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Anaphylaxis Caused by Helminths: Review of the Literature

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Anaphylaxis Caused by Helminths: Review of the Literature European Review for Medical and Pharmacological Sciences 2012; 16: 1513-1518 Anaphylaxis caused by helminths: review of the literature P.L. MINCIULLO1, A. CASCIO2, A. DAVID3, L.M. PERNICE2, G. CALAPAI4, S. GANGEMI1,5 1School and Unit of Allergy and Clinical Immunology, Department of Clinical and Experimental Medicine, University of Messina, Italy 2Department of Human Pathology, University of Messina, Italy 3Department of Neurosciences, Psychiatric and Anesthesiological Sciences, University of Messina, Italy 4Department of Clinical and Experimental Medicine and Pharmacology, Section of Pharmacology, University of Messina, Italy 5Institute of Biomedicine and Molecular Immunology, National Research Council, Palermo, Italy Abstract. – BACKGROUND: Anaphylaxis is a Introduction severe, life-threatening, generalized or systemic hypersensitivity reaction. In many individuals Anaphylaxis is a severe, life-threatening, gen- with anaphylaxis a pivotal role is played by IgE and the high-affinity IgE receptor on mast cells eralized or systemic hypersensitivity reaction. or basophils. Less commonly, it is triggered The reaction usually develops gradually, most of- through other immunologic mechanisms, or ten starting with itching of the gums/throat, the through nonimmunologic mechanisms. The hu- palms, or the soles, and local urticaria; develop- man immune response to helminth infections ing to a multiple organ reaction often dominated is associated with elevated levels of IgE, tis- by severe asthma; and culminating in hypoten- sue eosinophilia and mastocytosis, and the 1 presence of CD4+ T cells that preferentially sion and shock . produce IL-4, IL-5, and IL-13. Individuals ex- In many individuals with anaphylaxis a pivotal posed to helminth infections may have allergic role is played by IgE and the high-affinity IgE re- inflammatory responses to parasites and para- ceptor on mast cells or basophils. Less common- site antigens. ly, it is triggered through other immunologic AIM: To summarize the evidences about the mechanisms, or through nonimmunologic mech- role of helmiths in triggering anaphylaxis anisms2. MATERIALS AND METHODS: PubMed search was performed by combining the terms (ana- Anaphylaxis episodes range in severity from phylaxis, anaphylactic, anaphylactoid) with those that are mild and resolve spontaneously to each one of the etiological agents of human those that are fatal within minutes2. helminthiasis for the period January 1950 to Helminths are eukaryotic worm-like organ- September 2012. isms that live and feed off living hosts, receiving RESULTS: The PubMed search identified 609 nourishment and protection while disrupting papers. Only four genera of helminths were as- sociated with anaphylaxis. (Echinococcus spp, their hosts’ nutrient absorption, causing weak- 302 papers; Anisakis spp, 73 papers; Taenia soli- ness and disease. From a taxonomic point of um cysticercosis, 7 papers; and Ascaris spp., 243 view they are classified in cestodes (tapeworms), papers). trematodes (flukes) and nematodes (round- CONCLUSIONS: The risk of anaphylaxis in pa- worms). They can live inside humans as well as tients with helminthiasis can vary according to other animals. Helminths can invade the intesti- the pathogens, occurring more frequently during nal tract as well as urinary tract, and blood. In ef- echinococcosis of after anisakis infestation and being extremely rare after other helminth infesta- fect, any organ can be affected by adult worms or 3,4 tions. However, physicians, allergist and para- their larvae . sitologist in particular, should be aware of a po- The human immune response to helminth in- tential anaphylaxis caused by helminths. fections is associated with elevated levels of IgE, tissue eosinophilia and mastocytosis, and the Key Words: Anisakis Echinococcus presence of CD4+ T cells that preferentially pro- Anaphylaxis, , Ascaris, , 5 Helminth, Taenia. duce IL-4, IL-5, and IL-13 . Individuals exposed to helminth infections may have allergic inflam- Corresponding Author: Antonio Cascio, MD; e-mail: [email protected] 1513 P.L. Minciullo, A. Cascio, A. David, L.M. Pernice, G. Calapai, S. Gangemi matory responses to parasites and parasite anti- for inclusion in the systematic review if it report- gens. Parasitic helminths in endemic areas tend ed data on patients with helminthiasis who had to cause chronic infections – individual adult par- signs or symptoms of anaphylaxis. asites may survive for many years in their human host – that are associated with few allergic-type reactions and a more tightly controlled Th2 re- Results sponse. Regulation of the Th2 response may be important for parasite survival and may allow the The PubMed search identified 609 papers. On- host to escape potentially damaging inflamma- ly four genera of helminths were associated with tion in the tissues6. anaphylaxis (Echinococcus spp, 302 papers; Today, it is largely assumed an inverse associ- Anisakis spp, 73 papers; Taenia solium cysticer- ation between helminth infection and allergy, al- cosis, 7 papers; and Ascaris spp., 243 papers). though helminths induce a polarized Th2 re- Echinococcosis in humans occurs as a result of sponse7,8. However, very little data are available infection by the larval stages of taeniid cestodes of to explain how helminth infection might protect the genus Echinococcus (E.). Six species have been against allergy. Some Authors demonstrated that recognized, but four are of public health concern: this protection involves immunoregulatory Echinococcus granulosus (which causes cystic mechanisms that block production of allergen- echinococcosis), E. multilocularis (which causes specific IgE9, with protection being mediated at alveolar echinococcosis), and E. vogeli and E. oli- least in part by the production of IL-10. Studies garthrus (which cause polycystic echinococcosis)14. on animal models showed that infection by E. granulosus is a cestode whose life cycle in- helminths as Schistosoma mansoni protects mice volves dogs and other canids as definitive hosts from an experimental model of systemic fatal for the intestinal tapeworm, as well as domestic anaphylaxis10. However, another study demon- and wild ungulates as intermediate hosts for the strated that Trichinella spiralis-infected mice had tissue-invading metacestode (larval) stage. The exacerbated anaphylaxis11. The differences be- metacestode (echinococcal cyst) is a fluid-filled, tween the studies could be due to the differences spherical, unilocular cyst15. Each cyst is sur- in the infectivity and immunity of the parasites rounded by a host-produced layer of granuloma- and in the allergy models used. tous adventitial reaction. Small vesicles called It is also known that helminths may be rare brood capsules bud internally from the germinal causes of acute and chronic urticaria, through an layer and produce multiple protoscolices by IgE mediated release of histamine12,13. Moreover, asexual division. In humans, the slowly growing anaphylactic reactions are extremely rare. hydatid cysts can attain a volume of several liters and contain many thousands of protoscolices. Literature Review With time, internal septations and daughter PubMed search of human cases of anaphylaxis cysts can form, disrupting the unilocular pattern occurring during helminthic diseases was per- typical of the young echinococcal cysts14. formed combining the terms (anaphylaxis, ana- It is well known that anaphylaxis, including phylactic, anaphylactoid) with each one of the urticaria, edema, and respiratory symptoms, may etiological agents indicated in Table I for the pe- occur in persons infected with E. granulosus. riod January 1950 to September 2012; references The first reports in literature about anaphylactic were also checked for relevant articles, including shock due to echinococcus infestation dates back review papers. A study was considered eligible to the 70’s16-18. Table I. Parasitic helminths. Ancylostoma spp, Angiostrongylus spp, Anisakis spp, Ascaris spp, Baylisascaris procyonis; Brugia spp; Clonorchis spp; Dicrocoelium dendriticum; Dioctophyme renale; Diphyllobothrium spp, Dirofilaria spp, Dracunculus medinensis, Echinococcus spp, Echinostoma echinatum, Enterobius vermicularis, Fasciola spp, Fasciolopsis buski, Gnathostoma spp, Hymenolepis nana, Hymenolepis diminuta, Loa loa, Mansonella streptocerca; Metagonimus sp, Necator americanus, Onchocerca volvulus, Opisthorchis spp, Paragonimus spp, Schistosoma spp, Spirometra erinaceieuropaei, Strongyloides stercoralis, Taenia spp, Thelazia spp, Toxocara spp, Trichinella spp, Trichobilharzia regenti, Trichuris trichiura, Wuchereria bancrofti 1514 Anaphylaxis caused by helminths: review of the literature Anaphylaxis may occur if fluid from the cyst is studied only in the late 1990s33, from then reports released into a host who has developed IgE from are becoming more and more widespread. A. previous leakage of fluid; a severe reaction can re- simplex. is one of the most frequent causes of sult from release of fluid from the cyst, either anaphylaxis in Countries were the use of raw fish spontaneously or after trauma or surgery19. Ana- is common30,34. In the literature there are several phylaxis complicates 10% of all intraperitoneal case reports about anaphylaxis due to Anisakis ruptures of cysts20. The prevalence of anaphylactic simplex34-42. Among the anaphylaxis occurred in shock during surgery treatment for cystic the Emergency Unit in Spain, A. simplex was re- echinococcosis consistently varies in the studies. sponsible in 10.8% of cases
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