Molecular diagnosis of polycystic echinococcosis due to Echinococcus vogeli in a Paraguayan
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1 JCM Accepts, published online ahead of print on 3 July 2013 J. Clin. Microbiol. doi: /jcm Copyright 2013, American Society for Microbiology. All Rights Reserved. 1 2 Molecular diagnosis of polycystic echinococcosis due to Echinococcus vogeli in a Paraguayan immigrant in Argentina F. Grenouillet 1,2#, B. Frider 3, J. Alvarez Rodriguez 4, M. Amante 5, M.L. Pestalardo 5, A. Cazorla 1, S. Bresson Hadni 1,2, L. Millon 1,2 1. WHO Collaborating Centre for Prevention and Treatment of Human Echinococcosis, French National Reference Centre for Alveolar Echinococcosis - Parasitology-Mycology Department, University Hospital, Besançon, France 2. Chrono-Environnement UMR 6249 Research Team, CNRS-University of Franche-Comté, Besançon, France 3. Hepatology-Medicine departement, Cosme Argerich Hospital, Buenos Aires, Argentina 4. Digestive surgery department, Cosme Argerich Hospital, Buenos Aires, Argentina 5. Pathology department, Cosme Argerich Hospital, Buenos Aires, Argentina Running title : Echinococcosis due to Echinococcus vogeli in Argentina # Corresponding author : Dr Frédéric Grenouillet, WHO Collaborating Centre for Prevention and Treatment of Human Echinococcosis, French National Reference Centre for Alveolar Echinococcosis - Parasitology- Mycology Department, University Hospital Besançon, Boulevard Fleming, Besançon, France Tel : ; fax : ; fgrenouillet@chu-besancon.fr
2 ABSTRACT Polycystic echinococcosis due to Echinococcus vogeli is a rare parasitic infection that occurs in rural areas of Central and South America. Only molecular identification performed on formalinfixed paraffin-embedded liver tissue gave an unequivocal diagnosis of this disease in a Paraguayan immigrant in Argentina. CASE REPORT A 37-year old male immigrant from Paraguay presenting with jaundice and abdominal pain in the right hypochondriac region was hospitalized in Cosme Argerich Hospital, Buenos Aires, Argentina. An abdominal CT-scan revealed a large hypodense liver lesion (11 x 7 cm) in segments IV and VIII, with multiple cystic vesicles, and irregular margins (Figure 1). No cystic lesions were observed in the abdominal cavity or chest. The biliary obstruction was initially treated with percutaneous biliary drainage; a secondary infection of the lesion followed this. The abscess was drained percutaneously and a biopsy was taken from its peripheral margin. The biopsy revealed the presence of cyst layers evoking echinococcosis, but there was no evidence of scolices or rostellar hooks. Diagnosis of echinococcosis was confirmed by positive serology: Elisa using Echinococcus granulosus crude fluid antigen (Bordier Affinity Products, Crissier, Switzerland), immunoelectrophoresis with arc 5 positivity (crude E. granulosus cyst fluid antigen), and Western Blot (LD Bio Products, Lyon, France) (Figure 2). At radiological imaging and analysis of pathological data, alveolar echinococcosis (AE) was first hypothesized, although the patient had never been in the Northern Hemisphere. The patient was discharged with albendazole treatment (800 mg/day). Because of persistent suppurative drainage, atypical surgical liver resection that included segments IV and VIII was performed 7 months later; the biliary
3 catheter was left in place. Histopathology of the operative liver specimen confirmed the hypothesis of AE. There was a polycystic lesion, showing cyst layers surrounded by granulomatous reaction with histiocytes (Figure 3). Because of the postoperative biliary fistula, surgeons performed a right hepatectomy. The patient was discharged with albendazole treatment and his follow-up stopped. He died two years later from pneumonia, with AIDS co-infection. Parasite DNA was extracted from formalin-fixed, paraffin-embedded (FFPE) operative liver tissue (five cuts, tissue area 2 cm 2, thickness 5 µm), using NucleoSpin Tissue (Macherey- Nagel, Düren, Germany) with a xylene pre-treatment step following manufacturer s recommendations. Two PCRs were conducted for amplification of Echinococcus mitochondrial DNA (mdna), respectively a 155 bp DNA fragment cytochrome b (cob) using previously described forward primer Cob-f (5 -GTCAGATGTCTTATTGGGCTGC-3 ) (1) and a new reverse primer Cob-r2 (5 -AAACCCCAAACAAATATGAACC-3 ), and a 276 bp target on mitochondrial cytochrome c oxidase subunit 1 (cox1) using EgCoxI-876F (5 - GTTTACTGTTGGGTTGGATG-3 ) and previously published EgCOI-F (5 - TAACGACATAACATAATGAAAATG-3 ) (2). Amplicons were sequenced using a BigDye Terminator v3.1 kit (Applied Biosystems, Foster City, CA, USA) with the same primers used in the PCR step using the ABI Prism 3130 DNA analyzer (Applied Biosystems). Sequences were compared to those available in the GenBank database using BLAST software ( Both sequences showed 100% homology with the E. vogeli complete mitochondrial genome (GenBank Access Number AB208546) (3). Percent identities with other Echinococcus species were much lower: 88% for Cob and 92% for Cox1 with Echinococcus oligarthus, 89% and 91% with Echinococcus multilocularis, 91% and 93% with species belonging to E. granulosus sensu lato group, respectively. Thus a retrospective diagnosis of polycystic echinococcosis (PE) due to E. vogeli was made.
4 DISCUSSION Echinococcus vogeli is a neotropical parasite which causes polycystic echinococcosis (PE) in humans in the rural areas of Central America and northern South America, mainly in Brazil. E. vogeli is found in humid tropical forests and has primarily a sylvatic life cycle involving bush dogs (Speothos venaticus) and domestic dogs (Canis familiaris) as definitive hosts, and pacas (Cuniculus paca) and agouti (Dasyprocta aguti) as natural intermediate hosts (4). Cystic echinococcosis (CE), due to E. granulosus, is highly endemic in livestock-raising countries of the southern part of South America, especially Argentina (5). One hundred and seventy-two cases of PE were reported up to 2007, but the actual prevalence of human PE has probably been underestimated (4, 6). Formal identification of parasite species based on morphology and size of parasite hooks was available in only one-third of cases, mainly E vogeli; cases were rare for its closely related species, Echinococcus oligarthus and E. granulosus (4). A century ago in Argentina, Marcelo Viñas reported several cases of multicystic parasitic hepatic disease, that he called alveolar echinococcus (7, 8). In these cases, as in the present case, the histopathology was very similar to that of AE but no Echinococcus hooks were observed. However, E. multilocularis, which causes AE, is now known to be restricted to temperate, holoarctic regions (9). Thus, Viñas s cases were later categorized as PE by others, although proof of E. vogeli infection was never formally established (4, 9). To our knowledge, our case is the first unequivocally proven case of PE due to E. vogeli diagnosed in Argentina. Our patient was originally from Paraguay but PE due to E. vogeli has never been reported in Paraguay, even though parasite intermediate hosts (pacas, agouti) are present in this country, and also in northern areas of Argentina (4). However, we could not determine the exact geographical origin of the patient s contamination, because he lived in rural areas of both countries. In highly
5 endemic CE countries such as Argentina (10), clinicians need to be aware that the diagnosis of PE is possible when multicystic lesions are observed, especially in immigrants originating from the rural areas of Central or northern South America. At present, there are no clear guidelines for the management of PE patients. E. vogeli is thought to be the most pathogenic species of the genus Echinococcus, associated with poor outcome (29% mortality rate) (4). As higher survival rates have been observed in patients treated surgically in combination with chemotherapy, a better management of PE would probably be to duplicate that of AE. It would include, therefore, radical surgery, if possible, as soon as possible, followed by long-term albendazole therapy (4, 11). Given the higher mortality risk of PE, diagnosis of the exact causative Echinococcus species is required when multicystic parasitic lesions are observed. No specific serological tools are available for E. vogeli. Patient serologies often show high reactivity against E. granulosus or E. multilocularis antigens, and without a specific species pattern, the diagnosis will only be that of echinococcosis. This lack of specificity could also lead to PE being misdiagnosed as CE or AE. (12, 13) Histopathology remains the gold standard for the diagnosis of PE, but the definitive diagnosis of E. vogeli infection cannot be made when hooks are not present, as was the case for our patient. Recently, molecular tools were used on a fresh operative specimen to confirm diagnosis of PE due to E. vogeli in a patient from French Guiana, and the results of the sequences were in agreement with hook morphology (14). In our case, the FFPE liver tissue was the only available specimen for further molecular study. Amplification failed using previously published pan- Echinococcus PCR targeting mdna genes (cox1, cob: data not shown) (1, 2, 4, 15) or E. vogeli specific PCR (14). As these techniques require amplification of long DNA fragments (>400 bp), we designed new primers, which target DNA polymorphic sequences (<300 bp), i.e. cox1 and
6 cob. Thus, we were able to identify E. vogeli on this sample. This underlines the difficulty of DNA extraction from FFPE (degradation of DNA, low yield of extraction of long DNA fragments) and the need for shorter PCR targets for identification of infectious agents using PCR and sequencing in FFPE tissue (16-18). An alternative qpcr approach that targets short mitochondrial DNA fragments could also be of interest on FFPE DNA extract, either by combining species-specific targets or by defining genus-specific system, followed by melting curve analysis for species diagnosis (19, 20). However, given the genetic variability of this parasite, the design of the specific primers and probes must be based on sequence data from a wide panel of E. vogeli samples (21). In this case report, we report the first proven case of PE from Paraguay, diagnosed by PCR followed by sequencing on FFPE tissue. This case underlines the difficulty in diagnosing PE in South America, especially in highly endemic areas of CE. PE must be suspected in any patient coming from an E. vogeli endemic area, who presents with multicystic lesions and a highly positive Echinococcus serology. Molecular tools and/or hook sizing must be used to make this differential diagnosis and to optimize patient management. Figure 1 - Computed tomography of liver at time of diagnosis: Large hypodense lesion (11.2 x 7.7 cm) in segments IV and VIII, with multiple cystic vesicles, irregular margins, without contrast enhancement at the margins. Figure 2 - Echinococcus Western Blot IgG (LDBioDiagnostics). Significant bands are indicated by arrows. Molecular sizes (in kda) are indicated on the right. Band 1: positive control serum (alveolar echinococcosis). Band 2: patient sera.
7 Figure 3 - Histopathology of liver resection tissue Close up of the polycystic lesion, showing parasitic laminated layer (black star), surrounded by chronic inflammatory reaction, with multinucleated giant cells (black arrows) and histiocytes (bar = 200 µm) using hematoxylin-eosin stain (Fig. 2B) Downloaded from on April 23, 2018 by guest
8 AKNOWLEDGMENTS: The authors declare that they do not have anything to disclose regarding funding or any other conflict of interest with respect to this manuscript. We are grateful to Florence Grenouillet for her excellent technical support. We thank Lois Rose, Didier Hocquet for their editorial assistance and Gloria Ragot for Spanish translating of Viñas papers Downloaded from on April 23, 2018 by guest
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