Giardia duodenalis genetic assemblages and hosts

Parasite 2016, 23, 13 Review Article Giardia duodenalis genetic assemblages and hosts Assemblages génétiques et hôtes de Giardia duodenalis Martin F. Heyworth1,2* 1 Research Service (151), Corporal Michael J. Crescenz Veterans Affairs (VA) Medical Center, University and Woodland Avenues, Philadelphia, PA 19104, USA 2 Department of Medicine, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA * Corresponding author: Received: 17 December 2015 Accepted: 6 March 2016 Abstract 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. Résumé 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) [54], 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) [15], G. microti (voles, muskrats) [57], G. psittaci (budgerigars) [11], G. ardeae (great blue herons) [12] and G. agilis (amphibians) [14]. 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 [32]. Additional evidence for heterogeneity of G. duodenalis emerged from study of the electrophoretic mobility of Giardia chromosomes [46]. 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) [15]. 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) [39], 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 [7]. A comprehensive review, published in 2011, includes detailed information about assemblages of G. duodenalis, and non-human hosts for the respective assemblages [15]. Table 1. 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 [59]. 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 [55]. 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 [55]. 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 [22]. Dogs have been infected with G. duodenalis of human origin, by oral administration of trophozoites or cysts of (...truncated)