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Preplanned Studies: Soil-Transmitted Helminthiasis — China, 2018

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  • Summary

    What is already known about this topic?

    Soil-transmitted helminthiasis (STH) is distributed widely in China and a large number of the population is afflicted. However, trends of STH infections are decreasing.

    What is added by this report?

    The most recent data indicates that the overall prevalence of STH was 1.29% in 2018 in China, which was based on the national sentinel surveillance and demonstrates a continuous decline pattern.

    What are the implications for public health practice?

    Considering the current prevalence in China and various endemic statuses in different regions, precision control measures should be implemented for the control and elimination of STH in China.

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  • [1] Jourdan PM, Lamberton PHL, Fenwick A, Addiss DG. Soil-transmitted helminth infections. Lancet 2018;391(10117):252 − 65. http://dx.doi.org/10.1016/S0140-6736(17)31930-XCrossRef
    [2] GBD 2015 DALYs, HALE Collaborators. Global, regional, and national disability-adjusted life-years (DALYs) for 315 diseases and injuries and healthy life expectancy (HALE), 1990−2015: a systematic analysis for the Global Burden of Disease Study 2015. Lancet 2016;388(10053):1603 − 58. http://dx.doi.org/10.1016/S0140-6736(16)31460-XCrossRef
    [3] Xu LQ, Yu SH, Jiang ZX, Yang JL, Lai LQ, Zhang XJ, et al. Soil-transmitted helminthiases: nationwide survey in China. Bull World Health Organ 1995;73(4):507 − 13. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2486772/.https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2486772/
    [4] Coordinating Office of the National Survey on the Important Human Parasitic Diseases. A national survey on current status of the important parasitic diseases in human population. Chin J Parasitol Parasit Dis 2005;23(S5):332 − 40. http://www.cqvip.com/qk/96021X/2005B10/20995452.html. (In Chinese).http://www.cqvip.com/qk/96021X/2005B10/20995452.html
    [5] Zhou XN. Report on the national survey of important human parasitic diseases in China (2015). People’s Medical Publishing House.
    [6] Zhu HH, Huang JL, Zhu TJ, Duan L, Zhou CH, Qian MB, et al. National surveillance of soil-transmitted helminth infections in 2017. Chin J Parasitol Parasit Dis 2019;37(1):12 − 7. http://dx.doi.org/10.12140/j.issn.1000-7423.2019.01.003 (In Chinese)CrossRef
    [7] Chen YD, Zhu HH, Huang JL, Zhu TJ, Zhou CH, Qian MB, et al. Status and working principals of soil-transmitted nematodiasis during new period in China. Chin J Schisto Control 2019;31(1):23 − 5. http://dx.doi.org/10.16250/j.32.1374.2018309 (In Chinese)CrossRef
    [8] China CDC. Annual Report on Surveillance of Selected Infectious Diseases and Vectors, China, 2006–2015.
    [9] Chen YD, Zang W. Current situation of soil-transmitted nematodiasis monitoring in China and working keys in future. Chin J Schisto Control 2015;27(2):111 − 4. http://dx.doi.org/10.16250/j.32.1374.2015004 (In Chinese)CrossRef
    [10] Qian MB, Chen YD, Zhou XN. Research priorities for the control and elimination of major helminthiases. Chin J Parasitol Parasit Dis, 2013;31(2):155 − 9. http://www.wanfangdata.com.cn/details/detail.do?_type=perio&id=zgjscxyjscbzz201302020. (In Chinese).http://www.wanfangdata.com.cn/details/detail.do?_type=perio&id=zgjscxyjscbzz201302020
  • FIGURE 1.  Infection rate of soil-transmitted helminth in each provincial-level administrative divisions of China according to the 2018 National Sentinel Surveillance.

    FIGURE 2.  Infection rate of soil-transmitted helminth by different age groups in China according to the 2018 National Sentinel Surveillance.

    TABLE 1.  Infection rate of soil-transmitted helminth in China according to the 2018 National Sentinel Surveillance.

    PLADsNo. of examinationSoil-transmitted helminthHookwormAscaris lumbricoides Trichuris trichiura
    No. of infectionsPrevalence %
    (95% CI)
    No. of infectionsPrevalence %
    (95% CI)
    No. of infectionsPrevalence %
    (95% CI)
    No. of infectionsPrevalence %
    (95% CI)
    Beijing 3,087 0 0.00 (0.00−0.00) 0 0.00 (0.00−0.00) 0 0.00 (0.00−0.00) 0 0.00 (0.00−0.00)
    Tianjin* 3,023 4 0.13 (0.00−0.26) 0 0.00 (0.00−0.00) 4 0.13 (0.00−0.26) 0 0.00 (0.00−0.00)
    Hebei 15,048 1 0.01 (0.00−0.02) 0 0.00 (0.00−0.00) 1 0.01 (0.00−0.02) 0 0.00 (0.00−0.00)
    Inner Mongolia* 10,034 1 0.01 (0.00−0.03) 0 0.00 (0.00−0.00) 0 0.00 (0.00−0.00) 1 0.01 (0.00−0.03)
    Liaoning* 12,042 31 0.26 (0.17−0.35) 0 0.00 (0.00−0.00) 29 0.24 (0.15−0.33) 2 0.02 (0.00−0.04)
    Jilin* 21,812 61 0.28 (0.21−0.35) 0 0.00 (0.00−0.00) 60 0.28 (0.21−0.34) 1 0.00 (0.00−0.01)
    Heilongjiang 19,065 0 0.00 (0.00−0.00) 0 0.00 (0.00−0.00) 0 0.00 (0.00−0.00) 0 0.00 (0.00−0.00)
    Shanghai 2,003 0 0.00 (0.00−0.00) 0 0.00 (0.00−0.00) 0 0.00 (0.00−0.00) 0 0.00 (0.00−0.00)
    Jiangsu 4,003 7 0.17 (0.05−0.30) 1 0.02 (0.00−0.07) 4 0.10 (0.00−0.20) 2 0.05 (0.00−0.12)
    Zhejiang* 9,120 124 1.36 (1.12−1.60) 122 1.34 (1.10−1.57) 0 0.00 (0.00−0.00) 2 0.02 (0.00−0.05)
    Anhui 14,689 166 1.13 (0.96−1.30) 157 1.07 (0.90−1.24) 1 0.01 (0.00−0.02) 8 0.05 (0.02−0.09)
    Fujian 12,475 215 1.72 (1.50−1.95) 201 1.61 (1.39−1.83) 0 0.00 (0.00−0.00) 14 0.11 (0.05−0.17)
    Jiangxi 13,082 109 0.83 (0.68−0.99) 82 0.63 (0.49−0.76) 14 0.11 (0.05−0.16) 13 0.10 (0.05−0.15)
    Shandong 14,399 96 0.67 (0.53−0.80) 0 0.00 (0.00−0.00) 21 0.15 (0.08−0.21) 76 0.53 (0.41−0.65)
    Henan 19,856 16 0.08 (0.04−0.12) 7 0.04 (0.01−0.06) 8 0.04 (0.01−0.07) 1 0.01 (0.00−0.01)
    Hubei 10,099 2 0.02 (0.00−0.05) 1 0.01 (0.00−0.03) 0 0.00 (0.00−0.00) 1 0.01 (0.00−0.03)
    Hunan 37,398 251 0.67 (0.59−0.75) 57 0.15 (0.11−0.19) 184 0.49 (0.42−0.56) 14 0.04 (0.02−0.06)
    Guangdong 19,463 44 0.23 (0.16−0.29) 19 0.10 (0.05−0.14) 11 0.06 (0.02−0.09) 16 0.08 (0.04−0.12)
    Guangxi 13,727 334 2.43 (2.18−2.69) 305 2.22 (1.98−2.47) 4 0.03 (0.00−0.06) 26 0.19 (0.12−0.26)
    Hainan 2,959 212 7.16 (6.24−8.09) 201 6.79 (5.89−7.70) 0 0.00 (0.00−0.00) 11 0.37 (0.15−0.59)
    Chongqing 6,372 367 5.76 (5.19−6.33) 356 5.59 (5.02−6.15) 12 0.19 (0.08−0.29) 2 0.03 (0.00−0.07)
    Sichuan 14,292 1,064 7.44 (7.01−7.88) 867 6.07 (5.67−6.46) 185 1.29 (1.11−1.48) 47 0.33 (0.23−0.42)
    Guizhou 4,617 213 4.61 (4.01−5.22) 9 0.19 (0.07−0.32) 126 2.73 (2.26−3.20) 92 1.99 (1.59−2.40)
    Yunnan 5,567 784 14.08 (13.17−15.00) 526 9.45 (8.68−10.22) 113 2.03 (1.66−2.40) 214 3.84 (3.34−4.35)
    Shaanxi* 8,993 15 0.17 (0.08−0.25) 0 0.00 (0.00−0.00) 15 0.17 (0.08−0.25) 0 0.00 (0.00−0.00)
    Gansu 8,750 12 0.14 (0.06−0.21) 0 0.00 (0.00−0.00) 12 0.14 (0.06−0.21) 0 0.00 (0.00−0.00)
    Qinghai 3,906 23 0.59 (0.35−0.83) 0 0.00 (0.00−0.00) 23 0.59 (0.35−0.83) 0 0.00 (0.00−0.00)
    Ningxia* 2,948 40 1.36 (0.94−1.77) 0 0.00 (0.00−0.00) 40 1.36 (0.94−1.77) 0 0.00 (0.00−0.00)
    Xinjiang* 13,378 8 0.06 (0.02−0.10) 0 0.00 (0.00−0.00) 8 0.06 (0.02−0.10) 0 0.00 (0.00−0.00)
    Total 326,207 4,200 1.29 (1.25−1.33) 2,911 0.89 (0.86−0.92) 875 0.27 (0.25−0.29) 543 0.17 (0.15−0.18)
    Abbreviations: PLADs=provincial-level administrative divisions.
    *These PLADs have no national surveillance spots before 2015 and started NSS since 2016.
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Soil-Transmitted Helminthiasis — China, 2018

View author affiliation

Summary

What is already known about this topic?

Soil-transmitted helminthiasis (STH) is distributed widely in China and a large number of the population is afflicted. However, trends of STH infections are decreasing.

What is added by this report?

The most recent data indicates that the overall prevalence of STH was 1.29% in 2018 in China, which was based on the national sentinel surveillance and demonstrates a continuous decline pattern.

What are the implications for public health practice?

Considering the current prevalence in China and various endemic statuses in different regions, precision control measures should be implemented for the control and elimination of STH in China.

  • 1 National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention; Chinese Center for Tropical Diseases Research; WHO Collaborating Centre for Tropical Diseases; National Center for International Research on Tropical Diseases, Ministry of Science and Technology; Key Laboratory of Parasite and Vector Biology, Ministry of Health, Shanghai, China
  • Corresponding authors:

    Yingdan Chen, chenyd@nipd.chinacdc.cn

    Shizhu Li, stoneli1130@126.com

    doi: 10.46234/ccdcw2020.010
  • Soil-transmitted helminthiasis (STH) is caused by infections with parasitic worms such as hookworms (Necator americanus and Ancylostoma duodenale), Ascaris lumbricoides, and Trichuris trichiura. STH is highly endemic in underdeveloped areas and causes a burden of 3.38 million disability-adjusted life years globally (1-2). Based on the three national surveys implemented in 1988−1992, 2001−2004, and 2014−2015 in China, the infection rate of STH was 53.58%, 19.56%, and 4.49%, respectively. Correspondingly, the estimated number of population infected was 646 million, 129 million, and 29.12 million, respectively (3-5).

    China’s National Sentinel Surveillance (NSS) on STH started in 2006 when 22 sites from 22 provincial-level administrative divisions (PLADs) were launched for ten successive years. The range of the system has been greatly expanded since 2016, covering 30 of the 31 PLADs in Mainland China with more than 250 sentinel surveillance spots each year (6). The results of NSS on STH in 2018 are reported here.

    In 2018, 29 PLADs were included in the NSS, and 10%–15% of counties from each PLAD were included. Five townships were selected in each sentinel surveillance site, which was county-based, with one from the east, west, north, south, and central regions of the site. One village was then sampled from each township, and finally about 200 people were investigated from each village by cluster sampling. Thus, a total of 1,000 people were investigated at each site. Stool samples (>30 grams) were collected from each participant and examined by the Kato-Katz method (double smears for each sample). An infection was defined as one or more eggs detected in either of the two smears. The data were analyzed using SAS software (Version 9.3, SAS Institute Inc.). The infection rate of STH was categorized by PLAD, sex, and age group, and chi-square tests were used to compare the differences between categories. Statistical significance was set as 0.05.

  • A total of 325 sentinel surveillance spots from 29 PLADs were included in 2018. The overall infection rate of STH was 1.29% (4,200/326,207). The infection rate in 2018 was significantly lower than that found in 2017 (${\chi ^2}\!=\!253.14$, p<0.0001). The infection rate of hookworm was the highest (0.89%), followed by A. lumbricoides (0.27%), and T. trichiura (0.17%) (Table 1).

    PLADsNo. of examinationSoil-transmitted helminthHookwormAscaris lumbricoides Trichuris trichiura
    No. of infectionsPrevalence %
    (95% CI)
    No. of infectionsPrevalence %
    (95% CI)
    No. of infectionsPrevalence %
    (95% CI)
    No. of infectionsPrevalence %
    (95% CI)
    Beijing 3,087 0 0.00 (0.00−0.00) 0 0.00 (0.00−0.00) 0 0.00 (0.00−0.00) 0 0.00 (0.00−0.00)
    Tianjin* 3,023 4 0.13 (0.00−0.26) 0 0.00 (0.00−0.00) 4 0.13 (0.00−0.26) 0 0.00 (0.00−0.00)
    Hebei 15,048 1 0.01 (0.00−0.02) 0 0.00 (0.00−0.00) 1 0.01 (0.00−0.02) 0 0.00 (0.00−0.00)
    Inner Mongolia* 10,034 1 0.01 (0.00−0.03) 0 0.00 (0.00−0.00) 0 0.00 (0.00−0.00) 1 0.01 (0.00−0.03)
    Liaoning* 12,042 31 0.26 (0.17−0.35) 0 0.00 (0.00−0.00) 29 0.24 (0.15−0.33) 2 0.02 (0.00−0.04)
    Jilin* 21,812 61 0.28 (0.21−0.35) 0 0.00 (0.00−0.00) 60 0.28 (0.21−0.34) 1 0.00 (0.00−0.01)
    Heilongjiang 19,065 0 0.00 (0.00−0.00) 0 0.00 (0.00−0.00) 0 0.00 (0.00−0.00) 0 0.00 (0.00−0.00)
    Shanghai 2,003 0 0.00 (0.00−0.00) 0 0.00 (0.00−0.00) 0 0.00 (0.00−0.00) 0 0.00 (0.00−0.00)
    Jiangsu 4,003 7 0.17 (0.05−0.30) 1 0.02 (0.00−0.07) 4 0.10 (0.00−0.20) 2 0.05 (0.00−0.12)
    Zhejiang* 9,120 124 1.36 (1.12−1.60) 122 1.34 (1.10−1.57) 0 0.00 (0.00−0.00) 2 0.02 (0.00−0.05)
    Anhui 14,689 166 1.13 (0.96−1.30) 157 1.07 (0.90−1.24) 1 0.01 (0.00−0.02) 8 0.05 (0.02−0.09)
    Fujian 12,475 215 1.72 (1.50−1.95) 201 1.61 (1.39−1.83) 0 0.00 (0.00−0.00) 14 0.11 (0.05−0.17)
    Jiangxi 13,082 109 0.83 (0.68−0.99) 82 0.63 (0.49−0.76) 14 0.11 (0.05−0.16) 13 0.10 (0.05−0.15)
    Shandong 14,399 96 0.67 (0.53−0.80) 0 0.00 (0.00−0.00) 21 0.15 (0.08−0.21) 76 0.53 (0.41−0.65)
    Henan 19,856 16 0.08 (0.04−0.12) 7 0.04 (0.01−0.06) 8 0.04 (0.01−0.07) 1 0.01 (0.00−0.01)
    Hubei 10,099 2 0.02 (0.00−0.05) 1 0.01 (0.00−0.03) 0 0.00 (0.00−0.00) 1 0.01 (0.00−0.03)
    Hunan 37,398 251 0.67 (0.59−0.75) 57 0.15 (0.11−0.19) 184 0.49 (0.42−0.56) 14 0.04 (0.02−0.06)
    Guangdong 19,463 44 0.23 (0.16−0.29) 19 0.10 (0.05−0.14) 11 0.06 (0.02−0.09) 16 0.08 (0.04−0.12)
    Guangxi 13,727 334 2.43 (2.18−2.69) 305 2.22 (1.98−2.47) 4 0.03 (0.00−0.06) 26 0.19 (0.12−0.26)
    Hainan 2,959 212 7.16 (6.24−8.09) 201 6.79 (5.89−7.70) 0 0.00 (0.00−0.00) 11 0.37 (0.15−0.59)
    Chongqing 6,372 367 5.76 (5.19−6.33) 356 5.59 (5.02−6.15) 12 0.19 (0.08−0.29) 2 0.03 (0.00−0.07)
    Sichuan 14,292 1,064 7.44 (7.01−7.88) 867 6.07 (5.67−6.46) 185 1.29 (1.11−1.48) 47 0.33 (0.23−0.42)
    Guizhou 4,617 213 4.61 (4.01−5.22) 9 0.19 (0.07−0.32) 126 2.73 (2.26−3.20) 92 1.99 (1.59−2.40)
    Yunnan 5,567 784 14.08 (13.17−15.00) 526 9.45 (8.68−10.22) 113 2.03 (1.66−2.40) 214 3.84 (3.34−4.35)
    Shaanxi* 8,993 15 0.17 (0.08−0.25) 0 0.00 (0.00−0.00) 15 0.17 (0.08−0.25) 0 0.00 (0.00−0.00)
    Gansu 8,750 12 0.14 (0.06−0.21) 0 0.00 (0.00−0.00) 12 0.14 (0.06−0.21) 0 0.00 (0.00−0.00)
    Qinghai 3,906 23 0.59 (0.35−0.83) 0 0.00 (0.00−0.00) 23 0.59 (0.35−0.83) 0 0.00 (0.00−0.00)
    Ningxia* 2,948 40 1.36 (0.94−1.77) 0 0.00 (0.00−0.00) 40 1.36 (0.94−1.77) 0 0.00 (0.00−0.00)
    Xinjiang* 13,378 8 0.06 (0.02−0.10) 0 0.00 (0.00−0.00) 8 0.06 (0.02−0.10) 0 0.00 (0.00−0.00)
    Total 326,207 4,200 1.29 (1.25−1.33) 2,911 0.89 (0.86−0.92) 875 0.27 (0.25−0.29) 543 0.17 (0.15−0.18)
    Abbreviations: PLADs=provincial-level administrative divisions.
    *These PLADs have no national surveillance spots before 2015 and started NSS since 2016.

    Table 1.  Infection rate of soil-transmitted helminth in China according to the 2018 National Sentinel Surveillance.

    Yunnan showed the highest infection rate (14.08%), followed by Sichuan (7.44%) and Hainan (7.16%). No infection was detected in Beijing, Heilongjiang, and Shanghai. As revealed by the NSS in 2018, STH was mainly prevalent in southern and southeastern parts of China (Table 1, Figure 1). In PLADs with infection rates over 0.5%, Yunnan, Hainan, and Sichuan were mainly prevalent with hookworm infection; Guizhou, Hunan, Qinghai, and Ningxia with ascariasis; and Shandong with trichuriasis.

    Figure 1.  Infection rate of soil-transmitted helminth in each provincial-level administrative divisions of China according to the 2018 National Sentinel Surveillance.

    The infection rate in males and females was 1.16% (1,849/159,925) and 1.41% (2,351/166,282), respectively. It was higher in females than in males (${\chi ^2}\!=\!42.59$, p<0.0001). The overall infection rate was the highest in those aged 60 and above, followed by the age group of 45 to 59, 7 to 14, 15 to 44, and 0 to 6, which was also significant (${\chi ^2}\!=\!1,030.84$, p<0.0001). However, the infection rate by A. lumbricoides and T. trichiura was higher in children than that of other age groups, while the pattern of hookworm infection was similar to that of overall STH (Figure 2).

    Figure 2.  Infection rate of soil-transmitted helminth by different age groups in China according to the 2018 National Sentinel Surveillance.

  • STH declined in China based on the 22 NSS sites, and the rates in each year from 2006 to 2015 are as follows: 20.88%, 18.93%, 16.59%, 13.30%, 11.25%, 9.67%, 6.90%, 3.12%, 4.49%, and 4.95% (7-8). This is consistent with the results of the second and third national survey (4-5). Also, the expanded NSS from 2016 to 2018 revealed that STH infection rates were 2.46%, 1.78%, and 1.29%, respectively (8). These results indicated a continuous pattern of decline for prevalence for the 13 years following sentinel surveillance implementation. This can be attributed to improved economy and living standards of the population and effective implementation of control measures such as health education, chemotherapy, and improved sanitation and water safety in China (9).

    The prevalence of ascariasis and hookworm infection was demonstrated to be similar between 2006 and 2010 and that trichuriasis was the lowest. However, the prevalence between types has changed since 2011 with hookworm infection becoming the highest one, followed by ascariasis and trichuriasis. Also, children rank highest with ascariasis and trichuriasis while the age group of 45-year-old and above ranks highest with hookworm infection as indicated by the NSS system (8). This is because elderly people usually have more exposure with hookworm, while A. lumbricoides and T. trichiura mostly infect children. Recognizing the predominant species of soil-transmitted helminth and different age group predisposed to risk of infection are crucially importance for implementing control strategies.

    The NSS system provides basic information on STH’s endemic status and trends, which are important for developing control strategies. Many PLADs have started or improved their own provincial sentinel surveillance following the efforts made by the NSS system regarding prevention and control of STH (9). In addition, this has greatly enhanced the capacity of staff members at the provincial, city, and county levels through training, communication, and other regular work during surveillance.

    This study is subject to some limitations. Only 29 PLADs were included in the NSS in 2018 and Shanxi and Tibet were excluded, and the infection rates of STH in both PLADs were below average according to the third national survey (5). As a result, the infection rate of STH may therefore be slightly overestimated. Also, during the implementation of the surveillance system, participants may have become more aware and changed their behaviors, which would then contribute to further decreases of STH. Moreover, field investigations need to consider feasibility and scientific rigor because of increasing difficulties in field work, expanding surveillance ranges, and methods changing, such as the Kato-Katz method being changed from 3 slides to 2 slides since 2015 (8).

    The National Control Program for Echinococcosis and Other Important Parasitic Diseases (2016–2020) was issued and included STH. Establishment of national surveillance is vitally important in the control of STH as it provides platforms to achieve the control targets set by the national control program and to evaluate control effectiveness. The control of STH should be combined with poverty alleviation in China, which might increase effectiveness. Additionally, precise control of STH was needed by implementing different strategies in different endemic level areas. High endemic-disease areas should be addressed with health education, with provision of water, sanitation, and hygiene (WASH), and with chemotherapy, while low endemic-disease areas should be addressed with health education and with improvement of compliance for examination and chemotherapy of STH. Children and the elderly should be given special attention when controlling STH.

    Overall, the infection rate of STH approaches 1.00%, with some areas achieving infection control and other areas still having endemic disease (10). The “Criteria for Transmission Control and Interruption of Soil-Transmitted Nematodiasis” has been issued in China. Therefore, China should pursue higher targets in national control of STH to eventually achieve interruption.

  • The authors would like to thank all participants of the national sentinel surveillance. This work was supported by the National Health Commission of China and China CDC.

  • The authors declare no competing interests.

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