Opinion
Parasites ramble on: Focus on food security
Searching for Trichinella: not all pigs are created equal Edoardo Pozio Department of Infectious, Parasitic, and Immunomediated Diseases, Istituto Superiore di Sanita`, viale Regina Elena 299, 00161 Rome, Italy
Each year, millions of pigs worldwide are tested for Trichinella spp. at slaughterhouses with negative results. Yet, thousands of people acquire trichinellosis by consuming pork. So, where is the problem? Testing for Trichinella spp. is often performed on the ‘wrong’ animals; while the parasites are mainly circulating in backyard and free-ranging pigs, herds kept under controlled management conditions are the ones tested. Veterinary services should: (i) introduce a risk-based surveillance system for Trichinella by documenting the control of housing conditions and feedstuff sources, and (ii) introduce a capillary network of field laboratories for monitoring the parasites in free-ranging and backyard pigs. Investment of funds into the education of farmers, hunters, and consumers should be a priority for public health services. Notions for defining the Trichinella problem in pigs Nematode worms of the genus Trichinella are zoonotic parasites with a cosmopolitan distribution on all continents but Antarctica [1]. These pathogens are the etiological agents of trichinellosis, a serious, sometimes fatal, human disease, which has been documented in 55 countries of the world [2,3]. Humans acquire the infection by the ingestion of raw or semi-raw meat and meat derived products from domestic pigs, horses, dogs, and wild animals (e.g., wild boars, bears, badgers, and walruses) [3]. At the country level, the occurrence of Trichinella spp. in domestic and/ or wild animals is a necessary but not sufficient condition for the occurrence of trichinellosis. Food behavior is the main risk factor to acquire this zoonotic infection [4]. At present, nine species and three genotypes divided into two clades are recognized in the genus Trichinella [1]. All taxa are potentially zoonotic, but to date only six species and one genotype have been detected in humans [1,2]. More than 100 species of mammals, birds, and reptiles are known hosts of Trichinella parasites [5]; although most are wild animals, these parasites have also been detected in domestic pigs, horses, dogs, and cats [5]. Corresponding author: Pozio, E. ([email protected]). Keywords: pigs; Trichinella; backyard; free-ranging; risk-based surveillance; audit; controlled housing. 1471-4922/$ – see front matter ß 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.pt.2013.11.001
4
Trends in Parasitology, January 2014, Vol. 30, No. 1
In 1860, the German pathologist F.A. Zenker first identified the domestic pig as a possible source of infection for humans. Over the next few years, the domestic pig was identified as the main reservoir of Trichinella spiralis, and pork was recognized as the main source of trichinellosis for humans, both of which have substantial consequences for public health and the meat trade [6]. In 1863, the German state of Ducky of Brunswick introduced mandatory inspection of pig carcasses for Trichinella larvae by a hand lens and a microscope at 100 magnification. By the end of the 19th century, the trichinoscopy of slaughtered pigs had become common in Germany and in much of Western Europe. In the USA, the trichinoscopy examination of pig carcasses was introduced in Chicago in 1891 for pork exported to Europe, but not for the local market [6]. Before World War II, trichinellosis caused by the consumption of infected pork continued to be an important public health concern with thousands of cases in North, Central, and South America (mainly in the USA, Mexico, Argentina, and Chile), and in Europe (mainly in Germany, Poland, Romania, Spain, and former Yugoslavia) [7]. Following the War, the prevalence of Trichinella spp. in domestic pigs was drastically reduced, owing to the improvement of rearing practices in most pig production. However, even in industrialized countries where the majority of pigs originate from herds kept under controlled management conditions, there is almost always a percentage of them that often elude veterinary oversight, for example, backyard and free-ranging animals. Thus, thousands of people end up acquiring trichinellosis by consuming pork from these animals. Furthermore, there are several examples where countries had suitable controls in place for parasite management in domestic pigs, but changes in pork production affected by socioeconomic conflicts have resulted in the reemergence of trichinellosis as a serious public health problem [8,9]. Epidemiology of Trichinella spp. Trichinella spp. are transmitted from one animal to another, or to a human, solely by the ingestion of muscle tissues infected with encysted Trichinella larvae. Wild mammals serve as the major reservoir hosts, and the role of wildlife is underscored by the biomass of the parasites, which is greater in wild than domestic animals, unlike other nematode infections that involve both sylvatic and domestic animals. When humans fail to properly manage domestic pigs and wildlife, Trichinella spp., particularly
Opinion
(A)
Trends in Parasitology January 2014, Vol. 30, No. 1
(B)
(D)
(C)
(E)
TRENDS in Parasitology
Figure 1. Pig-rearing practices and Trichinella spp. transmission. When humans fail in the proper management of domestic animals and wildlife, Trichinella (especially T. spiralis) infection is transmitted from the sylvatic to the domestic environment. In addition, Trichinella species can be transferred in a reversible path from domestic animals to wildlife. (A) Pigs under controlled housing conditions; Trichinella spp. larvae have never been detected in these pigs, which should not be tested or monitored for Trichinella spp. infections. Veterinary services ensure the good rearing practices by farm audits. (B) and (C) are backyard and free-ranging pigs, respectively; these pigs are at high risk for Trichinella spp. infections. (D) and (E) are wild carnivorous and omnivorous mammals, respectively. These animals are the natural reservoirs of most Trichinella species.
T. spiralis, are transmitted from the sylvatic to the domestic environment, triggering the onset of the domestic cycle. This cycle occurs where there are high-risk farming practices, such as the intentional feeding of food waste, which may contain pork scraps, or unintentionally through exposure to carcasses of dead swine or infected wildlife; unsecured, free-range pasturing is typically to blame [10]. Farming practices at risk for Trichinella spp. transmission occur, in general, in disadvantaged and poor areas where veterinary services do not exist or are unable to control the myriad of small pig units (Figure 1). A comprehensive epidemiological picture of the domestic transmission cycle also includes other sources: (i) pigs allowed to scavenge in garbage dumps; (ii) feeding of wild game carcasses or scraps from hunting; and (iii) the use of carcasses of slaughtered fur animals as feed (Box 1). The intersection of hunters, the manner in which they deal with wild game carcasses, and free-ranging and/or backyard pig farming practices combine to perpetuate infection with Trichinella spp. Global pig production According to the Food and Agricultural Organization (www.fao.org/ag/againfo/themes/en/pigs/home.html), out of all terrestrial animals, pork meat has the highest consumption worldwide. In recent decades, changes in consumption patterns have pushed up the demand for pork as incomes have increased in developing countries with fast-
growing economies. The global yearly pig production is forecast to reach 1 billion by 2015, which is double compared with the 1970s; approximately half of the pigs are raised in China. Pig production is global, except for some regions with cultural and religious reservations regarding the consumption of pork and is characterized by an increasing dichotomy of production systems: traditional subsistence-driven smallscale production on the one side, and specialized industrial farming on the other. Indoor farms are now responsible for more than half of the global pig production, but indoor farming alone does not prevent Trichinella spp. transmission if controlled management conditions are not in place. Trichinella species infecting swine Because Trichinella spp./genotypes lack or differ in the level of infectivity to pigs, it is important to know what taxon/taxa is/are circulating or can be introduced into a country by different hosts (Figure 2). Out of the 12 taxa of the Trichinella genus, T. spiralis is the species better adapted to, and more frequently detected in swine (both domestic and sylvatic), in which it can reach a high worm burden (up to 8000 larvae/g in the diaphragm pillar) without causing clinical disease [1]. Moreover, T. spiralis shows a cosmopolitan distribution because humans have passively introduced it on most continents by animal movement, increasing the risk for public health [11,12]. 5
Opinion Box 1. Rearing practices favoring or preventing transmission of Trichinella spp. Rearing practices involved in transmission of Trichinella spp. to domestic pigs Feed on wild animal carcasses. Hunters who leave animal carcasses in the field after skinning, or remove and discard the entrails, or dispose of in dumps. Hunters who feed pigs with animal carcasses. Road-killed wild animals. Introduction of new pigs on a farm without any information on the farm of origin and previous farming conditions. Cannibalism due to a high mortality rate. Feed on garbage containing pork or wild animal scraps. Feed on pork scraps from pigs slaughtered at the farm. Feed on carcasses or scraps from farmed fur animals (both mammals and reptiles). Feed on rats, which can play the role of Trichinella spp. ‘vector’ from one farm to another. Feed origin and correct daily feed intake not always controlled. Lack of mechanical barriers to prevent entry of synanthropic and wild animals (both mammals and birds) into the pigsty. Rearing practices to prevent Trichinella spp. transmission to domestic pigs Facilities and the surrounding environment should be managed to prevent exposure of pigs to rodents and wildlife (both mammals and birds). Raw food waste of animal origin should not be present on farms. Feed should be obtained from a facility with production in accordance with feed hygiene and should be stored in a manner to prevent access by rodents and wildlife. A rodent control program should be in place [Box 2 (role of rats in Trichinella spp. transmission)]. Dead pigs should be immediately removed and disposed of in accordance with good rearing practices. Introduced pigs should originate from herds officially recognized as being under controlled management conditions, or from herds of a compartment with a negligible risk of Trichinella spp. infection. Pigs present at the farm should be identifiable so that each animal can be traced back to the holding. Pigs should only have access to outdoor facilities if they do not pose a danger for the introduction of Trichinella spp. in the holding.
Trends in Parasitology January 2014, Vol. 30, No. 1
98%
T. nava Trichinella T6
97%
Trichinella T9 T. murelli
99%
Trichinella T8 63%
36%
T. britovi 99%
T. patagoniesis
94%
6%
T. nelsoni
86%
T. spiralis
T. papuae
10% 35%
48%
98%
T. zimbabwensis
9%
T. pseudospiralis 54%
27%
TRENDS in Parasitology
To improve the pig compartment at the national level, veterinary services can develop a swine registry, a reporting system of Trichinella spp. infections in both pigs and humans, and georeference Trichinella-infected pig herds with information on the management conditions, that is, controlled versus uncontrolled conditions.
Trichinella britovi and Trichinella nelsoni can infect both domestic and sylvatic swine, but to a lesser degree than T. spiralis, in terms of larval burden and the length of time that the larva are able to survive in muscles [13,14]. Furthermore, these two species show a restricted geographical distribution compared with T. spiralis; T. britovi circulates in the temperate regions of Europe, West Asia, North and West Africa, and T. nelsoni circulates in East Africa [1]. Trichinella nativa, Trichinella murrelli, Trichinella patagoniensis, and the genotype Trichinella T6 show a very low larval burden in the muscles of experimentally infected swine even when challenged with high infectious doses and, consequently, do not represent a concern for public health [13–15]. Trichinella pseudospiralis, which infects mammals and birds, and Trichinella papuae and Trichinella zimbabwensis, which are both infectious to 6
Figure 2. Trichinella taxa and their main hosts. The fox and hyena are shown as representatives of carnivores of the American, Asian, and European continents, and of Africa, respectively. The pig is meant to represent all domestic and wild swine races and species. The crocodile represents the Nile crocodile (for Trichinella zimbabwensis) or the saltwater crocodile (for Trichinella papuae). The raptorial bird represents carnivorous birds. The percentages refer to the probability of detecting the Trichinella taxon in a host group. Host groups of minor epidemiological importance are not shown. Data on the relationships between Trichinella spp. and hosts, and the maximum likelihood tree of the genus Trichinella are from [1].
mammals and reptiles, develop in pigs but with a worm burden lower than that of T. spiralis [13,14] (Figure 1). No information is available on the infectivity of the other two taxa, Trichinella T8 and T9, to pigs. Epidemiology of Trichinella in pigs Europe Most of the pig population is subjected to routine testing for Trichinella spp. on the European continent. In the past 20 years, Trichinella spp. have not been detected in domestic pigs of Austria, Belgium, Cyprus, Czech Republic, Denmark, Iceland, Ireland, Luxembourg, Malta, The Netherlands, Norway, Portugal, Slovenia, Sweden,
Opinion
Trends in Parasitology January 2014, Vol. 30, No. 1
Table 1. Foci of Trichinella spp. infections in domestic pigs of Europe and America Country Belarus Bosnia and Herzegovina Bulgaria Croatia Estonia Finland France Germany Greece Hungary
Controlled systems a No data No data 0.0/0.35 million 2288c/7 068 532 0.0/0.48 million 0.0/4.8 million 0.0/16 million 0.0/49 million 0.0/4.5 million 0.0/4.0 million
Reference period 1980–1989 1997–2000 2006–2012 1998–2006 1994–2012 1995–2004 2004–2012 2003–2012 2009–2012 2000–2012
0.0/9.0 million 0.0/0.3 million 0.0/0.8 million 0.0/20 million 0.0/0.1 million 0.0/0.05 million 0.0/3.0 million 0.0/1.7 million
Non-controlled systems b 0.0005% 300/unknown 40/unknown 13 866/6 294 308 d 1 in 1994, 1 in 1999 343/unknown 19e/unknown 8/unknown 36/12,717 2 in 2000, 6 in 2003, 4 in 2009 17/unknown 2/unknown 84/unknown 342/unknown Not available 26–42/unknown 404/unknown 461–2875/unknown
Italy Latvia Lithuania Poland Macedonia Montenegro Romania Serbia Slovakia Spain Argentina Canada Chile Mexico USA
0.0/0.8 million 0.0/38 million 0.0/1.5 million 0.0/30 000 287/56 million 0.0/10 million 0.0/85 million
Sporadic reports 160/9000 100/1 million 0.0/30 000 Sporadic reports 10/150 000 f 10–20/15 million
2000–2011 2004–2008 2008–2012 1998–2012 2001–2012 2009–2012 2003–2012
2005–2012 2011 2006–2011 2001–2011 2000–2003 2000–2003 2007–2011 2001–2010
Refs [57] [9] [58–64] (A. Marinculic, personal communication) [58–65] [58–64,66] (I. Vallee, personal communication) (K. No¨ckler, personal communication) [71] (T. Sreter, personal communication) [58–64,67] (E. Pozio, unpublished) (M. Kirjusina, personal communication) (R. Bubulienne, personal communication) (M. Ro´z˙ycki, personal communication) [9] [9] [58–64] (Lj. Sofronic-Milosavljevic, personal communication) [53] [68] [58–64] (M. Ribicich, personal communication) [20] (H. Schenone, personal communication) [24,25] (R. Gamble, personal communication)
a
Prevalence or number of infected pigs in controlled systems per year.
b
Prevalence or number of infected pigs in non-controlled systems per year.
c
By intentional infection.
d
In the whole 9-year period.
e
On Corsica island.
f
Modified from [25] for the period 1981–1994.
Switzerland, and the UK [2]. In five city states, Andorra, Liechtenstein, Monaco, San Marino, and the Vatican City, there were no epidemiological conditions to support the circulation of Trichinella. No information is available for Albania, Armenia, Azerbaijan, Moldova, and Turkey. Trichinella spp. have been documented in backyard and free-ranging pigs of Georgia, Russia, and the Ukraine, but no quantitative data are available. In other European countries (Table 1), T. spiralis, T. britovi, and/or T. pseudospiralis have been detected sporadically, compared with the number of slaughtered pigs, in domestic pigs reared in herds kept without controlled management conditions. In the 27 EU countries, the distribution of the pig population by size of the pig herds (in numbers of fattening pigs) showed that 1.5% of pig farms have at least 400 fattening pigs and manage 75.7% of them (approximately 120 million animals) [16]. These figures conceal national differences; for example, only 21.6% of fattening pigs in Poland are kept under controlled conditions on farms as compared with 90% or more in nine other EU countries. However, pigs kept in units of less than 10 animals represent a consistent part of the pig population in Bulgaria (34.8%), Lithuania (31.9%), and Romania (66.2%). These small units manage 5.3% of fattening pigs (approximately 8.5 million animals), but account for 85.8% of the pig farms [16].
Routine testing of most slaughtered pigs according to Regulation 2075/2005 in the EU [17] allowed removal of several hundred Trichinella spp. infected animals from the food chain per year and identification of the farms at risk for these parasites. However, the EU regulation only affects pigs slaughtered for the market; those used for private consumption, many of which are backyard and/or free-ranging pigs, frequently escape veterinary controls. The Americas In Canada, from 1998 to 2012, Trichinella spp. were not detected in the 30 000 tested out of the 12 million pigs slaughtered yearly, and no trichinellosis cases occurred from the consumption of pork [18–20]. Similar to what is found in the EU, the distribution of the pig population in the USA by size of the pig herds showed that 21.4% of pig farms have at least 500 pigs and manage 97.3% of the total pig population (approximately 115 million animals), whereas 78.6% of pig farms are small units (
Parasites ramble on: Focus on food security
Searching for Trichinella: not all pigs are created equal Edoardo Pozio Department of Infectious, Parasitic, and Immunomediated Diseases, Istituto Superiore di Sanita`, viale Regina Elena 299, 00161 Rome, Italy
Each year, millions of pigs worldwide are tested for Trichinella spp. at slaughterhouses with negative results. Yet, thousands of people acquire trichinellosis by consuming pork. So, where is the problem? Testing for Trichinella spp. is often performed on the ‘wrong’ animals; while the parasites are mainly circulating in backyard and free-ranging pigs, herds kept under controlled management conditions are the ones tested. Veterinary services should: (i) introduce a risk-based surveillance system for Trichinella by documenting the control of housing conditions and feedstuff sources, and (ii) introduce a capillary network of field laboratories for monitoring the parasites in free-ranging and backyard pigs. Investment of funds into the education of farmers, hunters, and consumers should be a priority for public health services. Notions for defining the Trichinella problem in pigs Nematode worms of the genus Trichinella are zoonotic parasites with a cosmopolitan distribution on all continents but Antarctica [1]. These pathogens are the etiological agents of trichinellosis, a serious, sometimes fatal, human disease, which has been documented in 55 countries of the world [2,3]. Humans acquire the infection by the ingestion of raw or semi-raw meat and meat derived products from domestic pigs, horses, dogs, and wild animals (e.g., wild boars, bears, badgers, and walruses) [3]. At the country level, the occurrence of Trichinella spp. in domestic and/ or wild animals is a necessary but not sufficient condition for the occurrence of trichinellosis. Food behavior is the main risk factor to acquire this zoonotic infection [4]. At present, nine species and three genotypes divided into two clades are recognized in the genus Trichinella [1]. All taxa are potentially zoonotic, but to date only six species and one genotype have been detected in humans [1,2]. More than 100 species of mammals, birds, and reptiles are known hosts of Trichinella parasites [5]; although most are wild animals, these parasites have also been detected in domestic pigs, horses, dogs, and cats [5]. Corresponding author: Pozio, E. ([email protected]). Keywords: pigs; Trichinella; backyard; free-ranging; risk-based surveillance; audit; controlled housing. 1471-4922/$ – see front matter ß 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.pt.2013.11.001
4
Trends in Parasitology, January 2014, Vol. 30, No. 1
In 1860, the German pathologist F.A. Zenker first identified the domestic pig as a possible source of infection for humans. Over the next few years, the domestic pig was identified as the main reservoir of Trichinella spiralis, and pork was recognized as the main source of trichinellosis for humans, both of which have substantial consequences for public health and the meat trade [6]. In 1863, the German state of Ducky of Brunswick introduced mandatory inspection of pig carcasses for Trichinella larvae by a hand lens and a microscope at 100 magnification. By the end of the 19th century, the trichinoscopy of slaughtered pigs had become common in Germany and in much of Western Europe. In the USA, the trichinoscopy examination of pig carcasses was introduced in Chicago in 1891 for pork exported to Europe, but not for the local market [6]. Before World War II, trichinellosis caused by the consumption of infected pork continued to be an important public health concern with thousands of cases in North, Central, and South America (mainly in the USA, Mexico, Argentina, and Chile), and in Europe (mainly in Germany, Poland, Romania, Spain, and former Yugoslavia) [7]. Following the War, the prevalence of Trichinella spp. in domestic pigs was drastically reduced, owing to the improvement of rearing practices in most pig production. However, even in industrialized countries where the majority of pigs originate from herds kept under controlled management conditions, there is almost always a percentage of them that often elude veterinary oversight, for example, backyard and free-ranging animals. Thus, thousands of people end up acquiring trichinellosis by consuming pork from these animals. Furthermore, there are several examples where countries had suitable controls in place for parasite management in domestic pigs, but changes in pork production affected by socioeconomic conflicts have resulted in the reemergence of trichinellosis as a serious public health problem [8,9]. Epidemiology of Trichinella spp. Trichinella spp. are transmitted from one animal to another, or to a human, solely by the ingestion of muscle tissues infected with encysted Trichinella larvae. Wild mammals serve as the major reservoir hosts, and the role of wildlife is underscored by the biomass of the parasites, which is greater in wild than domestic animals, unlike other nematode infections that involve both sylvatic and domestic animals. When humans fail to properly manage domestic pigs and wildlife, Trichinella spp., particularly
Opinion
(A)
Trends in Parasitology January 2014, Vol. 30, No. 1
(B)
(D)
(C)
(E)
TRENDS in Parasitology
Figure 1. Pig-rearing practices and Trichinella spp. transmission. When humans fail in the proper management of domestic animals and wildlife, Trichinella (especially T. spiralis) infection is transmitted from the sylvatic to the domestic environment. In addition, Trichinella species can be transferred in a reversible path from domestic animals to wildlife. (A) Pigs under controlled housing conditions; Trichinella spp. larvae have never been detected in these pigs, which should not be tested or monitored for Trichinella spp. infections. Veterinary services ensure the good rearing practices by farm audits. (B) and (C) are backyard and free-ranging pigs, respectively; these pigs are at high risk for Trichinella spp. infections. (D) and (E) are wild carnivorous and omnivorous mammals, respectively. These animals are the natural reservoirs of most Trichinella species.
T. spiralis, are transmitted from the sylvatic to the domestic environment, triggering the onset of the domestic cycle. This cycle occurs where there are high-risk farming practices, such as the intentional feeding of food waste, which may contain pork scraps, or unintentionally through exposure to carcasses of dead swine or infected wildlife; unsecured, free-range pasturing is typically to blame [10]. Farming practices at risk for Trichinella spp. transmission occur, in general, in disadvantaged and poor areas where veterinary services do not exist or are unable to control the myriad of small pig units (Figure 1). A comprehensive epidemiological picture of the domestic transmission cycle also includes other sources: (i) pigs allowed to scavenge in garbage dumps; (ii) feeding of wild game carcasses or scraps from hunting; and (iii) the use of carcasses of slaughtered fur animals as feed (Box 1). The intersection of hunters, the manner in which they deal with wild game carcasses, and free-ranging and/or backyard pig farming practices combine to perpetuate infection with Trichinella spp. Global pig production According to the Food and Agricultural Organization (www.fao.org/ag/againfo/themes/en/pigs/home.html), out of all terrestrial animals, pork meat has the highest consumption worldwide. In recent decades, changes in consumption patterns have pushed up the demand for pork as incomes have increased in developing countries with fast-
growing economies. The global yearly pig production is forecast to reach 1 billion by 2015, which is double compared with the 1970s; approximately half of the pigs are raised in China. Pig production is global, except for some regions with cultural and religious reservations regarding the consumption of pork and is characterized by an increasing dichotomy of production systems: traditional subsistence-driven smallscale production on the one side, and specialized industrial farming on the other. Indoor farms are now responsible for more than half of the global pig production, but indoor farming alone does not prevent Trichinella spp. transmission if controlled management conditions are not in place. Trichinella species infecting swine Because Trichinella spp./genotypes lack or differ in the level of infectivity to pigs, it is important to know what taxon/taxa is/are circulating or can be introduced into a country by different hosts (Figure 2). Out of the 12 taxa of the Trichinella genus, T. spiralis is the species better adapted to, and more frequently detected in swine (both domestic and sylvatic), in which it can reach a high worm burden (up to 8000 larvae/g in the diaphragm pillar) without causing clinical disease [1]. Moreover, T. spiralis shows a cosmopolitan distribution because humans have passively introduced it on most continents by animal movement, increasing the risk for public health [11,12]. 5
Opinion Box 1. Rearing practices favoring or preventing transmission of Trichinella spp. Rearing practices involved in transmission of Trichinella spp. to domestic pigs Feed on wild animal carcasses. Hunters who leave animal carcasses in the field after skinning, or remove and discard the entrails, or dispose of in dumps. Hunters who feed pigs with animal carcasses. Road-killed wild animals. Introduction of new pigs on a farm without any information on the farm of origin and previous farming conditions. Cannibalism due to a high mortality rate. Feed on garbage containing pork or wild animal scraps. Feed on pork scraps from pigs slaughtered at the farm. Feed on carcasses or scraps from farmed fur animals (both mammals and reptiles). Feed on rats, which can play the role of Trichinella spp. ‘vector’ from one farm to another. Feed origin and correct daily feed intake not always controlled. Lack of mechanical barriers to prevent entry of synanthropic and wild animals (both mammals and birds) into the pigsty. Rearing practices to prevent Trichinella spp. transmission to domestic pigs Facilities and the surrounding environment should be managed to prevent exposure of pigs to rodents and wildlife (both mammals and birds). Raw food waste of animal origin should not be present on farms. Feed should be obtained from a facility with production in accordance with feed hygiene and should be stored in a manner to prevent access by rodents and wildlife. A rodent control program should be in place [Box 2 (role of rats in Trichinella spp. transmission)]. Dead pigs should be immediately removed and disposed of in accordance with good rearing practices. Introduced pigs should originate from herds officially recognized as being under controlled management conditions, or from herds of a compartment with a negligible risk of Trichinella spp. infection. Pigs present at the farm should be identifiable so that each animal can be traced back to the holding. Pigs should only have access to outdoor facilities if they do not pose a danger for the introduction of Trichinella spp. in the holding.
Trends in Parasitology January 2014, Vol. 30, No. 1
98%
T. nava Trichinella T6
97%
Trichinella T9 T. murelli
99%
Trichinella T8 63%
36%
T. britovi 99%
T. patagoniesis
94%
6%
T. nelsoni
86%
T. spiralis
T. papuae
10% 35%
48%
98%
T. zimbabwensis
9%
T. pseudospiralis 54%
27%
TRENDS in Parasitology
To improve the pig compartment at the national level, veterinary services can develop a swine registry, a reporting system of Trichinella spp. infections in both pigs and humans, and georeference Trichinella-infected pig herds with information on the management conditions, that is, controlled versus uncontrolled conditions.
Trichinella britovi and Trichinella nelsoni can infect both domestic and sylvatic swine, but to a lesser degree than T. spiralis, in terms of larval burden and the length of time that the larva are able to survive in muscles [13,14]. Furthermore, these two species show a restricted geographical distribution compared with T. spiralis; T. britovi circulates in the temperate regions of Europe, West Asia, North and West Africa, and T. nelsoni circulates in East Africa [1]. Trichinella nativa, Trichinella murrelli, Trichinella patagoniensis, and the genotype Trichinella T6 show a very low larval burden in the muscles of experimentally infected swine even when challenged with high infectious doses and, consequently, do not represent a concern for public health [13–15]. Trichinella pseudospiralis, which infects mammals and birds, and Trichinella papuae and Trichinella zimbabwensis, which are both infectious to 6
Figure 2. Trichinella taxa and their main hosts. The fox and hyena are shown as representatives of carnivores of the American, Asian, and European continents, and of Africa, respectively. The pig is meant to represent all domestic and wild swine races and species. The crocodile represents the Nile crocodile (for Trichinella zimbabwensis) or the saltwater crocodile (for Trichinella papuae). The raptorial bird represents carnivorous birds. The percentages refer to the probability of detecting the Trichinella taxon in a host group. Host groups of minor epidemiological importance are not shown. Data on the relationships between Trichinella spp. and hosts, and the maximum likelihood tree of the genus Trichinella are from [1].
mammals and reptiles, develop in pigs but with a worm burden lower than that of T. spiralis [13,14] (Figure 1). No information is available on the infectivity of the other two taxa, Trichinella T8 and T9, to pigs. Epidemiology of Trichinella in pigs Europe Most of the pig population is subjected to routine testing for Trichinella spp. on the European continent. In the past 20 years, Trichinella spp. have not been detected in domestic pigs of Austria, Belgium, Cyprus, Czech Republic, Denmark, Iceland, Ireland, Luxembourg, Malta, The Netherlands, Norway, Portugal, Slovenia, Sweden,
Opinion
Trends in Parasitology January 2014, Vol. 30, No. 1
Table 1. Foci of Trichinella spp. infections in domestic pigs of Europe and America Country Belarus Bosnia and Herzegovina Bulgaria Croatia Estonia Finland France Germany Greece Hungary
Controlled systems a No data No data 0.0/0.35 million 2288c/7 068 532 0.0/0.48 million 0.0/4.8 million 0.0/16 million 0.0/49 million 0.0/4.5 million 0.0/4.0 million
Reference period 1980–1989 1997–2000 2006–2012 1998–2006 1994–2012 1995–2004 2004–2012 2003–2012 2009–2012 2000–2012
0.0/9.0 million 0.0/0.3 million 0.0/0.8 million 0.0/20 million 0.0/0.1 million 0.0/0.05 million 0.0/3.0 million 0.0/1.7 million
Non-controlled systems b 0.0005% 300/unknown 40/unknown 13 866/6 294 308 d 1 in 1994, 1 in 1999 343/unknown 19e/unknown 8/unknown 36/12,717 2 in 2000, 6 in 2003, 4 in 2009 17/unknown 2/unknown 84/unknown 342/unknown Not available 26–42/unknown 404/unknown 461–2875/unknown
Italy Latvia Lithuania Poland Macedonia Montenegro Romania Serbia Slovakia Spain Argentina Canada Chile Mexico USA
0.0/0.8 million 0.0/38 million 0.0/1.5 million 0.0/30 000 287/56 million 0.0/10 million 0.0/85 million
Sporadic reports 160/9000 100/1 million 0.0/30 000 Sporadic reports 10/150 000 f 10–20/15 million
2000–2011 2004–2008 2008–2012 1998–2012 2001–2012 2009–2012 2003–2012
2005–2012 2011 2006–2011 2001–2011 2000–2003 2000–2003 2007–2011 2001–2010
Refs [57] [9] [58–64] (A. Marinculic, personal communication) [58–65] [58–64,66] (I. Vallee, personal communication) (K. No¨ckler, personal communication) [71] (T. Sreter, personal communication) [58–64,67] (E. Pozio, unpublished) (M. Kirjusina, personal communication) (R. Bubulienne, personal communication) (M. Ro´z˙ycki, personal communication) [9] [9] [58–64] (Lj. Sofronic-Milosavljevic, personal communication) [53] [68] [58–64] (M. Ribicich, personal communication) [20] (H. Schenone, personal communication) [24,25] (R. Gamble, personal communication)
a
Prevalence or number of infected pigs in controlled systems per year.
b
Prevalence or number of infected pigs in non-controlled systems per year.
c
By intentional infection.
d
In the whole 9-year period.
e
On Corsica island.
f
Modified from [25] for the period 1981–1994.
Switzerland, and the UK [2]. In five city states, Andorra, Liechtenstein, Monaco, San Marino, and the Vatican City, there were no epidemiological conditions to support the circulation of Trichinella. No information is available for Albania, Armenia, Azerbaijan, Moldova, and Turkey. Trichinella spp. have been documented in backyard and free-ranging pigs of Georgia, Russia, and the Ukraine, but no quantitative data are available. In other European countries (Table 1), T. spiralis, T. britovi, and/or T. pseudospiralis have been detected sporadically, compared with the number of slaughtered pigs, in domestic pigs reared in herds kept without controlled management conditions. In the 27 EU countries, the distribution of the pig population by size of the pig herds (in numbers of fattening pigs) showed that 1.5% of pig farms have at least 400 fattening pigs and manage 75.7% of them (approximately 120 million animals) [16]. These figures conceal national differences; for example, only 21.6% of fattening pigs in Poland are kept under controlled conditions on farms as compared with 90% or more in nine other EU countries. However, pigs kept in units of less than 10 animals represent a consistent part of the pig population in Bulgaria (34.8%), Lithuania (31.9%), and Romania (66.2%). These small units manage 5.3% of fattening pigs (approximately 8.5 million animals), but account for 85.8% of the pig farms [16].
Routine testing of most slaughtered pigs according to Regulation 2075/2005 in the EU [17] allowed removal of several hundred Trichinella spp. infected animals from the food chain per year and identification of the farms at risk for these parasites. However, the EU regulation only affects pigs slaughtered for the market; those used for private consumption, many of which are backyard and/or free-ranging pigs, frequently escape veterinary controls. The Americas In Canada, from 1998 to 2012, Trichinella spp. were not detected in the 30 000 tested out of the 12 million pigs slaughtered yearly, and no trichinellosis cases occurred from the consumption of pork [18–20]. Similar to what is found in the EU, the distribution of the pig population in the USA by size of the pig herds showed that 21.4% of pig farms have at least 500 pigs and manage 97.3% of the total pig population (approximately 115 million animals), whereas 78.6% of pig farms are small units (
