Clinical Features Associated with Strongyloidiasis in Migrants and the Potential Impact of Immunosuppression: A Case Control Study

Strongyloides stercoralis is a widely distributed nematode more frequent in tropical areas and particularly severe in immunosuppressed patients. The aim of this study was to determine factors associated with strongyloidiasis in migrants living in a non-endemic area and to assess the response to treatment and follow-up in those diagnosed with the infection. We performed a multicenter case-control study with 158 cases and 294 controls matched 1:2 by a department service. Participants were recruited simultaneously at six hospitals or clinics in Spain. A paired-match analysis was then performed looking for associations and odds ratios in sociodemographic characteristics, pathological background, clinical presentation and analytical details. Cases outcomes after a six-month follow-up visit were also registered and their particularities described. Most cases and controls came from Latin America (63%–47%) or sub-Saharan Africa (26%–35%). The number of years residing in Spain (9.9 vs. 9.8, p = 0.9) and immunosuppression status (30% vs. 36.3%, p = 0.2) were also similar in both groups. Clinical symptoms such as diffuse abdominal pain (21% vs. 13%, p = 0.02), and epigastralgia (29% vs. 18%, p < 0.001); along with a higher eosinophil count (483 vs. 224 cells/mL in cases and controls, p < 0.001) and the mean total Immunoglobulin E (IgE) (354 U/L vs. 157.9 U/L; p < 0.001) were associated with having strongyloidiasis. Finally, 98.2% percent of the cases were treated with ivermectin in different schedules, and 94.5% met the cure criteria at least six months after their first consultation. Abdominal pain, epigastralgia, eosinophilia, increased levels of IgE and Latin American origin remain the main features associated with S. stercoralis infection, although this association is less evident in immunosuppressed patients. The appropriate follow-up time to evaluate treatment response based on serology titers should be extended beyond 6 months if the cure criteria are not achieved.

[1]  I. Molina,et al.  Strongyloidiasis screening in migrants living in Spain: systematic review and meta‐analysis , 2019, Tropical medicine & international health : TM & IH.

[2]  F. Salvador,et al.  High Prevalence of Strongyloidiasis in Spain: A Hospital-Based Study , 2019, bioRxiv.

[3]  P. Chiodini,et al.  Multiple-dose versus single-dose ivermectin for Strongyloides stercoralis infection (Strong Treat 1 to 4): a multicentre, open-label, phase 3, randomised controlled superiority trial. , 2019, The Lancet. Infectious diseases.

[4]  R. López-Vélez,et al.  Imported strongyloidiasis: Data from 1245 cases registered in the +REDIVI Spanish Collaborative Network (2009-2017) , 2019, PLoS neglected tropical diseases.

[5]  G. Schwarzer,et al.  Prevalence of strongyloidiasis and schistosomiasis among migrants: a systematic review and meta-analysis. , 2019, The Lancet. Global health.

[6]  Ethel Sequeira-Aymar,et al.  [Recommendations for the screening for infectious diseases, mental health, and female genital mutilation in immigrant patients seen in Primary Care]. , 2019, Atencion primaria.

[7]  Ingrid Arevalo-Rodriguez,et al.  Effectiveness of Screening and Treatment Approaches for Schistosomiasis and Strongyloidiasis in Newly-Arrived Migrants from Endemic Countries in the EU/EEA: A Systematic Review , 2018, International journal of environmental research and public health.

[8]  A. Hassan,et al.  Knowledge, attitude and practice with respect to soil contamination by Soil-Transmitted Helminths in Ibadan, Southwestern Nigeria , 2018, Parasite epidemiology and control.

[9]  R. López-Vélez,et al.  Community screening campaign for Strongyloides stercoralis among Latin American immigrants in Spain. , 2018, Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases.

[10]  F. Gobbi,et al.  Accuracy of molecular biology techniques for the diagnosis of Strongyloides stercoralis infection—A systematic review and meta-analysis , 2018, PLoS neglected tropical diseases.

[11]  M. Díaz-Menéndez,et al.  Management of severe strongyloidiasis attended at reference centers in Spain , 2018, PLoS neglected tropical diseases.

[12]  J. Llenas-García,et al.  Strongyloides stercoralis infection in a Spanish regional hospital: Not just an imported disease. , 2018, Enfermedades infecciosas y microbiologia clinica.

[13]  F. Salvador,et al.  Surveillance of strongyloidiasis in Spanish in-patients (1998–2014) , 2017, PloS one.

[14]  Z. Bisoffi,et al.  Evidence-Based Guidelines for Screening and Management of Strongyloidiasis in Non-Endemic Countries. , 2017, The American journal of tropical medicine and hygiene.

[15]  J. Utzinger,et al.  StrongNet: An International Network to Improve Diagnostics and Access to Treatment for Strongyloidiasis Control , 2016, PLoS neglected tropical diseases.

[16]  D. Malvy,et al.  Strongyloidiasis in a young French woman raises concern about possible ongoing autochthonous transmission in Spain. , 2016, International journal of infectious diseases : IJID : official publication of the International Society for Infectious Diseases.

[17]  T. Nutman,et al.  Accuracy of Five Serologic Tests for the Follow up of Strongyloides stercoralis Infection , 2015, PLoS neglected tropical diseases.

[18]  Santhosh Puthiyakunnon,et al.  Strongyloidiasis—An Insight into Its Global Prevalence and Management , 2014, PLoS neglected tropical diseases.

[19]  J. Saugar,et al.  Usefulness of Strongyloides stercoralis serology in the management of patients with eosinophilia. , 2014, The American journal of tropical medicine and hygiene.

[20]  Xavier Ramos,et al.  Strongyloides stercoralis, the hidden worm. Epidemiological and clinical characteristics of 70 cases diagnosed in the North Metropolitan Area of Barcelona, Spain, 2003-2012. , 2013, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[21]  P. Vounatsou,et al.  Strongyloides stercoralis: Global Distribution and Risk Factors , 2013, PLoS neglected tropical diseases.

[22]  P. Chiodini,et al.  Strongyloides stercoralis: A Plea for Action , 2013, PLoS neglected tropical diseases.

[23]  F. Gobbi,et al.  Severe strongyloidiasis: a systematic review of case reports , 2013, BMC Infectious Diseases.

[24]  P. Chiodini,et al.  The Laboratory Diagnosis and Follow Up of Strongyloidiasis: A Systematic Review , 2013, PLoS neglected tropical diseases.

[25]  F. Gobbi,et al.  Imported Strongyloidiasis: Epidemiology, Presentations, and Treatment , 2012, Current Infectious Disease Reports.

[26]  Charu Sawhney,et al.  Strongyloides stercoralis: there but not seen , 2010, Current opinion in infectious diseases.

[27]  Tigran Nikoghosyan,et al.  United Nations Children’s Fund (UNICEF) , 2018, Yearbook of International Cooperation on Environment and Development 1998–99.

[28]  C. Olmos,et al.  Endemic strongyloidiasis on the Spanish Mediterranean coast. , 2001, QJM : monthly journal of the Association of Physicians.

[29]  R. Genta,et al.  Strongyloidiasis in US veterans of the Vietnam and other wars. , 1987, JAMA.