Evaluation of Visceral Toxocariasis Seropositivity and Possible Risk Factors in Patients with a Clinical Preliminary Diagnosis of Cystic Echinococcosis

Öz

Aim: This study aimed to evaluate the seropositivity and possible risk factors for visceral toxocariasis in patients with a clinical preliminary diagnosis of cystic echinococcosis. Material and Methods: Between October 2022 and December 2023, 184 blood serum samples, which were taken from patients with a clinical preliminary diagnosis of cystic echinococcosis and sent to the Medical Parasitology Laboratory of the Health Research and Training Hospital of Kafkas University, were analyzed for anti-Toxocara canis IgG using ELISA. Anti-Ascaris lumbricoides IgG ELISA was applied to the positive samples to differentiate cross-reactions. Results: In this study, anti-T.canis IgG positivity was detected in 73 (39.67%) of the 184 serum samples. Among the sera determined to be positive for anti-T.canis IgG, mixed infection with A.lumbricoides was detected in 38 (52.05%) samples, and cross-reactions were identified in 10 (13.7%) samples. The study revealed the overall positivity rate for anti-T.canis IgG alone as 23.97% (35/146), with rates of 24.47% (23/94) in women and 23.08% (12/52) in men. Out of the 6 samples positive for cystic echinococcosis (6/184; 3.26%), 3 (3/6; 50%) were also seropositive for visceral toxocariasis. Anti-T. canis IgG was detected at higher rates in women, individuals over 65 years of age, illiterates, farmers, and rural inhabitants (P >0.05). The levels of anti-T.canis IgG were significantly higher in individuals with detached houses with gardens, those who kept dogs in their gardens, those with vegetable patches, those with neighboring gardens and surroundings with dogs, and those engaged in soil-related garden work (P <0.05). Conclusions: In Kars and its surroundings, visceral toxocariasis was significant for public health, especially among individuals in contact with stray dogs and in soil-related occupations. Further studies are needed to determine the correlation between visceral toxocariasis and cystic echinococcosis, which share similar epidemiologic risks and clinical complaints.

Anahtar Kelimeler

• anti-Toxocara canis IgG
• risk factor
• visceral toxocariasis
• cystic echinococcosis

Kaynakça

1. 1. Korkmaz M. Toxocariosis. In: Özcel MA. ed. Özcel’in Tıbbi Parazit Hastalıkları. İzmir: Türkiye Parazitoloji Derneği Yayını No:22. 2007. p. 649–660. (In Turkish) .
2. 2. Ma G, Rostami A, Wang T, Hofmann A, Hotez PJ, Gasser RB. Global and regional seroprevalence estimates for human toxocariasis: A call for action. In: Bowman DD. ed. Advances in Parasitology. Toxocara and Toxocariasis, Volume 109, Elsevier Ltd. 2020. p. 275–290.
3. 3. Akdemir C. Visceral larva migrans among children in Kutahya (Turkey) and an evaluation of playgrounds for T. canis eggs. Turk J Pediatr. 2010;52:158–62.
4. 4. Çiçek M, Yılmaz H. Prevalence of Toxocariasis in human and dogs in Van Province. Kafkas Univ Vet Fak Derg. 2012;18:531–6.
5. 5. Kustimur S, Dogruman Al F, Oguzulgen K, Bakir H, Maral I, Turktas H, et al. Toxocara seroprevalence in adults with bronchial asthma. Trans R Soc Trop Med Hyg. 2007;101:270–4.
6. 6. Kutun S. Seroprevalance of Toxocariasis on people in Bolu and its region. Bolu Abant İzzet Baysal University, Health Sciences Intitute, Master Thesis, Bolu, Turkey, 2019.
7. 7. Artinyan E, Uysal HK, Akgul O, Altiparmak S, Oner YA. Research on Toxocara canis antibodies obtained from patients with eosinophilia. Indian J Med Microbiol. 2014;32:383–6.
8. 8. Kaplan M, Kalkan A, Kuk S, Demirdag K, Ozden M, Kilic SS. Toxocara seroprevalence in schizophrenic patients in Turkey.Yonsei Med J. 2008;49:224–9.

9. 9. Umur Ş, Arslan MÖ. The prevalence of helminth species in stray dogs in Kars District. Türkiye Parazitol Derg. 1998;22:188–93.
10. 10. Gıcık Y, Kara M, Sarı B, Kılıç K, Arslan MÖ. Intestinal parasites of Red foxes (Vulpes vulpes) and their zoonotic importance for humans in Kars province. Kafkas Univ Vet Fak Derg. 2009;15:135–40.
11. 11. Arslan MÖ, Mor N, Bedir H. Seropozitifity of anti-Echinococcus granulosus in patients with clinical prediagnosis of Cystic Echinococcosis at Kafkas University Health Research and Application Hospital. Türkiye Parazitol Derg. 2022;46:129–32.
12. 12. Rostami A, Riahi SM, Holland CV, Taghipour A, Khalili- Fomeshi M, Fakhri Y, et al. Seroprevalence estimates for toxocariasis in people worldwide: A systematic review and meta-analysis. PLoS Negl Trop Dis. 2019;13:e0007809.
13. 13. Ulloque-Badaracco JR, Hernandez-Bustamante EA, Alarcón- Braga EA, Huayta-Cortez M, Carballo-Tello XL, Seminario-Amez RA, et al. Seroprevalence of human toxocariasis in Latin America and the Caribbean: A systematic review and metaanalysis. Front Public Health. 2023;11:1181230.
14. 14. Said A, Khattak I, Abbas RZ, Khan MK, Saleemi MK, Budke CM, et al. Toxocara canis seropositivity in different exposure groups in the Khyber Pakhtunkhwa province of Northwest Pakistan. Parasitol Res. 2023;122:1159–66.
15. 15. Pezeshkian F, Pouryousef A, Omidian M, Mikaeili F, Safarpour AR, Shojaei-Zarghani S, et al. Seroprevalence of toxocariasis and its associated risk factors among adult population in Kavar District, Fars Province, South of Iran: A cross-sectional community-based seroepidemiological survey. Interdiscip Perspect Infect Dis. 2023;2721202.
16. 16. Luca I, Sîrbu CB, Sîrbu BJ, Cireşan A, Garedaghi Y, Dărăbuş G. A retrospective study on the seroprevalence of anti-T. canis antibodies in the human population of a Romanian City. Int J Med Parasitol Epidemiol Sci. 2022;3:24.
17. 17. Wang S, Li H, Yao Z, Li P, Wang D, Zhang H, et al. Toxocara infection: Seroprevalence and associated risk factors among primary school children in central China. Parasite. 2020;27:30.
18. 18. Pourgholaminejad A, Razipour H, Heydarian P, Ashrafi K, Roushan ZA, Sharifdini M. A Survey on the seroprevalence of toxocariasis and related risk factors in Eosinophilic Children of Northwest Iran. Afri Health Sci. 2022;22:617–25.
19. 19. Santarem VA, do Couto AC, Lescano SZ, Roldán WH, Delai RR, Giuffrida R. Serosurvey of anti-Toxocara canis antibodies in people experiencing homelessness and shelter workers from São Paulo, Brazil. Parasit Vectors. 2022;15:373.
20. 20. Taylan-Ozkan A. Sources and seroprevalence of toxocariasis in Turkey. Adv Parasitol. 2020;109:465–82.
21. 21. Demirci M, Kaya S, Çetin ES, Arıdoğan B, Onal S, Korkmaz M. Seroepidemiological investigation of toxocariasis in the Isparta region of Turkey. Iranian Parasitol. 2010;5:52.
22. 22. Sozen H, Citil BE, Caylak S, Gokmen AA, Kaya S, Demirci M, et al. Seroepidemiological study of toxocariasis among volunteers animal husbandry workers and veterinary in Southern Anatolia in Turkey in 2014. Iran J Parasitol. 2015;10:473.
23. 23. Selek MB, Baylan O, Kutlu A, Özyurt M. Toxocara canis IgG seropositivity in patients with chronic urticaria. Iran J Allergy Asthma Immunol. 2015;14:450–6.
24. 24. Kustimur S, Dogruman Al F, Oguzulgen K, Bakir H, Maral I, Turktas H. Toxocara seroprevalence in adults with bronchial asthma. Trans R Soc Trop Med Hyg. 2007;101:270–4.
25. 25. Yazar S, Yaman O, Cetinkaya U, Hamamcı B, Şahin İ. Investigation of anti-Toxocara canis IgG antibodies in patients presenting at the Erciyes University Medical Faculty, Department of Parasitology. Türkiye Parazitol Derg. 2010;34:24–6.
26. 26. Doğan N, Dinleyici EC, Bor O, Töz SO, Ozbel Y. Seroepidemiological survey for Toxocara canis infection in the northwestern part of Turkey. Türkiye Parasitol Derg. 2007;31:288–91.
27. 27. Oğuztürk H, Saygı G. Investigation of infection caused by larvae of Toxocara canis in elementary school students. Türkiye Parasitol Derg. 2002;26:409–14.
28. 28. Jones JL, Kruszon-Moran D, Won K, Wilson M, Schantz PM. Toxoplasma gondii and Toxocara spp. co-infection. Am J Trop Med Hyg. 2008;78:35–9.
29. 29. Kim SW, Jang BK. Toxocara canis and Fasciola hepatica coinfection leading to hepatic abscess: A case report. J Korean Med Sci. 2023;38:e323.
30. 30. Huang L, Sun L, Liu C, Li S, Zhang T, Luo X, et al. Diagnosis of ocular toxocariasis by serum and aqueous humor IgG ELISA. Transl Vis Sci Technol. 2021;10:33.
31. 31. Zibaei M, Najmi M, Bahadory S, Miahipour A, Firoozeh F, Bakhshipour F. Sero-epidemiology of Toxocara canis infection in people attending four educational and therapeutic centres in Alborz Province, Iran. Med Srod. 2021;24:25–9.
32. 32. Phuong NTN, Trung TT, Ha PH, Ha PTT, Anh LHN, Thao NTP, et al. Prevalence of Toxocara spp. infection: Investigate from the Thong Nhat Dong Nai General Hospital from 2019 to 2020. Am J Sci Eng Res. 2021;4:1.
33. 33. Feckova M, Antolová D, Zaleśny G, Halánová M, Štrkolcová G, Goldová M, et al. Seroepidemiology of human toxocariasis in selected population groups in Slovakia: A cross-sectional study. J Infect Public Health. 2020;13:1107–11.
34. 34. Mubarak AG, Mohammed ES, Elaadli H, Alzaylaee H, Hamad RS, Elkholy WA, et al. Prevalence and risk factors associated with Toxocara canis in dogs and humans in Egypt: A comparative approach. Vet Med Sci. 2023;29.
35. 35. Na-Ek P, Narkkul U, Phasuk N, Punsawad C. Seroprevalence of anti-Toxocara canis antibodies and associated risk factors among dog owners in the rural community of Nakhon Si Thammarat province, southern Thailand. Trop Med Health. 2022;50:32.
36. 36. Khoshsima-Shahraki M, Dabirzadeh M, Azizi H, Khedri J, Djahed B, Neshat AA. Seroepidemiology of Toxocara canis in children under 14 years referring to laboratories of Sistan and Baluchestan Province in Southeast of Iran. Iran J Parasitol. 2019;14:89–94.
37. 37. Lee JY, Yang MH, Hwang JH, Kang M, Paeng JW, Yune S, et al. The prevalence of toxocariasis and diagnostic value of serologic tests in asymptomatic Korean adults. Allergy Asthma Immunol Res. 2015;7:467–75.
38. 38. Bayoumy A, Atallah R, Mohamed K, Zaalouk TK, Ghazy MES, El-Kenany MA. Seroepidemiological evaluation of toxocariasis in Egyptian children suffering from recurrent urticaria. Egypt J Hosp Med. 2019;76:4262–8.
39. 39. Etewa SE, Abdel-Rahman SA, Abd El-Aal NF, Fathy GM, El-Shafey MA, Ewis AM. Geohelminths distribution as affected by soil properties, physicochemical factors and climate in Sharkyia governorate. Egypt J Parasit Dis. 2016;40:496–504.