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Morphological and molecular characterization of Bertiella sp. (Cestoda, Anoplocephalidae) infection in a human and howler monkeys in Argentina

  • Helminthology - Original Paper
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Abstract

Bertiella sp. is a typical parasite in non-human primates and only a few cases of bertiellosis have been reported in humans. We present a new case study of bertiellosis in a 42-year-old woman caretaker of howler monkeys in a wild rehabilitation center in Argentina. Bertiella sp. infection was also diagnosed in the monkeys. Proglottids and feces were collected from the caretaker and monkeys; the samples were submitted for parasitological examination by morphological characterization and molecular identification using both nuclear (18S and ITS1-5.8-ITS2 rDNA) and mitochondrial (cox1) markers. Morphological and molecular data were consistent and allowed the classification of the specimen to the genus level. The analyses also showed the presence of cysts of Giardia lamblia and oocysts of Cryptosporidium spp. in howler monkeys, and cysts of Blastocystis sp. in both the caretaker and monkeys. This study recorded the fourth case of bertiellosis in a human host from Argentina and the eighth case in South America. Moreover, this is the first study that compares the morphological and molecular features of Bertiella sp. found in both a human and monkeys from the same geographical region. These results suggest that the cohabitation between humans and monkeys increases the opportunities of infection by Bertiella sp. and other potential zoonotic parasites.

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References

  • Acha PN, Szyfres B (2003) Zoonosis y enfermedades transmisibles comunes al hombre y a los animales. In: Tercera (ed) En: Bertielasis, vol III. Pan American Health Organization, Washington, DC, USA, pp 165–166

    Google Scholar 

  • Achir I, Zait H, Hamrioui B (2008) Human infection due to Bertiella sp. (Cestode: Anoplocephalidae) in a man originating from Yemen in Algeria. Bull Soc Pathol Exot 101:107–108

    CAS  PubMed  Google Scholar 

  • Aibar MA, De Escalante B, Ramírez E, Garcés V (2010) Infección por Bertiella studeri en una niña de Guinea Ecuatorial. Cartas científicas/Enferm Infecc Microbiol Clín 28:652–653

  • Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402. https://doi.org/10.1093/nar/25.17.3389

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bacigalupo J (1949) Primer caso humano de Bertiella sp. en Sud América. Rev Soc Mex Hist Nat 10:177–183

    Google Scholar 

  • Beveridge I (1994) Family anoplocephalidae Cholodkovsky, 1902. In: Khalil LF, Jones A, Bray RA (eds) Keys to the cestode parasites of vertebrates. U.K pp, CAB International, Wallingford, pp 315–366

    Google Scholar 

  • Bhagwant S (2004) Human Bertiella studeri (family Anoplocephalidae) infection of probable Southeast Asian origin in Mauritian children and an adult. Am J Trop Med Hyg 72:225–228. https://doi.org/10.4269/ajtmh.2004.70.225

    Article  Google Scholar 

  • Caira JN, Jensen K, Barbeau E (2012) Global cestode database. World Wide Web electronic publication. https://tapewormdb.Uconn.Edu/.

  • Cameron TWM (1929) A new record of the occurrence of a tapeworm of the genus Bertiella in man. J Helminthol 7:231–234

    Article  Google Scholar 

  • Chandler AC (1925) New records of Bertiella satyri (Cestoda) in man and apes. Parasitol 17:421–425

    Article  Google Scholar 

  • Cociancic P, Rinaldi L, Zonta ML, Navone GT (2018) Formalin-ethyl acetate concentration, FLOTAC Pellet and anal swab techniques for the diagnosis of intestinal parasites. Parasitol Res 117:3567–3573. https://doi.org/10.1007/s00436-018-6054-9

    Article  PubMed  Google Scholar 

  • Cringoli G, Rinaldi L, Maurelli MP, Utzinger J (2010) FLOTAC: new multivalent techniques for qualitative and quantitative copromicroscopic diagnosis of parasites in animals and humans. Nat Protoc 5:503–515

    Article  CAS  Google Scholar 

  • D’alessandro A, Beaver P, Mas Pallares R (1963) Bertiella infection in man in Paraguay. Amer J Trop Med Hyg 12:193–198

    Article  Google Scholar 

  • Daszak P, Cunningham AA, Hyatt AD (2000) Emerging infectious diseases of wildlife — threats to biodiversity and human health. Science 287:443–449

    Article  CAS  Google Scholar 

  • Denegri GM (1985) Consideraciones sobre sistemática y distribución geográfica del género Bertiella (Cestoda-Anoplocephalidae) en el hombre y en primates no humanos. Neotropica 31:55–63

    Google Scholar 

  • Denegri GM, Perez-Serrano J (1997) Bertiellosis in man: a review of cases. Rev Inst Med Trop São Paulo 39:123–127

    Article  CAS  Google Scholar 

  • Doležalová J, Vallo P, Petrzelkova KJ, Foitová I, Nurcahyo W, Mudakikwa A (2015) Molecular phylogeny of anoplocephalid tapeworms (Cestoda: Anoplocephalidae) infecting humans and non-human primates. Parasitol 142:1278–1289. https://doi.org/10.1017/S003118201500058X

    Article  Google Scholar 

  • El-Dib NA, Al-Rufaii A, El-Badry AA, Al-Zoheiry AA, El-Aall AA (2004) Human infection with Bertiella species in Saudi Arabia. Saudi Pharm J 2:168–169

    Google Scholar 

  • Feldman R, Denegri G, Avolio J, Cantu N (1983) Nuevo caso humano de teniasis por Bertiella mucronata Meyner, 1895 en la Argentina I. Diagnóstico y tratamiento Acta Bioquim Clin Latinoam 17:571–578

    Google Scholar 

  • Foitová I, Mašová S, Tenora F, Koubková B, Hodová I, Vyskočilová M, Baruš V, Nurcahyo W (2011) Redescription and resurrection of Bertiella satyri (Cestoda, Anoplocephalidae) parasitizing the orangutan (Pongo abelii) in Indonesia. Parasitol Res 109:689–697. https://doi.org/10.1007/s00436-011-2300-0

    Article  PubMed  Google Scholar 

  • Galán-Puchades MT, Fuentes MV, Mas-Coma S (1997) Human Bertiella studeri in Spain, probably of African origin. Am J Trop Med Hyg 56:610–612. https://doi.org/10.4269/ajtmh.1997.56.610

    Article  PubMed  Google Scholar 

  • Galán-Puchades MT, Fuentes MV, Mas-Coma S (2000) Morphology of Bertiella studeri (Blanchard, 1891) sensu Stunkard (1940) (Cestoda: Anoplocephalidae) of human origin and a proposal of criteria for the specific diagnosis of bertiellosis. Folia Parasitol 47:23–28

    Article  Google Scholar 

  • Garaguso P. and Méndez O (1983) - Primer caso argentino de parasitismo humano por Bertiella mucronata (Meyner, 1895). En: Congreso Latinoamericano de Parasitología, 6., Sao Paulo, p 232

  • Gomez-Puerta LA, Lapez-Urbina MT, Gonzalez AE (2009) Occurrence of tapeworm Bertiella mucronata (Cestoda: Anoplocephalidae) in the Titi monkey Callicebus oenanthe from Peru: a new definitive host and geographical record. Vet Parasitol 163:161–163. https://doi.org/10.1016/j.vetpar.2009.04.008

    Article  PubMed  Google Scholar 

  • Kaminsky RG (2014) Manual de Parasitología: Técnicas para Laboratorios de Atención Primaria de Salud y para el Diagnóstico de las Enfermedades Infecciosas Desatendidas. 3ra. Edición, Organización Panamericana de la Salud e Instituto de Enfermedades Infecciosas y Parasitología, pp. 187

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    Article  CAS  Google Scholar 

  • Kowalewski MM, Gillespie TR (2009) Ecological and anthropogenic influences on patterns of parasitism in free-ranging primates: a meta-analysis of the genus Alouatta. In: Garber PA, Estrada A, Bicca-Marques JC, Heymann EW, Strier KB (eds) South American primates. Developments in primatology: progress and prospects. Springer, New York, pp 433–461

    Chapter  Google Scholar 

  • Kowalewski MM, Salzer JS, Deutsch JC, Rano M, Kuhlenschmidt MS, Gillespie TR (2011) Black and gold howler monkeys (Alouatta caraya) as sentinels of ecosystem health: patterns of zoonotic protozoa infection relative to degree of human-primate contact. Am J Primatol 73:75–83. https://doi.org/10.1002/ajp.20803

    Article  PubMed  Google Scholar 

  • Kowalewski M, Torres J, Milozzi C, Gillespie TR (2017) Bertiella sp. infection patterns in black and gold howler monkeys across their distribution. In: Sociedad Argentina para Estudio de los Mamíferos SAREM, 1st edn. Primatology in Argentina, Mendoza, pp 219–233

    Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948. https://doi.org/10.1093/bioinformatics/btm404

    Article  CAS  PubMed  Google Scholar 

  • Lopes VV, Santos HAD, Silva AV, Fontes G, Vieira GL, Ferreira AC, Silva ESD (2015) First case of human infection by Bertiella studeri (Blanchard, 1891) Stunkard, 1940 (Cestoda; Anoplocephalidae) in Brazil. Rev Inst Med Trop São Paulo 57:447–450. https://doi.org/10.1590/S0036-46652015000500015

    Article  PubMed  PubMed Central  Google Scholar 

  • Macnish MG, Morgan-Ryan UM, Monis PT, Behnke JM, Thompson RCA (2002) A molecular phylogeny of nuclear and mitochondrial sequences in Hymenolepis nana (Cestoda) supports the existence of a cryptic species. Parasitology 125:567–575. https://doi.org/10.1017/S0031182002002366

    Article  CAS  PubMed  Google Scholar 

  • Malik S, Srivastava VK, Samantaray JC (2013) Human bertiellosis from North India. Indian J Pediatr 80:258–260. https://doi.org/10.1007/s12098-012-0718-8

    Article  PubMed  Google Scholar 

  • Medlin L, Elwood HJ, Stickel S, Sogin ML (1988) The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. Gene 71:491–499

    Article  CAS  Google Scholar 

  • Milozzi C, Bruno G, Cundom E, Mudry MD, Navone GT (2012) Intestinal parasites of Alouatta caraya (Primates, Ceboidea): preliminary study in semi-captivity and in the wild in Argentina. Mastozool Neotrop 19:271–2788

    Google Scholar 

  • Okamoto M, Agatsuma T, Kurosawa T, Ito A (1997) Phylogenetic relationships of three hymenolepidid species inferred from nuclear ribosomal and mitochondrial DNA sequences. Parasitology 115:661–666. https://doi.org/10.1017/S0031182097001741

    Article  CAS  PubMed  Google Scholar 

  • Paçô JM, Campos DM, Araujo JL (2003) Human bertiellosis in Goias, Brazil: a case report on human infection by Bertiella sp. (Cestoda: Anoplocephalidae). Rev Inst Med Trop Sao Paulo 45:159–161

  • Pope BL (1966) Some parasites of the howler monkey of northern Argentina. J Parasitol 52:166–168

    Article  CAS  Google Scholar 

  • Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256. https://doi.org/10.1093/molbev/msn083

    Article  CAS  Google Scholar 

  • Santa Cruz A, Gomez L, De Rott M (1995) El parasitismo en Alouatta carayá y Saimiri boliviensis ingresados al “Centro Argentino de Primates”. Rev Med Vet (B Aires) 76:150–152

    Google Scholar 

  • Schmidt GD (1986) Handbook of tapeworm identification. CRS Press, Boca Raton, p 675

    Google Scholar 

  • Souza Júnior JC, Goulart JAG, Varnier S, Denegri G, Silva Filho HH, Hirano ZMB, et al. (2008) Bertiellosis in Brazilian non-human primates: natural infection in Alouatta guariba clamitans (Cabrera, 1940) (Primates: Atelidae) in Santa Catarina State, Brazil. Rev Patol Trop 37(1):48–56

  • Stunkard H, Koivastik T, Healy G (1964) Infection of child in Minnessota by Bertiella studeri (Cestoda-Anoplocephalidae). Amer J Trop Med Hyg 13:402–409. https://doi.org/10.4269/ajtmh.1964.13.402

    Article  CAS  Google Scholar 

  • Sun X, Fang Q, Chen XZ, Hu SF, Xia H, Wang XM (2006) Bertiella studeri infection, China. Emerg Infect Dis 12:176–177

  • Taleb-Hossenkhan N, Bhagwant S (2012) Molecular characterization of the parasitic tapeworm Bertiella studeri from the island of Mauritius. Parasitol Res 110:759–768. https://doi.org/10.1007/s00436-011-2550-x

    Article  PubMed  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  CAS  Google Scholar 

  • Vilas R, Criscione CD, Blouin MS (2005) A comparison between mitochondrial DNA and the ribosomal internal transcribed regions in prospecting for cryptic species of platyhelminth parasites. Parasitology 131:839–846. https://doi.org/10.1017/S0031182005008437

    Article  CAS  PubMed  Google Scholar 

  • World Health Organization (2019) Bench aids for the diagnosis of intestinal parasites. WHO, Geneva, p 32

    Google Scholar 

  • Yamaguti S (1959) Systema helminthum. In: The cestodes of vertebrates, vol II. Interscience Publishers Inc., New York, pp 435–436

    Google Scholar 

  • Yanagida T, Lavikainen A, Hoberg EP, Konyaev S, Ito A, Sato MO, Nakao M (2017) Specific status of Echinococcus canadensis (Cestoda: Taeniidae) inferred from nuclear and mitochondrial gene sequences. Int J Parasitol 47:971–979. https://doi.org/10.1016/j.ijpara.2017.07.001

    Article  CAS  PubMed  Google Scholar 

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Funding

Financial support was given by PUE (22920160100036-CONICET).

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Authors and Affiliations

  1. Centro de Estudios Parasitológicos y de Vectores (CEPAVE-CONICET-UNLP), Boulevard 120 S/N entre 60 y 64, 1900, La Plata, Argentina

    Andrea Servián, María Lorena Zonta, Paola Cociancic, Andrea Falcone, Sofía Capasso & Graciela Teresa Navone

  2. Laboratorio de Biodiversidad y Epidemiología Parasitaria, Centro de Estudios Parasitológicos y de Vectores, La Plata, Buenos Aires, Argentina

    Andrea Servián

  3. Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET). Instituto de Investigaciones en Microbiología y Parasitología Médica (IMPaM). Facultad de Medicina, Universidad de Buenos Aires, Paraguay 2155 Piso: 12, 1121, CABA, Argentina

    Paula Ruybal

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  1. Andrea Servián
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  2. María Lorena Zonta
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Correspondence to Andrea Servián.

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Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the national research committee (Comité Consultivo de Bioética de la Universidad Nacional de La Plata 100-20120/18) and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. Informed consent was obtained from the individual participant included in this study. The patient gave consent for scientific examination of materials and to have her case details published. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. Permits were obtained for the collection of the animal samples from the wild rehabilitation center (Dirección de Flora y Fauna EX 2019-36163,701-GDEBA DGLYCNMAGP).

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Servián, A., Zonta, M.L., Cociancic, P. et al. Morphological and molecular characterization of Bertiella sp. (Cestoda, Anoplocephalidae) infection in a human and howler monkeys in Argentina. Parasitol Res 119, 1291–1300 (2020). https://doi.org/10.1007/s00436-020-06615-5

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