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Genotyping Approach for Potential Common Source of Enterocytozoon

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Genotyping Approach for Potential Common Source of Enterocytozoon SYNOPSIS Genotyping Approach for Potential Common Source of Enterocytozoon bieneusi Infection in Hematology Unit Guillaume Desoubeaux, Céline Nourrisson, Maxime Moniot, Marie-Alix De Kyvon, Virginie Bonnin, Marjan Ertault De La Bretonniére, Virginie Morange, Éric Bailly, Adrien Lemaignen, Florent Morio, Philippe Poirier Microsporidiosis is a fungal infection that generally causes wide range of host species (1,4). At least 16 microsporidian digestive disorders, especially in immunocompromised species have been described in humans, but Enterocytozoon hosts. Over a 4-day period in January 2018, 3 patients with bieneusi is the most common (5). However, little is known hematologic malignancies who were admitted to the hema- about the actual epidemiology of E. bieneusi microsporidi- tology unit of a hospital in France received diagnoses of En- osis, and there is a need for a better understanding of its terocytozoon bieneusi microsporidiosis. This unusually high pathophysiology and parasitic cycle (3,5). Unfortunately, incidence was investigated by sequence analysis at the in- ternal transcribed spacer rDNA locus and then by 3 micro- epidemiologic studies are complicated because E. bieneusi satellites and 1 minisatellite for multilocus genotyping. The infection has a low incidence rate worldwide (6), and its 3 isolates had many sequence similarities and belonged to microbiological diagnosis is difficult and likely often over- a new genotype closely related to genotype C. In addition, looked (7). In addition, the species is not easy to cultivate multilocus genotyping showed high genetic distances with in vitro in routine practice. Investigations can be carried out all the other strains collected from epidemiologically unre- directly only from infected biologic samples, which usually lated persons; none of these strains belonged to the new use DNA from fecal specimens (1,3,7). genotype. These data confirm the epidemiologic link among More than 250 genotypes of E. bieneusi have been the 3 patients and support a common source of infection. identified on the basis of their internal transcribed spacer (ITS) region (8,9). Depending on the ITS genotypes, zoo- icrosporidia are spore-forming eukaryotic and oppor- notic or host-adapted groups have been identified within Mtunistic intracellular pathogens related to fungi (1,2). species. Phylogenetic studies were able to distinguish >10 Microsporidiosis usually occurs in the form of isolated groups; most ITS genotypes belonged to group 1, which cases in immunocompromised patients, including HIV-in- contains genotypes found in both humans and animals, in- fected persons and solid-organ transplant recipients (1) but cluding cats, pigs, and cattle (2). However, ITS sequencing can also arise in travelers and is common in children in de- has certain limitations because the same ITS genotype can veloping countries. Infection causes digestive disorders, in- be isolated from different host species and from different cluding diarrhea (1,3). Microsporidia are orally transmitted regions. This possible strain diversity within 1 ITS geno- by interindividual contacts and likely less frequently trans- type cannot be addressed by a single sequence-based geno- mitted by foodborne or waterborne spores from excreta of a typing technique (10). In human and animal medicine, several molecular Author affiliations: Université de Tours, Tours, France techniques have been developed to investigate the epidemi- (G. Desoubeaux); CHU Bretonneau, Tours (G. Desoubeaux, ology of transmissible agents (11–15), such as multilocus M.-A. De Kyvon, M. Ertault De La Bretonniére, V. Morange, sequence typing (MLST) analysis or mini/microsatellite É. Bailly, A. Lemaignen); Université Clermont-Auvergne, Aubière, length polymorphism using short tandem-repeat markers. France (C. Nourrisson, M. Moniot, V. Bonnin, P. Poirier); CHU A MLST method was developed in 2011 to discriminate Gabriel-Montpied, Clermont-Ferrand, France (C. Nourrisson, among E. bieneusi isolates (16). Four loci were analyzed M. Moniot, P. Poirier); CHU Hôtel Dieu, Nantes, France (F. Morio); with 1 minisatellite (MS4) and 3 microsatellites (MS1, Université de Nantes, Nantes (F. Morio) MS3, and MS7). The combination of these 4 markers with DOI: https://doi.org/10.3201/eid2509.190311 the ITS genotype allows for the determination of multilocus Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 25, No. 9, September 2019 1625 SYNOPSIS genotypes (MLGs). MLG analyses are useful to discrimi- screened for microsporidia in the parasitology–mycology nate between isolates derived from various hosts (17) and laboratory of center 1. The first-line diagnostic procedure to detect mixed infections (18). used a real-time qualitative PCR (qPCR) that targets the To assess epidemiologic links among 3 cases of E. bi- 18S rRNA gene of E. bieneusi. We performed genomic eneusi infections occurring concomitantly in a single he- DNA extraction with the QIAmp DNA Stool Mini Kit matology unit in a hospital in France, we used the MLG (QIAGEN, https://www.qiagen.com), according to the analysis method. The results showed the utility of this ap- manufacturer’s instructions. We stored DNA extracts at proach in the investigation of a cluster of cases. –20°C until subsequent analysis. We completed amplifica- tion with Eb and Eb5 oligonucleotide primers at a final con- Materials and Methods centration of 0.5 µmol/L and detected the 180-bp product using the specific fluorescent TaqMan probe EbS2 in the Ethics LightCycler 480 II apparatus (Roche, https://www.roche. The study patients gave informed consent for the use of com) as described previously (7,21). We set the positive their samples in the research project. All their personal data cutoff value of qPCR at <39 quantitative cycles (Cq) and were anonymous. We received approval from the ethics tested each clinical sample in duplicate. We assessed in- committee of the University Hospital of Tours (Center 1, hibition with a positive exogenous internal control (Uni- Espace de Réflexion Éthique, Région Centre-Val de Loire, versal Inhibition Control Cy5; Diagenode, https://www. France). The study registration number 2015_003 was is- diagenode.com). We confirmed all samples with positive sued by the National Commission for Information Tech- qPCR results using microscopy with specific staining of nology and Individual Freedom (Commission Nationale de microsporidia spores by the Uvitex 2B brightener (Ciba- l’Informatique et des Libertés) on January 10, 2015. We Geigy, https://www.novartis.com) according to van Gool’s performed the study in accordance with the Code of Ethics method (22) (Appendix Figure 1, http://wwwnc.cdc.gov/ of the World Medical Association (Declaration of Helsin- EID/article/25/9/19-0311-App1.pdf). ki) and complied with BRISQ guidelines (19). We received technical and financial support from the French Microspo- Study Population and Biologic Samples ridiosis Network, assisted by the Clinical Research and In- In this study, we included all patients from center 1 who novation Department (DRCI) of the University Hospital were found to be positive for E. bieneusi detection dur- of Clermont-Ferrand (Center 2) and the French National ing January 2011–December 2018; they were considered Reference Center for Cryptosporidiosis. a priori to be epidemiologically unrelated to the 3 cluster cases (M01-05 to M01-07). We included 8 supplementary Context of the Study control cases in the study: 4 were provided by a second uni- Center 1 is a university hospital in France that contains versity hospital, center 2 (Clermont-Ferrand, France; lati- 2,008 inpatient beds and comprises 3 main sites spread tude 45.759549, longitude 3.089723), and the remaining over a distance of a few kilometers. The hematology unit 4 by another university hospital, center 3 (Nantes, France; is located in the Center for Adult Medicine (Tours, France; latitude 47.2121974, longitude –1.554346). latitude 47.3900474, longitude 0.6889268). Systematic sur- veillance and exhaustive registration of all cases of micro- Genotyping of Clinical E. bieneusi Strains sporidiosis began in the hospital in January 2011. During January 2011–January 2018, there were 33,769 inpatient Genotype Identification by Sequence Typing admissions. Only 2 cases of E. bieneusi were diagnosed in of ITS rDNA Region the hematology unit and the oncology department in pa- We amplified the DNA extract in a 25-µL final volume tients admitted in 2017; these cases occurred at different and sequenced it for the ITS rDNA region. For patients times. In contrast, 3 patients with hematologic malignan- with multiple positive samples, we tested only the first cies, designated M01-05 to M01-07, received diagnoses of sample by genotyping. We used the MSP3 and MSP4B E. bieneusi microsporidiosis during a 4-day period, January primers (23). ITS PCR products were purified and nucle- 12–16, 2018. otide sequencing performed on both strands by Eurofins Laboratories (https://www.eurofins.com). We compared Biologic Procedures for Routine Diagnosis the 243-bp sequences obtained with all E. bieneusi se- of E. bieneusi Infection quences available from the National Center for Biotech- All diarrheic fecal specimens and feces obtained from nology Information using the BLAST algorithm (http:// high-risk patients, including HIV-positive persons, solid- blast.ncbi.nlm.nih.gov/Blast.cgi). We performed the organ/bone-marrow transplant recipients, and patients with evolutionary analysis of E. bieneusi ITS genotypes with cancer or autoimmune diseases
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