Abstract

Strongyloidiasis is a soil‐transmitted helmithiasis with worldwide distribution. Contrary to chronic form, hyperinfestation and life‐threatening dissemination, first (invasive) stages of the disease are not well characterized. This paper describes two cases of acute strongyloidiasis in travelers returning from Southeast Asia and highlights the need to take strongyloidiasis into account also among acute travel‐related illnesses.

Strongyloidiasis is an intestinal nematode infection caused by Strongyloides stercoralis and occasionally Strongyloides fuellerborni. The disease is distributed worldwide, but more common in populations of the tropical and subtropical areas. 1,2 It is rarely observed in temperate regions 3,4 where it is more frequently described in migrants, expatriates, elderly local population and very occasionally in travelers. 5

Strongyloidiasis usually causes a chronic infection with mild, if any symptoms except in immunosuppressed patients who may suffer from the disseminated and almost invariably fatal form of disease. The symptoms and signs of chronic strongyloidiasis (abdominal pain, diarrhea, and urticaria) occur irregularly, often with prolonged asymptomatic intervals. The penetration phase usually does not give rise to skin signs, whereas little is known about the invasive (acute) stage of the disease which has been infrequently reported.

We describe two cases of invasive strongyloidiasis observed in a couple of Italian tourists returning from Thailand, Malaysia, and Singapore.

Case Description

Mr S.F. and Mrs P.F., respectively 32 and 29 years old, native of Apulia, South Italy, traveled to Southeast Asia (Malaysia, Singapore, and Thailand) on honeymoon from August 27 to September 12, 2008.

A few days after returning to Italy they developed a diffuse urticarial rash, itching, high fever, cough, and fatigue. The signs appeared 7 days after return in S.F. and 10 days in P.F. (incubation period after presumed exposure in Koh Samui Island, Thailand ranging from 7–11 and 10–14 d, respectively). The patients were admitted to the Infectious Disease Unit of Triggiano Hospital, Bari. They both had splenomegaly. Blood tests showed a marked eosinophilia in both patients (absolute eosinophil count 5,130 mm−3, 38.5% for S.F. and 5,740 mm−3, 37% for P.F; normal values <450 eosinophils mm−3, <7%), mild hepatic cytolysis (alanine aminotransferase 56 and 77 U/L, respectively, normal value <41 U/L), increased C‐reactive protein (108.2 and 49.1 mg/L, respectively, normal value <5 mg/L), and no other abnormal result. During hospitalization, they were treated with antibiotics and their clinical status partially improved, whereas the eosinophil counts further increased for both. They were then addressed to our center about 1 month after travel. On arrival, they still complained of itching, episodes of cough, and weakness. P.F. also showed transient urticaria. Eosinophilia was still present (absolute count 8,270 mm−3, 55% for S.F. and 8,700 mm−3, 60% for P.F.).

Rhabditoid larvae of S stercoralis were found in one of five stool samples provided by S.F. but in none of the five samples provided by P.F. (using Ritchie's fecal enrichment technique). Serology (an in‐house IFAT for S stercoralis, with 97.4% sensitivity and 97.9% specificity), 6 was positive, at minimum titer (ie, 1/20), only for S.F., whereas P.F. had a negative result. Fecal culture for S stercoralis resulted positive for both.

Patients were treated with ivermectin, 200 µg/kg/d for 2 days, repeated after 1 month. All clinical signs disappeared. After 6 months, both patients were asymptomatic, with normal eosinophil count. Serology was found positive at minimum titer (1/20 ) in both patients 1 month after discharge and resulted negative 3 and 6 months after treatment.

Discussion and Conclusions

We describe here the clinical and biological characteristics of acute strongyloidiasis, in a couple of travelers. This early invasive phase of human strongyloidiasis has never been reported in clinical settings, to our knowledge. Our two patients give the opportunity to more precisely describe this phase of the disease.

Strongyloidiasis was probably acquired in Thailand where the disease prevalence, depending on the diagnostic technique and population under study, ranges from 2.3 to 19.2% (respectively in schoolchildren from West‐Central Thailand and Thai workers who pursue overseas employment). 7,8

Patients did not visit any other disease‐endemic country before. We identified Koh Samui Island as the most likely site of infection. Indeed no bare skin exposure to humid soil was reported by the patients in Apulia where they came from or during travel in Malaysia, Singapore, and Bangkok where the patients always wore shoes.

In contrast, during the last 4 days spent in the tourist resort in Koh Samui Island, they reported walking barefoot on the grass around the bungalow. As Koh Samui is a very important touristic place, we may assume that other exposed travelers could have similarly acquired strongyloidiasis, an infection which goes largely under‐reported.

Little is known about the clinical manifestations of acute strongyloidiasis. Freedman gives a description of experimental infections in humans. 9 Interestingly, he noticed a transient skin reaction at the site of larval entry that appears almost immediately after exposure to the larvae and lasted 1 to 21 days depending on the study. Within 10 days after exposure, a larval migration syndrome or Loeffler's‐like syndrome with pulmonary symptoms (cough, tracheal irritation, and asthma) and skin signs (acute urticaria and itching) may occur. Gastrointestinal symptoms (diarrhea, constipation, anorexia, and abdominal pain) begin about 2 to 3 weeks after exposure and larvae are detectable in the stool after 21 to 28 days. Eosinophilia is usually observed. We interestingly recorded that mild splenomegaly and increased transaminase levels can be transiently present also during the early phase of infection while this has been previously described only in the hyperinfection syndrome or disseminated strongyloidiasis. 10 Strongyloidiasis is rarely described in travelers to endemic countries (2% in a German study on travelers with eosinophilia, 11 0.8% in a Belgian case series 5 ). More than one third of patients with imported chronic strongyloidiasis described by Nuesch and colleagues were travelers. 12 To our knowledge in the current literature no cases of acute strongyloidiasis are described in clinical settings.

These two cases thus underline the need to take into account acute strongyloidiasis as well as other invasive helminth infections (eg, schistosomiasis, trichinosis, fascioliasis, and toxocariasis) within the causes of urticaria and/or fever in returning travelers, particularly when eosinophilia is present. 13

Our cases confirm that not only migrants but also travelers may be at risk of acquiring strongyloidiasis and therefore potentially exposed to hyperinfection and disseminated, life‐threatening illness in case of immunosuppression and/or corticosteroid treatment. This is a real cause of concern given that physicians are largely unaware of strongyloidiasis and of its potential, life‐threatening complications. In a recent survey among US physicians‐in‐training, only 9% recognized the need for parasitic screening in a hypothetical case of strongyloidiasis and 23% advocated steroids for wheezing and eosinophilia. 14 If we add the low sensitivity of direct diagnostic methods, 6,15 with the consequent risk of missing the infection even when this is correctly suspected, the scenario becomes much more worrisome. As a consequence, the use of an antihelminthic drug efficient against strongyloidiasis (ivermectin, thiabendazole) might be discussed to prevent disseminated strongyloidiasis in all patients candidated to immunosuppression if they have been resident or traveled in disease‐endemic countries, regardless of the result of parasitic screening. 16

In conclusion, acute strongyloidiasis is a potential cause of fever and/or urticaria associated with eosinophilia in returning travelers. Western doctors should thus be aware of this unusual occurrence, potentially affecting also the travelers. Single exposure of the skin to garden terrain in apparently “safe” touristic resorts is a largely unknown risk factor for developing strongyloidiasis as well as hookworm infections and prevention measures should be discussed during pretravel advice. As the diagnosis is difficult during the invasive, acute phase, direct (stool) and indirect (serologic) examinations should be repeated up to at least 1 month after return.

Declaration of Interests

The authors state that they have no conflicts of interest to declare.

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