Armillifer Armillatus Pentastomiasis in African Immigrant, Germany
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LETTERS Armillifer of acute myeloid leukemia. He was sequenced, and BLAST analysis subsequently underwent stem cell (www.ncbi.nlm.hih.gov/blast) armillatus transplantation, which was followed confirmed 100% identity with A. Pentastomiasis in by graft versus host disease. The armillatus (GenBank accession no. African Immigrant, patient died of sudden intracerebral HM756289.1) and 99% homology hemorrhage and leukencephalopathy. with A. agkistrodontis (FJ607339.1) Germany His medical history also included and A. moniliformis (HM048870.1). To the Editor: Pentastomiasis a-thalassemia and a heterocygotous Visceral pentastomiasis in is a parasitic zoonotic disease with sickle cell trait, chronic hemolytic humans is often asymptomatic and an an incremental number of reported anemia, splenomegaly, and incidental finding during surgery 1,3( ) human infections caused by larval cardiomyopathy. He had been treated or autopsy (8,9). In a large autopsy stages (nymphs) of pentastomes for schistosomiasis and filariasis. series from Malaysia, a pentastomiasis (1–3). The vermiform parasites are An autopsy specimen showed prevalence of 45.5% was found in in their own phylum and are related several living pentastome nymphs adult Aborigines (8). In Nigeria, a rate to branchiuran crustaceans (2). Most of ≈2 cm in size, which were found of 33% was seen during autopsies of human infections with these parasites in the subscapular region of liver patients who had died of malignancies are caused by Armillifer armillatus parenchyma. A presumptive diagnosis (9). However, a few severe and even (2), a parasite endemic to western and of visceral pentastomiasis caused lethal cases have been described for central Africa. Most cases are reported by A. armillatus nymphs was made heavy A. armillatus and A. grandis from the Congo region and Nigeria, in accordance with the origin of the infections in persons from Africa (4,6). and occasionally infections in African patient and the geographic distribution Diagnosis is achieved by gross immigrants to Europe and North of the parasite. pathologic and histopathologic America have been reported (4,5). Microscopic slides from patient analyses. Nymphs are found in Imported cases to Germany have not specimens were retrieved from an the serosa around the liver and been reported. A. grandis, a related archive and reanalyzed (Figure; spleen, in liver parenchyma, parasite from central Africa, has been online Technical Appendix Figure, mesenterium, intestine wall, and rarely found (6), but A. moniliformis, wwwnc.cdc.gov/EID/article/19/3/12- abdominal lymph nodes. The lungs a pentastome species from Asia, has 1508-Techapp1.pdf). A pentastome- or pleura are occasionally infected recently reemerged and caused a specific PCR targeting the 18S rRNA (3). Radiographic analysis may human infection after ≈40 years in gene (2,7) was conducted after DNA show typical C-shaped chest or Malaysia (1). extraction from formalin-fixed tissue abdominal calcifications (10). Species Adult Armillifer spp. inhabit on a remaining unstained microscope identification is performed by counting the respiratory tract of large snakes slide. The resulting 383-bp amplicon annulations (A. armillatus 18–22, (Python spp.). These dioecious parasites produce large amounts of ova that are shed into the environment by snake feces and secretions. When intermediate hosts, such as rodents or other small mammals, ingest ova, larvae hatch, migrate to the viscera, encyst, and molt several times (3). Humans become accidental intermediate hosts after uptake of environmental parasite ova or by consumption of contaminated snake meat. We report an infection with A. armillatus in an African immigrant to Germany that was diagnosed Figure. Oblique cross-section of liver of a patient (immigrant) from Togo, showing a well- preserved Armillifer armillatus nymph in a subcapsular location. The annulated parasite by histopathologic analysis and is encapsulated by its shed cuticle (exuvia) and dense fibrosis. Consistent with the viable confirmed by PCR. type of a pentastomid lesion (3), no inflammatory infiltrate is visible. This image also shows In 2005, a 23-year-old man from internal structures of the pentastome, such as prominent bunches of acidophilic glands Togo who had immigrated to Germany surrounding the intestine (Masson’s trichrome stain, original magnification ×10). A color 3 years earlier showed development version of this figure is available online (wwwnc.cdc.gov/EID/article/19/3/12-1508-F1.htm). Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 19, No. 3, March 2013 507 LETTERS A. grandis >25) and measuring the Nocht-Institute for Tropical Medicine, Mycobacterium size of larval parasites (3). Recently, Hamburg, Germany (A. Haeupler, P. PCR has been used for diagnosis in Racz, S. Poppert); and University Medical kyorinense veterinary infections (2,7). Center Hamburg–Eppendorf, Hamburg (H. Infection For the patient in our study, Schäfer, J.P. Cramer) To the Editor: Mycobacterium molecular analysis identified human DOI: http://dx.doi.org/10.3201/eid1903.121508 pentastomiasis by using a formalin- kyorinense is a nonpigmented, slowly growing mycobacterium that was fixed microscope slide that had been References stored for 7 years. A difference of 2 initially isolated in 2007 from a patient nt each was seen when the amplified 1. Latif B, Omar E, Heo CC, Othman with pneumonia in Japan (1,2). The nucleotide sequence was compared N, Tappe D. Human pentastomiasis sequences of the 16S rRNA, hsp65, caused by Armillifer moniliformis in with database sequences of A. and rpoB genes of M. kyorinense Malaysian Borneo. Am J Trop Med were closely related to, but different agkistrodontis and A. moniliformis. Hyg. 2011;85:878–81. http://dx.doi. However, there is no database entry org/10.4269/ajtmh.2011.11-0404 from, those of the type strains of M. in GenBank for A. grandis, the 2. Tappe D, Meyer M, Oesterlein A, Jaye A, celatum and M. branderi, the 2 most Frosch M, Schoen C, et al. Transmission geographically closest Armillifer phylogenetically related species (1). of Armillifer armillatus ova at snake Biochemical tests, such as those species. Serologic assays have been farm, The Gambia, West Africa. Emerg developed for identification of A. Infect Dis. 2011;17:251–4. http://dx.doi. for arylsulfatase activity, tellurite armillatus (2), but no serum was org/10.3201/eid1702.101118 reduction, and heat-stable catalase, 3. Tappe D, Büttner DW. Diagnosis of available for retrospective analysis. also distinguish M. kyorinense from human visceral pentastomiasis. PLoS M. celatum and M. branderi. In our In special settings, such as tropical Negl Trop Dis. 2009;3:e320. http://dx.doi. snake farming and pet keeping, org/10.1371/journal.pntd.0000320 initial report, in which this species pentastomiasis may be a public health 4. Lavarde V, Fornes P. Lethal infection due was first recognized, we described 3 to Armillifer armillatus (Porocephalida): concern (2). However, most infections strains isolated from Japanese patients a snake-related parasitic disease. Clin (1). Recently, 1 additional case have been linked to consumption of Infect Dis. 1999;29:1346–7. http://dx.doi. undercooked snake meat or other org/10.1086/313460 was reported in Brazil (3). Here we snake products (1). 5. Guardia SN, Sepp H, Scholten T, Morava- describe 7 newly identified patients Protzner I. Pentastomiasis in Canada. Most immigrants who were given whose infection may have been caused Arch Pathol Lab Med. 1991;115:515–7. by M. kyorinense. a diagnosis of visceral pentastomiasis 6. Cagnard V, Nicolas-Randegger J, Dago were from Nigeria or the Congo Akribi A, Rain B, Nozais JP, Essoh In reviewing the characteristics of region, and diagnoses were made Nomel P, et al. Generalized and lethal these 11 patients (10 from Japan and pentastomiasis due to Armillifer grandis after death. Molecular analysis is 1 from Brazil), we found no apparent (Hett, 1915) [in French]. Bull Soc Pathol contacts among them. Nine of the 11 particularly valuable when only Exot Filiales. 1979;72:345–52. autoptic paraffin-embedded patient 7. Brookins MD, Wellehan JF, Roberts JF, patients had respiratory infections, 1 material is available. For industrialized Allison K, Curran SS, Childress AL, et al. had lymphadenitis, and 1 had arthritis Massive visceral pentastomiasis caused by countries, where experience in (Table). Of these, 9 patients fulfilled Porocephalus crotali in a dog. Vet Pathol. the criteria for infections of clinical morphologic identification of unusual 2009;46:460–3. http://dx.doi.org/10.1354/ parasite species is limited, molecular vp.07-VP-0246-R-BC significance 4( ) and were considered analysis is a valuable diagnostic 8. Prathap K, Lau KS, Bolton JM. to harbor infection by M. kyorinense. Pentastomiasis: a common finding at tool. Our case-patient constitutes a Of the 9 patients with respiratory autopsy among Malaysian aborigines. Am infections, 4 died as a result of the record of imported Armillifer species J Trop Med Hyg. 1969;18:20–7. pentastomiasis to Germany. Because 9. Smith JA, Oladiran B, Lagundoye SB. infection. These data suggest that of increasing international migration, Pentastomiasis and malignancy. Ann Trop M. kyorinense belongs to a class of Med Parasitol. 1975;69:503–12. more cases of pentastomiasis are nontuberculous mycobacteria that 10. Tiendrebeogo H, Levy D, Schmidt D. are pathogenic for humans and have likely to be seen. Human pentastomiasis in Abidjan. A report on 29 cases [in French]. Rev Fr Mal substantial clinical effects. Dennis Tappe, Respir. 1982;10:351–8. Among the 10 patients for Alexandra Haeupler, whom precise clinical records were Hansjörg Schäfer, Paul Racz, Address for correspondence: Dennis Tappe, available, 7 patients were treated Jakob P. Cramer, Institute of Hygiene and Microbiology, with first-line tuberculosis drugs, and Sven Poppert University of Würzburg, Josef-Schneider-Str mainly rifampin, isoniazid, and Author affiliations: University of Würzburg, 2, 97080 Würzburg, Germany; email: dtappe@ ethambutol, but these therapies Würzburg, Germany (D. Tappe); Bernhard- hygiene.uni-wuerzburg.de were ineffective for all patients. 508 Emerging Infectious Diseases • www.cdc.gov/eid • Vol.