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Intestinal Parasite Co-infection among Pulmonary Tuberculosis Cases without Human Immunodeficiency Virus Infection in a Rural County in China
Xin-Xu Li
Xin-Xu Li
National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, Key Laboratory of Parasite and Vector Biology, Ministry of Health, World Health Organization Collaborating Centre for Malaria, Schistosomiasis and Filariasis, Shanghai, China; National Center for Tuberculosis Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, China; Gushi County Center for Disease Control and Prevention, Henan Province, Gushi, China; Anhui Province Institute of Parasitic Disease Control, Hefei, China; Henan Province Center for Disease Control and Prevention, Zhengzhou, China
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Jia-Xu Chen
Jia-Xu Chen
National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, Key Laboratory of Parasite and Vector Biology, Ministry of Health, World Health Organization Collaborating Centre for Malaria, Schistosomiasis and Filariasis, Shanghai, China; National Center for Tuberculosis Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, China; Gushi County Center for Disease Control and Prevention, Henan Province, Gushi, China; Anhui Province Institute of Parasitic Disease Control, Hefei, China; Henan Province Center for Disease Control and Prevention, Zhengzhou, China
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Li-Xia Wang
Li-Xia Wang
National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, Key Laboratory of Parasite and Vector Biology, Ministry of Health, World Health Organization Collaborating Centre for Malaria, Schistosomiasis and Filariasis, Shanghai, China; National Center for Tuberculosis Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, China; Gushi County Center for Disease Control and Prevention, Henan Province, Gushi, China; Anhui Province Institute of Parasitic Disease Control, Hefei, China; Henan Province Center for Disease Control and Prevention, Zhengzhou, China
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Li-Guang Tian
Li-Guang Tian
National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, Key Laboratory of Parasite and Vector Biology, Ministry of Health, World Health Organization Collaborating Centre for Malaria, Schistosomiasis and Filariasis, Shanghai, China; National Center for Tuberculosis Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, China; Gushi County Center for Disease Control and Prevention, Henan Province, Gushi, China; Anhui Province Institute of Parasitic Disease Control, Hefei, China; Henan Province Center for Disease Control and Prevention, Zhengzhou, China
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Yu-Ping Zhang
Yu-Ping Zhang
National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, Key Laboratory of Parasite and Vector Biology, Ministry of Health, World Health Organization Collaborating Centre for Malaria, Schistosomiasis and Filariasis, Shanghai, China; National Center for Tuberculosis Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, China; Gushi County Center for Disease Control and Prevention, Henan Province, Gushi, China; Anhui Province Institute of Parasitic Disease Control, Hefei, China; Henan Province Center for Disease Control and Prevention, Zhengzhou, China
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Shuang-Pin Dong
Shuang-Pin Dong
National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, Key Laboratory of Parasite and Vector Biology, Ministry of Health, World Health Organization Collaborating Centre for Malaria, Schistosomiasis and Filariasis, Shanghai, China; National Center for Tuberculosis Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, China; Gushi County Center for Disease Control and Prevention, Henan Province, Gushi, China; Anhui Province Institute of Parasitic Disease Control, Hefei, China; Henan Province Center for Disease Control and Prevention, Zhengzhou, China
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Xue-Guang Hu
Xue-Guang Hu
National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, Key Laboratory of Parasite and Vector Biology, Ministry of Health, World Health Organization Collaborating Centre for Malaria, Schistosomiasis and Filariasis, Shanghai, China; National Center for Tuberculosis Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, China; Gushi County Center for Disease Control and Prevention, Henan Province, Gushi, China; Anhui Province Institute of Parasitic Disease Control, Hefei, China; Henan Province Center for Disease Control and Prevention, Zhengzhou, China
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Jian Liu
Jian Liu
National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, Key Laboratory of Parasite and Vector Biology, Ministry of Health, World Health Organization Collaborating Centre for Malaria, Schistosomiasis and Filariasis, Shanghai, China; National Center for Tuberculosis Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, China; Gushi County Center for Disease Control and Prevention, Henan Province, Gushi, China; Anhui Province Institute of Parasitic Disease Control, Hefei, China; Henan Province Center for Disease Control and Prevention, Zhengzhou, China
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Feng-Feng Wang
Feng-Feng Wang
National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, Key Laboratory of Parasite and Vector Biology, Ministry of Health, World Health Organization Collaborating Centre for Malaria, Schistosomiasis and Filariasis, Shanghai, China; National Center for Tuberculosis Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, China; Gushi County Center for Disease Control and Prevention, Henan Province, Gushi, China; Anhui Province Institute of Parasitic Disease Control, Hefei, China; Henan Province Center for Disease Control and Prevention, Zhengzhou, China
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Yue Wang
Yue Wang
National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, Key Laboratory of Parasite and Vector Biology, Ministry of Health, World Health Organization Collaborating Centre for Malaria, Schistosomiasis and Filariasis, Shanghai, China; National Center for Tuberculosis Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, China; Gushi County Center for Disease Control and Prevention, Henan Province, Gushi, China; Anhui Province Institute of Parasitic Disease Control, Hefei, China; Henan Province Center for Disease Control and Prevention, Zhengzhou, China
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Xiao-Mei Yin
Xiao-Mei Yin
National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, Key Laboratory of Parasite and Vector Biology, Ministry of Health, World Health Organization Collaborating Centre for Malaria, Schistosomiasis and Filariasis, Shanghai, China; National Center for Tuberculosis Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, China; Gushi County Center for Disease Control and Prevention, Henan Province, Gushi, China; Anhui Province Institute of Parasitic Disease Control, Hefei, China; Henan Province Center for Disease Control and Prevention, Zhengzhou, China
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Li-Jun He
Li-Jun He
National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, Key Laboratory of Parasite and Vector Biology, Ministry of Health, World Health Organization Collaborating Centre for Malaria, Schistosomiasis and Filariasis, Shanghai, China; National Center for Tuberculosis Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, China; Gushi County Center for Disease Control and Prevention, Henan Province, Gushi, China; Anhui Province Institute of Parasitic Disease Control, Hefei, China; Henan Province Center for Disease Control and Prevention, Zhengzhou, China
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Qiu-Ye Yan
Qiu-Ye Yan
National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, Key Laboratory of Parasite and Vector Biology, Ministry of Health, World Health Organization Collaborating Centre for Malaria, Schistosomiasis and Filariasis, Shanghai, China; National Center for Tuberculosis Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, China; Gushi County Center for Disease Control and Prevention, Henan Province, Gushi, China; Anhui Province Institute of Parasitic Disease Control, Hefei, China; Henan Province Center for Disease Control and Prevention, Zhengzhou, China
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Hong-Wei Zhang
Hong-Wei Zhang
National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, Key Laboratory of Parasite and Vector Biology, Ministry of Health, World Health Organization Collaborating Centre for Malaria, Schistosomiasis and Filariasis, Shanghai, China; National Center for Tuberculosis Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, China; Gushi County Center for Disease Control and Prevention, Henan Province, Gushi, China; Anhui Province Institute of Parasitic Disease Control, Hefei, China; Henan Province Center for Disease Control and Prevention, Zhengzhou, China
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Bian-Li Xu
Bian-Li Xu
National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, Key Laboratory of Parasite and Vector Biology, Ministry of Health, World Health Organization Collaborating Centre for Malaria, Schistosomiasis and Filariasis, Shanghai, China; National Center for Tuberculosis Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, China; Gushi County Center for Disease Control and Prevention, Henan Province, Gushi, China; Anhui Province Institute of Parasitic Disease Control, Hefei, China; Henan Province Center for Disease Control and Prevention, Zhengzhou, China
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Xiao-Nong Zhou
Xiao-Nong Zhou
National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, Key Laboratory of Parasite and Vector Biology, Ministry of Health, World Health Organization Collaborating Centre for Malaria, Schistosomiasis and Filariasis, Shanghai, China; National Center for Tuberculosis Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, China; Gushi County Center for Disease Control and Prevention, Henan Province, Gushi, China; Anhui Province Institute of Parasitic Disease Control, Hefei, China; Henan Province Center for Disease Control and Prevention, Zhengzhou, China
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Epidemiologic studies of co-infection with tuberculosis (TB) and intestinal parasites in humans have not been extensively investigated in China. A cross-section study was conducted in a rural county of Henan Province, China. Pulmonary TB (PTB) case-patients receiving treatment for infection with Mycobacterium tuberculosis and healthy controls matched for geographic area, age, and sex were surveyed by using questionnaires. Fecal and blood specimens were collected for detection of intestinal parasites, routine blood examination, and infection with human immunodeficiency virus. The chi-square test was used for univariate analysis and multivariate logistic regression models were used to adjust for potential confounding factors. A total of 369 persons with PTB and 366 healthy controls were included; all participants were negative for human immunodeficiency virus. The overall prevalence of intestinal parasites in persons with PTB was 14.9%, including intestinal protozoa (7.9%) and helminthes (7.6%). The infection spectrum of intestinal parasites was Entamoeba spp. (1.4%), Blastocystis hominis (6.2%), Trichomonas hominis (0.3%), Clonorchis sinensis (0.3%), Ascaris lumbricoides (0.5%), Trichuris trichiura (2.2%), and hookworm (4.6%). The prevalence of intestinal parasites showed no significant difference between persons with PTB and healthy controls after adjusting for potential confounding factors. There was no factor that affected infection rates for intestinal parasites between the two groups. Infection with intestinal parasites of persons with PTB was associated with female sex (adjusted odds ratio [AOR] = 2.05, 95% confidence interval [CI] = 1.01–4.17), body mass index ≤ 19 (AOR = 3.02, 95% CI = 1.47–6.20), and anemia (AOR = 2.43, 95% CI = 1.17–5.03). Infection of healthy controls was only associated with an annual labor time in farmlands > 2 months (AOR = 4.50, 95% CI = 2.03–10.00). In addition, there was no significant trend between rates of infection with intestinal parasites and duration of receiving treatment for infection with M. tuberculosis in persons with PTB. The prevalence of intestinal parasites was not higher in persons with PTB, and there was no evidence that PTB increased susceptibility to intestinal parasites in this study. However, for patients with PTB, women and patients with comorbidities were more likely to be infected with intestinal parasites.
Author Notes
Authors' contributions: Xin-Xu Li, Jia-Xu Chen, Li-Xia Wang, and Xiao-Nong Zhou conceived and designed the study; Xin-Xu Li, Li-Guang Tian, Yu-Ping Zhang, Shuang-Pin Dong, Xue-Guang Hu, Jian Lu, Feng-Feng Wang, Yue Wang, Xiao-Mei Yin, Li-Jun He, Qiu-Ye Yan, Hong-Wei Zhang, and Bian-Li Xu conducted the study; Xin-Xu Li and Li-Guang Tian analyzed the data; Xin-Xu Li wrote the first draft of the manuscript; Jia-Xu Chen, Li-Xia Wang, and Bian-Li Xu provided constructive opinions and suggestions; Xiao-Nong Zhou provided strategic advice and assisted with editing of the manuscript; and all authors read and approved the final version of the manuscript.
Financial support: This study was supported by National Science and Technology Major Program (grant no. 2012ZX10004-220).
Disclosure: None of the authors have any conflicts of interest.
Authors' addresses: Xin-Xu Li, National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, Key Laboratory of Parasite and Vector Biology, Ministry of Health, World Health Organization Collaborating Centre for Malaria, Schistosomiasis and Filariasis, Shanghai 200025, China, and National Center for Tuberculosis Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, China, E-mail: lixinxu@chinatb.org. Jia-Xu Chen, Li-Guang Tian, and Xiao-Nong Zhou, National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, Key Laboratory of Parasite and Vector Biology, Ministry of Health, World Health Organization Collaborating Centre for Malaria, Schistosomiasis and Filariasis, Shanghai 200025, China, E-mails: chenjiaxu1962@163.com, jztlg@126.com, and xiaonongzhou1962@gmail.com. Li-Xia Wang, National Center for Tuberculosis Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing 102206, China, E-mail: wanglx@chinatb.org. Yu-Ping Zhang, Shuang-Pin Dong, Xue-Guang Hu, and Jian Liu, Gushi County Center for Disease Control and Prevention, Henan Province, Gushi 465200, China, E-mails: wuhen19870103@126.com, dsp.2525@163.com, and gsxnfk@163.com. Feng-Feng Wang, Yue Wang, and Xiao-Mei Yin, Anhui Province Institute of Parasitic Disease Control, Hefei 230061, China, E-mails: wangfengahwh@163.com, bridgety@foxmail.com, and xmyahwh@126.com. Li-Jun He, Qiu-Ye Yan, Hong-Wei Zhang, and Bian-Li Xu, Henan Province Center for Disease Control and Prevention, Zhengzhou 450016, China, E-mails: helj@hncdc.com.cn, yanqiuye@126.com, zhanghw@hncdc.com.cn, and xubl@hncdc.com.cn.
ProCite
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-
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Tian LG, Wang TP, Lv S, Wang FF, Guo J, Yin XM, Cai YC, Dickey MK, Steinmann P, Chen JX, 2013. HIV and intestinal parasite co-infections among a Chinese population: an immunological profile. Infect Dis Poverty 2: 18.
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7.
Mofid LS, Bickle Q, Jiang JY, Du ZW, Patrick E, 2011. Soil-transmitted helminthiasis in rural south-west China: prevalence, intensity and risk factor analysis. Southeast Asian J Trop Med Public Health 42: 513–526.
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8.
Tang N, Luo NJ, 2003. A cross-sectional study of intestinal parasitic infections in a rural district of west China. Can J Infect Dis Med Microbiol 14: 159–162.
-
9.
Resende Co T, Hirsch CS, Toossi Z, Dietze R, Ribeiro-Rodrigues R, 2007. Intestinal helminth co-infection has a negative impact on both anti-Mycobacterium tuberculosis immunity and clinical response to tuberculosis therapy. Clin Exp Immunol 147: 45–52.
-
10.
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-
11.
Kashuba EA, Rusakova LI, 1992. Anthelmintic therapy of opisthorchiasis in patients with active tuberculosis [in Russian]. Probl Tuberk 3–4: 33–36.
-
12.
Ferreira AP, Aguiar AS, Fava MW, Correa JO, Teixeira FM, Teixeira HC, 2002. Can the efficacy of Bacille Calmette-Guerin tuberculosis vaccine be affected by intestinal parasitic infections? J Infect Dis 186: 441–442, author reply 442–443.
-
13.
Elias D, Akuffo H, Pawlowski A, Haile M, Schon T, Britton S, 2005. Schistosoma mansoni infection reduces the protective efficacy of BCG vaccination against virulent Mycobacterium tuberculosis. Vaccine 23: 1326–1334.
-
14.
Disease Control Bureau of the Ministry of Health, Department of Medical Administration of the Ministry of Health, Chinese Center for Disease Control and Prevention, 2009. Guidelines for Implementing the National Tuberculosis Control Program in China, 2008. Beijing, China: Peking Union Medical College Press.
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15.
Lu Z, Zhong N, 2008. Internal Medicine. Beijing, China: People's Medical Publishing House.
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16.
Leelayoova S, Taamasri P, Rangsin R, Naaglor T, Thathaisong U, Mungthin M, 2002. In-vitro cultivation: a sensitive method for detecting Blastocystis hominis. Ann Trop Med Parasitol 96: 803–807.
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