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Control of cestode zoonoses in Asia: role of basic and applied science

Published online by Cambridge University Press:  11 October 2013

AKIRA ITO*
Affiliation:
Department of Parasitology and Laboratory of NTDs, Asahikawa Medical University, Asahikawa 078-8510, Japan
XIAO-NONG ZHOU
Affiliation:
National Institute of Parasitic Diseases, China CDC, Shanghai 200025, PR China
PHILIP S. CRAIG
Affiliation:
Cestode Zoonoses Research Group, School of Environment and Life Sciences, University of Salford, Greater Manchester, UK
PATRICK GIRAUDOUX
Affiliation:
Department of Chrono-environment, University of Franche-Comté/CNRS and Institut Universitaire de France, Besançon, France
*
*Corresponding author: Department of Parasitology and Laboratory of NTDs, Asahikawa Medical University, Asahikawa 078-8510, Japan. Tel: +81 166 68 2686. Fax: +81 166 68 2429. E-mail: akiraito@asahikawa-med.ac.jp
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Abstract

Type
Preface
Copyright
Copyright © Cambridge University Press 2013 

On a global scale, human cystic and alveolar echinococcoses and cysticercosis, caused by Taenia solium, are classed as neglected zoonotic diseases (NZD) due to their high burden of disease which together is greater than 2 million lost DALYs (WHO, 2005, 2010; Budke et al. Reference Budke, Deplazes and Torgerson2006; Craig et al. Reference Craig, Budke, Schantz, Li, Qiu, Yang, Zeyhle, Rogan and Ito2007). These cestodes require two mammalian hosts for the completion of their life-cycle through natural or anthropogenic-mediated predator–prey systems.

Human taeniases are caused by the adult stage of three species, Taenia solium, T. saginata and T. asiatica all of which are food- or meat-borne cestodiases (Ito et al. Reference Ito, Nakao and Wandra2003a; Pawlowski, Reference Pawlowski2006; Flisser et al. Reference Flisser, Craig, Ito, Palmer, Soulsby, Torgerson and Brown2011). T. solium is unique, since it is the only one of these three species that can cause human cysticercosis, one of the most potentially lethal helminthiases contracted from accidental ingestion of eggs of this species (Ito et al. Reference Ito, Nakao and Wandra2003a). Animal cysticercoses, caused by the three human Taenia species as well as several other Taenia species, normally infect domestic and/or wild animals. In developed countries, where meat inspection is routine and livestock generally raised under strict controls, human taeniases are uncommon.

In this special issue, we mainly focus on taeniases/cysticercoses and echinococcoses in developing countries and regions of Eurasia. To begin with Ito (Reference Ito2013) reviews the caveats and advances in immunological and molecular studies of cestode zoonoses based on over 40-years’ experience. The first topics in this special issue focus on human taeniases as food-borne infections. They are generally more common in rural areas where under-cooked contaminated meat (muscle) or viscera are consumed in local communities without meat inspection (Li et al. Reference Li, Chen, Yanagida, Wang, Long, Sako, Okamoto, Wu, Giraudoux, Raoul, Nkouawa, Nakao, Craig and Ito2013; Wandra et al. Reference Wandra, Ito, Swastika, Dharmawan, Sako and Okamoto2013). Human cysticercosis, caused by the ingestion of the eggs of T. solium, has been considered to be the major causative agent of the late-onset epilepsy in developing countries where pork consumption is common (Lightowlers, Reference Lightowlers2013; Raoul et al. Reference Raoul, Li, Sako, Chen, Long, Yanagida, Wu, Nakao, Okamoto, Craig, Giraudoux and Ito2013). T. solium is unique, since it causes two different parasitoses in humans through its life-cycle completion: (i) cysticercosis due to the ingestion of eggs with development of cysticerci, mainly in muscles but also, more problematically, in the brain (neurocysticercosis), and (ii) taeniasis due to the ingestion of cysticerci from uncooked pork contaminated with the metacestode stage (Wandra et al. Reference Wandra, Ito, Swastika, Dharmawan, Sako and Okamoto2013). Pigs may be infected with Eggs not only of T. solium or T. asiatica but also other non-human Taenia species, such as T. hydatigena (Ito, Reference Ito2013). The occurrence of T. solium transmission in a region presents a high risk for humans acquiring accidental cysticercosis, either from self-infection (e.g. adult worm carrier) or from tapeworm carriers living in the same community (Sorvillo et al. Reference Sorvillo, Waterman, Richard and Schantz1992; Li et al. Reference Li, Chen, Yanagida, Wang, Long, Sako, Okamoto, Wu, Giraudoux, Raoul, Nkouawa, Nakao, Craig and Ito2013; Wandra et al. Reference Wandra, Ito, Swastika, Dharmawan, Sako and Okamoto2013). Taeniid eggs cannot be differentiated morphologically; therefore advanced immunological and molecular methods are essential for accurate diagnosis and should be combined with the analysis of spatial patterns of distribution for evidence-based control (Raoul et al. Reference Raoul, Li, Sako, Chen, Long, Yanagida, Wu, Nakao, Okamoto, Craig, Giraudoux and Ito2013; Sako et al. Reference Sako, Itoh, Okamto, Nakaya and Ito2013). T. solium cysticercosis has also been classed as a potentially eradicable disease (Schantz et al. Reference Schantz, Cruz, Sarti and Pawlowski1983; Pawlowski, Reference Pawlowski2006) for which accurate surveillance is of paramount importance.

Lightowlers (Reference Lightowlers2013) overviews the future prospects for control of T. solium taeniasis/cysticercosis (T/C). Raoul et al. (Reference Raoul, Li, Sako, Chen, Long, Yanagida, Wu, Nakao, Okamoto, Craig, Giraudoux and Ito2013) discuss spatially explicit approaches for epidemiological studies on T/C, while Sako et al. (Reference Sako, Itoh, Okamto, Nakaya and Ito2013) describe a new simple method for purification of diagnostic antigens applicable in endemic T. solium areas. Yamane et al. (Reference Yamane, Yanagida, Li, Chen, Dekumyoy, Waikagul, Nkouawa, Nakao, Sako, Ito, Sato and Okamoto2013) present data that confirms occurrence of hybrids between T. saginata and T. asiatica. Li et al. (Reference Li, Chen, Yanagida, Wang, Long, Sako, Okamoto, Wu, Giraudoux, Raoul, Nkouawa, Nakao, Craig and Ito2013) stress the usefulness of self-detection and stool microscopy in community-based mass screening for taeniases. The final article in the opening section is an overview by Wandra et al. (Reference Wandra, Ito, Swastika, Dharmawan, Sako and Okamoto2013) on T/C in Indonesia.

By contrast with Taenia spp., the life cycles of Echinococcus species are completed through domestic animals and/or wildlife. In echinococcoses, humans are infected by accidental ingestion of parasite eggs, and are generally a dead-end for the parasite (Macpherson, Reference Macpherson1983; Rausch, Reference Rausch, Thompson and Lymbery1995). However, echinococcoses caused by metacestodes established in parenteral tissues, mainly the liver and the lungs, are severe and potentially lethal to humans.

Echinococcoses are widespread diseases caused by environmental contamination of parasite eggs by canid definitive hosts such as dogs, foxes and wolves via faeces. Human alveolar echinococcosis (AE) due to Echinococcus multilocularis occurs focally in regions of developed and developing countries of the northern hemisphere, while human cystic echinococcosis (CE) due to E. granulosus is of greater concern because it has a worldwide distribution (Giraudoux et al. Reference Giraudoux, Raoul, Afonso, Ziadinov, Yang, Li, Li, Quéré, Feng, Wang, Wen, Ito and Craig2013a; Said Ali et al. Reference Said Ali, Grenouillet, Knapp, Bresson-Hadni, Vuitton, Raoul, Richou, Millon and Giraudoux2013; Torgerson, Reference Torgerson2013).

Cystic echinococcosis, caused by the ingestion of eggs of the dog tapeworm E. granulosus sensu stricto (genotypes G1–G3), has been widely recognized as an endemic disease in pastoral regions. Recent molecular re-evaluation of E. granulosus has revealed that E. granulosus sensu lato includes 5 different independent species: E. granulosus s.s., E. equinus, E. ortleppi, E. canadensis and E. felidis (Nakao et al. Reference Nakao, Yanagida, Okamoto, Knapp, Nkouawa, Sako and Ito2010). Molecular approaches for identification of pathogenic Echinococcus species will become more essential for future epidemiological studies. E. multilocularis was originally considered to be mainly distributed in European alpine countries and in western Alaska half a century ago (Rausch and Fay, Reference Rausch, Fay, Craig and Pawlowski2002); however, it has since been found widely distributed in mountainous or upland areas in almost all countries in the holarctic and central regions of Eurasia and has expanded its range in temperate areas of Europe (Craig et al. Reference Craig, Giraudoux, Shi, Barethlomot, Barnish, Delattre, Quere, Harraga, Bao, Wang, Lu, Ito and Vuitton2000, Reference Craig, Li, Qiu, Zhen, Wang, Giraudoux, Ito, Heath, Warnock, Schantz and Yang2008; Romig et al. Reference Romig, Dinkel and Mackenstedt2006; Torgerson et al. Reference Torgerson, Oguljahan, Muminov, Karaeva, Kuttubaev, Aminjanov and Shaikenov2006; Beiromvand et al. Reference Beiromvand, Akhlaghi, Massom, Mobedi, Meamar, Oormazdi, Motevalian and Razmjou2012; Combes et al. Reference Combes, Comte, Raton, Raoul, Boué, Umhang, Favier, Dunoyer, Woronoff and Giraudoux2012; Konyaev et al. Reference Konyaev, Yanagida, Ingovatova, Shoikhet, Nakao, Sako, Bondarev and Ito2012).

The second topic in this section concerns the taxonomy of the genus Echinococcus. McManus (Reference McManus2013) overviews some historical observations on the biology and taxonomy of Echinococcus. Nakao et al. (Reference Nakao, Yanagida, Konyaev, Lavikainen, Odnokurtsev, Zaikov and Ito2013) consider the taxonomic status of E. canadensis, and Konyaev et al. (Reference Konyaev, Yanagida, Nakao, Ingovatova, Shoykhet, Bondarev, Odnokurtsev, Lostutova, Lukmanova, Dokuchaev, Spiridonov, Alshinecky, Tatyana, Andreyanov, Abramov, Krivopalov, Karpenko, Lopatina, Dupal, Sako and Ito2013) report recent data on Echinococcus spp. in Russia and describe, for the first time, different genotypes of E. multilocularis and E. canadensis, G6, G7 and G10 in that country. Ito et al. (Reference Ito, Chuluunbaatar, Yanagida, Davaasuren, Sumiya, Asakawa, Ki, Nakaya, Davaajav, Dorjsuren, Nakao and Sako2013) also consider E. multilocularis and E. canadensis, G6/7 and G10 from wild canids and describe, for the first time, the sympatric occurrence of G6/7 and G10 genotypes in wolves.

Thirdly, various aspects of transmission ecology and epidemiology of echinococcoses in Eurasia are discussed. Giraudoux et al. (Reference Giraudoux, Raoul, Afonso, Ziadinov, Yang, Li, Li, Quéré, Feng, Wang, Wen, Ito and Craig2013a) present regional types of transmission of E. multilocularis and their ecological characteristics in China and Central Asia. Torgerson (Reference Torgerson2013) overviews the current position of echinococcoses in Central Asia while Van Kesteren et al. (Reference Van Kesteren, Mastin, Mytynova, Ziadinov, Boufana, Torgerson, Rogan and Craig2013) assess dog demographics, roles of dogs, dog movements and faecal environmental contamination of rural communities of southern Kyrgyzstan. Moss et al. (Reference Moss, Chen, Li, Qiu, Wang, Giraudoux, Ito, Torgerson and Craig2013) attempt to evaluate Echinococcus spp. re-infection patterns of treated dogs on the Tibetan plateau, China. The last article in this section points out the importance of investigating distributions at several scales to better understand their nested clustered structure using data from the French National Registry on human AE (Said Ali et al. Reference Said Ali, Grenouillet, Knapp, Bresson-Hadni, Vuitton, Raoul, Richou, Millon and Giraudoux2013).

There are several common problems for control or eradication of NTDs (including echinococcoses and cysticercosis). (1) Major endemic areas of cysticercosis and CE are predominantly in developing countries, especially in rural or remote areas where people are living under poor socio-economic conditions; (2) The lack of priority for control of NTDs in developing countries; and (3) The absence of reliable data due to the lack of scientifically reliable tools and methods for identifying infected people in their communities.

In addition, echinococcoses and cysticercosis/taeniases are NZDs and thus present a greater problem for control because of the necessity to manage or treat domestic animals (dogs, livestock) or wildlife (foxes, wolves). This is usually complicated by the lack of communication on surveillance between human and animal health authorities. Therefore, the burden of zoonotic cestodiases is largely underestimated (Budke et al. Reference Budke, Deplazes and Torgerson2006; WHO, 2010).

Towards control of these cestode zoonoses, we have to clarify which are the risk factors (Van Kesteren et al. Reference Van Kesteren, Mastin, Mytynova, Ziadinov, Boufana, Torgerson, Rogan and Craig2013; Lightowlers, Reference Lightowlers2013; Moss et al. Reference Moss, Chen, Li, Qiu, Wang, Giraudoux, Ito, Torgerson and Craig2013; Torgerson, Reference Torgerson2013) and their distribution in time and space (Giraudoux et al. Reference Giraudoux, Raoul, Afonso, Ziadinov, Yang, Li, Li, Quéré, Feng, Wang, Wen, Ito and Craig2013a; Raoul et al. Reference Raoul, Li, Sako, Chen, Long, Yanagida, Wu, Nakao, Okamoto, Craig, Giraudoux and Ito2013). It also requires us to identify the parasite species (Ito et al. Reference Ito, Chuluunbaatar, Yanagida, Davaasuren, Sumiya, Asakawa, Ki, Nakaya, Davaajav, Dorjsuren, Nakao and Sako2013; Konyaev et al. Reference Konyaev, Yanagida, Nakao, Ingovatova, Shoykhet, Bondarev, Odnokurtsev, Lostutova, Lukmanova, Dokuchaev, Spiridonov, Alshinecky, Tatyana, Andreyanov, Abramov, Krivopalov, Karpenko, Lopatina, Dupal, Sako and Ito2013; Nakao et al. Reference Nakao, Yanagida, Konyaev, Lavikainen, Odnokurtsev, Zaikov and Ito2013; Said Ali et al. Reference Said Ali, Grenouillet, Knapp, Bresson-Hadni, Vuitton, Raoul, Richou, Millon and Giraudoux2013; Sako et al. Reference Sako, Itoh, Okamto, Nakaya and Ito2013). This can be effected by integrating human and animal epidemiology with host behaviour and parasite ecology (Raoul et al. Reference Raoul, Li, Sako, Chen, Long, Yanagida, Wu, Nakao, Okamoto, Craig, Giraudoux and Ito2013). In this symposium, we have tried to link molecular (Ito et al. Reference Ito, Chuluunbaatar, Yanagida, Davaasuren, Sumiya, Asakawa, Ki, Nakaya, Davaajav, Dorjsuren, Nakao and Sako2013; Konyaev et al. Reference Konyaev, Yanagida, Nakao, Ingovatova, Shoykhet, Bondarev, Odnokurtsev, Lostutova, Lukmanova, Dokuchaev, Spiridonov, Alshinecky, Tatyana, Andreyanov, Abramov, Krivopalov, Karpenko, Lopatina, Dupal, Sako and Ito2013; McManus, Reference McManus2013; Nakao et al. Reference Nakao, Yanagida, Konyaev, Lavikainen, Odnokurtsev, Zaikov and Ito2013), immunological (Sako et al. Reference Sako, Itoh, Okamto, Nakaya and Ito2013) and spatial ecology approaches (Giraudoux et al. Reference Giraudoux, Raoul, Afonso, Ziadinov, Yang, Li, Li, Quéré, Feng, Wang, Wen, Ito and Craig2013a; Van Kesteren et al. Reference Van Kesteren, Mastin, Mytynova, Ziadinov, Boufana, Torgerson, Rogan and Craig2013; Moss et al. Reference Moss, Chen, Li, Qiu, Wang, Giraudoux, Ito, Torgerson and Craig2013; Raoul et al. Reference Raoul, Li, Sako, Chen, Long, Yanagida, Wu, Nakao, Okamoto, Craig, Giraudoux and Ito2013) in order to provide research-based evidence towards control of cestode zoonoses (Danson et al. Reference Danson, Giraudoux and Craig2006; Giraudoux et al. Reference Giraudoux, Pleydell, Raoul, Quéré, Wang, Yang, Vuitton, Qiu, Yang and Craig2006, Reference Giraudoux, Pleydell, Raoul, Quéré, Qian, Yang, Vuitton, Qiu, Yang and Craig2007, Reference Giraudoux, Raoul, Pleydell and Craig2008, Reference Giraudoux, Raoul, Afonso, Ziadinov, Yang, Li, Li, Quéré, Feng, Wang, Wen, Ito and Craig2013b). One of the most important strategies for efficient control of taeniasis and cysticercosis may be to establish or to introduce real-time detection of patients in the endemic areas themselves (Raoul et al. Reference Raoul, Li, Sako, Chen, Long, Yanagida, Wu, Nakao, Okamoto, Craig, Giraudoux and Ito2013; Sako et al. Reference Sako, Itoh, Okamto, Nakaya and Ito2013).

A series of meetings on Cestode Zoonoses has been organized in Asia, sponsored by the Japanese Society for the Promotion of Science since 2000 (Ito, Reference Ito2007). Here we have to acknowledge the pioneering contributions in China towards control of echinococcoses that have been coordinated through a team of scientists from America, Europe, Australia, New Zealand and Japan (Andersen et al. Reference Andersen, Chai and Liu1993; Craig et al. Reference Craig, Giraudoux, Shi, Barethlomot, Barnish, Delattre, Quere, Harraga, Bao, Wang, Lu, Ito and Vuitton2000, Reference Craig, McManus and Chappell2003; Craig and Pawlowski, Reference Craig and Pawlowski2002; Ito et al. Reference Ito, Urbani, Qiu, Vuitton, Qiu, Heath, Craig, Feng and Schantz2003b, Reference Ito, Craig and Schantz2006; Schantz et al. Reference Schantz, Wang, Qiu, Liu, Saito, Emshoff, Ito, Roberts and Delker2003; Xiao et al. Reference Xiao, Qiu, Nakao, Nakaya, Yamasaki, Sako, Mamuti, Schantz, Craig and Ito2003, Reference Xiao, Qiu, Nakao, Li, Yang, Chen, Schantz, Craig and Ito2005; Mamuti et al. Reference Mamuti, Yamasaki, Sako, Nakao, Xiao, Nakaya, Sato, Vuitton, Piarroux, Lightowlers, Craig and Ito2004, Reference Mamuti, Sako, Bart, Nakao, Ma, Wen and Ito2007; Heath et al. Reference Heath, Zhang and McManus2005; Li et al. Reference Li, Qiu, Yang, Craig, Chen, Xiao, Ito, Giraudoux, Mamuti, Yu and Schantz2005, Reference Li, Craig, Ito, Chen, Qiu, Qiu, Sato, Wandra, Bradshaw, Li, Yang and Wang2006; Bart et al. Reference Nakao, Yanagida, Okamoto, Knapp, Nkouawa, Sako and Ito2006; Nakao et al. Reference Heath, Zhang and McManus2010; Giraudoux et al. Reference Giraudoux, Raoul, Pleydell, Li, Han, Qiu, Xie, Wang, Ito and Craig2013b) as well as the contribution towards the control of echinococcoses made by scientists from China (Wen et al. Reference Wen, Wang and Zhou2005) and of cysticercosis (Chen et al. Reference Chen, Xu and Zhou2005) as joint projects with scientists from Japan (Ito et al. Reference Ito, Urbani, Qiu, Vuitton, Qiu, Heath, Craig, Feng and Schantz2003b, Reference Ito, Wen and Yamasaki2005).

This symposium, held in Shanghai in 2012, was launched and co-organized by two of the Guest-Editors, Akira Ito (Japan) and Xiao-Nong Zhou (China) and supported by the Asian Science and Technology Strategic Cooperation Promotion Programs sponsored by the Special Coordination Funds for Promoting Science and Technology, Ministry of Education, Japan (MEXT) (2010–2012) and the national office of the Chinese Center for Disease Control and Prevention.

ACKNOWLEDGEMENT

We dedicate this Special Issue of Parasitology to the late Professor Robert L. Rausch, a great pioneer of the biology of cestodes, especially on Echinococcus which was as his life's work, who died on 6th October 2012.

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