• Angela GUILA PMSI Institute of Phthisiopneumology „Chiril Draganiuc”



parasitic diseases, toxocara canis, tuberculosis, immunity


Introduction. Parasitic diseases continue to affect the population of many countries of the world. About 2 billion people on the planet are infected with helminths, including Toxocara canis. Invasion with Toxocara canis represents a strong endogenous factor in the formation of the regulatory imbalance of the immune system. The integral evaluation of these indices serves as an important criterion in the diagnosis of toxocarosis and the effectiveness of the applied therapy. In the context of the above, information about research on immune reactivity and natural resistance of tuberculosis patients in association with toxocariasis is of interest. Material and methods. This article is a systematic review of the relevant literature between the year 2001 and 2022. The material for the study was electronic sources published through the web Medline, EMBASE, Global Health, Scopus and Web of science; PubMed; crossref; Google Scholar and others. The following keywords were used “immunological reactivity”, “natural resistance”, “parasitic diseases”, “toxocara canis”, “tuberculosis and toxocariasis”, “immunity”, “helminthiasis”, “toxocariasis”. Bibliographic resources have been systematized by subject and content. The results were grouped and systematized according to the relevant criteria and the level of scientific evidence. Results. Parasites, in particular, Toxocara canis and M. tuberculosis use different mechanisms to alter the immune response, but these mechanisms can interact with significant consequences for the immunological reactivity of each infection. Chronic helminthic infection causes a wide range of changes in the immune system. Conclusion. The immune reactivity and natural resistance of tuberculosis patients in association with toxocarosis is insufficiently elucidated.

Author Biography

Angela GUILA, PMSI Institute of Phthisiopneumology „Chiril Draganiuc”

PhD student


Timothy K. Wu., Dwight D Bowman. Toxocara canis.Trends Parasitol. 2022;38[8]:709-710.

Guangxu Ma, Rostami Ali, Wang Tao, Hofmann Andreas, Hotez Peter J., Gasser Robin B. Chapter Fourteen Global and regional seroprevalence estimates for human toxocariasis: A call for action. Advances in Parasitology. 2020;[109]:275-290.

Guangxu Ma, Celia V Holland, Tao Wang, Andreas Hofmann, Chia-Kwung Fan, Rick M Maizels et al., Human toxocariasis. The Lancet. Infect 2018; 18[1]:14-24.

Placinta Gh. Toxocarosis – current problem of the medical and public health service. Chisinau. Publishing house: Sirius Typography, 2017; 240 p. [In Ro].

Ahn S.J., Ryoo N.K., Woo S.J. Ocular toxocariasis: clinical features, diagnosis, treatment, and prevention. Asia Pac Allergy. Jul 2014;4[3]:134–41.

Lee R.M., Moore L.B., Bottazzi M.E., Hotez P.J. Toxocariasis in north america: a systematic review. PLoS Negl Trop Dis. Aug 2014;8[8]:e3116.

Moreira G.M., Telmo P.D., Mendonça M., Moreira A.N., McBride A.J., Scaini C., et al. Human toxocariasis: current advances in diagnostics, treatment, and interventions. Trends Parasitol. 2014;30[9]:456–464.

Peng J., Federman H.G., Hernandez C.M. and Siracusa M.C. Communication is key: Innate immune cells regulate host protection to helminths. Front. Immunol. 2022;13:995432.

Kim J.H., Chung W.B., Chang K.Y., Ko S.Y., Park M.H., Sa Y.K., et al. Eosinophilic myocarditis associated with visceral larva migrans caused by Toxocara canis infection. J Cardiovasc Ultrasound. 2012;20[3]:150–3.

Placinta Gh. Toxocarosis: medico-social aspects; clinical-evolutionary manifestations; managerial and therapeutic conduct. Autoref. thesis dhşm. Chisinau, 2019. 45 p.

Prisacaru V. Special epidemiology [manual]. Chisinau. 2015, p. 323-326. [In Ro].

Placinta Gh., Tibuleac S., Onu V. et al. Some particularities of blood hypereosinophilia in patients from the Republic of Moldova. Medical Courier. 2007;1[295]: 41-43. [In Ro].

Placinta Gh., Tibuleac S., Conovali C. Some epidemiological characteristics of blood hypereosinophilia in patients with lung lesions. Materials of the II national congress of immunologists, allergologists and immunorehabilitologists with international participation. Ghisinau, 2007:167-172. [In Ro].

Ţibuleac S., Plăcinta Gh., Mudreac K. et al. Canine ascaridosis and human toxocarosis in the city of Chisinau. Medical Courier. 2006; 6: 13-15. [In Ro].

Bredikhin D.A., Nikonov S.D., Cherednichenko A.G., Petrenko T.I. Photodynamic inactivation of Mycobacterium tuberculezis with radachlorin in vitro. Tuberculosis and Lung Diseases, vol. 96, 2018;96[1]:5-10. [In Russ.].

Durmaz B., Yakinci C., Koroglu M., Rafiq M., Durmaz R. Concentration of total serum IgE in parasitized children and the effects of the antiparasitic therapy on IgE levels. J. Trop. Pediatr. 1998; 44[2]:121.

Todoriko L.D., Boiko A.V., Yeremenchuk I.V. et al. Еstablishing risk groups of multidrug-resistant tuberculosis and planiing its therapeutic approach. Бук. мед. вісник. 2011; 2: 173-178. [In Ukr].

Kholodnyak G. E. Clinical and epidemiological features, diagnosis and new approaches to the treatment of toxocariasis in children. Abstract diss. Candidate of Medical Sciences, Moscow. 2009: 24. [In Russ.].

Tarasyuk O.O., Verbinets A.V., Tkach O.A. et al. The role of some factors in reactivation of tubercular process. The 4th National Congress of Phthisiopneumology from the Republic of Moldova “News in the etiology, pftogenesis, prophylaxis, diagnosis and treatment of tuberculosis and non-specific lung diseases”, Chisinau. 2009; 28. [In Ro].

Elliott A.M., Namujju P.B., Mawa P.A., Quigley M.A., Nampijja M., Nkurunziza P.M., Belisle J.T., Muwanga M., Whitworth J.A.. A randomised controlled trial of the effects of albendazole in pregnancy on maternal responses to mycobacterial antigens and infant responses to Bacille Calmette-Guérin immunization. BMC Infect Dis. 2005;21;5:115.

Atkins D, Best D, Briss PA, et al. Grading quality of evidence and strength of recommendations. BMJ. 2004;328[7454]:1490.

Zurochka V. A. Immunobiological properties of synthetic peptides of the active center of the granulocyte-macrophage colony-stimulating factor. Abstract dis. MD.2016. [In Russ.].

Mendez-Samperio P. Immunological Mechanisms by Which Concomitant Helminth Infections Predispose to the Development of Human Tuberculosis. Korean J Parasitol. 2012;50[4]:281-286.

Mendez-Samperio P. Role of interleukin-12 family cytokines in the cellular response to mycobacterial disease. Int J Infect Dis 2010:14: e366-e371.

Venugopal P.G., Nutman T.B., Semnani R.T. Activation and regulation of Toll-like receptors by helminth parasites. Immunol Res. 2009;43:252-263.

Korbel D.S., Schneider B.E., Schaible U.E. Innate immunity in tuberculosis: Myths and truth. Microbes Infect. 2008;10:995-1004.

Cooper A.M., Khader S.A. The role of cytokines in the initiation, expansion, and control of cellular immunity to tuberculosis. Immunol Rev. 2008;226:191-204.

Zibaei M., Shayesteh Z., Moradi N., Bahadory S. Human Toxocara Infection: Allergy and Immune Responses. Anti-Inflammatory & Anti-Allergy Agents in Medicinal Chemistry. 2019;2:82-90.

Maizels R.M., Yazdanbakhsh M. Immune regulation by helminth parasites: Cellular and molecular mechanisms. Nat Rev Immunol. 2003;3:733-744.

Belkaid Y., Rouse B.T. Natural regulatory T cells in infectious disease. Nat Immunol. 2005;6:353-360.

Masamba P., Kappo A. Immunological and Biochemical Interplay between Cytokines, Oxidative Stress and Schistosomiasis. Int. J. Mol. Sci. 2021;22[13]:7216.

Bobardt S.D., Dillman A.R., Nair M.G. The Two Faces of Nematode Infection: Virulence and Immunomodulatory Molecules From Nematode Parasites of Mammals, Insects and Plants. Front. Microbiol. 2020;11:577846.

Babu S, Bhat SQ, Kumar NP, Anuradha R, Kumaran P, Gopi PG, Kolappan C, Kumaraswami V, Nutman TB. Attenuation of Toll-like receptor expression and function in latent tuberculosis by coexistent filarial infection with restoration following antifilarial chemotherapy. PLoS Negl Trop Dis. 2009;3:e489.

Elias D., Britton S., Aseffa A., Engers H., Akuffo H. Poor immunogenicity of BCG in helminth infected population is associated with increased in vitro TGF-beta production. Vaccine. 2008;26:3897-3902.

Resende Co T., Hirsch C.S., Toossi Z., Dietze R., Ribeiro-Rodrigues R. Intestinal helminth co-infection has a negative impact on both anti-Mycobacterium tuberculosis immunity and clinical response to tuberculosis therapy. Clin Exp Immunol. 2007;147:45-52.

Salgame P. Host innate and Th1 responses and the bacterial factors that control Mycobacterium tuberculosis infection. Curr Opin Immunol. 2005;17:374-380.

Oldenhove G., de Heusch M., Urbain-Vansanten G., Urbain J., Maliszewski C., Leo O., Moser M. CD4+ CD25+ regulatory T cells control T helper cell type 1 responses to foreign antigens induced by mature dendritic cells in vivo. J Exp Med. 2003;198:259-266.

Elias D., Wolday D., Akuffo H. Petros B., Bronner U., Britton S. Effect of deworming on human T cell responses to mycobacterial antigens in helminth-exposed individuals before and after bacille Calmette-Guerin vaccination. Clin Exp Immunol. 2001;123:219-225.

Rosada R.S., Torre L.G., Frantz F.G., Trombone A.P., Zarate-Blades C.R., et al. Protection against tuberculosis by a single intranasal administration of DNAhsp65 vaccine complexed with cationic liposomes. BMC Immunol. 2008,9:38.

Michaluart P., Abdallah K.A., Lima F.D., Smith R., Moyses R.A., et al. Phase I trial of DNA-hsp65 immunotherapy for advanced squamous cell carcinoma ofthe head and neck. Cancer Gene Ther. 2008;15:676–684.

Elias D., Akuffo H., Pawlowski A., Haile M., Schon T., Britton S. Schistosoma mansoni infection reduces the protective efficacy of BCG vaccination against virulent Mycobacterium tuberculosis. Vaccine. 2005;23:1326-1334.

Boitelle A., Scales H.E., Di Lorenzo C., Devaney E., Kennedy M.W., Garside P., Lawrence C.E. Investigating the impact of helminth products on immune responsiveness using a TCR transgenic adoptive transfer system. J Immunol. 2003;171:447-454.

Borkow G., Weisman Z., Leng Q., Stein M., Kalinkovich A., Wolday D., Bentwich Z.. Helminths, human immunodeficiency virus and tuberculosis. Scand J Infect Dis. 2001;33:568-571.

Frantz F.G., Rosada R.S., Turato W.M., Peres C.M., Coelho-Castelo A.A, Ramos S.G., Aronoff D.M., Silva C.L., Faccioli L.H. The immune response to toxocariasis does not modify susceptibility to Mycobacterium tuberculosis infection in BALB/c mice. Am J Trop Med Hyg. 2007;77:691-8.

Elias D., Akuffo H., Thors C., Pawlowski A., Britton S.. Low dose chronic Schistosoma mansoni infection increases susceptibility to Mycobacterium bovis BCG infection in mice. Clin Exp Immunol. 2005;139:398-404.

Natukunda A, Zirimenya L, Nassuuna J, et al. The effect of helminth infection on vaccine responses in humans and animal models: A systematic review and meta‐analysis. Parasite Immunol. 2022;44[9]:e12939.

Nechaev V.V., Ivanov A.K., Panteleev A.M. Socially significant infections associated with tuberculosis: epidemiology and prevention. Topical issues of infectious pathology. Vitebsk, 2008; 61-62. [In Russ.].

Vacca, F., Le Gros, G. Tissue-specific immunity in helminth infections. Mucosal Immunol. 2022;15: 1212– 1223.

Inclan-Rico Juan M. Siracusa Mark C. First Responders: Innate Immunity to Helminths. Trends in Parasitology. 2018;34[10]:861-880.

Shishkanova L. V. Toxocariasis in the south of Russia; epidemiological, sanitary parasitological and seroepidemiological characteristics. Abstract diss. … cand. biol. Sciences. M., 2010. [In Russ.].

Andries L., Raba T., Ţurcan A., Barbu D. Toxocarosis. Methodical materials. Chisinau. 2003;19. [In Ro].

Weatherhead J.E., Gazzinelli-Guimaraes P., Knight J.M., Fujiwara R., Hotez P.J., Bottazzi M.E. Corry D.B. Host Immunity and Inflammation to Pulmonary Helminth Infections. Front. Immunol. 2020;11:594520.

Zaikov S.V. Helminthiasis and allergic diseases. Clinical Immunology. Allergology. Infectology. 2009;3/2. [In Russ.].

Salvador S., Ribeiro R., Winckler M.I., Ohlweiler L., Riesgo R. Pediatric neuro-toxocariasis with concomitant cerebral, cerebellar, and peripheral nervous system involvement: case report and review of the literature. J Pediatr [Rio J]. 2010;86[6]:531-4.

Bekish L.E., Semenov V.M. Features of the clinical course of visceral and ocular toxocariasis in children and adults in Vitebsk and Vitebsk region. Topical issues of infectology: a collection of articles. Grodno. 2012:27-30. [In Russ.].

Tobin E.H., Zhang J., Maton B. Meningoencephalitis and visceral larva migrans in a woman with intense exposure to cats. Infect Dis Clin Pract. 2011;3[51]:19[3]:221–2.

Baranova O.P., Ilkovich M.M., Speranskaya A.A. Difficulties in diagnosing respiratory sarcoidosis. Practical Medicine. 2011;3:58-62. [In Russ.].

Zhmakin D.A. Epidemiological and clinical-immunological aspects of geohelminthiases [ascariasis, toxocariasis]. Abstract of diss. med., 2010: 24 [In Russ.].

Bodnya E.I., Bodnya I.P. Clinical and immunological aspects of parasitic diseases. Clinical immunology. Allergology. Infectology. 2007; 78. [In Russ.].

Derzhavina T.Yu. Human geohelminthosis monitoring in theTula Region. Med. Parasitol. 2010;3:42 [In Russ.].

Bell R.G. IgE, allergies and helminth parasites: a new perspective on an old conundrum Immunol. Cell. Biol. 2003;74: 337–345.

Feodorova V.A., Lyapina A.M., Ulianova O.V., Polyania T.I.,Eliseev Yu.Yu. High Potency of Novel Polymeric Adjuvant in Eliciting of the Immune Response in Mice to Major Antigens of Chlamydia and Yersinia. Procedia in Vaccinology. 2012; 6: 93–97. [In Russ.].

Togarsimalemath S.K., Pushpamithran G., Schön T., Stendahl O., Blomgran R. Helminth Antigen Exposure Enhances Early Immune Control of Mycobacterium tuberculosis in Monocytes and Macrophages. J Innate Immun. 2021;13:148–163.

Hassan A., Blanchard N. Microbial [co]infections: Powerful immune influencers. PLoS Pathog. 2022;18[2]:e1010212.

Titova N.D. Clinical significance of the spectrum of antibodies and cellular sensitization to toxocar antigens in children with allergic diseases. Pediatrics. 2011; 2:46-51. [In Russ.].

Botkina A.S., Dubrovskaya M.I. Lavral helminthiases. Toxocariasis in pediatric practice. The attending physician. 2016; 6.

Nechaeva A. S., Starkova T. V., Chernikova E. A. Optimization of the method for recording the results of ELISA in toxocariasis. Medical parasitology and parasitic disease., 2013;2: 39–41. [In Russ.].

Kolobovnikova Yu. V., Urazova O. I., Novitsky V. V., Voronkova O. V., Mikheeva K. O., Ignatov M. V., Filinyuk O. V., Stepanova E.P. Indicators of cellular and humoral immune response in pulmonary tuberculosis accompanied by eosinophilia. Bulletin of Siberian Medicine. 2012;1:39-45. [In Russ.].

Kirman J., Zakaria Z., McCoy K. Role of eosinophils in the pathogenesis of Mycobacterium bovis BCG infection in gamma interferon receptor-deficient mice. Infect. Immun. 2009;68[5]:2976-2978.

Speirs R.S., Speirs E.E., Ponzio N.M. A Role for eosinophils in adaptive humoral immunity. The Open Immunology Journal. 2009;2:168-186.

Hogan S.P., Rosenberg H.F., Moqbel R. Eosinophils: biological properties and role in health and disease. Clinical & Experimental Allergy. 2008;38:709-750.

Piskun T., Yakimovich N., Mirutko D. Toxocariasis in children. Medical Bulletin. 2008; 16[850]. [In Russ.].

Miropolskaya N. Yu. Scientific rationale for the prevention of broncho-obstructive conditions in children infested with toxocars. Abstract dis. cand. honey. Sciences. Khabarovsk, 2008;23. [In Russ.].

Shpilevaya T. I. Clinical features of the course of pregnancy and allergo-immunological status of pregnant women seropositive for toxocariasis. Abstract dis. ... cand. honey. Sciences. Saint Petersburg. 2009. [In Russ.].

Klion A. D., Mitre E. Eosinophils and helminth infection: protective or pathogenic? Seminars in Immunopathology. 2021;43: 363–381.

Ecevit Ç, Bag Ö, Vergin C, Öztürk A. Visceral larva migrans presenting with hypereosinophilia. Turkiye Parazitol Derg. 2013;37[1]:58–60.

Mukund A., Arora A., Patidar Y., Mangla V., Bihari C., Rastogi A., et al. Eosinophilic abscesses: a new facet of hepatic visceral larva migrans. Abdom Imaging. 2012;17.

Adamenko G.P., Nikulin Yu.T. Toxocarosis – an actual healthcare problem. Medical news. 2004;2:31–5. [In Russ.].

Babachenko I. V:, Timchenko V. N., Stebunova T. K., Antykova L; P., Mikueva T. N., Sertakova. L. Khovaiko, E. K. Toxocariasis in the practice of an infectious disease specialist. Pediatrics. 2002;2: 41-43. [In Russ.].

Elias Daniel, Mengistu Getahun, Akuffo Hannah and Britton Sven. Are intestinal helminths risk factors for developing active tuberculosis? Med Int Health. 2006;11[4]:551-8.

Fabiani Gai Frantz, et al. The Immune Response to Toxocariasis Does Not Modify Susceptibility to Mycobacterium tuberculosis Infection in BALB/c Mice. Am. J. Trop. Med. Hyg. 2007;77[4]:691–698.

Novitskii V.V., Strelis A.K., Serebryakova V.A. and others Immune status of patients with infiltrative drug-resistant tuberculosis on anti-tuberculosis therapy. Immunology. 2007;[1]: 27-30. [In Russ.]






Research Article