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New Pieces of the Trichinella Puzzle View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by DigitalCommons@University of Nebraska University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln U.S. Department of Agriculture: Agricultural Publications from USDA-ARS / UNL Faculty Research Service, Lincoln, Nebraska 6-28-2013 New pieces of the Trichinella puzzle Edoardo Pozio Dante S. Zarlenga Follow this and additional works at: https://digitalcommons.unl.edu/usdaarsfacpub This Article is brought to you for free and open access by the U.S. Department of Agriculture: Agricultural Research Service, Lincoln, Nebraska at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Publications from USDA-ARS / UNL Faculty by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. International Journal for Parasitology 43 (2013) 983–997 Contents lists available at SciVerse ScienceDirect International Journal for Parasitology journal homepage: www.elsevier.com/locate/ijpara Invited Review New pieces of the Trichinella puzzle ⇑ Edoardo Pozio a, , Dante S. Zarlenga b a European Union Reference Laboratory for Parasites, Istituto Superiore di Sanità, viale Regina Elena 299, 00161 Rome, Italy b Animal Parasitic Diseases Laboratory, USDA, Agricultural Research Service, BARC-East B1180, Beltsville, MD 20705, USA article info abstract Article history: Contrary to our understanding of just a few decades ago, the genus Trichinella now consists of a complex Received 11 April 2013 assemblage of no less than nine different species and three additional genotypes whose taxonomic status Received in revised form 27 May 2013 remains in flux. New data and methodologies have allowed advancements in detection and differentia- Accepted 29 May 2013 tion at the population level which in turn have demonstrably advanced epidemiological, immunological Available online 28 June 2013 and genetic investigations. In like manner, molecular and genetic studies have permitted us to hypothe- sise biohistorical events leading to the worldwide dissemination of this genus, and to begin crystalising Keywords: the evolution of Trichinella on a macro scale. The identification of species in countries and continents Trichinella otherwise considered Trichinella-free has raised questions regarding host adaptation and associations, Taxonomy Phylogeny and advanced important findings on the biogeographical histories of its members. Using past reviews Biology as a backdrop, we have ventured to present an up-to-date assessment of the taxonomy, phylogenetic Epidemiology relationships and epidemiology of the genus Trichinella with additional insights on host species, survival Genomics strategies in nature and the shortcomings of our current understanding of the epidemiology of the genus. Proteomics In addition, we have begun compiling information available to date on genomics, proteomics, transcripto- mics and population studies of consequence in the hope we can build on this in years to come. Ó 2013 Australian Society for Parasitology Inc. Published by Elsevier Ltd. All rights reserved. 1. Introduction sults from consumer perceptions of ingesting infected meat, acci- dentally introduced into the food chain. However, even if Nematodes of the genus Trichinella are zoonotic parasites with a Trichinella infections have never been documented in pigs raised cosmopolitan distribution and which infect over 2,500 people in high containment facilities, testing for Trichinella is still required annually (Murrell and Pozio, 2011). This nematode was discovered for pork products within the international trade market. This addi- 177 years ago in the United Kingdom during an autopsy on a tional testing and product validation can in many cases escalate woman of Italian origin and was named Trichina spiralis Owen, the price of imported meats making them less competitive at 1835. At first, this parasite was considered only a scientific curios- neighbourhood food stores. ity. However, in 1860, the pathologist Zenker demonstrated its In addition to persistent economic and sanitary interests, the pathogenicity to humans (Campbell, 1983). This heightened its genus Trichinella represents a very interesting model to study bio- interest for the scientific community. This was followed in 1895 logical mechanisms due its uniqueness among nematodes and its with a change in name of the genus to Trichinella Railliet, 1895 broad host spectrum which includes more than 100 species of as the designation Trichina had been utilised for a genus of Diptera mammals, birds and reptiles (Pozio, 2005). For these reasons, the since 1830 (Gould, 1970). At that time and for the next hundred scientific literature has become substantially enriched in recent years, the large number of human infections due to the consump- times. The aim of this review is to amalgamate past knowledge tion of domestic pork products focused the attention of veterinar- with new data on the taxonomy, phylogeny, genome and epidemi- ians, physicians and public health authorities on the important role ology of Trichinella parasites, and provide a comprehensive view of of pigs in the natural cycle of this nematode (Campbell, 1983). our understanding of the genus to date. However, as with all scien- However, the basic science related to the biology and epidemiology tific research, each contemporary piece of the ‘‘Trichinella puzzle’’ of these zoonotic nematodes was not sufficiently studied. will be met with new questions to be addressed. Even amidst a strong reduction in Trichinella infections in domestic pigs and humans over the last decade, this parasite group continues to represent a ‘‘black mark’’ for the pig industry. This re- 2. Taxonomy and epidemiology For more than 130 years after its discovery, Trichinella spiralis ⇑ Corresponding author. Tel.: +39 06 4990 2304; fax: +39 06 4990 3561. was considered the only species in the genus even amidst increas- E-mail address: [email protected] (E. Pozio). ing numbers of studies showing substantial biological variability 0020-7519/$36.00 Ó 2013 Australian Society for Parasitology Inc. Published by Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ijpara.2013.05.010 984 E. Pozio, D.S. Zarlenga / International Journal for Parasitology 43 (2013) 983–997 among isolates originating from different geographical regions and animals (Pozio and Murrell, 2006). This species is well adapted to hosts (Dick, 1983). In 1972, three new species, named Trichinella domestic and wild pigs (Sus scrofa) which represent the most nativa, Trichinella nelsoni and Trichinella pseudospiralis, were de- important reservoir for this parasite. Furthermore, T. spiralis has scribed (Britov and Boev, 1972; Garkavi, 1972). Twenty years later, been detected frequently in carnivores and rodents, and less so in the genus was revised and a new species, designated Trichinella horses and armadillos (International Trichinella Reference Centre britovi, was identified in addition to three other genotypes, (ITRC) http://www.iss.it/site/Trichinella/scripts/; Table 1). The core Trichinella T5, T6 and T8 (Pozio et al., 1992). During the last distribution area of T. spiralis extends to eastern Asia (China, Laos, 12 years, the increasing number of investigations in different geo- Myanmar, South Korea, Thailand, Vietnam). Trichinella spiralis is graphical regions and hosts coupled with the availability of new widespread throughout Europe, Egypt, North America (Mexico and highly sensitive molecular techniques has allowed the descrip- and USA) and South America (Argentina, Bolivia and Chile), Hawaii tion of four new species (Trichinella murrelli, Trichinella papuae, and New Zealand (Fig. 1A). A previous focus of T. spiralis in Canada Trichinella zimbabwensis and Trichinella patagoniensis) and one seems to have been eradicated inasmuch as T. spiralis has not been new genotype (Trichinella T9) (Pozio and Zarlenga, 2005; Krivokap- isolated from domestic or wild animals from this region in over ich et al., 2012). The distribution of each Trichinella taxon are 40 years (Gajadhar and Forbes, 2010). In T. spiralis endemic areas, shown in Figs. 1 and 2. the number of infected domestic and wild animals tends to coincide Today, two main clades have been recognised in the genus with the integrity of pig husbandry and wildlife management (Raf- Trichinella; one that encompasses species that encapsulate in host ter et al., 2005; Burke et al., 2008; Blaga et al., 2009; Pozio et al., muscle tissues following muscle cell reprogramming, and a second 2009b). The genetic variability of the T. spiralis population from that does not encapsulate (Zarlenga et al., 2006; Pozio et al., eastern Asia is substantially higher than that observed in other geo- 2009a). The species and genotypes of the first clade parasitise only graphical locations, suggesting the recent introduction of this spe- mammals. Among the three species that comprise the second cies into Europe and the Americas (Zarlenga et al., 2006; clade, one infects mammals and birds (T. pseudospiralis) and two Rosenthal et al., 2008; La Rosa et al., 2012). The first appearances parasitise mammals and reptiles (T. papuae and T. zimbabwensis) of T. spiralis in North and South America and New Zealand are likely (Pozio et al., 2009a). to have been the result of passive introduction with domestic pigs The existence of two clades within the genus Trichinella is also and/or synanthropic rats during colonisations by European immi- supported by the geographical distribution
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