Date Published: July 21, 2017
Publisher: Public Library of Science
Author(s): Aline do Nascimento Benitez, Felippe Danyel Cardoso Martins, Marcelle Mareze, Nelson Jessé Rodrigues Santos, Fernanda Pinto Ferreira, Camila Marinelli Martins, João Luis Garcia, Regina Mitsuka-Breganó, Roberta Lemos Freire, Alexander Welker Biondo, Italmar Teodorico Navarro, W.F. de Boer.
Toxoplasmosis, caused by Toxoplasma gondii, has traditionally been considered an important water and foodborne protozoonosis with important public health considerations. Although felids play a well-established role as definitive hosts, canine epidemiological involvement in the parasite’s life cycle remains questionable and controversial. The increasing closeness of the human-dog bond, particularly seen in urban settings, has been recognized as a historically unprecedented worldwide movement. Sharing daily lives in the same households, dogs may be exposed to similar associated risks of T. gondii infection as their owners. Thus, epidemiological assessment of the intra-domiciled environment, especially among socio-economically different human populations, may provide novel information regarding the actual role of dogs in animal and human toxoplasmosis. Despite spatial approaches being recently used for other water and foodborne diseases, no study has been conducted on the simultaneous spatial seroprevalence of both human and animal IgG anti-T. gondii antibodies in urban areas of major cities. Accordingly, the aim of the present study was to assess the seroprevalence and associated variables of Toxoplasma infection in owners and their domiciled dogs in Londrina, southern Brazil. Human and canine seroprevalence rates and variables associated with seroprevalence were investigated through representative random sampling among 564 households, which included 597 owners and 729 dogs. Overall, statistically significant differences between the seroprevalence of human and dog anti-T. gondii antibodies were found by Immunofluorescence Antibody Testing in 248/597 (41.54%) owners and 119/729 (16.32%) dogs. Through multiple analysis, significant concomitant variables for seropositivity of household individuals (people and dogs) were determined, including public sewer service, yard cleaning frequency, and having a dirty yard. Although no statistically significant multiple logistic model was observed among owners, univariate analysis detected associations with monthly income, soil contact, and occupation. Among dogs, the absence of other dogs and the absence of a dirty yard were concomitant significantly protective associated factors. Age differences between seropositive and seronegative individuals was significant only for human beings, with the median age of negative individuals significantly higher than positive individuals. Although no spatial clusters were identified for humans or residences, a significant cluster was identified for dogs. In conclusion, characteristics of urban toxoplasmosis may include significantly higher owner seroprevalence than their owned dogs, with canine seroprevalence directly associated with having more dogs and a dirty backyard, and spatial differences in both human and dog exposures. Although not a good indicator for human foodborne diseases, dogs may be a reliable sentinel for environmental infection. Moreover, such a holistic approach may provide crucial information for more focused prevention and monitoring programs, particularly in households with multiple pets and trash-filled backyards.
T. gondii has been described as an obligate intracellular parasite capable of infecting warm-blooded animals. The only known definitive hosts are the Felidae family, which may eliminate environmentally resistant oocysts, and a wide range of intermediate hosts including human beings [1,2]. Environmental settings may play an important role in Toxoplasma transmission and persistence, since oocysts shed within feces still require favorable conditions to become infectious .
This study has been approved by the National Human Ethics Research Committee (protocol number 1,025,861/2014) and the Animal Use Ethics Committee (protocol n° 181/2014), both through the State University of Londrina, southern Brazil. In addition, the present study has also been approved by the Londrina City Secretary of Health and officially included as part of the annual activities.
The total number of visits exceeded the minimum sampling calculation of 289/461 (62.67%; 95% CI: 58.19–66.98) households, mainly due to random volunteer requests from neighbors during regular visits. However, failure to obtain biological samples or incomplete questionnaires in 186/289 (64.35%) households led to a final sampling of 564 households.
The present study has been, to the authors’ knowledge, the first simultaneous study of T. gondii seroprevalence in owners and their domiciled dogs. Households where owners and dogs lived were assessed for the potential risk of seropositivity to each other. Although previous studies have shown that infection in companion animals may be accompanied by T. gondii dissemination in shared habitats with human beings [32,49], a low frequency of households (17.62%) showed simultaneous seropositivity in owners and dogs when compared to solely seropositive owners (82.37%) or dogs (26.22%), suggesting that the intra-domicile environment may have no impact, or at least not a similar impact, between owners and their dogs for T. gondii infection.
In conclusion, characteristics of urban toxoplasmosis may include significantly higher owner seroprevalence than their own dogs, with spatial differences for both human and dog exposures. In addition, no descriptive or spatial evidence was found in this study regarding a potential dog role as sentinels for human toxoplasmosis in urban areas of major cities. Although not a good indicator for human foodborne diseases inside the household, such as toxoplasmosis, dogs may still be a useful sentinel for environmental infection and outbreaks.