Bloody Diarrhea Associated with Hookworm Infection in Traveler Returning to France from Myanmar
Identifieur interne : 000165 ( Pmc/Corpus ); précédent : 000164; suivant : 000166Bloody Diarrhea Associated with Hookworm Infection in Traveler Returning to France from Myanmar
Auteurs : Julie Brunet ; Jean-Philippe Lemoine ; Nicolas Lefebvre ; Julie Denis ; Alexander W. Pfaff ; Ahmed Abou-Bacar ; Rebecca J. Traub ; Bernard Pesson ; Ermanno CandolfiSource :
- Emerging Infectious Diseases [ 1080-6040 ] ; 2015.
Url:
DOI: 10.3201/eid2110.150695
PubMed: 26402483
PubMed Central: 4593448
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Bloody Diarrhea Associated with Hookworm Infection in Traveler Returning to France from Myanmar</title><author><name sortKey="Brunet, Julie" sort="Brunet, Julie" uniqKey="Brunet J" first="Julie" last="Brunet">Julie Brunet</name></author><author><name sortKey="Lemoine, Jean Philippe" sort="Lemoine, Jean Philippe" uniqKey="Lemoine J" first="Jean-Philippe" last="Lemoine">Jean-Philippe Lemoine</name></author><author><name sortKey="Lefebvre, Nicolas" sort="Lefebvre, Nicolas" uniqKey="Lefebvre N" first="Nicolas" last="Lefebvre">Nicolas Lefebvre</name></author><author><name sortKey="Denis, Julie" sort="Denis, Julie" uniqKey="Denis J" first="Julie" last="Denis">Julie Denis</name></author><author><name sortKey="Pfaff, Alexander W" sort="Pfaff, Alexander W" uniqKey="Pfaff A" first="Alexander W." last="Pfaff">Alexander W. Pfaff</name></author><author><name sortKey="Abou Bacar, Ahmed" sort="Abou Bacar, Ahmed" uniqKey="Abou Bacar A" first="Ahmed" last="Abou-Bacar">Ahmed Abou-Bacar</name></author><author><name sortKey="Traub, Rebecca J" sort="Traub, Rebecca J" uniqKey="Traub R" first="Rebecca J." last="Traub">Rebecca J. Traub</name></author><author><name sortKey="Pesson, Bernard" sort="Pesson, Bernard" uniqKey="Pesson B" first="Bernard" last="Pesson">Bernard Pesson</name></author><author><name sortKey="Candolfi, Ermanno" sort="Candolfi, Ermanno" uniqKey="Candolfi E" first="Ermanno" last="Candolfi">Ermanno Candolfi</name></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">26402483</idno><idno type="pmc">4593448</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4593448</idno><idno type="RBID">PMC:4593448</idno><idno type="doi">10.3201/eid2110.150695</idno><date when="2015">2015</date><idno type="wicri:Area/Pmc/Corpus">000165</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000165</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Bloody Diarrhea Associated with Hookworm Infection in Traveler Returning to France from Myanmar</title><author><name sortKey="Brunet, Julie" sort="Brunet, Julie" uniqKey="Brunet J" first="Julie" last="Brunet">Julie Brunet</name></author><author><name sortKey="Lemoine, Jean Philippe" sort="Lemoine, Jean Philippe" uniqKey="Lemoine J" first="Jean-Philippe" last="Lemoine">Jean-Philippe Lemoine</name></author><author><name sortKey="Lefebvre, Nicolas" sort="Lefebvre, Nicolas" uniqKey="Lefebvre N" first="Nicolas" last="Lefebvre">Nicolas Lefebvre</name></author><author><name sortKey="Denis, Julie" sort="Denis, Julie" uniqKey="Denis J" first="Julie" last="Denis">Julie Denis</name></author><author><name sortKey="Pfaff, Alexander W" sort="Pfaff, Alexander W" uniqKey="Pfaff A" first="Alexander W." last="Pfaff">Alexander W. Pfaff</name></author><author><name sortKey="Abou Bacar, Ahmed" sort="Abou Bacar, Ahmed" uniqKey="Abou Bacar A" first="Ahmed" last="Abou-Bacar">Ahmed Abou-Bacar</name></author><author><name sortKey="Traub, Rebecca J" sort="Traub, Rebecca J" uniqKey="Traub R" first="Rebecca J." last="Traub">Rebecca J. Traub</name></author><author><name sortKey="Pesson, Bernard" sort="Pesson, Bernard" uniqKey="Pesson B" first="Bernard" last="Pesson">Bernard Pesson</name></author><author><name sortKey="Candolfi, Ermanno" sort="Candolfi, Ermanno" uniqKey="Candolfi E" first="Ermanno" last="Candolfi">Ermanno Candolfi</name></author></analytic><series><title level="j">Emerging Infectious Diseases</title><idno type="ISSN">1080-6040</idno><idno type="eISSN">1080-6059</idno><imprint><date when="2015">2015</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><back><div1 type="bibliography"><listBibl><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct></listBibl></div1></back></TEI><pmc article-type="letter"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Emerg Infect Dis</journal-id><journal-id journal-id-type="iso-abbrev">Emerging Infect. Dis</journal-id><journal-id journal-id-type="publisher-id">EID</journal-id><journal-title-group><journal-title>Emerging Infectious Diseases</journal-title></journal-title-group><issn pub-type="ppub">1080-6040</issn><issn pub-type="epub">1080-6059</issn><publisher><publisher-name>Centers for Disease Control and Prevention</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">26402483</article-id><article-id pub-id-type="pmc">4593448</article-id><article-id pub-id-type="publisher-id">15-0695</article-id><article-id pub-id-type="doi">10.3201/eid2110.150695</article-id><article-categories><subj-group subj-group-type="heading"><subject>Letters to the Editor</subject></subj-group><subj-group subj-group-type="article-type"><subject>Letter</subject></subj-group><subj-group subj-group-type="TOC-title"><subject>Bloody Diarrhea Associated with Hookworm Infection in Traveler Returning to France from Myanmar</subject></subj-group></article-categories><title-group><article-title>Bloody Diarrhea Associated with Hookworm Infection in Traveler Returning to France from Myanmar</article-title><alt-title alt-title-type="running-head">Bloody Diarrhea Associated with Hookworm Infection</alt-title></title-group><contrib-group><contrib contrib-type="author" corresp="yes"><name><surname>Brunet</surname><given-names>Julie</given-names></name></contrib><contrib contrib-type="author"><name><surname>Lemoine</surname><given-names>Jean-Philippe</given-names></name></contrib><contrib contrib-type="author"><name><surname>Lefebvre</surname><given-names>Nicolas</given-names></name></contrib><contrib contrib-type="author"><name><surname>Denis</surname><given-names>Julie</given-names></name></contrib><contrib contrib-type="author"><name><surname>Pfaff</surname><given-names>Alexander W.</given-names></name></contrib><contrib contrib-type="author"><name><surname>Abou-Bacar</surname><given-names>Ahmed</given-names></name></contrib><contrib contrib-type="author"><name><surname>Traub</surname><given-names>Rebecca J.</given-names></name></contrib><contrib contrib-type="author"><name><surname>Pesson</surname><given-names>Bernard</given-names></name></contrib><contrib contrib-type="author"><name><surname>Candolfi</surname><given-names>Ermanno</given-names></name></contrib><aff id="aff1">Hôpitaux Universitaires de Strasbourg, Strasbourg, France (J. Brunet, J.-P. Lemoine, N. Lefebvre, J. Denis, A.W. Pfaff, A. Abou-Bacar, B. Pesson, E. Candolfi);</aff><aff id="aff2">Université de Strasbourg, Strasbourg (J. Brunet, A.W. Pfaff, E. Candolfi);</aff><aff id="aff3">University of Melbourne, Parkville, Victoria, Australia (R.J. Traub)</aff></contrib-group><author-notes><corresp id="cor1">Address for correspondence: Julie Brunet, Institut de Parasitologie et Pathologie Tropicale, EA 7292, Fédération de Médecine Translationelle, Université de Strasbourg, 3 rue Koeberlé, 67000 Strasbourg, France; e-mail: <email xlink:href="jbrunet@unistra.fr">jbrunet@unistra.fr</email></corresp></author-notes><pub-date pub-type="ppub"><month>10</month><year>2015</year></pub-date><volume>21</volume><issue>10</issue><fpage>1878</fpage><lpage>1879</lpage><kwd-group kwd-group-type="author"><title>Keywords: </title><kwd>Ancylostoma ceylanicum</kwd><kwd>hookworm</kwd><kwd>infection</kwd><kwd>bloody diarrhea</kwd><kwd>tourist</kwd><kwd>parasites</kwd><kwd>zoonoses</kwd><kwd>Myanmar</kwd></kwd-group></article-meta></front><body><p><bold>To the Editor:</bold> Human hookworm infections are commonly caused by 2 anthroponotic species, <italic>Necator americanus</italic> and <italic>Ancylostoma duodenale</italic>. However, <italic>A. ceylanicum</italic>, a zoonotic hookworm of canids and felids, is emerging as the second most common human hookworm in Southeast Asia (<xref rid="R1" ref-type="bibr"><italic>1</italic></xref><italic>–</italic><xref rid="R4" ref-type="bibr"><italic>4</italic></xref>). Two haplotypes of <italic>A</italic>. <italic>ceylanicum</italic> hookworm have been identified, 1 specific to humans and 1 specific to humans, dogs, and cats (<xref rid="R4" ref-type="bibr"><italic>4</italic></xref><italic>,</italic><xref rid="R5" ref-type="bibr"><italic>5</italic></xref>). We report a case of patent enteric <italic>A. ceylanicum</italic> hookworm infection in a man from France who had visited Myanmar.</p><p>In December 2014, a 33-year-old man with no medical history sought care in France after 3 weeks of fever, vomiting, dyspnea, bloody diarrhea, and weight loss (7 kg). He had returned from a 3-week trip to Myanmar 1 month earlier. Two days after his arrival in Myanmar, he had pruritic erythematous macules on the buttocks after sitting in a public park in Rangoon while wearing short pants; this sign was followed by a dry cough.</p><p>Laboratory data showed leukocytosis (17.43 × 10<sup>9</sup> cells/L) with hypereosinophilia (55%) and a hemocrit of 56.1%. Direct examination of hemorrhagic stool showed numerous Charcot-Leyden crystals (CLCs) and 150–200 eggs/g feces of unembryonated hookworm ova (mean size 57.6 × 38.4 µm) (<xref ref-type="fig" rid="F1">Figure</xref>, panel A). Rhabditiform and filariform larvae were isolated by stool culture (<xref ref-type="fig" rid="F1">Figure</xref>, panel B). On the basis of clinical history and data suggestive of eosinophilic enteritis, which is uncommon in patients infected with parasites adapted to humans, a zoonotic hookworm species was suspected.</p><fig id="F1" fig-type="figure" position="float"><label>Figure</label><caption><p><italic>Ancylostoma ceylanicum</italic> hookworm isolated from a French tourist returning from Myanmar. A) Ova and blood cells in fecal specimen. B) Filiform larvae after stool culture. Original magnifications ×40.</p></caption><graphic xlink:href="15-0695-F"></graphic></fig><p>For species identification, DNA was extracted from larvae by using the DNeasy Tissue Kit (QIAGEN, Hilden, Germany) at the Faculty of Veterinary and Agricultural Sciences, University of Melbourne (Parkville, Victoria, Australia) and subjected to PCR specific for the ribosomal internal transcribed spacer region of hookworms (<xref rid="R1" ref-type="bibr"><italic>1</italic></xref>). Testing was conducted at the University of Melbourne because this institution has the technical expertise for identifying hookworm. In addition, haplotype characterization was performed by using PCR specific for the mitochondrial cytochrome oxidase-1 gene (<xref rid="R4" ref-type="bibr"><italic>4</italic></xref>). Bidirectional DNA sequences of PCR products (Macrogen Inc., Seoul, South Korea) were analyzed by using Finch TV 1.4.0 (Geospiza Inc., Seattle, WA, USA). The ribosomal internal transcribed spacer region had 100% sequence identity with an <italic>A. ceylanicum</italic> sequence in GenBank (DQ381541). Neighbor-joining analyses with MEGA 4.1 (<ext-link ext-link-type="uri" xlink:href="http://www.megasoftware.net">http://www.megasoftware.net</ext-link>) clustered the isolate within the <italic>A. ceylanicum</italic> haplotype specific for animals and humans (<xref rid="R4" ref-type="bibr"><italic>4</italic></xref>).</p><p>By the third day of albendazole therapy (400 mg/d), clinical improvement was observed and stool specimens were negative for hookworm ova. However, eosinophilia (59%) was persistent. Three months later, the patient was hospitalized because of diarrhea and abdominal pain. CLCs and hookworm ova were observed, and the patient received a second course of albendazole.</p><p><italic>A. ceylanicum</italic> hookworm was unequivocally identified by using molecular methods as the etiologic cause of the original signs and symptoms for this patient. In Asia, <italic>A. ceylanicum</italic> hookworm is reported at a prevalence of 62%–92% in stray dogs and cats (<xref rid="R3" ref-type="bibr"><italic>3</italic></xref>) and environmental contamination of the public park by dog feces was the probable source of infection for this patient.</p><p><italic>A. ceylanicum</italic> hookworms have been experimentally shown to develop to patency in humans within 26–35 days (<xref rid="R6" ref-type="bibr"><italic>6</italic></xref>), but abdominal symptoms and eosinophilia may occur earlier (within 21 days). Natural human infections have been described in most regions where <italic>A. ceylanicum</italic> hookworm is endemic to animals, but clinical and pathologic data are scarce. In Taiwan and Malaysia, this hookworm was visualized in the mid-jejunum in patients with acute, severe abdominal pain and nausea and in terminal ileum in patients with anemia caused by chronic blood loss, nausea, and melena (<xref rid="R7" ref-type="bibr"><italic>7</italic></xref><italic>–</italic><xref rid="R9" ref-type="bibr"><italic>9</italic></xref>).</p><p>In all cases, leukocytosis with eosinophilia (22%–50%) was observed. In the patient we describe, transdermal infection causing cutaneous larva migrans was followed by development of eosinophilic enteritis within a 2-week period. Enteric signs were similar to those observed in previous cases in Taiwan. A 3-day course of benzimidazole is the anthelminthic drug of choice. However, clinicians must be aware of possible relapse, potentially caused by failure of the adulticidal drug to kill developing larvae before full patency is reached (<xref rid="R3" ref-type="bibr"><italic>3</italic></xref><italic>,</italic><xref rid="R8" ref-type="bibr"><italic>8</italic></xref><italic>,</italic><xref rid="R9" ref-type="bibr"><italic>9</italic></xref>).</p><p>Differentiation of larvae and eggs of anthroponotic and zoonotic <italic>Ancylostoma</italic> spp. is difficult. Definitive diagnosis relies on detailed morphologic identification of adult worms or molecular identification of adults, eggs, or larvae in stool specimens. Thus, human infection in travelers returning from parasite-endemic regions is likely to be misdiagnosed as an anthroponotic hookworm species. Clinically, the presence of hookworm ova and an unusually high number of CLCs and eosinophils in stool should alert clinicians to the possibility of an infection with <italic>A. ceylanicum</italic> hookworm.</p><p><italic>A. ceylanicum</italic> hookworm is reported primarily in tropical climates; the possibility of spread in temperate countries remains low because development of filariforme larva requires high temperatures and a moist environment. However, recent climate changes, coupled with poor sanitary conditions, could promote emergence of tropical species, and recently, rare cases of autochthonous hookworm-related cutaneous larva migrans have been reported in Europe (<xref rid="R10" ref-type="bibr"><italic>10</italic></xref>).</p><p>This report highlights the risk for zoonotic ancylostomiasis in travelers visiting countries to which <italic>A. ceylanicum</italic> hookworm is endemic among animals. It also emphasizes the usefulness of copromolecular techniques for species-specific diagnosis.</p></body><back><fn-group><fn fn-type="citation"><p><italic>Suggested citation for this article</italic>: Brunet J, Lemoine J.P, Lefebvre N, Denis J, Pfaff AW, Abou-Bacar A, et al. Bloody diarrhea associated with hookworm infection in traveler returning to France from Myanmar [letter]. 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