Volume 23, 2016
|Number of page(s)||5|
|Published online||16 March 2016|
Giardia duodenalis genetic assemblages and hosts
Assemblages génétiques et hôtes de Giardia duodenalis
Research Service (151), Corporal Michael J. Crescenz Veterans Affairs (VA) Medical Center, University and Woodland Avenues, Philadelphia, PA
2 Department of Medicine, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA
* Corresponding author: email@example.com
Accepted: 6 March 2016
Techniques for sub-classifying morphologically identical Giardia duodenalis trophozoites have included comparisons of the electrophoretic mobility of enzymes and of chromosomes, and sequencing of genes encoding β-giardin, triose phosphate isomerase, the small subunit of ribosomal RNA and glutamate dehydrogenase. To date, G. duodenalis organisms have been sub-classified into eight genetic assemblages (designated A–H). Genotyping of G. duodenalis organisms isolated from various hosts has shown that assemblages A and B infect the largest range of host species, and appear to be the main (or possibly only) G. duodenalis assemblages that undeniably infect human subjects. In at least some cases of assemblage A or B infection in wild mammals, there is suggestive evidence that the infection had resulted from environmental contamination by G. duodenalis cysts of human origin.
Les techniques pour sous-classer morphologiquement des trophozoïtes identiques de Giardia duodenalis ont inclus des comparaisons de la mobilité électrophorétique des enzymes et des chromosomes et le séquençage des gènes codant pour la β-giardine, la triose-phosphate isomérase, la petite sous-unité ribosomique de l’ARN et la glutamate déshydrogénase. À ce jour, G. duodenalis a été sous-classé en 8 assemblages génétiques (désignés par A-H). Le génotypage de G. duodenalis isolés à partir de divers hôtes a montré que les assemblages A et B infectent le grand plus grand nombre d’espèces d’hôtes, et semblent être les assemblages principaux (ou peut-être uniques) qui infectent les sujets humains de manière indéniable. Dans au moins certains cas d’infection chez les mammifères sauvages par les assemblages A ou B, des éléments indiquent que l’infection était due à la contamination de l’environnement par des kystes de G. duodenalis d’origine humaine.
Key words: Assemblage / Genotype / Giardia / Giardia infections / Giardiasis
© M.F. Heyworth, published by EDP Sciences, 2016
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Morphologically similar or identical Giardia organisms, designated Giardia duodenalis (synonyms G. intestinalis and G. lamblia) , can infect the intestine of numerous species of mammalian host. G. duodenalis is the only Giardia species that causes human infection; other currently recognised species in this genus include the following (hosts are mentioned in parentheses): Giardia muris (rodents) , G. microti (voles, muskrats) , G. psittaci (budgerigars) , G. ardeae (great blue herons)  and G. agilis (amphibians) .
From the 1980s onwards, increasingly precise methods have been developed to sub-classify morphologically identical G. duodenalis organisms. Early work of this type involved examination of the electrophoretic mobility of G. duodenalis enzymes [1, 23]. In the mid-1990s, such work delineated two distinct sub-populations of G. duodenalis, designated assemblages A and B . Additional evidence for heterogeneity of G. duodenalis emerged from study of the electrophoretic mobility of Giardia chromosomes . Polymerase Chain Reaction (PCR) amplification of G. duodenalis DNA, and restriction fragment length polymorphism (RFLP) analysis and sequencing of the resulting PCR products, added further insight into the heterogeneity of the organism, confirming the existence of assemblages A and B, and – in conjunction with data from enzyme electrophoresis – delineating six additional assemblages (C–H) [5, 26, 27, 34–37].
Giardia duodenalis genes (genetic loci) used for genotyping the organisms include genes encoding β-giardin (bg), triose phosphate isomerase (tpi), the small subunit of ribosomal RNA (ssu) and glutamate dehydrogenase (gdh) . Giardia duodenalis assemblages have been shown to be either relatively specific to certain hosts (assemblages C–H) or essentially unrestricted in terms of the species of host that they can infect (assemblages A and B; Table 1). Within a single “isolate” of G. duodenalis, different genetic loci may have DNA sequences typical of different assemblages (e.g., ssu typical of assemblage B, and tpi and bg typical of assemblage A) , a situation that may make it unrealistic to try to assign a given isolate of G. duodenalis exclusively to one or other assemblage. This point is pertinent to Table 1, which may present an oversimplified classification, in not discriminating between data obtained from a single genetic locus and from several loci . A comprehensive review, published in 2011, includes detailed information about assemblages of G. duodenalis, and non-human hosts for the respective assemblages .
Giardia duodenalis assemblages and corresponding hosts.
Unambiguous direct evidence that human giardiasis can be an example of a zoonosis, i.e. a human infection acquired from non-human hosts under “natural” conditions (via ingestion of G. duodenalis cysts excreted by animals), is limited. One study from the United Kingdom suggested that contact with farm animals (especially pigs) and with pets (especially dogs and cats) was a risk factor for giardiasis in human subjects . Suggestive evidence that G. duodenalis can be transmitted between dogs and human subjects was obtained from a study in a tea-growing community in northeast India . In this work, an association was found between the presence of G. duodenalis infection in human subjects and in dog(s) occupying the same household. For one such household, genetic identity between G. duodenalis in a dog and in human subject(s) was reported . In this example, the direction of presumed inter-species transmission of G. duodenalis might have been either, or both, dog-to-human or human-to-dog. One caveat that applies to genetic studies of G. duodenalis that rely on faecal cysts as the starting material for molecular analysis is whether the presence of such cysts necessarily reflects infection, rather than resulting merely from coprophagy of faecal material containing cysts, and passage of these cysts through an animal’s gastrointestinal tract without causing infection .
Dogs have been infected with G. duodenalis of human origin, by oral administration of trophozoites or cysts of this organism . There is an anecdotal report of an investigator developing giardiasis as a result of deliberately ingesting a gel capsule containing Giardia trophozoites that had originated from an animal host (a Gambian giant pouched rat) . This work showed that animal-to-human transmission of Giardia infection can occur under experimental conditions. It is, however, unclear whether the result of the experiment just described constitutes evidence for the zoonotic transmissibility of G. duodenalis, under “normal field conditions”.
Genotyping of G. duodenalis organisms obtained from human subjects with Giardia infection has shown that assemblages A and B appear to be the only ones that undeniably cause human infections , although there have been occasional reports of the isolation, from human subjects, of G. duodenalis organisms that have genetic markers characteristic of non-A, non-B, assemblages [6, 49]. Mixed infections of human and non-human hosts with more than one assemblage of G. duodenalis concurrently have been described [15, 16, 18, 28]. Table 1 of the present article does not identify which infections, among those documented in the references cited, were part of a mixed infection resulting from more than one assemblage of G. duodenalis.
Although much of the literature on inter-species transmission of G. duodenalis has focussed on actual or presumed animal-to-human transmission, there is increasing evidence that Giardia cysts of human origin can contaminate the environment and infect wild mammals (which, in turn, may act as a reservoir for future infection of human subjects) . The ability to identify G. duodenalis genetic assemblages has provided a level of precision and specificity that was lacking when essentially the only tool was morphological examination of trophozoites. For example, excretion of assemblage B cysts by Australian sea lions, and relative proximity of colonies of these animals to human settlements at coastal sites, speaks to the probability of initial infection of the animals by cysts of human origin . Similarly, presence of assemblage A and B G. duodenalis infection in freely ranging gorillas may reflect human-to-gorilla transmission of the parasite [20, 21].
Of two outbreaks of human G. duodenalis infection in Canadian communities during the 1990s, one ceased and the other diminished after, in each case, a beaver excreting G. duodenalis cysts was removed from the water source supplying the respective community . These observations suggested that the human cases of giardiasis had resulted from ingesting G. duodenalis cysts excreted by the beavers. The respective studies predated current knowledge of G. duodenalis assemblages. Archival material (Giardia organisms) from these outbreaks was, however, available for study by modern molecular techniques some two decades later . Using such techniques, it was found that, in one of the outbreaks, the beaver was infected with assemblage A G. duodenalis, whereas the water contained G. duodenalis of assemblage B, and assemblages A and B were isolated from the infected human subjects. In the other outbreak, the beaver was found to be infected with assemblage B, whereas the infected human subjects included one with assemblage A infection . Consequently, a straightforward causal relationship between the beavers and all the human cases was not found. Anthropocentric historical assumptions, that a relationship between Giardia infection in beavers and in human subjects merely involves beaver-to-human transmission of the parasite, have yielded to a more nuanced appreciation of environmental contamination by human-derived G. duodenalis cysts that may infect beavers .
The author is grateful to Dr. Yejia Zhang for guidance in designing the table, and to staff in the Medical Library at the Philadelphia VA Medical Center for obtaining online copies of publications. There are no competing interests.
- Andrews RH, Adams M, Boreham PFL, Mayrhofer G, Meloni BP. 1989. Giardia intestinalis: electrophoretic evidence for a species complex. International Journal for Parasitology, 19, 183–190. [CrossRef] [PubMed] [Google Scholar]
- Ankarklev J, Svärd SG, Lebbad M. 2012. Allelic sequence heterozygosity in single Giardia parasites. BMC Microbiology, 12, 65. [CrossRef] [PubMed] [Google Scholar]
- Armson A, Yang R, Thompson J, Johnson J, Reid S, Ryan UM. 2009. Giardia genotypes in pigs in Western Australia: prevalence and association with diarrhea. Experimental Parasitology, 121, 381–383. [CrossRef] [PubMed] [Google Scholar]
- Beck R, Sprong H, Bata I, Lucinger S, Pozio E, Cacciò SM. 2011. Prevalence and molecular typing of Giardia spp. in captive mammals at the zoo of Zagreb, Croatia. Veterinary Parasitology, 175, 40–46. [CrossRef] [PubMed] [Google Scholar]
- Berrilli F, D’Alfonso R, Giangaspero A, Marangi M, Brandonisio O, Kaboré Y, Glé C, Cianfanelli C, Lauro R, Di Cave D. 2012. Giardia duodenalis genotypes and Cryptosporidium species in humans and domestic animals in Côte d’Ivoire: occurrence and evidence for environmental contamination. Transactions of the Royal Society of Tropical Medicine and Hygiene, 106, 191–195. [CrossRef] [PubMed] [Google Scholar]
- Broglia A, Weitzel T, Harms G, Cacciò SM, Nöckler K. 2013. Molecular typing of Giardia duodenalis isolates from German travellers. Parasitology Research, 112, 3449–3456. [CrossRef] [PubMed] [Google Scholar]
- Cacciò SM, Ryan U. 2008. Molecular epidemiology of giardiasis. Molecular & Biochemical Parasitology, 160, 75–80. [CrossRef] [PubMed] [Google Scholar]
- Covacin C, Aucoin DP, Elliot A, Thompson RCA. 2011. Genotypic characterisation of Giardia from domestic dogs in the USA. Veterinary Parasitology, 177, 28–32. [CrossRef] [PubMed] [Google Scholar]
- Davidson RK, Amundsen H, Lie NO, Luyckx K, Robertson LJ, Verocai GG, Kutz SJ, Ytrehus B. 2014. Sentinels in a climatic outpost: endoparasites in the introduced muskox (Ovibos moschatus wardi) population of Dovrefjell, Norway. International Journal for Parasitology: Parasites and Wildlife, 3, 154–160. [CrossRef] [Google Scholar]
- Delport TC, Asher AJ, Beaumont LJ, Webster KN, Harcourt RG, Power ML. 2014. Giardia duodenalis and Cryptosporidium occurrence in Australian sea lions (Neophoca cinerea) exposed to varied levels of human interaction. International Journal for Parasitology: Parasites and Wildlife, 3, 269–275. [CrossRef] [Google Scholar]
- Erlandsen SL, Bemrick WJ. 1987. SEM evidence for a new species, Giardia psittaci. Journal of Parasitology, 73, 623–629. [CrossRef] [Google Scholar]
- Erlandsen SL, Bemrick WJ, Wells CL, Feely DE, Knudson L, Campbell SR, van Keulen H, Jarroll EL. 1990. Axenic culture and characterization of Giardia ardeae from the great blue heron (Ardea herodias). Journal of Parasitology, 76, 717–724. [CrossRef] [Google Scholar]
- Farzan A, Parrington L, Coklin T, Cook A, Pintar K, Pollari F, Friendship R, Farber J, Dixon B. 2011. Detection and characterization of Giardia duodenalis and Cryptosporidium spp. on swine farms in Ontario, Canada. Foodborne Pathogens and Disease, 8, 1207–1213. [CrossRef] [PubMed] [Google Scholar]
- Feely DE, Erlandsen SL. 1985. Morphology of Giardia agilis: observation by scanning electron microscopy and interference reflexion microscopy. Journal of Protozoology, 32, 691–693. [CrossRef] [Google Scholar]
- Feng Y, Xiao L. 2011. Zoonotic potential and molecular epidemiology of Giardia species and giardiasis. Clinical Microbiology Reviews, 24, 110–140. [CrossRef] [PubMed] [Google Scholar]
- Gelanew T, Lalle M, Hailu A, Pozio E, Cacciò SM. 2007. Molecular characterization of human isolates of Giardia duodenalis from Ethiopia. Acta Tropica, 102, 92–99. [CrossRef] [PubMed] [Google Scholar]
- Geurden T, Thomas P, Casaert S, Vercruysse J, Claerebout E. 2008. Prevalence and molecular characterisation of Cryptosporidium and Giardia in lambs and goat kids in Belgium. Veterinary Parasitology, 155, 142–145. [CrossRef] [PubMed] [Google Scholar]
- Geurden T, Levecke B, Cacciò SM, Visser A, de Groote G, Casaert S, Vercruysse J, Claerebout E. 2009. Multilocus genotyping of Cryptosporidium and Giardia in non-outbreak related cases of diarrhoea in human patients in Belgium. Parasitology, 136, 1161–1168. [CrossRef] [PubMed] [Google Scholar]
- Gomez-Puerta LA, Lopez-Urbina MT, Alarcon V, Cama V, Gonzalez AE, Xiao L. 2014. Occurrence of Giardia duodenalis assemblages in alpacas in the Andean region. Parasitology International, 63, 31–34. [CrossRef] [PubMed] [Google Scholar]
- Graczyk TK, Bosco-Nizeyi J, Ssebide B, Thompson RCA, Read C, Cranfield MR. 2002. Anthropozoonotic Giardia duodenalis genotype (assemblage) A infections in habitats of free-ranging human-habituated gorillas, Uganda. Journal of Parasitology, 88, 905–909. [CrossRef] [Google Scholar]
- Hogan JN, Miller WA, Cranfield MR, Ramer J, Hassell J, Noheri JB, Conrad PA, Gilardi KVK. 2014. Giardia in mountain gorillas (Gorilla beringei beringei), forest buffalo (Syncerus caffer), and domestic cattle in Volcanoes National Park, Rwanda. Journal of Wildlife Diseases, 50, 21–30. [CrossRef] [PubMed] [Google Scholar]
- Inpankaew T, Schär F, Odermatt P, Dalsgaard A, Chimnoi W, Khieu V, Muth S, Traub RJ. 2014. Low risk for transmission of zoonotic Giardia duodenalis from dogs to humans in rural Cambodia. Parasites & Vectors, 7, 412. [CrossRef] [PubMed] [Google Scholar]
- Isaac-Renton JL, Cordeiro C, Sarafis K, Shahriari H. 1993. Characterization of Giardia duodenalis isolates from a waterborne outbreak. Journal of Infectious Diseases, 167, 431–440. [CrossRef] [Google Scholar]
- Khan SM, Debnath C, Pramanik AK, Xiao L, Nozaki T, Ganguly S. 2011. Molecular evidence for zoonotic transmission of Giardia duodenalis among dairy farm workers in West Bengal, India. Veterinary Parasitology, 178, 342–345. [CrossRef] [PubMed] [Google Scholar]
- Lasek-Nesselquist E, Bogomolni AL, Gast RJ, Welch DM, Ellis JC, Sogin ML, Moore MJ. 2008. Molecular characterization of Giardia intestinalis haplotypes in marine animals: variation and zoonotic potential. Diseases of Aquatic Organisms, 81, 39–51. [CrossRef] [PubMed] [Google Scholar]
- Lasek-Nesselquist E, Welch DM, Sogin ML. 2010. The identification of a new Giardia duodenalis assemblage in marine vertebrates and a preliminary analysis of G. duodenalis population biology in marine systems. International Journal for Parasitology, 40, 1063–1074. [CrossRef] [PubMed] [Google Scholar]
- Lebbad M, Mattsson JG, Christensson B, Ljungström B, Backhans A, Andersson JO, Svärd SG. 2010. From mouse to moose: multilocus genotyping of Giardia isolates from various animal species. Veterinary Parasitology, 168, 231–239. [CrossRef] [PubMed] [Google Scholar]
- Levecke B, Geldhof P, Claerebout E, Dorny P, Vercammen F, Cacciò SM, Vercruysse J, Geurden T. 2009. Molecular characterisation of Giardia duodenalis in captive non-human primates reveals mixed assemblage A and B infections and novel polymorphisms. International Journal for Parasitology, 39, 1595–1601. [CrossRef] [PubMed] [Google Scholar]
- Li W, Liu C, Yu Y, Li J, Gong P, Song M, Xiao L, Zhang X. 2013. Molecular characterization of Giardia duodenalis isolates from police and farm dogs in China. Experimental Parasitology, 135, 223–226. [CrossRef] [PubMed] [Google Scholar]
- Liu A, Yang F, Shen Y, Zhang W, Wang R, Zhao W, Zhang L, Ling H, Cao J. 2014. Genetic analysis of the Gdh and Bg genes of animal-derived Giardia duodenalis isolates in Northeastern China and evaluation of zoonotic transmission potential. PLoS One, 9(4), e95291. [CrossRef] [PubMed] [Google Scholar]
- Majewska AC. 1994. Successful experimental infections of a human volunteer and Mongolian gerbils with Giardia of animal origin. Transactions of the Royal Society of Tropical Medicine and Hygiene, 88, 360–362. [CrossRef] [PubMed] [Google Scholar]
- Mayrhofer G, Andrews RH, Ey PL, Chilton NB. 1995. Division of Giardia isolates from humans into two genetically distinct assemblages by electrophoretic analysis of enzymes encoded at 27 loci and comparison with Giardia muris. Parasitology, 111, 11–17. [CrossRef] [PubMed] [Google Scholar]
- Minetti C, Taweenan W, Hogg R, Featherstone C, Randle N, Latham SM, Wastling JM. 2014. Occurrence and diversity of Giardia duodenalis assemblages in livestock in the UK. Transboundary and Emerging Diseases, 61, e60–e67. [CrossRef] [PubMed] [Google Scholar]
- Monis PT, Mayrhofer G, Andrews RH, Homan WL, Limper L, Ey PL. 1996. Molecular genetic analysis of Giardia intestinalis isolates at the glutamate dehydrogenase locus. Parasitology, 112, 1–12. [CrossRef] [PubMed] [Google Scholar]
- Monis PT, Andrews RH, Mayrhofer G, Mackrill J, Kulda J, Isaac-Renton JL, Ey PL. 1998. Novel lineages of Giardia intestinalis identified by genetic analysis of organisms isolated from dogs in Australia. Parasitology, 116, 7–19. [CrossRef] [PubMed] [Google Scholar]
- Monis PT, Andrews RH, Mayrhofer G, Ey PL. 1999. Molecular systematics of the parasitic protozoan Giardia intestinalis. Molecular Biology and Evolution, 16, 1135–1144. [CrossRef] [PubMed] [Google Scholar]
- Monis PT, Andrews RH, Mayrhofer G, Ey PL. 2003. Genetic diversity within the morphological species Giardia intestinalis and its relationship to host origin. Infection, Genetics and Evolution, 3, 29–38. [CrossRef] [Google Scholar]
- Ng J, Yang R, Whiffin V, Cox P, Ryan U. 2011. Identification of zoonotic Cryptosporidium and Giardia genotypes infecting animals in Sydney’s water catchments. Experimental Parasitology, 128, 138–144. [CrossRef] [PubMed] [Google Scholar]
- Pantchev N, Broglia A, Paoletti B, Globokar Vrhovec M, Bertram A, Nöckler K, Cacciò SM. 2014. Occurrence and molecular typing of Giardia isolates in pet rabbits, chinchillas, guinea pigs and ferrets collected in Europe during 2006–2012. Veterinary Record, 175, 18. [CrossRef] [Google Scholar]
- Prystajecky N, Tsui CK-M, Hsiao WWL, Uyaguari-Diaz MI, Ho J, Tang P, Isaac-Renton J. 2015. Giardia spp. are commonly found in mixed assemblages in surface water, as revealed by molecular and whole-genome characterization. Applied and Environmental Microbiology, 81, 4827–4834. [CrossRef] [PubMed] [Google Scholar]
- Reboredo-Fernández A, Gómez-Couso H, Martínez-Cedeira JA, Cacciò SM, Ares-Mazás E. 2014. Detection and molecular characterization of Giardia and Cryptosporidium in common dolphins (Delphinus delphis) stranded along the Galician coast (Northwest Spain). Veterinary Parasitology, 202, 132–137. [CrossRef] [PubMed] [Google Scholar]
- Reboredo-Fernández A, Ares-Mazás E, Martínez-Cedeira JA, Romero-Suances R, Cacciò SM, Gómez-Couso H. 2015. Giardia and Cryptosporidium in cetaceans on the European Atlantic coast. Parasitology Research, 114, 693–698. [CrossRef] [PubMed] [Google Scholar]
- Robertson LJ, Forberg T, Hermansen L, Hamnes IS, Gjerde B. 2007. Giardia duodenalis cysts isolated from wild moose and reindeer in Norway: genetic characterization by PCR-RFLP and sequence analysis at two genes. Journal of Wildlife Diseases, 43, 576–585. [CrossRef] [PubMed] [Google Scholar]
- Rosa LAG, Gomes MA, Mundim AV, Mundim MJS, Pozzer EL, Faria ESM, Viana JC, Cury MC. 2007. Infection of dogs by experimental inoculation with human isolates of Giardia duodenalis: clinical and laboratory manifestations. Veterinary Parasitology, 145, 37–44. [CrossRef] [PubMed] [Google Scholar]
- Santín M, Fayer R. 2015. Enterocytozoon bieneusi, Giardia, and Cryptosporidium infecting white-tailed deer. Journal of Eukaryotic Microbiology, 62, 34–43. [CrossRef] [Google Scholar]
- Sarafis K, Isaac-Renton J. 1993. Pulsed-field gel electrophoresis as a method of biotyping of Giardia duodenalis. American Journal of Tropical Medicine and Hygiene, 48, 134–144. [Google Scholar]
- Soares RM, de Souza SLP, Silveira LH, Funada MR, Richtzenhain LJ, Gennari SM. 2011. Genotyping of potentially zoonotic Giardia duodenalis from exotic and wild animals kept in captivity in Brazil. Veterinary Parasitology, 180, 344–348. [CrossRef] [PubMed] [Google Scholar]
- Solarczyk P, Majewska AC, Słodkowicz-Kowalska A. 2014. Axenic in vitro culture and molecular characterization of Giardia duodenalis from red deer (Cervus elaphus) and Thomson’s gazelle (Gazella thomsonii). Acta Parasitologica, 59, 763–766. [CrossRef] [Google Scholar]
- Soliman RH, Fuentes I, Rubio JM. 2011. Identification of a novel Assemblage B subgenotype and a zoonotic Assemblage C in human isolates of Giardia intestinalis in Egypt. Parasitology International, 60, 507–511. [CrossRef] [PubMed] [Google Scholar]
- Sulaiman IM, Fayer R, Bern C, Gilman RH, Trout JM, Schantz PM, Das P, Lal AA, Xiao L. 2003. Triosephosphate isomerase gene characterization and potential zoonotic transmission of Giardia duodenalis. Emerging Infectious Diseases, 9, 1444–1452. [CrossRef] [PubMed] [Google Scholar]
- Suzuki J, Murata R, Kobayashi S, Sadamasu K, Kai A, Takeuchi T. 2011. Risk of human infection with Giardia duodenalis from cats in Japan and genotyping of the isolates to assess the route of infection in cats. Parasitology, 138, 493–500. [CrossRef] [PubMed] [Google Scholar]
- Thompson J, Yang R, Power M, Hufschmid J, Beveridge I, Reid S, Ng J, Armson A, Ryan U. 2008. Identification of zoonotic Giardia genotypes in marsupials in Australia. Experimental Parasitology, 120, 88–93. [CrossRef] [PubMed] [Google Scholar]
- Thompson RCA, Monis P. 2012. Giardia – from genome to proteome. Advances in Parasitology, 78, 57–95. [CrossRef] [PubMed] [Google Scholar]
- Thompson RCA, Monis PT. 2004. Variation in Giardia: implications for taxonomy and epidemiology. Advances in Parasitology, 58, 69–137. [CrossRef] [PubMed] [Google Scholar]
- Traub RJ, Monis PT, Robertson I, Irwin P, Mencke N, Thompson RCA. 2004. Epidemiological and molecular evidence supports the zoonotic transmission of Giardia among humans and dogs living in the same community. Parasitology, 128, 253–262. [CrossRef] [PubMed] [Google Scholar]
- Traversa D, Otranto D, Milillo P, Latrofa MS, Giangaspero A, Di Cesare A, Paoletti B. 2012. Giardia duodenalis sub-assemblage of animal and human origin in horses. Infection, Genetics and Evolution, 12, 1642–1646. [CrossRef] [Google Scholar]
- van Keulen H, Feely DE, Macechko PT, Jarroll EL, Erlandsen SL. 1998. The sequence of Giardia small subunit rRNA shows that voles and muskrats are parasitized by a unique species Giardia microti. Journal of Parasitology, 84, 294–300. [CrossRef] [Google Scholar]
- Volotão ACC, Ramos NMD, Fantinatti M, de Moraes MVP, Netto HA, Storti-Melo LM, de Godoy EAM, Rossit ARB, Fernandes O, Machado RLD. 2011. Giardiasis as zoonosis: between proof of principle and paradigm in the Northwestern region of São Paulo State, Brazil. Brazilian Journal of Infectious Diseases, 15, 382–383. [CrossRef] [Google Scholar]
- Warburton ARE, Jones PH, Bruce J. 1994. Zoonotic transmission of giardiasis: a case control study. Communicable Disease Report. CDR Review, 4, R32–R36. [PubMed] [Google Scholar]
- Ye J, Xiao L, Ma J, Guo M, Liu L, Feng Y. 2012. Anthroponotic enteric parasites in monkeys in public park, China. Emerging Infectious Diseases, 18, 1640–1643. [CrossRef] [PubMed] [Google Scholar]
- Ye J, Xiao L, Li J, Huang W, Amer SE, Guo Y, Roellig D, Feng Y. 2014. Occurrence of human-pathogenic Enterocytozoon bieneusi, Giardia duodenalis and Cryptosporidium genotypes in laboratory macaques in Guangxi, China. Parasitology International, 63, 132–137. [CrossRef] [PubMed] [Google Scholar]
- Zhang W, Zhang X, Wang R, Liu A, Shen Y, Ling H, Cao J, Yang F, Zhang X, Zhang L. 2012. Genetic characterizations of Giardia duodenalis in sheep and goats in Heilongjiang Province, China and possibility of zoonotic transmission. PLoS Neglected Tropical Diseases, 6(9), e1826. [CrossRef] [PubMed] [Google Scholar]
- Zhao Z, Wang R, Zhao W, Qi M, Zhao J, Zhang L, Li J, Liu A. 2015. Genotyping and subtyping of Giardia and Cryptosporidium isolates from commensal rodents in China. Parasitology, 142, 800–806. [CrossRef] [PubMed] [Google Scholar]
Cite this article as: Heyworth MF: Giardia duodenalis genetic assemblages and hosts. Parasite, 2016, 23, 13.
Current usage metrics show cumulative count of Article Views (full-text article views including HTML views, PDF and ePub downloads, according to the available data) and Abstracts Views on Vision4Press platform.
Data correspond to usage on the plateform after 2015. The current usage metrics is available 48-96 hours after online publication and is updated daily on week days.
Initial download of the metrics may take a while.