of Medical and Surgical Sciences and Advanced Technologies “G.F.
Ingrassia”, Section of Neurosciences, University of Catania, Catania,
2 Department of Experimental and Clinical Medicine, Infectious and Tropical Diseases Unit, University of Florence, Florence, Italy.
3 Italian Society of General Medicine (SIMG), Catania, Italy.
Received: February 6, 2019
Accepted: April 13, 2019
Mediterr J Hematol Infect Dis 2019, 11(1): e2019031 DOI 10.4084/MJHID.2019.031
| This is an Open Access article distributed
under the terms of the Creative Commons Attribution License
(https://creativecommons.org/licenses/by-nc/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
is one of the most common helminthiases worldwide. However, there is a
lack of data regarding Southern Italy. We have evaluated the
seroprevalence and associated environmental factors of toxocariasis in
a sample of adults living in the city of Catania.
The aim of the present study was to describe the seroprevalence of T. canis and the association between demographic and environmental factors in a sample of the adult population in the city of Catania.
Materials and Methods
After enrolment in the study, a blood sample was collected. Samples have been coded and processed to obtain serum aliquots and then stored at -20°C in the laboratories of the “Azienda Ospedaliera Policlinico Vittorio Emanuele.” Serum samples have been shipped in dry ice to the laboratories of the Infectious Diseases Institute (Malattie Infettive e Tropicali, AOU Careggi) of the University of Florence and have been analysed by a biologist blinded to the status of the participants. Specific T. canis IgG has been detected with a commercial ELISA kit (Ridascreen Toxocara IgG; R-Bio farm, Milan, Italy) using excretory/secretory antigens (Toxocara excretory-secretory antigen [TES-Ag]) from second-stage T. canis larvae. A face-to-face semi-structured standardized questionnaire about demographic and environmental factors has been administered to all the participants.
All the analyses have been conducted with the software STATA 12.0. For the prevalence of anti-T. canis antibodies the 95% CI have been calculated. Quantitative variables were described using mean and standard deviation. The difference between means and the difference between proportions were evaluated by the t-test and the chi-square test, respectively.
Unconditional logistic regression analysis was performed, and for each study variable, we calculated OR, 95% CI, and p-value (two-tailed test, α=0.05). Multivariate analysis was conducted to investigate the independent effect of risk or protective factor after adjustment for one or several other factors or to adjust for confounding variables. Parameters associated with the outcome at the univariate analysis with a threshold of P = 0.25 were included in the model. The model was manually constructed using the likelihood ratio test (LRT) to compare the log-likelihood of the model with and without a specific variable. Sex, age, and education have been considered a priori confounder variables. Whenever variables were dichotomized, the cutoffs were derived from the median value of the pooled distribution. Each participant was asked to sign an informed consent. The study has been approved by the Local Ethical Committee (code 64/2018/PO).
Subjects had a mean age of 48.1±15.6 years, and 193 (67.3%) were women. The majority of them were professionals (n=103, 36.4%) or housewives (n=79, 28.0%). The demographic characteristics of the population are reported in Table 1.
|Table 1. Demographic characteristics of the population.|
Presence of anti-T. canis antibodies were found in 23 subjects (18 women, 78.2%; mean age 51.1±14.0 years) resulting in seroprevalence of 8.0% (95%CI 5.4-11.7). At the univariate analysis, no association has been found with sex, age, profession or owning pets; a number of siblings were significantly associated with T. canis seropositivity with an OR of 3.46 (95%CI 1.41-8.47) for subjects with more than 3 siblings. A close association was found at multivariate analysis adjusting by age, sex and education (adj OR 3.17; 95%CI 1.09-9.25) as shown in Table 2.
|Table 2. Univariate and multivariate analysis of variables associated with the presence of anti-Toxocara canis antibodies.|
This is the first study carried out to assess the seroprevalence of toxocariasis in a sample of the adult population (over 14 years) in the city of Catania, Sicily. We found a seroprevalence of 8.0%, a value slightly higher with respect to data reported in other urban areas of European countries, as well as to those previously reported in two earlier studies carried out Italy, 1.6 in Central Italy in 2003 and 4.0 in Northern Italy in 1990.
The higher seroprevalence found in the city of Catania can be explained by the environmental factors such as the degree of humidity and temperature that increase the overall survival of T. canis eggs in the soil. However, another critical aspect of being considered is environmental contamination due to the presence of infected dog feces that contribute to the dissemination of T. canis eggs. While we have no data about the prevalence of T. canis infected dog feces in the urban areas of Catania, a study conducted in the neighbouring city of Messina, that shares with Catania the same environmental factors, found a prevalence of T. canis eggs of 3.6% in a random sample of dog feces. Furthermore, another contribution to the increased seroprevalence is the increased presence of dogs living in the households, considering the high level of infestation they bear, up to a prevalence of 76% in puppies in a recent study conducted in Italy.
Presence of T. canis IgG was assessed using a TES-ELISA, considered the standard serological test commonly used in epidemiological surveys to determine the seroprevalence of T. canis in a defined population. While we are aware of the limitations of ELISA test, such as the low specificity, we believe that the lack of a confirmatory Western Blot, considered the gold standard procedure, has not influenced our results because the low specificity depends on the frequent cross-reactions with other nematode infections such as Ascaris lumbricoides, filariasis or strongyloidiasis, which are rare in western countries. In our sample T. canis seropositivity was not associated with age , as expected according to recent literature.
Furthermore in our sample pet ownership was not associated with the risk of T. canis seropositivity, probably because the risk of being infected by the direct contact with domestic animals has been showed to be low.
On the other hand, the number of siblings (more than 3) was significantly associated with T. canis seropositivity. Even if we have not a clear explanation for this association, it is possible to hypothesize that a larger number of siblings could act as a proxy indicator of a lower socio-economic level, a risk factor for being infected with T. canis eggs. The size of the study and the selection of a sample from the general population using an equal probability selection method (a multi-stage sampling) represent the main strengths of our study. However, we are aware that the sex and age distribution of the sampled population may not be entirely representative of the general population. It should be underlined in fact that this study is part of a larger population-based case-control study on MS and to this reason, healthy subjects were recruited matched by age and sex with the enrolled MS cases.
FundingThis research was funded by the Department of Medical and Surgical Sciences and Advanced Technologies “G.F. Ingrassia”, University of Catania, Italy (Piano Triennale di Sviluppo delle Attività di Ricerca Scientifica del Dipartimento 2016-18).
- Ma G, Holland CV, Wang T, Hofmann A, Fan CK,
Maizels RM, Hotez PJ, Gasser RB. Human toxocariasis. Lancet Infect Dis.
2018 Jan;18(1):e14-e24. https://doi.org/10.1016/S1473-3099(17)30331-6
- Glickman LT, Schantz PM. Epidemiology and pathogenesis of zoonotic toxocariasis. Epidemiol Rev. 1981; 3:230-250. https://doi.org/10.1093/oxfordjournals.epirev.a036235
- Schantz PM, Glickman LT. Toxocaral visceral larva migrans. N Engl J Med. 1978; 298(8):436-439. https://doi.org/10.1056/NEJM197802232980806 PMid:622118
MR, Keane CT, O'Connor P, Girdwood RW, Smith H. Clinical features of
covert toxocariasis. Scand J Infect Dis. 1987; 19(6):693-696. https://doi.org/10.3109/00365548709117206
S, Bonhomme J, de La Blanchardière A. Neurotoxocariasis: a systematic
literature review. Infection. 2016; 44(5):565-574. https://doi.org/10.1007/s15010-016-0889-8
- Hotez PJ. Neglected infections of poverty in the United States of America. PLoS Negl Trop Dis. 2008; 2(6):e256. https://doi.org/10.1371/journal.pntd.0000256
- Hotez PJ, Gurwith M. Europe's neglected infections of poverty. Int J Infect Dis. 2011 15(9):e611-619. https://doi.org/10.1016/j.ijid.2011.05.006 PMid:21763173
C-K, Holland CV, Loxton K, Barghouth U. Cerebral Toxocariasis: Silent
Progression to Neurodegenerative Disorders? Clin Microbiol Rev. 2015;
C, Di Sacco B, Gatti S, Sangalli G, Scaglia M. Epidemiology of human
toxocariasis in northern Italy. Parassitologia. 1990; 32(3):313-319.
- Habluetzel A, Traldi G,
Ruggieri S, Attili AR, Scuppa P, Marchetti R, Menghini G, Esposito F. .
An estimation of Toxocara canis prevalence in dogs, environmental egg
contamination and risk of human infection in the Marche region of
Italy. Vet Parasitol. 2003, 113(3-4):243-252. https://doi.org/10.1016/S0304-4017(03)00082-7
- Istituto Nazionale di Statistica, 2011. 15° Censimento generale della popolazione.
A, Messina S, Bruno E, Mostile G, Quattrocchi G, Raciti L, Dibilio V,
Cappellani R, D'Amico E, Sciacca G, Lo Fermo S, Paradisi V, Patti F,
Zappia M. Risk factors in multiple sclerosis: a population-based
case-control study in Sicily. Background and methods. Neurol Sci. 2016
Savigny DH, Voller A, Woodruff AW. Toxocariasis: serological diagnosis
by enzyme immunoassay. J Clin Pathol. 1979; 32(3):284-288. https://doi.org/10.1136/jcp.32.3.284 PMid:372253 PMCid:PMC1145636
- Fillaux J, Magnaval J-F. Laboratory diagnosis of human toxocariasis. Vet Parasitol. 2013; 193(4):327-336. https://doi.org/10.1016/j.vetpar.2012.12.028 PMid:23318165
AL., Brianti E., Gaglio G., Ferlazzo M., Giannetto S. Environmental
contamination by canine feces in the city of Messina: parasitological
aspects and zoonotic hazards. In Proceedings of LXI Congress of the
Italian Society for Veterinary Science (S.I.S.Vet.). Salsomaggiore
Terme, Italy: 135-136.
- Corda A, Tamponi
C, Meloni R, Varcasia A, Parpaglia MLP, Gomez-Ochoa P, Scala A.
Ultrasonography for early diagnosis of Toxocara canis infection in
puppies. Parasitol Res. 2019 Mar;118(3):873-880. https://doi.org/10.1007/s00436-019-06239-4 PMid:30706166
AN, Erickson LD, Gale SD, Stone A, Brown BL, Hedges DW. Toxocara
Seroprevalence and Associated Risk Factors in the United States. Am J
Trop Med Hyg. 2017; 97(6):1846-1850. https://doi.org/10.4269/ajtmh.17-0542 PMid:29016316 PMCid:PMC5805073
W, Herkner H, Tobudic S, Faas A, Mooseder G, Burgmann H, Auer H.
Exposure to Echinococcus multilocularis, Toxocara canis, and Toxocara
cati in Austria: a nationwide cross-sectional seroprevalence study.
Vector Borne Zoonotic Dis. 2013; 13(11):798-803. https://doi.org/10.1089/vbz.2012.1283 PMid:24107202