixed success, and although some islands have been certified provisionally free of the tick, others remain infested or have reinfestations or recrudescences of A. variegatum. No attempts appear to have been made to control the populations of cattle egrets, which are hosts of A. variegatum and can migrate long distances, even as far as the Florida Keys (30).
Conclusions
Until A. variegatum is eradicated from the West Indies, local health workers and those treating persons who have traveled to the area should suspect ATBF in patients who seek treatment with a history of tick bites and clinical signs of fever, headache, and multiple eschars. Further, vigilance is required to prevent transportation of A. variegatum or rickettsemic animals to the mainlands of North, South, and Central America because this importation might enable R. africae and ATBF to become established in these areas. The potential impact of R. africae on the health of indigenous people and tourists in the West Indies and its potential introduction into the Americas further justifies the eradication of A. variegatum from the region.
Dr Kelly teaches topics in small animal medicine at Ross University School of Veterinary Medicine. His research interests include tickborne diseases of persons and animals.
References
Jensenius M, Fournier PE, Kelly P, Myrvang B, Raoult D. African tick bite fever. Lancet Infect Dis. 2003;3:557–64.
Jensenius M, Fournier PE, Vene S, Ringertz SH, Myrvang B, Raoult D. Comparison of immunofluorescence, Western blotting, and cross-adsorption assays for diagnosis of African tick bite fever. Clin Diagn Lab Immunol. 2004;11:786–8.
Dupont HT, Brouqui P, Faugere B, Raoult D. The prevalence of antibodies to Coxiella burnetii, Rickettsia conorii, and Rickettsia typhi in seven African countries. Clin Infect Dis. 1995;21:1126–33.
Barre N, Camus E, Fifi J, Fourgeaud P, Numa G, Rose-Rosette F, et al. Tropical bont tick eradication campaign in the French Antilles. Current status. Ann N Y Acad Sci. 1996;791:64–76.
Barre N, Garris G, Camus E. Propagation of the tick Amblyomma variegatum in the Caribbean. Rev Sci Tech. 1995;14:841–55.
Beati L, Kelly PJ, Matthewman LA, Mason PR, Raoult D. The prevalence of rickettsia-like organisms and spotted fever group rickettsiae in ticks (Acari: Ixodidae) from Zimbabwe. J Med Entomol. 1995;32:787–92.
Kelly PJ, Mason PR. Transmission of a spotted fever group rickettsia by Amblyomma hebraeum (Acari; Ixodidae). J Med Entomol. 1991;28:598–600.
Kelly PJ, Mason PR, Manning T, Slater S. Role of cattle in the epidemiology of tick-bite fever in Zimbabwe. J Clin Microbiol. 1991;29:256–9.
Kelly PJ, Mason PR, Rohde C, Dziva F, Matthewman LA. Transient infections of goats with a novel spotted fever group rickettsia from Zimbabwe. Res Vet Sci. 1991;51:268–71.
Norval RAI. The ticks of Zimbabwe. VII. The genus Amblyomma. Zimbabwe Vet J. 1993;14:3–18.
Morel PC. Etude sur les tiques du betail en Guadelope et Martinique. II. Agents pathogenes transmis par les tiques. Rev Elev Med Vet Pays Trop. 1967;20:291–9.
Tissot Dupont H, Cornet J-P, Raoult D. Identification of rickettsiae from ticks collected in the Central African Republic using polymerase chain reaction. Am J Trop Med Hyg. 1994;50:373–80.
Macaluso KR, Davis J, Alam U, Korman A, Rutherford JS, Rosenberg R, et al. Spotted fever group rickettsiae in ticks from the Masai Mara region of Kenya. Am J Trop Med Hyg. 2003;68:551–3.
Ndip LM, Fokam EB, Bouyer DH, Ndip RN, Titanji VPK, Walker DH, et al. Detection of Rickettsia africae in patients and ticks along the coastal region of Cameroon. Am J Trop Med Hyg. 2004;71:363–6.
Jelinek T, Loscher T. Clinical features and epidemiology of tick typhus in travelers. J Travel Med. 2001;8:57–9.
Jensenius M, Fournier PE, Vene S, Hoel T, Hasle G, Henriksen AZ, et al. African tick bite fever in travelers to rural sub-Equatorial Africa. Clin Infect Dis. 2003;36:1411–7.
Capponi M, Floch H, Chambon L, Camicas JL, Carteron B, Giroud P. Amblyomma variegatum d’ origine Africaine ou Antillaise et rickettsies du genre Dermacentroxenus. Bull Soc Pathol Exot Filiales. 1969;62:1011–7.
Parola P, Jourdan J, Raoult D. Tick-borne infection caused by Rickettsia africae in the West Indies. N Engl J Med. 1998;338:1391.
Raoult D, Fournier PE, Fenollar F, Jensenius M, Prioe T, de Pina JJ, et al. Rickettsia africae, a tick-borne pathogen in travelers to sub-Saharan Africa. N Engl J Med. 2001;344:1504–10.
Parola P, Vestris G, Martinez D, Brochier B, Roux V, Raoult D. Tick-borne rickettiosis in Guadeloupe, the French West Indies: isolation of Rickettsia africae from Amblyomma variegatum ticks and serosurvey in humans, cattle, and goats. Am J Trop Med Hyg. 1999; 60:888–93.
Robinson JB, Eremeeva ME, Olson PE, Thornton SA, Medina MJ, Sumner JW, et al. Confirmation of the presence of Rickettsia africae in Amblyomma variegatum from Antigua. In: Student competition ten-minute papers, section D. Medical and veterinary entomology. Presented at the 2002 Entomological Society of America Annual Meeting and Exhibition, Fort Lauderdale, Florida, November 2002. [cited 15 Dec 2005]. Available from http://esa.confex.com/esa/2002/techprogram/paper_7215.htm
Kelly PJ, Fournier PE, Parola P, Raoult D. A survey for spotted fever group rickettsiae and ehrlichiae in Amblyomma variegatum from St. Kitts and Nevis. Am J Trop Med Hyg. 2003;69:58–9.
Parola P, Attali J, Raoult D. First detection of Rickettsia africae on Martinique, in the French West Indies. Ann Trop Med Parasitol. 2003;97:535–7.
Camus E, Barre N. Vector situation of tick-borne diseases in the Caribbean Islands. Vet Parasitol. 1995;57:167–76.
Garris GI, Bokma BH, Strickland RK, Combs GP. Evaluation of the eradication program for Amblyomma variegatum (Acari: Ixodidae) on Puerto Rico. Exp Appl Acarol. 1989;6:67–76.
Rose-Rosette F, Barre N, Fourgeaud P. Successes and failures in the tropical bont tick eradication campaigns in the French antilles. Ann N Y Acad Sci. 1998;849:349–54.
Pegram R, Indar L, Eddi C, George J. The Caribbean Amblyomma Program: some ecologic factors affecting its success. Ann N Y Acad Sci. 2004;1026:302–11.
Gersabeck EF. The tropical bont tick in the Western Hemisphere. In: Comprehensive reports on technical items presented to the international committee, Paris. Paris: Organisation Mondiale de la Sante Animale; 1994. p. 121–32.
Burridge MJ, Simmons LA, Peter TF, Mahan SM. Increasing risks of introduction of heartwater onto the American mainland associated with animal movements. Ann N Y Acad Sci. 2002;969:269–74.
Corn JL, Barre N, Thiebot B, Creekmore TE, Garris GI, Nettles VF. Potential role of cattle egrets, Bubulcus ibis (Ciconiformes: Ardeidae), in the dissemination of Amblyomma variegatum (Acari: Ixodidae) in the eastern Caribbean. J Med Entomol. 1993;30:1029–37.(Patrick J. Kelly)
Rickettsia africae is the agent of African tick-bite fever, a mild but common disease of local persons and tourists in Africa. The major vector of this spotted fever group rickettsia is most likely Amblyomma variegatum, the tropical bont tick, which has become widely distributed through the West Indies in the last 30 years. This report reviews all available information on R. africae in the West Indies.
Rickettsia africae is a recently described spotted fever group (SFG) rickettsia that is the agent of African tick-bite fever (ATBF), a mild but common tickborne disease of local persons and tourists, in particular, in sub-Saharan Africa. The clinical and laboratory features of ATBF have recently been reviewed (1), as has the diagnosis of the disease (2). In Africa, the tropical bont tick, Amblyomma variegatum, is commonly infected with R. africae and is likely the major vector of the organism (3). This tick was introduced from Africa (Senegal) into the West Indies (Guadeloupe) in the early 1800s but has only spread widely and become endemic on many islands in the last 30 years (4). This spread was probably due to an increase in the between-island movement of livestock, major hosts of A. variegatum (5), and the introduction and spread of the cattle egret (Bubulcus ibis), a host of the immature stages of A. variegatum (5). Recent studies have demonstrated R. africae infections in A. variegatum, persons, and animals in the West Indies. In this report, the available information on R. africae in the region is reviewed.
Epidemiology of R. africae
Early studies in southern Africa showed the bont tick, A. hebraeum, was commonly infected with R. africae (6). In feeding experiments, R. africae was maintained transtadially and transovarially in A. hebraeum, and the tick transmitted the organism at each feeding stage (7). Cattle and goats are common hosts of A. hebraeum and, when infected with R. africae, show no clinical or laboratory signs of disease. They are, however, intermittently rickettsemic and may then be sources of infection for ticks (8,9). While A. hebraeum is the most common vector of R. africae in southern Africa, epidemiologic evidence indicates that A. variegatum is the predominant vector in the rest of sub-Saharan Africa. This tick readily feeds on people (10,11) and is commonly infected with R. africae (16%–75%) in widely separated areas in Africa (6,12–14).
Although R. africae is widely distributed in Africa, and serosurveys have shown infections are extremely common in humans (up to 100%) (1), reports of ATBF in indigenous people are unexpectedly rare. This finding could be because they are generally infected at a young age, when the disease might be very mild or subclinical, and medical attention is not sought. Also, inoculation eschars are difficult to see in pigmented skin, and definitive diagnosis of ATBF requires sophisticated diagnostic tests not available in developing countries. The disease, however, is quite common in international travelers; up to 11% of visitors to disease-endemic areas have evidence of infection (15,16).
R. africae in the West Indies
The first suspected cases of human spotted fever were reported from Guadeloupe in the 1960s (1). The patients had a history of tick bites and antibodies against SFG rickettsiae. Although rickettsiae were isolated from A. variegatum on the island, they were never definitively identified, and samples have been lost (17).
In 1998, Parola et al. (18) described a French woman who was bitten on the foot by a tick while visiting Guadeloupe. An erythematous nodule subsequently developed at the site as well as fever, elevated liver enzyme levels, and leukopenia. Serologic and adsorption studies suggested that she had been infected with R. africae. She recovered slowly when she was treated with doxycycline for 3 weeks. Subsequently, further human infections were documented on the island (19), and R. africae was detected in 27% of A. variegatum used for isolation experiments or polymerase chain reaction (PCR) analysis with rOmpA primers (20).
In 2002, Robinson et al. (21) used PCR with rOmpA and gltA primers to show that 84% of 75 A. variegatum collected from cattle in Antigua contained DNA of R. africae. In 2003, Kelly et al. (22) found 41% of A. variegatum from Saint Kitts and Nevis were positive for DNA of R. africae in PCRs in which rOmpA primers were used for the SFG rickettsiae. Positive ticks were found at 7 of 8 sites sampled, with prevalences varying from 14% to 71%. In the same year, Parola et al. (23) reported finding DNA of the ompA gene of R. africae in 7 (56%) of 12 A. variegatum tested from Martinique.
Although Rhipicephalus (Boophilus) microplus, the tropical/southern cattle tick, and Rhipicephalus sanguineus, the brown dog tick, are widespread in the Caribbean (24), they have not been implicated as vectors of R. africae. PCR with rOmpA primers of 52 R. sanguineus and 16 R. microplus from Saint Kitts and Nevis did not show DNA of SFG rickettsiae (unpub. data). Similarly, SFG rickettsial DNA was not identified in 6 R. microplus and 11 R. sanguineus from Martinique (23) or in 6 R. microplus from Antigua (21).
The studies described show that A. variegatum is commonly infected with R. africae in the West Indies. In the only published serosurvey conducted in the region (20), high prevalences of antibodies to R. africae were found in Guadeloupean cattle (81%) and goats (87%), which are common hosts of A. variegatum (24). Antibodies to R. africae were also highly prevalent (49%) in local people from Guadeloupe. The prevalence in men was significantly higher than in women, possibly because men were more likely to be exposed while working outdoors. The West Indian population, then, appears to be commonly exposed to A. variegatum that transmits R. africae. As is the case in Africa, however, clinical cases of ATBF in local persons are unexpectedly rare; the only reported cases of ATBF contracted in the region have been in tourists (18,19).
Recently, programs have been introduced to eradicate A. variegatum from the Caribbean (25–27). The principal justification for the projects has been the economic loses to island economies caused by animal diseases associated with A. variegatum, mainly heartwater and dermatophilosis. Also of great concern have been the huge economic loses that would be anticipated if the tick and its animal diseases were introduced into South, Central, and North America (28,29). The programs have met with mixed success, and although some islands have been certified provisionally free of the tick, others remain infested or have reinfestations or recrudescences of A. variegatum. No attempts appear to have been made to control the populations of cattle egrets, which are hosts of A. variegatum and can migrate long distances, even as far as the Florida Keys (30).
Conclusions
Until A. variegatum is eradicated from the West Indies, local health workers and those treating persons who have traveled to the area should suspect ATBF in patients who seek treatment with a history of tick bites and clinical signs of fever, headache, and multiple eschars. Further, vigilance is required to prevent transportation of A. variegatum or rickettsemic animals to the mainlands of North, South, and Central America because this importation might enable R. africae and ATBF to become established in these areas. The potential impact of R. africae on the health of indigenous people and tourists in the West Indies and its potential introduction into the Americas further justifies the eradication of A. variegatum from the region.
Dr Kelly teaches topics in small animal medicine at Ross University School of Veterinary Medicine. His research interests include tickborne diseases of persons and animals.
References
Jensenius M, Fournier PE, Kelly P, Myrvang B, Raoult D. African tick bite fever. Lancet Infect Dis. 2003;3:557–64.
Jensenius M, Fournier PE, Vene S, Ringertz SH, Myrvang B, Raoult D. Comparison of immunofluorescence, Western blotting, and cross-adsorption assays for diagnosis of African tick bite fever. Clin Diagn Lab Immunol. 2004;11:786–8.
Dupont HT, Brouqui P, Faugere B, Raoult D. The prevalence of antibodies to Coxiella burnetii, Rickettsia conorii, and Rickettsia typhi in seven African countries. Clin Infect Dis. 1995;21:1126–33.
Barre N, Camus E, Fifi J, Fourgeaud P, Numa G, Rose-Rosette F, et al. Tropical bont tick eradication campaign in the French Antilles. Current status. Ann N Y Acad Sci. 1996;791:64–76.
Barre N, Garris G, Camus E. Propagation of the tick Amblyomma variegatum in the Caribbean. Rev Sci Tech. 1995;14:841–55.
Beati L, Kelly PJ, Matthewman LA, Mason PR, Raoult D. The prevalence of rickettsia-like organisms and spotted fever group rickettsiae in ticks (Acari: Ixodidae) from Zimbabwe. J Med Entomol. 1995;32:787–92.
Kelly PJ, Mason PR. Transmission of a spotted fever group rickettsia by Amblyomma hebraeum (Acari; Ixodidae). J Med Entomol. 1991;28:598–600.
Kelly PJ, Mason PR, Manning T, Slater S. Role of cattle in the epidemiology of tick-bite fever in Zimbabwe. J Clin Microbiol. 1991;29:256–9.
Kelly PJ, Mason PR, Rohde C, Dziva F, Matthewman LA. Transient infections of goats with a novel spotted fever group rickettsia from Zimbabwe. Res Vet Sci. 1991;51:268–71.
Norval RAI. The ticks of Zimbabwe. VII. The genus Amblyomma. Zimbabwe Vet J. 1993;14:3–18.
Morel PC. Etude sur les tiques du betail en Guadelope et Martinique. II. Agents pathogenes transmis par les tiques. Rev Elev Med Vet Pays Trop. 1967;20:291–9.
Tissot Dupont H, Cornet J-P, Raoult D. Identification of rickettsiae from ticks collected in the Central African Republic using polymerase chain reaction. Am J Trop Med Hyg. 1994;50:373–80.
Macaluso KR, Davis J, Alam U, Korman A, Rutherford JS, Rosenberg R, et al. Spotted fever group rickettsiae in ticks from the Masai Mara region of Kenya. Am J Trop Med Hyg. 2003;68:551–3.
Ndip LM, Fokam EB, Bouyer DH, Ndip RN, Titanji VPK, Walker DH, et al. Detection of Rickettsia africae in patients and ticks along the coastal region of Cameroon. Am J Trop Med Hyg. 2004;71:363–6.
Jelinek T, Loscher T. Clinical features and epidemiology of tick typhus in travelers. J Travel Med. 2001;8:57–9.
Jensenius M, Fournier PE, Vene S, Hoel T, Hasle G, Henriksen AZ, et al. African tick bite fever in travelers to rural sub-Equatorial Africa. Clin Infect Dis. 2003;36:1411–7.
Capponi M, Floch H, Chambon L, Camicas JL, Carteron B, Giroud P. Amblyomma variegatum d’ origine Africaine ou Antillaise et rickettsies du genre Dermacentroxenus. Bull Soc Pathol Exot Filiales. 1969;62:1011–7.
Parola P, Jourdan J, Raoult D. Tick-borne infection caused by Rickettsia africae in the West Indies. N Engl J Med. 1998;338:1391.
Raoult D, Fournier PE, Fenollar F, Jensenius M, Prioe T, de Pina JJ, et al. Rickettsia africae, a tick-borne pathogen in travelers to sub-Saharan Africa. N Engl J Med. 2001;344:1504–10.
Parola P, Vestris G, Martinez D, Brochier B, Roux V, Raoult D. Tick-borne rickettiosis in Guadeloupe, the French West Indies: isolation of Rickettsia africae from Amblyomma variegatum ticks and serosurvey in humans, cattle, and goats. Am J Trop Med Hyg. 1999; 60:888–93.
Robinson JB, Eremeeva ME, Olson PE, Thornton SA, Medina MJ, Sumner JW, et al. Confirmation of the presence of Rickettsia africae in Amblyomma variegatum from Antigua. In: Student competition ten-minute papers, section D. Medical and veterinary entomology. Presented at the 2002 Entomological Society of America Annual Meeting and Exhibition, Fort Lauderdale, Florida, November 2002. [cited 15 Dec 2005]. Available from http://esa.confex.com/esa/2002/techprogram/paper_7215.htm
Kelly PJ, Fournier PE, Parola P, Raoult D. A survey for spotted fever group rickettsiae and ehrlichiae in Amblyomma variegatum from St. Kitts and Nevis. Am J Trop Med Hyg. 2003;69:58–9.
Parola P, Attali J, Raoult D. First detection of Rickettsia africae on Martinique, in the French West Indies. Ann Trop Med Parasitol. 2003;97:535–7.
Camus E, Barre N. Vector situation of tick-borne diseases in the Caribbean Islands. Vet Parasitol. 1995;57:167–76.
Garris GI, Bokma BH, Strickland RK, Combs GP. Evaluation of the eradication program for Amblyomma variegatum (Acari: Ixodidae) on Puerto Rico. Exp Appl Acarol. 1989;6:67–76.
Rose-Rosette F, Barre N, Fourgeaud P. Successes and failures in the tropical bont tick eradication campaigns in the French antilles. Ann N Y Acad Sci. 1998;849:349–54.
Pegram R, Indar L, Eddi C, George J. The Caribbean Amblyomma Program: some ecologic factors affecting its success. Ann N Y Acad Sci. 2004;1026:302–11.
Gersabeck EF. The tropical bont tick in the Western Hemisphere. In: Comprehensive reports on technical items presented to the international committee, Paris. Paris: Organisation Mondiale de la Sante Animale; 1994. p. 121–32.
Burridge MJ, Simmons LA, Peter TF, Mahan SM. Increasing risks of introduction of heartwater onto the American mainland associated with animal movements. Ann N Y Acad Sci. 2002;969:269–74.
Corn JL, Barre N, Thiebot B, Creekmore TE, Garris GI, Nettles VF. Potential role of cattle egrets, Bubulcus ibis (Ciconiformes: Ardeidae), in the dissemination of Amblyomma variegatum (Acari: Ixodidae) in the eastern Caribbean. J Med Entomol. 1993;30:1029–37.(Patrick J. Kelly)