Ascariasis in people and pigs: New inferences from DNA analysis of worm populations

Infection, Genetics and Evolution

Volumn 12, Issue 2, 2012, Pages 227-235

  Peng, Weidong ^a   Criscione, Charles D ^b  

^a NANCHANG UNIVERSITY   (China)

^b TEXAS A AND M UNIVERSITY   (United States)

Author keywords

Ascaris; Cross infection; Genetic structure; Host affiliation; Hybridization; Molecular epidemiology

Indexed keywords

INTERNAL TRANSCRIBED SPACER 1; MITOCHONDRIAL DNA; RIBOSOME DNA;

ASCARIASIS; ASCARIS; CROSS INFECTION; DISEASE TRANSMISSION; DNA DETERMINATION; ENZYME ELECTROPHORESIS; GENE FREQUENCY; GENETIC DIFFERENCE; GENETIC MARKER; GENETIC VARIABILITY; GENOTYPE; GEOGRAPHIC DISTRIBUTION; HAPLOTYPE; HUMAN; NONHUMAN; PHENOTYPE; PHYLOGENY; PRIORITY JOURNAL; REVIEW; SPECIES DIFFERENTIATION;

ANIMALS; ASCARIASIS; ASCARIS; DNA, HELMINTH; EVOLUTION, MOLECULAR; GENETIC MARKERS; GENETICS, POPULATION; HOST-PATHOGEN INTERACTIONS; HUMANS; SEQUENCE ANALYSIS, DNA; SEXUAL BEHAVIOR, ANIMAL; SWINE; SWINE DISEASES;

ASCARIS; ASCARIS SUUM; NEMATODA; SUIDAE;

EID: 84857641826     PISSN: 15671348     EISSN: 15677257     Source Type: Journal    
DOI: 10.1016/j.meegid.2012.01.012     Document Type: Review

References (110)

1. Abebe W., Tsuji N., Kasuga-Aoki H., Miyoshi T., Isobe T., Arakawa T., Matsumoto Y., Yoshihara S. Species-specific proteins identified in Ascaris lumbricoides and Ascaris suum using two-dimensional electrophoresis. Parasitol. Res. 2002, 88:868-871.
2. Abebe W., Tsuji N., Kasuga-Aoki H., Miyoshi T., Isobe T., Arakawa T., Matsumoto Y., Yoshihara S. Lung-stage protein profile and antigenic relationship between Ascaris lumbricoides and Ascaris suum. J. Parasitol. 2002, 88:826-828.
3. Alba J.E., Comia M.N., Oyong G., Claveria F. Ascaris lumbricoides and Ascaris suum: a comparison of electrophoretic banding patterns of protein extracts from the reproductive organs and body wall. Vet. Arh. 2009, 79:281-291.
4. Anderson T.J.C. Ascaris infections in humans from North America: molecular evidence for cross infection. Parasitology 1995, 110:215-219.
5. Anderson T.J.C. The dangers of using single locus markers in parasite epidemiology: Ascaris as a case study. Trends Parasitol. 2001, 17:183-188.
6. Anderson T.J.C., Jaenike J. Host specificity, evolutionary relationships and macrogeographic differentiation among Ascaris populations from humans and pigs. Parasitology 1997, 115:325-342.
7. Anderson E.C., Thompson E.A. A model-based method for identifying species hybrids using multilocus genetic data. Genetics 2002, 160:1217-1229.
8. Anderson T.J.C., Romero-Abal M.E., Jaenike J. Genetic structure and epidemiology of Ascaris populations: patterns of host affiliation in Guatemala. Parasitology 1993, 107:319-334.
9. Anderson T.J.C., Romero-Abal M.E., Jaenike J. Mitochondrial DNA and Ascaris microepidemiology: the composition of parasite populations from individual hosts, families and villages. Parasitology 1995, 110:221-229.
10. Arizono N., Yoshimura Y., Tohzaka N., Yamada M., Tegoshi T., Onishi K., Uchikawa R. Ascariasis in Japan: is pig-derived Ascaris infecting humans?. Jpn. J. Infect. Dis. 2010, 63:447-448.
11. Betson M., Halstead F.D., Nejsum P., Imison E., Khamis I.S., Sousa-Figueiredo J.C., Rollinson D., Stothard J.R. A molecular epidemiological investigation of Ascaris on Unguja, Zanzibar using isoenyzme analysis, DNA barcoding and microsatellite DNA profiling. Trans. R. Soc. Trop. Med. Hyg. 2011, 105:370-379.
12. Betson M., Nejsum P., Llewellyn-Hughes J., Griffin C., Atuhaire A., Arinaitwe M., Adriko M., Ruggiana A., Turyakira G., Kabatereine N.B., Stothard J.R. Genetic diversity of Ascaris in southwestern Uganda. Trans. R. Soc. Trop. Med. Hyg. 2012, 106:75-83.
13. Blouin M.S. Molecular prospecting for cryptic species of nematodes: mitochondrial DNA versus internal transcribed spacer. Int. J. Parasitol. 2002, 32:527-531.
14. Boes J., Willingham A.L., Fuhui S., Xuguang H., Eriksen L., Nansen P., Stewart T.B. Prevalence and distribution of pig helminths in the Dongting Lake Region (Hunan Province) of the People's Republic of China. J. Helminthol. 2000, 74:45-52.
15. Bundy, D.A.P., Guyatt, H. 1996. Schools for health: focus on health, education and the school-age child. Parasitol. Today 12 (Insert), 1-16.
16. Cabrera B.D. Reinfection and infection rates of ascariasis in relation to seasonal variation in the Philippines, Southeast Asian. J. Trop. Med. Public Health 1984, 15:394-401.
17. Carlsgart J., Roepstorff A., Nejsum P. Multiplex PCR on single unembryonated Ascaris (roundworm) eggs. Parasitol. Res. 2009, 104:939-943.
18. Chan M.S., Medley G.F., Jamison D., Bundy D.A.P. The evaluation of potential global morbidity attributable to intestinal nematode infections. Parasitology 1994, 109:373-387.
19. Copeman D.B., Gaafar S.M. Sequential development of hepatic lesions of ascaridosis in colostrum-deprived pigs. Aust. Vet. J. 1972, 48:263-268.
20. Criscione C.D., Blouin M.S. Effective sizes of macroparasite populations: a conceptual model. Trends Parasitol. 2005, 21:212-217.
21. Criscione C.D., Blouin M.S. Minimal selfing, few clones, and no among-host genetic structure in a hermaphroditic parasite with asexual larval propagation. Evolution 2006, 60:553-562.
22. Criscione C.D., Poulin R., Blouin M.S. Mol. Ecol. of parasites: elucidating ecological and microevolutionary processes. Mol. Ecol. 2005, 14:2247-2257.
23. Criscione C.D., Anderson J.D., Raby K., Sudimack D., Subedi J., Rai D.R., Upadhayay R.P., Jha B., Williams-Blangero S., Anderson T.J.C. Microsatellite markers for the human nematode parasite Ascaris lumbricoides: development and assessment of utility. J. Parasitol. 2007, 93:704-708.
24. Criscione C.D., Anderson J.D., Sudimack D., Peng W., Jha B., Williams-Blangero S., Anderson T.J.C. Disentangling hybridization and host colonization in parasitic roundworms of humans and pigs. Proc. R. Soc. Biol. Sci. Ser. B 2007, 274:2669-2677.
25. Criscione C.D., Anderson J.D., Sudimack D., Subedi J., Upadhayay R.P., Jha B., Williams K.D., Williams-Blangero S., Anderson T.J.C. Landscape genetics reveals focal transmission of a human macroparasite. PLoS Neg. Trop. Dis. 2010, 4:e665.
26. Crompton D.W.T. Biology of Ascaris lumbricoides. Ascariasis and its Prevention and Control 1989, 9-44. Taylor and Francis Ltd., London and Philadelphia. D.W.T. Crompton, M.C. Nesheim, Z.S. Pawlowski (Eds.).
27. Crompton D.W.T. Prevalence of ascariasis. Ascariasis and its Prevention and Control 1989, 45-69. Taylor and Francis Ltd., London and Philadelphia. D.W.T. Crompton, M.C. Nesheim, Z.S. Pawlowski (Eds.).
28. Crompton D.W.T. Ascaris and ascariasis. Adv. Parasitol. 2001, 48:285-375.
29. Crompton D.W., Nesheim M.C. Nutritional impact of intestinal helminthiasis during the human life cycle. Annu. Rev. Nutr. 2002, 22:35-59.
30. de Meeûs T., McCoy K.D., Prugnolle F., Chevillon C., Durand P., Hurtrez-Bousses S., Renaud F. Population genetics and molecular epidemiology or how to " debusquer la bete" Infect. Genet. Evol. 2007, 7:308-332.
31. de Silva N.R., Brooker S., Hotez P.J., Montresor A., Engels D., Savioli L. Soil-transmitted helminth infections: updating the global picture. Trends Parasitol. 2003, 19:547-551.
32. Detwiler J.T., Criscione C.D. An infectious topic in reticulate evolution: introgression and hybridization in animal parasites. Genes 2010, 1:102-123.
33. Dold C., Holland C.V. Ascaris and ascariasis. Microb. Infect. 2011, 13:632-637.
34. Dold C., Holland C.V. Investigating the underlying mechanism of resistance to Ascaris infection. Microb. Infect. 2011, 13:624-631.
35. Elkins D.B., Haswell-Elkins M. The weight/length profiles of Ascaris lumbricoides within a human community before mass treatment and following reinfection. Parasitology 1989, 99:293-299.
36. Excoffier L., Lischer H.E.L. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol. Ecol. Res. 2010, 10:564-567.
37. Forsum E., Göranzon H., Rundgren M., Thilén M., Hambraeus L. Protein evaluation of mixed diets. Comparative study in man and in the pig and rat of vegetable-animal and vegetable protein diets. Ann. Nutr. Metab. 1981, 25:137-150.
38. Galvin T.J. Development of human and pig Ascaris in the pig and rabbit. J. Parasitol. 1968, 54:1085-1091.
39. Hall A., Holland C. Geographical variation in Ascaris lumbricoides fecundity and its implications to helminth control. Parasit. Today 2000, 16:540-544.
40. Holland C.V. Predisposition to ascariasis: patterns, mechanisms and implications. Parasitology 2009, 136:1537-1547.
41. Hotez P.J., Brindley P.J., Bethony J.M., King C.H., Pearce E.J., Jacobson J. Helminth infections: the great neglected tropical diseases. J. Clin. Invest. 2008, 118:1311-1321.
42. Ibrahim A.P., Conway D.J., Hall A., Bundy D.A.P. Enzyme polymorphisms in Ascaris lumbricoides in Bangladesh. Trans. R. Soc. Trop. Med. Hyg. 1994, 88:600-603.
43. Irwin D.E. Phylogeographic breaks without geographic barriers to gene flow. Evolution 2002, 56:2383-2394.
44. Ishiwata K., Shinohara A., Yagi K., Horii Y., Tsuchiya K., Nawa Y. Identification of tissue-embedded ascarid larvae by ribosomal DNA sequencing. Parasitol. Res. 2004, 92:50-52.
45. Jex A.R., Liu S.P., Li B., Young N.D., Hall R.S., Li Y.R., Yang L.F., Zeng N., Xu X., Xiong Z.J., Chen F.Y., Wu X., Zhang G.J., Fang X.D., Kang Y., Anderson G.A., Harris T.W., Campbell B.E., Vlaminck J., Wang T., Cantacessi C., Schwarz E.M., Ranganathan S., Geldhof P., Nejsum P., Sternberg P.W., Yang H.M., Wang J., Gasser R.B. Ascaris suum draft genome. Nature 2011, 479:529-533.
46. Kennedy M.W., Qureshi F., Haswellelkins M., Elkins D.B. Homology and heterology between the secreted antigens of the parasitic larval stages of Ascaris lumbricoides and Ascaris suum. Clin. Exp. Immunol. 1987, 67:20-30.
47. Kuo C.H., Avise J. Phylogeographic breaks in low-dispersal species: the emergence of concordance across gene trees. Genetica 2005, 124:179-186.
48. Kurimoto H. Morphological, biochemical and immunological studies on the differences between Ascaris lumbricoides Linneaus, 1758 and Ascaris suum Goez, 1782. Jpn. J. Parasitol. 1974, 23:251-267.
49. Leles D., Araujo A., Ferreira L.F., Vicente A.C.P., Iniguez A.M. Molecular paleoparasitological diagnosis of Ascaris sp from coprolites: new scenery of ascariasis in pre-Columbian South America times. Mem. Inst. Oswaldo. Cruz. 2008, 103:106-108.
50. Leles D., Araujo A., Vicente A.C.P., Iniguez A.M. Molecular diagnosis of ascariasis from human feces and description of a new Ascaris sp genotype in Brazil. Vet. Parasitol. 2009, 163:167-170.
51. Leles D., Araujo A., Vicente A.C.P., Iniguez A.M. ITS1 intra-individual variability of Ascaris isolates from Brazil. Parasitol. Int. 2010, 59:93-96.
52. Leslie J.F., Cain G.D., Meffe G.K., Vrijenhoek R.C. Enzyme polymorphism in Ascaris suum (Nematoda). J. Parasitol. 1982, 68:576-587.
53. Liu G.-H., Wu C.-Y., Song H.-Q., Wei S.-J., Xu M.-J., Lin R.-Q., Zhao G.-H., Huang S.-Y., Zhu X.Q. Comparative analyses of the complete mitochondrial genomes of Ascaris lumbricoides and Ascaris suum from humans and pigs. Gene 2012, 492:110-116.
54. Loreille O., Bouchet F. Evolution of ascariasis in humans and pigs: a multi-disciplinary approach. Mem. Inst. Oswaldo. Cruz. 2003, 98:39-46.
55. Loreille O., Roumat E., Verneau O., Bouchet F., Hanni C. Ancient DNA from Ascaris: extraction amplification and sequences from eggs collected in coprolites. Int. J. Parasitol. 2001, 31:1101-1106.
56. Macko J.K., Dubinsky P. Taxonomic deliberations on human and pig ascarids. Helminthologia 1997, 34:167-171.
57. Maruyama H., Nawa Y., Noda S., Mimori T., Choi W.Y. An outbreak of visceral larva migrans due to Ascaris suum in Kyushu, Japan. Lancet 1996, 347:1766-1767.
58. McCoy K.D. Sympatric speciation in parasites - what is sympatry?. Trends Parasitol. 2003, 19:400-404.
59. Monzon R.B. Replacement patterns of Ascaris lumbricoides populations in Filipino children. Southeast Asian J. Trop. Med. Pub. Health 1991, 22:605-610.
60. Nadler S.A. Biochemical and immunological systematics of some ascaridoid nematodes: genetic divergence between congeners. J. Parasitol. 1987, 73:811-816.
61. Nadler S.A., Hudspeth D.S.S. Phylogeny of the ascaridoidea (Nematoda: Ascaridida) based on three genes and morphology: hypotheses of structural and sequence evolution. J. Parasitol. 2000, 86:380-393.
62. Nadler S.A., Lindquist R.L., Near T.J. Genetic structure of midwestern Ascaris suum populations: a comparison of isoenzyme and RAPD markers. J. Parasitol. 1995, 81:385-394.
63. Nansen P., Roepstorff A. Parasitic helminths of the pig: factors influencing transmission and infection levels. Int. J. Parasitol. 1999, 29:877-891.
64. Nascetti G., Grappelli C., Bullini L., Montalenti S.G. Ricerche sul differenziamento genetico di Ascaris lumbricoides e Ascaris suum. Atti della Accademia Nazionale dei Lincei Rendiconti Classe di Scienze Fisiche Matematiche e Naturali 1979, 67:457-465.
65. Nejsum P., Frydenberg J., Roepstorff A., Parker E.D.J. Population structure in Ascaris suum (Nematoda) among domestic swine in Denmark as measured by whole genome DNA fingerprinting. Hereditas 2005, 142:7-14.
66. Nejsum P., Parker E.D., Frydenberg J., Roepstorff A., Boes J., Haque R., Astrup I., Prag J., Sorensen U.B.S. Ascariasis is a zoonosis in Denmark. J. Clin. Microbiol. 2005, 43:1142-1148.
67. Nejsum P., Grondahl C., Murrell K.D. Molecular evidence for the infection of zoo chimpanzees by pig Ascaris. Vet. Parasitol. 2006, 139:203-210.
68. Nejsum P., Roepstorff A., Jorgensen C.B., Fredholm M., Goring H.H.H., Anderson T.J.C., Thamsborg S.M. High heritability for Ascaris and Trichuris infection levels in pigs. Heredity 2009, 102:357-364.
69. Nejsum P., Roepstorff A., Anderson T.J.C., Jorgensen C., Fredholm M., Thamsborg S.M. The dynamics of genetically marked Ascaris suum infections in pigs. Parasitology 2009, 136:193-201.
70. Nejsum P., Bertelsen M.F., Betson M., Stothard J.R., Murrell K.D. Molecular evidence for sustained transmission of zoonotic Ascaris suum among zoo chimpanzees (Pan troglodytes). Vet. Parasitol. 2010, 171:273-276.
71. Nganga C.J., Karanja D.N., Mutune M.N. The prevalence of gastrointestinal helminth infections in pigs in Kenya. Trop. Anim. Health Prod. 2008, 40:331-334.
72. Oh C.S., Seo M., Lim N.J., Lee S.J., Lee E.J., Lee S.D., Shin D.H. Paleoparasitological report on Ascaris aDNA from an ancient East Asian sample. Mem. Inst. Oswaldo. Cruz. 2010, 105:225-228.
73. O'Lorcain P., Holland C.V. The public health importance of Acaris lumbricoides. Parasitology 2000, 121:S51-S71.
74. Pecson B.M., Barrios J.A., Johnson D.R., Nelson K.L. A real-time PCR method for quantifying viable Ascaris eggs using the first internally transcribed spacer region of ribosomal DNA. Appl. Environ. Microbiol. 2006, 72:7864-7872.
75. Peng W., Zhou X., Cui X., Crompton D.W., Whitehead R.R., Xiong J., Wu H., Peng J., Yang Y., Wu X., Xu K., Yan Y. Ascaris, people and pigs in a rural community of Jiangxi Province, China. Parasitology 1996, 113:545-557.
76. Peng W., Zhou X., Crompton D.W.T. Ascariasis in China. Adv. Parasitol. 1998, 41:109-148.
77. Peng W., Anderson T.J.C., Zhou X., Kennedy M.W. Genetic variation in sympatric Ascaris populations from humans and pigs in China. Parasitology 1998, 117:355-361.
78. Peng W., Cui X., Zhou X. Comparison of the structures of natural and re-established populations of Ascaris in humans in a rural community of Jiangxi. China. Parasitology. 2002, 124:641-647.
79. Peng W., Yuan K., Zhou X.M., Hu M., El-Osta Y.G.A., Gasser R.B. Molecular epidemiological investigation of Ascaris genotypes in China based on single-strand conformation polymorphism analysis of ribosomal DNA. Electrophoresis 2003, 24:2308-2315.
80. Peng W., Yuan K., Hu M., Zhou X.M., Gasser R.B. Mutation scanning-coupled analysis of haplotypic variability in mitochondrial DNA regions reveals low gene flow between human and porcine Ascaris in endemic regions of China. Electrophoresis 2005, 26:4317-4326.
81. Peng W., Yuan K., Hu M., Peng G., Zhou X., Hu N., Gasser R.B. Experimental infections of pigs and mice with selected genotypes of Ascaris. Parasitology 2006, 133:651-657.
82. Peng W., Yuan K., Hu M., Gasser R.B. Recent insights into the epidemiology and genetics of Ascaris in China using molecular tools. Parasitology 2007, 134:325-330.
83. Pérez J., García P.M., Mozos E., Bautista M.J., Carrasco L. Immunohistochemical characterization of hepatic lesions associated with migrating larvae of Ascaris suum in pigs. J. Comp. Pathol. 2001, 124:200-206.
84. Perkins S.L., Martinsen E.S., Falk B.G. Do molecules matter more than morphology? Promises and pitfalls in parasites. Parasitology 2011, 138:1664-1674.
85. Qiu, L., 2007. Migration and distribution of Ascaris representing different genotypes in C57BL/6 mice. Master's Thesis, Nanchang University, China (in Chinese with English summery). Available from: http://epub.cnki.net/grid2008/detail.aspx?filename=2008041426.nh&dbname=CMFD2008.
86. Roepstorff, A. Nansen, P., 1998. Epidemiology, diagnosis and control of helminth parasites of swine. In: FAO Animal Health Manual No. 3, Food and Agricultural Organization of the United Nations, Rome.
87. Roepstorff A., Nilsson O., O'Callaghan C.J., Oksanen A., Gjerde B., Richter S.H., Ortenberg E.O., Christensson D., Nansen P., Eriksen L., Medley G.F. Intestinal parasites in swine in the Nordic countries: multilevel modeling of Ascaris suum infections in relation to production factors. Parasitology 1999, 119:521-534.
88. Schwab A.E., Churcher T.S., Schwab A.J., Basanez M.G., Prichard R.K. Population genetics of concurrent selection with albendazole and ivermectin or diethylcarbamazine on the possible spread of albendazole resistance in Wuchereria bancrofti. Parasitology 2006, 133:589-601.
89. Seo B.S. Epidemiology and control of ascariasis in Korea. Korean J. Parasitol. 1990, 28(Suppl.):S49-S61.
90. Sharabi H.A., Abdel-Shafy S., Derbala A.A. The role of dogs in transmission of Ascaris lumbricoides for humans. Parasitol. Res. 2010, 106:1021-1026.
91. Stephenson L.S. The Impact of Helminth Infection on Human Nutrition 1987, Taylor and Francis Ltd., London, Philadelphia.
92. Stephenson L.S., Latham M.C., Ottesen E.A. Malnutrition and parasitic helminth infections. Parasitology 2000, 121:S23-S38.
93. Stewart T.B., Hale O.M. Losses to internal parasites in swine production. J. Ani. Sci. 1988, 66:1548-1554.
94. Sun F.H., Shen M.X., Xu X.Z., Cao H.J., Jiang W.C., Ji Z.H. Investigation on human ascaris infection in China. J. Path. Biol. 2008, 3:936-939.
95. Takata I. Experimental infection of man with Ascaris of man and pig. Kitasato Arch. Exp. Med. 1951, 23:49-59.
96. Thein-Hlaing Ascariasis and childhood malnutrition. Parasitology 1993, 107:S125-S136.
97. Vilas R., Criscione C.D., Blouin M.S. A comparison between mitochondrial DNA and the ribosomal internal transcribed regions in prospecting for cryptic species of platyhelminth parasites. Parasitology 2005, 131:839-846.
98. Wakelin D., Bradley J.E. Parasite strain diversity and host immune responses. The Geohelminths: Ascaris, Trichuris and Hookworm 2002, vol. 2:199-218. Kluwer Academic Publishers, Boston. C.V. Holland, M.W. Kennedy (Eds.).
99. Walker M., Hall A., Basanez M.G. Trickle or clumped infection process? An analysis of aggregation in the weights of the parasitic roundworm of humans, Ascaris lumbricoides. Int. J. Parasitol. 2010, 40:1373-1380.
100. Walker M., Hall A., Basanez M.G. Individual predisposition, household clustering and risk factors for human infection with Ascaris lumbricoides: new epidemiological insights. PLoS Neg. Trop. Dis. 2011, 5:e1047.
101. Weng Y.B., Hu Y.J., Li Y., Li B.S., Lin R.Q., Xie D.H., Gasser R.B., Zhu X.Q. Survey of intestinal parasites in pigs from intensive farms in Guangdong Province, People's Republic of China. Vet. Parasitol. 2005, 127:333-336.
102. WHO, 1987. Prevention and Control of Intestinal Parasitic Infections. Technical Report Series, 749. World Health Organization. Geneva.
103. WHO Preventative chemotherapy in human helminthiases: coordinated use of anthelminthic drugs in control interventions: a manual for health professionals and programme Managers 2006, World Health Organization, Geneva.
104. Williams-Blangero S., Subedi J., Upadhayay R.P., Manral D.B., Rai D.R., Jha B., Robinson E.S., Blangero J. Genetic analysis of susceptibility to infection with Ascaris lumbricoides. Am. J. Trop. Med. Hyg. 1999, 60:921-926.
105. Wu S.Q., Lin X.M., Zhu X.Q. Identification and functional analysis of differentially expressed genes of Ascaris suum Goeze, 1782 from Ascaris lumbricoides Linnaeus, 1758. Agric. Sci. China 2010, 9:903-910.
106. Zhang, S.K., Yuan, K., Yuan, F., Dai, Z.F., Hu, Y., Huang, Y.Q., Peng, W., 2008. Influence on host immunoregulation of Ascaris of selected genotypes. In: Proceedings of the Sixth National Immunology Academic Conference of China, p. 276. Available from: >http://cpfd.cnki.com.cn/Article/CPFDTOTAL-IGMD200810001396.htm.
107. Zhou, C.H., 2011. Further investigations of molecular genetics on Ascaris populations from humans and pigs from China. Doctoral dissertation, Nanchang University, China (in Chinese with English summery).
108. Zhou X., Peng W., Crompton D.W.T., Xiong J. Treatment of biliary ascariasis in China. Trans. Roy. Soc. Trop. Med. Hyg. 1999, 93:561-564.
109. Zhou C.H., Yuan K., Tang X., Hu N., Peng W. Molecular genetic evidence for polyandry in Ascaris suum. Parasitol. Res. 2011, 108:703-708.
110. Zhu X.Q., Chilton N.B., Jacobs D.E., Boes J., Gasser R.B. Characterisation of Ascaris from human and pig hosts by nuclear ribosomal DNA sequences. Int. J. Parasitol. 1999, 29:469-478.