G Model
ARTICLE IN PRESS
VETPAR-7662; No. of Pages 2
Veterinary Parasitology xxx (2015) xxx–xxx
Contents lists available at ScienceDirect
Veterinary Parasitology journal homepage: www.elsevier.com/locate/vetpar
Letter to the Editor About people, pig movements and pork ‘tapeworms’ To the Editor, Gabriël et al. (2015) stress the implications of human migration and pig/pork import in the introduction of new cases of Taenia solium (not only taeniosis but also cysticercosis) in the European Union (EU) in their recent article. The authors state that humans are the final host of the pork ‘tapeworm’, using the word in its singular form, while it would be more fitting to use the plural form, ‘tapeworms’. People and pigs do not only have T. solium in common. The third human Taenia, T. asiatica has the same life cycle as T. solium, therefore also affecting people and pigs. Indeed, the European Food Safety Authority (EFSA) has finally recognized that two Taenia species, T. solium and T. asiatica, are acquired by eating pork (EFSA, 2013, p. 33). We perfectly understand that the focus of the article by Gabriël et al. is exclusively T. solium, however, we would like to provide complementary information about other possible implications of human and pig/pork movements. Initially found in southeast Asian countries, T. asiatica is currently present in most of Asia and probably worldwide due to globalisation (Galán-Puchades and Fuentes, 2014a,b; Robertson et al., 2014). Its relative novelty (it was first described in 1993) (Eom and Rim, 1993), compared to the other two well-known human Taenia species (T. solium and T. saginata), as well as the general lack of awareness of the species at a global scale are probably hampering its diagnosis. As the authors of the article state, human cases of taeniasis, if analysed, are rarely investigated at species level. An appropriate molecular diagnostic method [the only tool to specifically distinguish the TriTaenias (Galán-Puchades and Fuentes, 2014a)] is, however, never performed by health professionals. Therefore, T. asiatica could well be present among all those non-specifically diagnosed cases of human taeniasis. From a veterinary point of view, the authors accurately underline the lack, not only of sensitivity, but also of specificity of meat inspection. They stress the necessity of distinguishing between T. solium and T. hydatigena at the early stages of infection. That assertion leads to the assumption that liver cysticerci are normally found in pigs at slaughterhouses. Pig liver is the dominant location of the cysticerci, not only of T. hydatigena, but also of T. asiatica. Therefore, unless a molecular confirmation is made, T. asiatica again could perfectly be among all those non-specifically diagnosed cases of pig cysticercosis. It is very likely that T. asiatica could be present in the EU due to the same human migratory movements that could import T. solium, according to Table 1 appearing in the article of Gabriël et al. (2015, p. 4), at least two of the top countries of origin of the immigrants into the EU are endemic for T. asiatica (China and Vietnam), and a third is highly suspected (Myanmar) (Ale et al., 2014), and although the
likelihood of the establishment of the T. asiatica life cycle in the EU by those supposed imported cases is remote, this probability is in fact higher than in the case of imported T. solium. The authors of the article underline the importance of the environmental contamination with Taenia eggs in the transmission of the infection (Gabriël et al., 2015; p. 4). T. asiatica, similarly to T. saginata, presents an active expulsion of the proglottids from of the body, therefore nonexclusively related to defecation, whereas T. solium only leaves the intestine with faeces. That means that migrating T. asiatica carriers would contaminate the environment considerably more with their shed eggs than those harbouring T. solium. Gabriël et al. (2015, p. 5–6) list several countries that are the origin of legal and illegal import of pig/pork to the EU and, among them, endemic countries for T. asiatica are also included (at least Japan, South Korea, China and Thailand), therefore the probability exists for this parasite to be also introduced at larval stage. If the detection of T. solium during meat inspection could be considered a challenge, the detection of the small T. asiatica cysticerci in the pork liver parenchyma might even be more difficult, particularly given the widespread lack of awareness among veterinarians with regard to T. asiatica as a pig parasite in addition to the other two well-known parasites T. solium and T. hydatigena (Galán-Puchades and Fuentes, 2014b). However, is the possibility that T. asiatica could be or has already been introduced in the EU a concern for public health? This question does not yet have a definite answer. On the one hand, it is still not known whether T. asiatica can cause human cysticercosis as T. solium does (Galán-Puchades and Fuentes, 2004). If this were the case, T. asiatica could actually be a threat to human health. On the other hand, it has been pointed out that due to interspecific competition, the presence of T. asiatica could limit the presence of T. solium since both species share the same hosts, humans and pigs (Conlan et al., 2009; Devleesschauwer et al., 2012). From this point of view, on the contrary, the introduction of T. asiatica in EU could even be beneficial. We absolutely agree with the authors of the paper that it is essential to make T. solium taeniasis/cysticercosis a notifiable disease, which had already been proposed 15 years ago (Román et al., 2000). If finally T. solium were declared notifiable, molecular tools should be used to specifically distinguish it from the other Taenia species, and it would be an excellent opportunity to investigate the true role of T. asiatica in this scenario of people and pig/pork moving around the world.
References Ale, A., Victor, B., Praet, N., Gabriel, S., Speybroek, N., Dorny, P., Devleesschauwer, B., 2014. Epidemiology and genetic diversity of Taenia asiatica: a systematic review. Parasite Vector 7, 45, http://dx.doi.org/10.1186/1756-3305-7-45 Devleesschauwer, B., Aryal, A., Joshi, D.D., Rijal, S., Sherchand, J.B., Praet, N., Speybroeck, N., Duchateau, L., Vercruysse, J., Dorny, P., 2012. Epidemiology of Taenia solium in Nepal: is it influenced by the social characteristics of the
http://dx.doi.org/10.1016/j.vetpar.2015.06.009 0304-4017/© 2015 Elsevier B.V. All rights reserved.
Please cite this article in press as: Galán-Puchades, M.T., Fuentes, M.V., About people, pig movements and pork ‘tapeworms’. Vet. Parasitol. (2015), http://dx.doi.org/10.1016/j.vetpar.2015.06.009
G Model VETPAR-7662; No. of Pages 2 2
ARTICLE IN PRESS Letter to the Editor / Veterinary Parasitology xxx (2015) xxx–xxx
population and the presence of Taenia asiatica. Trop. Med. Int. Health 17, 1019–1022. Conlan, J.V., Vongxay, K., Fenwick, S., Blacksell, S.D., Thompson, R.C., 2009. Does interspecific competition have a moderating effect on Taenia solium transmission dynamics in Southeast Asia. Trends Parasitol. 25, 398–403. EFSA, 2013. Technical specifications on harmonised epidemiological indicators for biological hazards to be covered by meat inspection of bovine animals. EFSA J. 11 (3276), 1–78. Eom, K.S., Rim, H.J., 1993. Morphologic descriptions of Taenia asiatica sp. n. Kor. J. Parasitol. 7, 1–6. Gabriël, S., Johansen, M.V., Pozio, E., Smit, G.S.A., Devleesschauwer, B., Allepuz, A., Papadopoulos, E., van der Giessen, J., Dorny, P., 2015. Human migration and pig/pork import in the European Union: What are the implications for Taenia solium infections? Vet. Parasitol., http://dx.doi.org/10.1016/j.vetpar.2015.03. 006 Galán-Puchades, M.T., Fuentes, M.V., 2004. Taenia asiatica intermediate hosts Taenia asiatica intermediate hosts. Lancet 363, 660. Galán-Puchades, M.T., Fuentes, M.V., 2014a. Taenia asiatica: left out by globalisation Taenia asiatica: left out by globalisation. Trends Parasitol. 30, 54–55. Galán-Puchades, M.T., Fuentes, M.V., 2014b. Parasitic porkborne hazards, globalisation, and meat inspection. Food Control 46, 546–547. Robertson, L.J., Sprong, H., Ortega, Y., van der Giessen, J., Fayer, R., 2014. Response to Galán-Puchades and Fuentes: Taenia asiatica: neglected – but not forgotten – and almost certainly being quietly globalized. Trends Parasitol. 30, 56–57.
Román, G., Sotelo, J., Brutto, O., Del Flisser, A., Dumas, M., Wadia, N., Botero, D., Cruz, M., Garcia, H., de Bittencourt, P.R.M., Trelles, L., Arriagada, C., Lorenzana, P., Nash, T.E., Spina-Franc¸a, A., 2000. A proposal to declare neurocysticercosis an international reportable disease. Bull. World Health Organ. 78, 399–406.
M.T. Galán-Puchades ∗ M.V. Fuentes University of València, Faculty of Pharmacy, Department of Parasitology, Av Vicent Andrés Estellés s/n, 46100 Burjassot, Valencia, Spain ∗ Corresponding
author. Fax: +34 963544769. E-mail address: [email protected] (M.T. Galán-Puchades) 30 April 2015 2 June 2015 6 June 2015
Please cite this article in press as: Galán-Puchades, M.T., Fuentes, M.V., About people, pig movements and pork ‘tapeworms’. Vet. Parasitol. (2015), http://dx.doi.org/10.1016/j.vetpar.2015.06.009
ARTICLE IN PRESS
VETPAR-7662; No. of Pages 2
Veterinary Parasitology xxx (2015) xxx–xxx
Contents lists available at ScienceDirect
Veterinary Parasitology journal homepage: www.elsevier.com/locate/vetpar
Letter to the Editor About people, pig movements and pork ‘tapeworms’ To the Editor, Gabriël et al. (2015) stress the implications of human migration and pig/pork import in the introduction of new cases of Taenia solium (not only taeniosis but also cysticercosis) in the European Union (EU) in their recent article. The authors state that humans are the final host of the pork ‘tapeworm’, using the word in its singular form, while it would be more fitting to use the plural form, ‘tapeworms’. People and pigs do not only have T. solium in common. The third human Taenia, T. asiatica has the same life cycle as T. solium, therefore also affecting people and pigs. Indeed, the European Food Safety Authority (EFSA) has finally recognized that two Taenia species, T. solium and T. asiatica, are acquired by eating pork (EFSA, 2013, p. 33). We perfectly understand that the focus of the article by Gabriël et al. is exclusively T. solium, however, we would like to provide complementary information about other possible implications of human and pig/pork movements. Initially found in southeast Asian countries, T. asiatica is currently present in most of Asia and probably worldwide due to globalisation (Galán-Puchades and Fuentes, 2014a,b; Robertson et al., 2014). Its relative novelty (it was first described in 1993) (Eom and Rim, 1993), compared to the other two well-known human Taenia species (T. solium and T. saginata), as well as the general lack of awareness of the species at a global scale are probably hampering its diagnosis. As the authors of the article state, human cases of taeniasis, if analysed, are rarely investigated at species level. An appropriate molecular diagnostic method [the only tool to specifically distinguish the TriTaenias (Galán-Puchades and Fuentes, 2014a)] is, however, never performed by health professionals. Therefore, T. asiatica could well be present among all those non-specifically diagnosed cases of human taeniasis. From a veterinary point of view, the authors accurately underline the lack, not only of sensitivity, but also of specificity of meat inspection. They stress the necessity of distinguishing between T. solium and T. hydatigena at the early stages of infection. That assertion leads to the assumption that liver cysticerci are normally found in pigs at slaughterhouses. Pig liver is the dominant location of the cysticerci, not only of T. hydatigena, but also of T. asiatica. Therefore, unless a molecular confirmation is made, T. asiatica again could perfectly be among all those non-specifically diagnosed cases of pig cysticercosis. It is very likely that T. asiatica could be present in the EU due to the same human migratory movements that could import T. solium, according to Table 1 appearing in the article of Gabriël et al. (2015, p. 4), at least two of the top countries of origin of the immigrants into the EU are endemic for T. asiatica (China and Vietnam), and a third is highly suspected (Myanmar) (Ale et al., 2014), and although the
likelihood of the establishment of the T. asiatica life cycle in the EU by those supposed imported cases is remote, this probability is in fact higher than in the case of imported T. solium. The authors of the article underline the importance of the environmental contamination with Taenia eggs in the transmission of the infection (Gabriël et al., 2015; p. 4). T. asiatica, similarly to T. saginata, presents an active expulsion of the proglottids from of the body, therefore nonexclusively related to defecation, whereas T. solium only leaves the intestine with faeces. That means that migrating T. asiatica carriers would contaminate the environment considerably more with their shed eggs than those harbouring T. solium. Gabriël et al. (2015, p. 5–6) list several countries that are the origin of legal and illegal import of pig/pork to the EU and, among them, endemic countries for T. asiatica are also included (at least Japan, South Korea, China and Thailand), therefore the probability exists for this parasite to be also introduced at larval stage. If the detection of T. solium during meat inspection could be considered a challenge, the detection of the small T. asiatica cysticerci in the pork liver parenchyma might even be more difficult, particularly given the widespread lack of awareness among veterinarians with regard to T. asiatica as a pig parasite in addition to the other two well-known parasites T. solium and T. hydatigena (Galán-Puchades and Fuentes, 2014b). However, is the possibility that T. asiatica could be or has already been introduced in the EU a concern for public health? This question does not yet have a definite answer. On the one hand, it is still not known whether T. asiatica can cause human cysticercosis as T. solium does (Galán-Puchades and Fuentes, 2004). If this were the case, T. asiatica could actually be a threat to human health. On the other hand, it has been pointed out that due to interspecific competition, the presence of T. asiatica could limit the presence of T. solium since both species share the same hosts, humans and pigs (Conlan et al., 2009; Devleesschauwer et al., 2012). From this point of view, on the contrary, the introduction of T. asiatica in EU could even be beneficial. We absolutely agree with the authors of the paper that it is essential to make T. solium taeniasis/cysticercosis a notifiable disease, which had already been proposed 15 years ago (Román et al., 2000). If finally T. solium were declared notifiable, molecular tools should be used to specifically distinguish it from the other Taenia species, and it would be an excellent opportunity to investigate the true role of T. asiatica in this scenario of people and pig/pork moving around the world.
References Ale, A., Victor, B., Praet, N., Gabriel, S., Speybroek, N., Dorny, P., Devleesschauwer, B., 2014. Epidemiology and genetic diversity of Taenia asiatica: a systematic review. Parasite Vector 7, 45, http://dx.doi.org/10.1186/1756-3305-7-45 Devleesschauwer, B., Aryal, A., Joshi, D.D., Rijal, S., Sherchand, J.B., Praet, N., Speybroeck, N., Duchateau, L., Vercruysse, J., Dorny, P., 2012. Epidemiology of Taenia solium in Nepal: is it influenced by the social characteristics of the
http://dx.doi.org/10.1016/j.vetpar.2015.06.009 0304-4017/© 2015 Elsevier B.V. All rights reserved.
Please cite this article in press as: Galán-Puchades, M.T., Fuentes, M.V., About people, pig movements and pork ‘tapeworms’. Vet. Parasitol. (2015), http://dx.doi.org/10.1016/j.vetpar.2015.06.009
G Model VETPAR-7662; No. of Pages 2 2
ARTICLE IN PRESS Letter to the Editor / Veterinary Parasitology xxx (2015) xxx–xxx
population and the presence of Taenia asiatica. Trop. Med. Int. Health 17, 1019–1022. Conlan, J.V., Vongxay, K., Fenwick, S., Blacksell, S.D., Thompson, R.C., 2009. Does interspecific competition have a moderating effect on Taenia solium transmission dynamics in Southeast Asia. Trends Parasitol. 25, 398–403. EFSA, 2013. Technical specifications on harmonised epidemiological indicators for biological hazards to be covered by meat inspection of bovine animals. EFSA J. 11 (3276), 1–78. Eom, K.S., Rim, H.J., 1993. Morphologic descriptions of Taenia asiatica sp. n. Kor. J. Parasitol. 7, 1–6. Gabriël, S., Johansen, M.V., Pozio, E., Smit, G.S.A., Devleesschauwer, B., Allepuz, A., Papadopoulos, E., van der Giessen, J., Dorny, P., 2015. Human migration and pig/pork import in the European Union: What are the implications for Taenia solium infections? Vet. Parasitol., http://dx.doi.org/10.1016/j.vetpar.2015.03. 006 Galán-Puchades, M.T., Fuentes, M.V., 2004. Taenia asiatica intermediate hosts Taenia asiatica intermediate hosts. Lancet 363, 660. Galán-Puchades, M.T., Fuentes, M.V., 2014a. Taenia asiatica: left out by globalisation Taenia asiatica: left out by globalisation. Trends Parasitol. 30, 54–55. Galán-Puchades, M.T., Fuentes, M.V., 2014b. Parasitic porkborne hazards, globalisation, and meat inspection. Food Control 46, 546–547. Robertson, L.J., Sprong, H., Ortega, Y., van der Giessen, J., Fayer, R., 2014. Response to Galán-Puchades and Fuentes: Taenia asiatica: neglected – but not forgotten – and almost certainly being quietly globalized. Trends Parasitol. 30, 56–57.
Román, G., Sotelo, J., Brutto, O., Del Flisser, A., Dumas, M., Wadia, N., Botero, D., Cruz, M., Garcia, H., de Bittencourt, P.R.M., Trelles, L., Arriagada, C., Lorenzana, P., Nash, T.E., Spina-Franc¸a, A., 2000. A proposal to declare neurocysticercosis an international reportable disease. Bull. World Health Organ. 78, 399–406.
M.T. Galán-Puchades ∗ M.V. Fuentes University of València, Faculty of Pharmacy, Department of Parasitology, Av Vicent Andrés Estellés s/n, 46100 Burjassot, Valencia, Spain ∗ Corresponding
author. Fax: +34 963544769. E-mail address: [email protected] (M.T. Galán-Puchades) 30 April 2015 2 June 2015 6 June 2015
Please cite this article in press as: Galán-Puchades, M.T., Fuentes, M.V., About people, pig movements and pork ‘tapeworms’. Vet. Parasitol. (2015), http://dx.doi.org/10.1016/j.vetpar.2015.06.009
