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Study on the tolerance and adaptation of rats to Angiostrongylus cantonensis infection

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Abstract

Angiostrongylus cantonensis (A. cantonensis) is the most common infectious agent causing eosinophilic meningitis. As an important food-borne parasitic disease, angiostrongyliasis cantonensis is an emerging infectious disease which brings severe harm to central nerve system of human. Rat, one of the few permissive hosts of A. cantonensis known to date, plays an indispensable role in the worm’s life cycle. However, the tolerance and adaptation of rat to A. cantonensis infection is rarely understood. In this study, we infected rats with different numbers the third stage larvae (L3) of A. cantonensis and explored their tolerance through analysis on survival curve, neurological function score, and detection of pathological damages in organs including the brain, lung, and heart of the animals. Results indicated that rats’ survival condition worsens, and body weight dropped more significantly as more worms were used for infection. Death appeared in groups infected with 80 and more A. cantonesnsis per rat. Morris water maze revealed that the neurological function of rats damaged gradually with increasing infection number of A. cantonensis larvae. When the number of infected parasite exceeded 240 per animal, rats showed significant neurological impairments. Collection of A. cantonensis from rat lung after 35 days of infection implied an upper limit for worm entry, and the average length of worm was inversely proportional to the infection amount, while the ratio between female and male worms was positively related to the infection number. The degree of pulmonary and cardiac inflammation was proportional to the infection number of A. cantonensis. Meanwhile, there existed considerable amount of adult worms in rat’s right atrium and right ventricle, leading to a right heart myocardial inflammation. The present study firstly reports the tolerance and adaptation of rat, a permissive host of A. cantonensis to its infection, which will not only provide accurate technical parameters for maintaining A. cantonensis life cycle under laboratory conditions but also help unveil the underlying mechanism of the distinct pathological outcomes in the permissive and non-permissive hosts with A. cantonensis infection.

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References

  • Chen HT (1935) Un nouveau nematode pulmonaire, Pulmonem A. cantonensis n.g., n. sp. des rats de Canton. Ann Parasitol 13(4):312–317

    Google Scholar 

  • Eamsobhana P (2014) Eosinophilic meningitis caused by Angiostrongylus cantonensis—a neglected disease with escalating importance. Trop Biomed 31(4):569–578

    CAS  PubMed  Google Scholar 

  • Feng F, Feng Y, Liu Z, Li WH, Wang WC, Wu ZD, Lv Z (2015) Effects of albendazole combined with TSII-A (a Chinese herb compound) on optic neuritis caused by Angiostrongylus cantonensis in BALB/c mice. Parasit Vectors 25(8):606

    Article  Google Scholar 

  • Gryseels B, Polman K, Clerinx J, Kestens L (2006) Human schistosomiasis. Lancet 368(9541):1106–1118

    Article  PubMed  Google Scholar 

  • Haukisalmi V, Henttonen H, Vikman P (1996) Variability of sex ratio, mating probability and egg production in an intestinal nematode in its fluctuating host population. Int J Parasitol 26(7):755–763

    Article  CAS  PubMed  Google Scholar 

  • Hirao A, Ehlers RU (2008) Influence of nematode inoculum density and temperature on development of Steinernema carpocapsae and S. feltiae in liquid culture. Commun Agric Appl Biol Sci 73(4):699–702

    CAS  PubMed  Google Scholar 

  • Huntley JW, De Baets K (2015) Trace fossil evidence of trematode-bivalve parasite-host interactions in deep time. Adv Parasitol 90:201–231

    Article  PubMed  Google Scholar 

  • Ishii AI, Kino H, Hayashi M, Fujio Y, Sano M (1980) Experimental light infection of Angiostrongylus cantonensis in hamsters. Int J Zoonoses 7(2):120–124

    CAS  PubMed  Google Scholar 

  • Jiang J, Gao K, Zhou Y, Xu A, Shi S, Liu G, Li Z (2015) Electroacupuncture treatment improves learning-memory ability and brain glucose metabolism in a mouse model of Alzheimer’s disease: using Morris water maze and Micro-PET. Evid Based Complement Alternat Med 2015:142129

    PubMed  PubMed Central  Google Scholar 

  • Ko RC (1978) Occurrence of Angiostrongylus cantonensis in the heart of a spider monkey. J Helminthol 52(3):229

    Article  CAS  PubMed  Google Scholar 

  • Lan KP, Lai SC (2008) Angiostrongylus cantonensis: induction of urokinase-type PA and degradation of type IV collagen in rat lung granulomatous fibrosis. Exp Parasitol 118(4):472–477

    Article  CAS  PubMed  Google Scholar 

  • Lee HH, Jiang ST, Shyu LY, Lin WL, Chian HC, Hsu CC, Chou FP, Wang CJ (1996) L ferritin accumulation in macrophages infiltrating the lung during rat Angiostrongylus cantonensis infection. Exp Parasitol 83(1):55–61

    Article  CAS  PubMed  Google Scholar 

  • Li S, Yang F, Ji P, Zeng X, Wu X, Wei J, Ouyang L, Liang J, Zheng H, Wu Z, Lv Z (2014a) Eosinophil chemotactic chemokine profilings of the brain from permissive and non-permissive hosts infected with Angiostrongylus cantonenis. Parasitol Res 113(2):517–525

    Article  PubMed  Google Scholar 

  • Li Z, Chen X, Zen X, Liang J, Wei J, Lv Z, Sun X, Wu ZD (2014b) MicroRNA expression profile in the third- and fourth-stage larvae of Angiostrongylus cantonensis. Parasitol Res 113(5):1883–1896

    Article  PubMed  Google Scholar 

  • Liu Z, Wu Y, Feng Y, Wu F, Liu RF, Wang LF, Liang JY, Liu JH, Sun X, Wu ZD (2017) Spleen atrophy related immune system changes attributed to infection of Angiostrongylus cantonensis in mouse model. Parasitol Res 116(2):577–587

    Article  PubMed  Google Scholar 

  • Lv S, Zhang Y, Liu HX, Hu L, Yang K, Steinmann P, Chen Z, Wang LY, Utzinger J, Zhou XN (2009) Invasive snails and an emerging infectious disease: results from the first national survey on Angiostrongylus cantonensis in China. PLoS Negl Trop Dis 3(2):e368

    Article  PubMed  PubMed Central  Google Scholar 

  • McBride A, Chau TT, Hong NT, Mai NT, Anh NT, Thanh TT, Van TT, Xuan LT, Sieu TP, Thai LH, Chuong LV, Sinh DX, Phong ND, Phu NH, Day J, Nghia HD, Hien TT, Chau NV, Thwaites G, Tan LV (2017) Angiostrongylus cantonensis is an important cause of eosinophilic meningitis in southern Vietnam. Clin Infect Dis. doi:10.1093/cid/cix118

  • Mutlu O, Akar F, Celikyurt IK, Tanyeri P, Ulak G, Erden F (2015) 7-NI and ODQ disturbs memory in the elevated plus maze, Morris water maze, and radial arm maze tests in mice. Drug Target Insights 9:1–8

    Article  PubMed  PubMed Central  Google Scholar 

  • New D, Little MD, Cross J (1995) Angiostrongylus cantonensis infection from eating raw snails. N Engl J Med 332(16):1105–1106

    Article  CAS  PubMed  Google Scholar 

  • Papkou A, Gokhale CS, Traulsen A, Schulenburg H (2016) Host-parasite coevolution: why changing population size matters. Zoology (Jena) 119(4):330–338

    Article  Google Scholar 

  • Paterson S, Viney ME (2002) Host immune responses are necessary for density dependence in nematode infections. Parasitology 125(Pt 3):283–292

    CAS  PubMed  Google Scholar 

  • Qvarnstrom Y, Xayavong M, da Silva AC, Park SY, Whelen AC, Calimlim PS, Sciulli RH, Honda SA, Higa K, Kitsutani P, Chea N, Heng S, Johnson S, Graeff-Teixeira C, Fox LM, da Silva AJ (2016) Real-time polymerase chain reaction detection of Angiostrongylus cantonensis DNA in cerebrospinal fluid from patients with eosinophilic meningitis. AmJTrop Med Hyg 94(1):176–181

    Article  CAS  Google Scholar 

  • Reynolds A, Lindström J, Johnson PC, Mable BK (2016) Evolution of drug-tolerant nematode populations in response to density reduction. Evol Appl 9(5):726–738

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Swann J, Jamshidi N, Lewis NE, Winzeler EA (2015) Systems analysis of host-parasite interactions. Wiley Interdiscip Rev Syst Biol Med 7(6):381–400

    Article  PubMed  PubMed Central  Google Scholar 

  • Szabo EK, Finney CA (2017) Toxoplasma gondii: one organism, multiple models. Trends Parasitol 33(2):113–127

    Article  PubMed  Google Scholar 

  • Tang ZL, Huang Y, Yu XB (2016) Current status and perspectives of Clonorchis sinensis and clonorchiasis: epidemiology, pathogenesis, omics, prevention and control. Infect Dis Poverty 5(1):71

    Article  PubMed  PubMed Central  Google Scholar 

  • Therese MO, Bashey F (2012) Natal-host environmental effects on juvenile size, transmission success, and operational sex ratio in the entomopathogenic nematode Steinernema carpocapsae. J Parasitol 98(6):1095–1100

    Article  CAS  PubMed  Google Scholar 

  • Tsai HC, Lee SS, Huang CK, Yen CM, Chen ER, Liu YC (2004) Outbreak of eosinophilic meningitis associated with drinking raw vegetable juice in southern Taiwan. AmJTrop Med Hyg 71(2):222–226

    Google Scholar 

  • Wang QP, Wu ZD, Wei J, Owen RL, Lun ZR (2012) Human Angiostrongylus cantonensis: an update. Eur J Clin Microbiol Infect Dis 31(4):389–395

    Article  PubMed  Google Scholar 

  • Wang LC, Jung SM, Chen KY, Wang TY, Li CH (2015) Temporal-spatial pathological changes in the brains of permissive and non-permissive hosts experimentally infected with Angiostrongylus cantonensis. Exp Parasitol 157:177–184

    Article  PubMed  Google Scholar 

  • Wei J, Wu F, He A, Zeng X, Ouyang LS, Liu MS, Zheng HQ, Lei WL, Wu ZD, Lv ZY (2015) Microglia activation: one of the checkpoints in the CNS inflammation caused by Angiostrongylus cantonensis infection in rodent model. Parasitol Res 114(9):3247–3254

    Article  PubMed  Google Scholar 

  • Yu L, Liao Q, Zeng X, Lv Z, Zheng H, Zhao Y, Sun X, Wu Z (2014) MicroRNA expressions associated with eosinophilic meningitis caused by Angiostrongylus cantonensis infection in a mouse model. Eur J Clin Microbiol Infect Dis 33(8):1457–1465

    Article  CAS  PubMed  Google Scholar 

  • Zhang L, Fang Y, Lian Y, Chen Y, Wu T, Zheng Y, Zong H, Sun L, Zhang R, Wang Z, Xu Y (2015) Brain-derived neurotrophic factor ameliorates learning deficits in a rat model of Alzheimer’s disease induced by aβ1-42. PLoS One 10(4):e0122415

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhong W, Yang M, Zhang W, Visocchi M, Chen X, Liao C (2017) Improved neural microcirculation and regeneration after peripheral nerve decompression in DPN rats. Neurol Res 14:1–7

    Google Scholar 

Download references

Acknowledgements

This work was supported by grants from the National Key Research and Development Program of China (grant no. 2016YFC1202003, 2016YFC1202005, and 2016YFC1200500), the National Natural Science Foundation of China (grant no. 81371836, 81572023, 81271855, 81261160324, and 81401689), Project of Basic Platform of National Science and Technology Resources of the Ministry of Sciences and Technology of China (grant no. TDRC-2017-22), Guangdong Natural Science Foundation (grant no. 2014A030313134 and 2014A030310228), Science and Technology Planning Project of Guangdong Province (grant no. 2016A050502008), Science and Technology Planning Project of Guangzhou (grant no. 201607010029), the Undergraduates Innovation Training Program of Guangdong Province (201410558274, 201601084), and the Laboratory of Parasite and Vector Biology, MOPH (grant no. WSBKTKT201401).

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Authors and Affiliations

  1. Zhongshan School of Medicine, Sun Yat-sen University, 74 2nd Zhongshan Road, Guangzhou, 510080, China

    Liu Ji, Zhang Mengying, Hu Yue, Wu Yanqi, Song Langui, Zeng Xin, Lin Datao, Wan Shuo, Zheng Huanqin, Wu Zhongdao & Lv Zhiyue

  2. Key Laboratory of Tropical Disease Control, Ministry of Education, Sun Yat-sen University, Guangzhou, 510080, China

    Liu Ji, Zhang Mengying, Hu Yue, Wu Yanqi, Song Langui, Zeng Xin, Lin Datao, Wan Shuo, Zheng Huanqin, Wu Zhongdao & Lv Zhiyue

  3. Provincial Engineering Technology Research Center for Biological Vector Control, Guangzhou, 510080, China

    Liu Ji, Zhang Mengying, Hu Yue, Wu Yanqi, Song Langui, Zeng Xin, Lin Datao, Wan Shuo, Zheng Huanqin, Wu Zhongdao & Lv Zhiyue

  4. School of Life Sciences, The Chinese University of Hong Kong, Hong Kong, SAR, China

    Xu Yiyue

  5. State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong, Hong Kong, SAR, China

    Xu Yiyue

  6. The Affiliated High School of South China Normal University, Guangzhou, 510630, China

    He Xujin

  7. Department of Clinical Laboratory, Sun Yat-sen Memorial Hospital of Sun Yat-sen University, Guangzhou, 510120, China

    Zheng Minghui

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  1. Liu Ji
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  14. Lv Zhiyue
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Corresponding author

Correspondence to Lv Zhiyue.

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Liu Ji, Xu Yiyue, and He Xujin are the joint first authors.

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Ji, L., Yiyue, X., Xujin, H. et al. Study on the tolerance and adaptation of rats to Angiostrongylus cantonensis infection. Parasitol Res 116, 1937–1945 (2017). https://doi.org/10.1007/s00436-017-5472-4

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  • DOI: https://doi.org/10.1007/s00436-017-5472-4

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