Seroprevalence of Babesia caballi and Theileria equi in five draught equine populated metropolises of Punjab, Pakistan
Introduction
Piroplasms (Apicomplexa: Piroplasmida) are tick-transmitted protozoa found in many wild and domestic animals. Equine piroplasmosis (EP), caused by intraerythrocytic parasites Babesia caballi (Nuttall and Strickland, 1910) and/or Theileria equi (Mehlhorn and Schein, 1998), is an important disease of solipeds (horses, donkeys, mules and zebras) worldwide (Kuttler, 1988). EP is mainly transmitted by ticks belonging to three genera, including Dermacentor, Rhipicephalus and Hyaloma (Thompson, 1969, Jongejan and Uilenberg, 2004); however, sometimes iatrogenic transmission of the disease can also occur through contaminated blood transfusion, injections and surgical instruments (de Waal and van Heerden, 2004, Uilenberg, 2006, Vial and Gorenflot, 2006). The disease is endemic in Asia and many parts of Europe, south and central Americas and Africa (OIE, 2008). As per the data from World Animal Health Information Database (WAHID) Interface, 2013, 30 countries reported the occurrence of EP in the year 2012.
Clinically, EP is usually characterized by fever, anorexia, depression, icterus, hemoglobinuria, bilirubinuria and regenerative hemolytic anemia and, in some cases, death can also occur (Seifi et al., 2000, Camacho et al., 2005). However, clinical signs are not always overt, particularly in endemic areas because it is often difficult to recognise the infection as many factors (such as infecting dose, genetics of the infecting parasites and immune status of the host) contribute to the severity of the disease. T. equi infected animals usually exhibit a severe and acute form of EP; whereas, B. caballi infection usually follows a chronic course (Shkap et al., 1998, Vial and Gorenflot, 2006, Radostits et al., 2007). In addition, horses and donkeys may act as carriers of the parasite for several years (as in T. equi infection) or for the rest of their lives, so acting as reservoirs for ticks (Knowles, 1996, Rüegg et al., 2007, Kumar et al., 2009).
Equines born and raised in the endemic areas enter into the carrier state of EP which can compromise their draught potential significantly (Abdelkebir et al., 2001) and these carriers are responsible for the maintenance of infection in endemic areas (Camacho et al., 2005). Heavy draught stress, strenuous exercise and poor nutrition can result into the recrudescent infection and clinical disease in these animals (Hailat et al., 1997, Seifi et al., 2000, Camacho et al., 2005). Severity of the clinical signs can vary depending on the host species involved. For instance, horses are more susceptible to B. caballi infections as compared to mules and donkeys (Acici et al., 2008) and susceptibility to the disease is directly proportional to the age of the animal (Abdelkebir et al., 2001).
Traditionally, piroplasms are detected and identified by microscopic examination of thin blood smears prepared from acutely infected animals. A number of serological assays, including the complement fixation test (CFT), the indirect fluorescent antibody test (IFAT) and the enzyme linked immunosorbent assays (ELISAs) have been developed mostly for large scale epidemiological studies and to monitor infections during the latent stage of EP (Brüning et al., 1997, Shkap et al., 1998, Ikadai et al., 2000, de Waal and van Heerden, 2004). Later, direct detection methods using molecular tools (such as polymerase chain reaction) have been developed and are considered reliable diagnostic tools (Cacciò et al., 2000, Nagore et al., 2004). The competitive ELISA (cELISAs) employing monoclonal antibodies to recombinant antigens of T. equi (merozoites antigen 1; EMA-1) and B. caballi (rophtry associated protein; RAP-1) have been reported to be successful in detection of antibodies in sera of horses from different parts of the world (Knowles et al., 1992, Kappmeyer et al., 1999, Sevinc et al., 2008) and are currently tests of choice recommended by the World Organization for Animal Health (OIE, 2008).
In Pakistan, very limited information is available on the status of EP in different species of draught equines (Kokab, 1986, Khan et al., 1987, Rashid et al., 2009) and these studies were based on conventional blood smear examination of T. equi and B. caballi, which does not always reveal the true picture of infections. The total equine population of Pakistan is ∼5.2 million (donkeys 4.6 million; horses 0.4; mules 0.2). From 1996 to 2006, the equine population increased in the country e.g., mules by 18%, donkeys by 20% and horses by 3% (Anonymous, 2006). Due to high fuel prices, marginalized communities use these animals as a cheap and economical means of transport that plays a key role in the provision of livelihood for their owners. Any disease (such as EP) or disability rendering these animals sick and unavailable for work can have serious effects on owners and their families.
Despite the importance of draught equines in Pakistan, we know very little about EP and its impact on these animals. Therefore, a cELISA-based cross-sectional serological survey was conducted to evaluate the level of exposure of draught equids (donkeys, horses and mules) to EP in five metropolises of Punjab Province of Pakistan.
Section snippets
Study areas and meteorological characteristics
A cross-sectional sero-epidemiological survey was conducted from July 2007 to March 2008 in five draught equine populated metropolises (Bahawalpur, Faisalabad, Gujranwala, Lahore and Multan) of Punjab, Pakistan. Geographic location and climatic characteristics of each metropolis included in the study are given in Table 1. Five districts included in the present study were selected based on the district equine population published in the Livestock Census of Pakistan (Anonymous, 2006). Wherever
Seroprevalence of EP
A total of 430 equids including 332 donkeys, 65 horses and 33 mules aging from ≤5 to ≥10 years of either sex, from five metropolises of Punjab, Pakistan were tested for antibodies against EP (Table 2) and 226 (52.6%) were detected positive for EP (T. equi and/or B. caballi infections). The seroprevalence of T. equi infection was 41.2% and that for B. caballi was 21.6%. A small proportion of equids (10.2%) was seropositive for both T. equi and B. caballi (mixed infection). Fig. 1 provides the
Discussion
Piroplasmosis caused by T. equi and/or B. caballi is an important disease of equines and can lead to serious health and economic impacts. Over the years, the diagnosis of EP remained a challenge for the researchers and veterinarians as the peripheral blood stained (Giemsa or Leishman) smears are rarely conclusive and most of the serological tests have problems, including reporting of false positive/negative results (Donnelly et al., 1980, Ribeiro et al., 1999, Abdelkebir et al., 2001, Akkan et
Conclusions
This study first time presents the seroprevalence of EP in draught equines from Pakistan and indicates that EP is endemic in equines of the studied metropolises of Pakistan. In order to understand the epidemiology of disease and devise control measures, future studies by employing conventional and molecular techniques are required to identify the competent tick vectors along with seasonal distribution and other factors responsible for the spread and maintenance of EP in the region.
Conflict of interest
None of the authors of this paper has a financial or personal relationship with other people or organizations that could inappropriately influence or bias the content of the paper.
Acknowledgement
The authors are extremely thankful to the Brooke Hospital for Animals, Pakistan for facilitating the field sampling in the communities of Faisalabad, Gujranwala, Lahore and Multan metropolises.
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