To examine prevalence changes and risk factors for canine leishmaniasis, we conducted a cross-sectional seroprevalence study and a survey during April–June 2006. Seroprevalence had increased at the meso-Mediterranean bioclimatic level over 22 years. Risk was highest for dogs that were older, large, lived outside, and lived at the meso-Mediterranean level

Alcalde Alonso

Carmen Acedo-Sánchez

Francisco Morillas-Márquez

Joaquina Martín-Sánchez

Killick-Kendrick

Kovats

Manuel Morales-Yuste

Martín-Sánchez

Moreira

Morillas

Morillas-Márquez

Reyes Magaña

Sergio Barón

Sutherst

Sánchez

Victoriano Díaz

Emerging Infectious Diseases

English

PubMed

To examine prevalence changes and risk factors for canine leishmaniasis, we conducted a cross-sectional seroprevalence study and a survey during April–June 2006. Seroprevalence had increased at the meso-Mediterranean bioclimatic level over 22 years. Risk was highest for dogs that were older, large, lived outside, and lived at the meso-Mediterranean level.The Ministerio de Educación y Ciencia, Madrid (AGL2004-06909-C02-02), and the Junta de Andalucía (group CVI176) provided financial assistance, and Emerging Diseases in a changing European eNvironment (EDEN; contract no. 010284, Integrated Project GOCE) awarded a PhD student grant to S.B. This publication is catalogued by the EDEN Steering Committee as EDEN0137 (www.eden-fp6project.net)

Martín Sánchez, Joaquina

Morales Yuste, Manuel

Acedo-Sánchez, Carmen

Barón, Sergio

Morillas Márquez, Francisco

Díaz Sáez, Victoriano

Repositorio Institucional Universidad de Granada

Canine Leishmaniasis in Southeastern SpainJoaquina Martín-Sánchez, Manuel Morales-Yuste, Carmen Acedo-Sánchez, Sergio Barón, Victoriano Díaz, and Francisco Morillas-MárquezTo examine prevalence changes and risk factors for canine leishmaniasis, we conducted a cross-sectional se-roprevalence study and a survey during April–June 2006. Seroprevalence had increased at the meso-Mediterranean bioclimatic level over 22 years. Risk was highest for dogs that were older, large, lived outside, and lived at the meso-Mediterranean level.It has been suggested that climate change has the poten-tial to change the transmission intensity of vector-borne diseases such as leishmaniasis, but supporting literature is lacking (1,2). Because long-term quality data on leishma-niasis caused by Leishmania infantum and its vector (3–9) are available for the Alpujarras region of southeastern Spain (Figure 1), this is an ideal area for studying changes in the prevalence of canine leishmaniasis in a changing environment. Our study objectives were to determine whether any changes had occurred in the prevalence of canine leishmaniasis over 22 years and to identify risk factors for this disease.The StudyTo achieve the fi rst objective, we conducted a cross-sectional study in the Alpujarras from April through June 2006. We then compared current leishmaniasis seropreva-lence data with data from 2 cross-sectional surveys con-ducted in 1984 and 1991 (3–5). The villages sampled for all 3 studies were similar and had been selected at random from within each of the 3 bioclimatic levels (thermo-, meso-, and supra-Mediterranean) that comprise the inhabited zone of the Alpujarras (Figure 1) (10). For each level, respectively, altitudes are 0–700, 600–900, and 900–1,800 m above sea level; annual mean temperatures are 17–19, 13–17, and 8–15°C; and annual rainfalls are 200–350, 600–1,000, and 1,000–1,600 inches. The dates for sample collection were set to coincide with organized events at which dogs were gathered (e.g., antirabies vaccination campaigns). All 3 surveys used indirect immunofl uorescence for diagnosis; protocols and positivity threshold were identical. Dogs with a titer >160 were considered positive. To determine and compare the existence or lack of statistically signifi cant differences between present and past prevalence rates, we used the χ2 or Fisher exact test.To achieve the second objective, we conducted a sur-vey. The owners of the dogs included in the cross-sectional study conducted in the Alpujarras from April to June 2006 were asked to complete an epidemiologic record for each dog tested; data on the animal and its environment were recorded for subsequent use in univariate and multivari-ate logistic regression analyses (Tables 1, 2). Density data were included for 2 vectors, Phlebotomus perniciosus and P. ariasi sandfl ies, captured with sticky traps in June 2006 in the same villages in which the surveys were conducted.  Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 15, No. 5, May 2009 795 Author affi liations: Universidad de Granada, Granada, Spain (J. Martín-Sánchez, M. Morales-Yuste, S. Barón, V. Díaz, F. Morillas-Márquez); and Laboratorio de Análisis Veterinarios ANLAVE, Gran-ada (C. Acedo-Sánchez)DOI: 10.3201/eid1505.080969Figure 1. A) Location of the Alpujarras in southeastern Spain (37º00’–37º20’N and 3º00’–3º30’W). B) Bioclimatic levels (shading) and villages (black dots) where serum samples were collected from dogs to examine for leishmaniasis prevalence and sandfl ies were collected to estimate densities, April–June 2006. Of 1,675 sandfl ies captured, 269 were identifi ed by morphologic appearance as Phlebotomus perniciosus (density 0–165 specimens/m2) and 22 as P. ariasi (0 and 11 specimens/m2).No retrospective entomologic analysis was performed as had been done for canine leishmaniasis.In our 2006 survey, 57 (13.0%) of 439 dogs had an an-tibody titer >160 (seroprevalence rate), 268 (61.0%) dogs had titers 20–80, and 114 (26.0%) had no titer. In terms of bioclimatic level, canine leishmaniasis seroprevalence was 20.1% at the meso-Mediterranean, 13.3% at the thermo-Mediterranean, and only 1.1% at the supra-Mediterranean levels. Statistically signifi cant differences (χ2 test p<0.001) indicate that these differences are not random. The evolu-tion-in-time analysis (Figure 2) shows how over 22 years (1984–2006), seroprevalence of canine leishmaniasis has DISPATCHES796 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 15, No. 5, May 2009Table 1. Possible factors associated with canine leishmaniasis, southeastern Spain* Variables No. dogs% Dogs with canine leishmaniasis Relative likelihood p value Bioclimatic level 439 13.0 – 0.005 Thermo-Mediterranean 210 13.3 Ref – Meso-Mediterranean 139 20.1 1.640 0.092 Supra-Mediterranean 90 1.1 0.073 0.011Habitat 438 13.0 – 0.999 Rural 435 13.1 Ref – Urban/peri-urban 3 0.0 <0.001 –Sex 435 12.4 – 0.178 Male 253 14.2 Ref Female 182 9.9 0.662Age, y 421 13.0 – <0.001<4 232 9.5 Ref >4 189 18.0 2.094Weight, kg 405 13.6 – 0.048<25 316 11.9 Ref >25 89 20.0 1.859Fur length 349 15.5 – 0.069 Short/ medium 255 17.6 Ref Long 94 9.6 0.494Activity 439 13.0 – <0.001 Pet 258 8.5 Ref – Hunting  133 15.0 1.899 0.052 Other† 48 31.3 4.876 <0.001Location during daytime 373 15.3 – <0.001 House 151 4.0 Ref – Outside 122 28.7 9.722 <0.001 In kennels 100 16.0 4.603 0.002Location at night 435 13.1 – 0.001 Outdoors 186 19.4 Ref Indoors 249 8.4 0.384Travel away from home 438 13.0 – 0.461 No 396 12.6 Ref Yes 42 16.7 1.384Clinical signs of leishmaniasis 439 13.0 – 0.122 No 413 12.3 Ref Yes 26 23.1 2.129Fly protection 375 15.2 – 0.969 No 361 15.0 Ref Yes 14 21.4 1.551Phlebotomus perniciosus density 439 13.0 – 0.005 <4 sandflies/m2 303 9.9 Ref4 sandflies/m2 136 19.9 2.254P. ariasi density 439 13.0 – <0.001 <6 sandflies/m2 383 10.7 Ref6 sandflies/m2 56 28.6 3.337*Univariate analysis by logistic regression. Dogs considered to have canine leishmaniasis were those with antibody titer >160. We investigated the existence of interaction and/or confusion between variables by constructing and comparing logistic regression models. The statistical analysis was performed using the software package SPSS 15.0 (www.spss.com). Confusion was noted between the location during daytime and location at night, so location during daytime was excluded from the multivariate analysis. No interaction was detected between any pair of independent variables. Ref, referent.†Guard dogs (n = 34), sheepdogs (n = 8), stray dogs (n = 4), dogs in kennel (n = 2). Canine Leishmaniasis in Southeastern Spainprogressively increased at the meso-Mediterranean level, climbing from 9.2% in 1984 to 15.4% in 1991 and fi nally to 20.1% in 2006 (p = 0.015); in contrast, no signifi cant changes have taken place in global prevalence or in the other 2 bioclimatic levels studied (3–5; this study).Dogs at greatest risk for canine leishmaniasis in the disease-endemic region of the Alpujarras were large dogs (>25 kg) and older dogs (>4 years) that worked as guard dogs or sheepdogs, slept outdoors, and lived at the ther-mo- or meso-Mediterranean level in a village such as Tor-vizcón, where the P. perniciosus density is >4 sandfl ies/m2. Risk for these dogs was 54,571× greater than for dogs that were kept as pets, were small, were <4 years of age, and slept inside a house in a village such as Mecina Bombarón or Pórtugos at the supra-Mediterranean level where P. per-niciosus density is <4 sandfl ies/m2.ConclusionsAmong the drivers of global change that have the po-tential to infl uence vector-borne diseases, climatic and non-climatic (socioeconomic, demographic, and environmental) factors have been cited (1,2). Although it is not easy to attri-bute our fi ndings—progressive increase in seroprevalence at the meso-Mediterranean level and drop and subsequent rise at the thermo-Mediterranean level (Figure 2)—to 1 or more drivers, we can attempt to fi nd some form of asso-ciation in the changes that have occurred in the Alpujarras throughout these 2 decades. Studies on climate change in Spain confi rm a warming tendency (refl ected at the global level), which provides evidence that temperatures have been increasing for a quarter of a century (11,12). Thus, we must assume that changes in temperature, rainfall, or humidity will have equally affected the 3 bioclimatic levels researched in the Alpujarras and may have infl uenced the spatial and temporal distribution and the seasonal dynam-ics of sandfl ies. An increase was detected in the period of P. perniciosus activity in the region; these effects were probably more notable at the meso-Mediterranean level be-cause this is where the density of this vector species is at its highest (6; Martín-Sánchez et al., unpub. data). During the time period researched, the human population remained  Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 15, No. 5, May 2009 797 Table 2. Factors associated with canine leishmaniasis, southeastern Spain, final model*Variables (no. dogs) OR (95% CI) p value Bioclimatic level – 0.001 Thermo-Mediterranean (189) – – Meso-Mediterranean (134) 0.538 (0.196–1.476) 0.228 Supra-Mediterranean (82) 0.013 (0.001–0.126) <0.001Age, y – 0.001<4 (224) – >4 (181) 3.223 (1.604–6.474) Weight, kg – 0.069<25 (316) – >25 (89) 1.985 (0.948–4.156) Activity – 0.00 Pet (232) – – Hunting (129) 2.401 (1.060–5.442) 0.036 Other (44)† 4.831 (1.909–12.226) 0.001Location at night – <0.001 Indoors (229) – Outdoors (176) 3.304 (1.704–6.406) Phlebotomus perniciosus density – <0.001 <4 sandflies/m2 (277) –>4 sandflies/m2 (128) 7.029 (2.632–18.769) *Determined by multivariate logistic regression. With age as continuous variable (0.1–25 years, average 4.7 years), odds ratio (OR) = 1.142; with weight as continuous variable (2–60 kg, average = 17.7), OR = 1.047. CI, confidence interval. †Guard dogs, sheepdogs, stray dogs, and dogs in kennels.     0   5   10   15   20   251984 1991 2006Seroprevalence, %Thermo-MediterraneanMeso-MediterraneanSupra-MediterraneanOverallFigure 2. Canine leishmaniasis seroprevalence rates in the Alpujarras, Spain, 1984–2006, by time and bioclimatic level.constant in the Alpujarras; it has, however, progressively decreased in the disperse populations and increased in population centers. Unfortunately, no offi cial fi gures for the canine population are available, although we were in-formed by staff of local town halls that in 1991, the 615 dogs analyzed accounted for ≈100% of the total number of dogs registered in the villages sampled (3). The Alpujarras economy is based mainly on agriculture and livestock. One change during the period studied was the gradual disap-pearance of livestock enclosures in rural population cen-ters. These enclosures appear to create a substantial risk for infection with Leishmania spp. (13,14) and are ideal places for sandfl y blood sucking, mating, and oviposition (15).With respect to risk factors, the increase in canine leishmaniasis seroprevalence as  animal’s age increases seems logical because in a leishmaniasis-endemic area, the greater the age, the longer the animal will have been exposed to sandfl ies and the greater the probability of hav-ing been bitten by an infected female sandfl y. Seropreva-lence of canine leishmaniasis also increases gradually with weight, which could be attributed to the vector being more attracted to larger animals. Dogs that sleep outdoors are at greater risk than those sleeping indoors because the density of the vector (P. perniciosus) is greater outdoors than in-side a house. The association between P. perniciosus densi-ty and canine leishmaniasis seems logical, considering that P. perniciosus is the main vector species in the Alpujarras. This is the only species found to have been infected in this region (8,9), although P. ariasi is a proven vector in the nearby region of the Axarquia (13).In the Alpujarras, the percentage of dogs kept as pets has increased from 42% in 1991 (3) to 59% in 2006 (p<0.001). This increase corresponds to a general increase in standard of living and, along with other factors such as the disappearance of livestock enclosures from within population centers, would have acted to reduce transmis-sion. Only the extension of the vector’s activity period, which was detected at some trap sites, would have acted to increase transmission. Such extension of activity may be related to the increase in temperature brought about by climate change (11,12).The Ministerio de Educación y Ciencia, Madrid (AGL2004-06909-C02-02), and the Junta de Andalucía (group CVI176) provided fi nancial assistance, and Emerging Diseases in a chang-ing European eNvironment (EDEN; contract no. 010284, Inte-grated Project GOCE) awarded a PhD student grant to S.B. This publication is catalogued by the EDEN Steering Committee as EDEN0137 (www.eden-fp6project.net). Dr Martín-Sánchez is a professor in the Parasitology Depart-ment of the University of Granada. Her main area of research is the epidemiology of leishmaniasis.References  1.   Kovats RS, Campbell-Lendrum DH, McMichael AJ, Woodward A, Cox JS. Early effects of climate change: do they include chang-es in vector-borne disease? Philos Trans R Soc Lond B Biol Sci. 2001;356:1057–68.  2.  Sutherst RW. Global change and human vulnerability to vector-borne diseases. Clin Microbiol Rev. 2004;17:136–73. DOI: 10.1128/CMR.17.1.136-173.2004  3.  Sánchez C, Martín Sánchez J, Vélez Bernal ID, Sanchís Marín MC, Louassini M, Maldonado JA, et al. Leishmaniasis eco-epidemiology in the Alpujarra region (Granada province, southern Spain). Int J Parasitol. 1996;26:303–10. DOI: 10.1016/0020-7519(95)00124-7  4.  Reyes Magaña A, Morillas-Márquez F, Valero-López A, González Castro J, Benavides-Delgado I, Sanchís Marín MC. Encuesta sobre la leishmaniosis canina en las comarcas naturales de la provincia de Granada (Sur de España). Rev Iber Parasitol. 1988;48:233–40.  5.  Reyes Magaña A, Morillas Márquez F, Monts Ramirez E, Sanchís Marín MC, Benavides Delgado I, González CJ. La leishmaniosis en la provincia de Granada: estudio de la enzootia canina. Ars Pharma-céutica. 1989;30:35–44.  6.  Morillas-Márquez F, Guevara-Benitez DC, Úbeda-Ontiveros JM, González CJ. Annual fl uctuations of Phlebotomus populations (Dip-tera, Phlebotomidae) in the province of Grenada (Spain) [in French]. Ann Parasitol Hum Comp. 1983;58:625–32.  7.  Alcalde Alonso M, Morillas Márquez F, Delgado V, Naranjo R. Epi-demiología de las leishmaniosis cutáneas en la provincia de Grana-da. Actas Dermosifi liogr. 1989;80:251–4.  8.  Martín-Sánchez J, Guilvard E, Acedo-Sánchez C, Volf-Echeverri M, Sanchiz-Marín MC, Morillas-Márquez F. Phlebotomus perniciosus Newstead, 1911, infection by various zymodemes of the Leishmania infantum complex in the Granada province (southern Spain). Int J Parasitol. 1994;24:405–8. DOI: 10.1016/0020-7519(94)90089-2  9.  Martín-Sánchez J, Gállego M, Barón S, Castillejo S, Morillas-Márquez F. Pool screen PCR for estimating the prevalence of Leish-mania infantum infection in sandfl ies (Diptera: Nematocera, Phle-botomidae). Trans R Soc Trop Med Hyg. 2006;100:527–32. DOI: 10.1016/j.trstmh.2005.08.00510.  Rivas Martínez S, Bandullo JM, Serrada R, Allue Andrade JL, Mo-nero del Burgo JL, González Rebollar JL. Memoria del mapa de series de vegetación de España. Madrid: Ministerio de Agricultura, Pesca y Alimentación, ICONA; 1987. p. 31–42. 11.  Abanades García JC, Cuadrat Prats JM, de Castro Muñoz de Lucas M, Fernández García F, Gallastegui Zulaica C, Garrote de Marcos L, et al. El cambio climático en España. Estado de situación. Informe para el Presidente del Gobierno elaborado por expertos en cambio climático; 2007 [cited 2007 Dec 31]. Available from http://www.mma.es/portal/secciones/cambio_climatico12.  Vargas Yáñez M, García Martínez MC, Moya Ruiz F, Tel E, Par-rilla G, Plaza F, et al. Cambio climático en el Mediterráneo español. Madrid: Impresos y Revistas, Instituto Español de Oceanografía, Ministerio de Educación y Ciencia; 2007. p. 32–41.13.  Morillas F, Sánchez Tabasco F, Ocaña J, Martín-Sánchez J, Ocaña-Wihelmi J, Acedo C, et al. Leishmaniasis in the focus of the Axar-quia region, Malaga province, southern Spain: a survey of the hu-man, dog and vector. Parasitol Res. 1996;82:269–70. DOI: 10.1007/s00436005016414.  Moreira ED, de Souza VMM, Sreenivasan M, Lopes NL, Barreto RB, de Carvalho LP. Peridomestic risk factors for canine leishma-niasis in urban dwellings: new fi ndings from a prospective study in Brazil. Am J Trop Med Hyg. 2003;69:393–7.15.  Killick-Kendrick R. Breeding places of Phlebotomus ariasi in the Cevennes focus of leishmaniasis in the south of France. Parassitolo-gia. 1987;29:181–91.Address for correspondence: Joaquina Martín-Sánchez, Parasitology Department, Granada University, Campus Universitario de Cartuja Granada 18.071, Spain: email: joaquina@ugr.esDISPATCHES798 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 15, No. 5, May 2009

Canine leishmaniasis in southeastern Spain

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Canine Leishmaniasis in Southeastern Spain

Martín-Sánchez, Joaquina

Morales-Yuste, Manuel

Morillas-Márquez, Francisco

Institutional Repository of the University of Granada

Crossref

Allue Andrade JL, Monero del Burgo JL, González Rebollar JL. Memoria del mapa de series de vegetación de España. Madrid: Ministerio de Agricultura, Pesca y Alimentación, ICONA;

Annual ﬂ uctuations of Phlebotomus populations (Diptera, Phlebotomidae) in the province of Grenada (Spain) [in French]. Ann Parasitol Hum Comp.

Breeding places of Phlebotomus ariasi in the Cevennes focus of leishmaniasis in the south of France.

Cambio climático en el Mediterráneo español. Madrid: Impresos y Revistas, Instituto Español de Oceanografía, Ministerio de Educación y Ciencia;

Early effects of climate change: do they include changes in vector-borne disease? Philos Trans R Soc Lond B Biol Sci.

El cambio climático en España. Estado de situación. Informe para el Presidente del Gobierno elaborado por expertos en cambio climático;

Epidemiología de las leishmaniosis cutáneas en la provincia de Granada. Actas Dermosiﬁ liogr.

Global change and human vulnerability to vectorborne diseases.

La leishmaniosis en la provincia de Granada: estudio de la enzootia canina. Ars Pharmacéutica.

Leishmaniasis eco-epidemiology in the Alpujarra region (Granada province, southern Spain). Int

Leishmaniasis in the focus of the Axarquia region, Malaga province, southern Spain: a survey of the human, dog and vector. Parasitol Res.

Peridomestic risk factors for canine leishmaniasis in urban dwellings: new ﬁ ndings from a prospective study in Brazil. Am J Trop Med Hyg.

Phlebotomus perniciosus Newstead,

Pool screen PCR for estimating the prevalence of Leishmania infantum infection in sandﬂ ies (Diptera: Nematocera, Phlebotomidae). Trans R Soc Trop Med Hyg.

Sanchís Marín MC. Encuesta sobre la leishmaniosis canina en las comarcas naturales de la provincia de Granada (Sur de España). Rev Iber Parasitol.

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Canine Leishmaniasis in Southeastern Spain

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Institutional Repository of the University of Granada

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