Volume 17, Number 7—July 2011
Visceral Larva Migrans in Immigrants from Latin America
To determine whether increased migration is associated with an increase in incidence of toxocariasis (visceral larva migrans), we analyzed clinical data obtained from immigrants from Latin America. Although infection with Toxocara sp. roundworm larvae is distributed worldwide, seroprevalence is highest in tropical and subtropical areas.
Human toxocariasis is a zoonosis caused by the larvae of Toxocara sp. roundworms. Although distribution is worldwide, seroprevalence is highest in tropical countries, including in Latin America. Immigration from tropical areas to Europe continues to increase, with Spain a frequent destination. Data on visceral larva migrans (VLM) among immigrants from Latin America in western countries (primarily European countries, the United States, and Canada) are scarce. To determine whether increased migration is associated with increased VLM incidence, we analyzed clinical and epidemiologic data from immigrants from Latin America.
We analyzed information about 634 immigrants from Latin America seen at the Tropical Medicine Unit of the Ramón y Cajal Hospital in Madrid, Spain, during April 1989–June 2008. Immigrants who were visiting friends and relatives were excluded. Patients with VLM were identified.
We used 5 strict criteria for diagnosing VLM: 1) positive serologic test for Toxocara sp. roundworm infection, performed by using a commercial ELISA Toxocara immunoglobulin (Ig) G Ridascreen (R-Biopharm GmbH, Darmstadt, Germany), following the manufacturer’s recommendations; 2) absolute peripheral blood eosinophil count >500 cells/mm3; 3) exclusion of other parasites causing eosinophilia, such as intestinal nematodes, particularly Strongyloides stercoralis (excluded by larval culture and serology by ELISA IgG), Schistosoma sp., Fasciola hepatica, Trichinella spiralis, Taenia solium, Echinococcus granulosus, and cutaneous and blood microfilariae; 4) symptoms associated with VLM (respiratory signs, such as asthma, dyspnea, and eosinophilic pneumonia; dermatologic symptoms, including pruritus and recurrent urticaria; and abdominal symptoms, including abdominal pain and hepatomegaly); and 5) response to treatment with albendazole (10–15 mg/kg/d in 2 doses orally for 5 days) assessed 6 months after treatment, decreased titers to Toxocara sp. roundworm infection, decreased eosinophil count, and clinical improvement or resolution of symptoms.
The most frequent countries of origin for patients were Ecuador 221/634 (34.9%), Bolivia 176/634 (27.8%), Peru 71/634 (11.2%), and Colombia 56/634 (8.8%). Median age was 32 years (range 4–40 years); 421 (66.4%) patients were male. The median number of months from arrival in Spain to first consultation at the Tropical Medicine Unit was 19 months.
Eosinophilia was present in 135 (21.3%) patients. Toxocara antibodies were detected by ELISA in 31 (4.9%) patients. Concomitant serologic results positive for Toxocara sp. roundworm infection and eosinophilia were found in 28 (4.4%) patients; 606 patients were excluded. Of these 28 patients, 11 were excluded because of other concomitant parasitic infections that also can cause eosinophilia: 8 patients had positive ELISA results for S. stercoralis nematodes (not detected in fecal samples or larval culture); 1 had Ascaris lumbricoides eggs in feces; 1 had a positive indirect hemagglutination result but negative ELISA result for E. granulosus tapeworm; and 1 had a positive ELISA serologic result for T. spiralis nematodes. Another 12 patients were not included because detection of Strongyloides antibodies was not attempted. Only 4 of the 5 remaining cases fulfilled the strict inclusion criteria (Table); 1 patient was asymptomatic. After 6 months of treatment with albendazole, titers for Toxocara sp. roundworm infection and eosinophil count decreased, and symptoms improved or resolved for the 4 patients. Symptoms developed 3–18 months after arrival in Spain.
Clinical toxocariasis is rarely diagnosed in western countries as previously described despite evidence of environmental exposure (1). Results of seroprevalence surveys performed in healthy adults in France were positive for 2%–5% of persons in urban areas, compared with 14%–37% in rural areas (2). In Latin America, rates vary from 1.8% to 51.6% (3,4). However, literature references to VLM imported by immigrants are scarce (5), and the disease may be underdiagnosed in the immigrant population, partly because of nonspecific symptoms and the limitations of serologic diagnosis. In our study, serologic prevalence of Toxocara antibodies was 4.9% (31/634).
Toxocariasis is a common cause of eosinophilia in peripheral blood, although its absence does not exclude infection by Toxocara sp. roundworms. In other studies, 27% of patients had reactive serologic results for Toxocara sp. roundworm infection without eosinophilia (6); similarly, 27% of patients with high antibody titers had eosinophil counts within the reference range (7). By including only patients with eosinophilia, our study applied more stringent criteria. Thus, 28 (90%) of 31 patients who had positive serologic results showed an elevated eosinophil count, in accordance with previously described high Toxocara sp. roundworm seroprevalence (<68%) in patients with eosinophilia of unknown cause (8).
Eleven of the 28 patients with positive serologic results for Toxocara sp. roundworm and eosinophilia also had positive serologic results for other parasites that cause eosinophilia. One patient who was infected with A. lumbricoides roundworm had asthma, hepatomegaly, and pruritus. The latter is not usually associated with this parasite, which suggests possible co-infection.
Serologic tests for Toxocara sp. roundworm infection should be interpreted with caution because commercial ELISA kits that use excretory and secretory antigens derived from second-stage larvae of Toxocara sp. roundworms exhibit a sensitivity of 91% and a specificity of 86%; cross-reactivity has also been described with other nematode infections. The positive serologic results for T. spiralis nematodes and E. granulosus tapeworms may have been caused by cross-reactivity (9). These patients had asthenia and asthma, respectively, and symptoms resolved after treatment with albendazole. Eight patients with Strongyloides antibodies were also excluded; however, this finding does not exclude co-infection by both parasites. Finally, a limitation of the study was that we could not definitively exclude cryptic strongyloidiasis for 12 patients because of the difficulty in finding S. stercoralis threadworms in feces and because detection of Strongyloides antibodies was not possible.
Other authors have already recommended caution when interpreting positive Toxocara sp. roundworm serologic results in asymptomatic persons or persons with equivocal symptoms (10). Therefore, the asymptomatic patient with positive serologic and eosinophilia results was also excluded.
This study illustrates the difficulties in diagnosing VLM in immigrants from tropical and subtropical areas of Latin America because only a very small proportion of patients in the series (n = 4) had VLM. The most common symptoms were respiratory (3/4); 2 patients had asthma-like syndrome and 1 had chest pain followed by abdominal pain (2/4). Typical manifestations of VLM are abdominal symptoms (pain, hepatomegaly) and respiratory symptoms (severe asthma, eosinophilic infiltrates). In addition to this, evidence points to Toxocara sp. roundworm infection as a risk factor for asthma in some populations (11,12).
Albendazole is the treatment of choice for VLM; for practical purposes, it could be recommended for presumptive treatment in immigrants from Latin America with eosinophilia in whom strongyloidiasis is suspected (13). However, the superiority of ivermectin over albendazole has been documented in the treatment of chronic strongyloidiasis (14).
VLM may be difficult to diagnose, especially in immigrants from regions in Latin America where polyparasitism is endemic. Positive serologic test results, marked eosinophilia, absence of other helminthic infections, compatible clinical signs, and disappearance of symptoms after specific treatment can help establish a VLM diagnosis, especially in areas of low parasitism. VLM should be included in the differential diagnosis of eosinophilia in immigrants (children and adults) from tropical areas if respiratory or abdominal symptoms are evident. Albendazole is an effective and relatively safe drug that could be used to treat suspected VLM and other concomitant nematode infections, including cryptic S. stercoralis threadworm infections. Empirically described treatment may lead to resolution of clinical symptoms, even though ivermectin is a better treatment for chronic strongyloidiasis.
Dr Turrientes is a senior scientist in the microbiology department of the Hospital Universitario Ramón y Cajal in Madrid. Her research interests include parasitic diseases and the biology and evolution of microorganisms.
The Red de Investigación de Centros de Enfermedades Tropicales (RED: RD06/0021/0020) provided funding for this study.
- Sharghi N, Schantz PM, Caramico L, Ballas K, Teague BA, Hotez PJ, Environmental exposure to Toxocara as a possible risk factor for asthma: a clinic-based case-control study. Clin Infect Dis. 2001;32:e111–6.
- Magnaval JF, Glickman LT, Dorchies P, Morassin B. Highlights of human toxocariasis. Korean J Parasitol. 2001;39:1–11.
- Lynch NR, Eddy K, Hodgen AN, Lopez RI, Turner KJ. Seroprevalence of. Toxocara canis infection in tropical Venezuela. Trans R Soc Trop Med Hyg. 1988;82:275–81.
- Colli CM, Rubinsky-Elefant G, Paludo ML, Falavigna DL, Guilherme EV, Mattia S, Serological, clinical and epidemiological evaluation of toxocariasis in urban areas of south Brazil. Rev Inst Med Trop Sao Paulo. 2010;52:69–74.
- Huerga Aramburu H, Lópéz-Vélez R. Comparative study of infectious diseases in immigrant children from various countries. An Pediatr (Barc). 2004;60:16–21.
- Ishida MM, Rubinsky-Elefant G, Ferreira AW, Hoshino-Shimizu S, Vaz AJ. Helminth antigens (Taenia solium, Taenia crassiceps, Toxocara canis, Schistosoma mansoni, and Echinococcus granulosus) and cross-reactivities in human infections and immunized animals. Acta Trop. 2003;89:73–84.
- Taylor MR, Keane CT, O’Connor P, Mulvihill E, Holland C. The expanded spectrum of toxocaral disease. Lancet. 1988;331:692–5.
- Kwon NH, Oh MJ, Lee SP, Lee BJ, Choi DC. The prevalence and diagnostic value of toxocariasis in unknown eosinophilia. Ann Hematol. 2006;85:233–8.
- Nasrieh MA, Abdel-Hafez SK. Echinococcus granulosus in Jordan: assessment of various antigenic preparations for use in the serodiagnosis of surgically confirmed cases using enzyme immuno assays and the indirect haemagglutination test. Diagn Microbiol Infect Dis. 2004;48:117–23.
- Smith H, Holland C, Taylor M, Magnaval J-F, Schantz P, Maizels R. How common is human toxocariasis? Towards standardizing our knowledge. Trends Parasitol. 2009;25:182–8.
- Cooper PJ. Toxocara canis infection an important and neglected risk factor for asthma? Clin Exp Allergy. 2008;38:551–3.
- Ferreira MU, Rubinsky-Elefant G, de Castro TG, Hoffmann EH, da Silva-Nunes M, Cardoso MA, Bottle feeding and exposure to Toxocara as risk factors for wheezing illness among under five Amazonian children: a population based cross-sectional study. J Trop Pediatr. 2007;53:119–24.
- Muennig P, Pallin D, Challah C, Khan K. The cost-effectiveness of ivermectin vs. albendazole in the presumptive treatment of strongyloidiasis in immigrants to the United States. Epidemiol Infect. 2004;132:1055–63.
- Suputtamongkol Y, Kungpanichkul N, Silpasakorn S, Beeching NJ. Efficacy and safety of a single-dose veterinary preparation of ivermectin versus 7-day high-dose albendazole for chronic strongyloidiasis. [PMID: 18023151]. Int J Antimicrob Agents. 2008;31:46–9.