The prevalence of soil transmitted helminths and its influential factors in Shandong Province, China: an analysis of surveillance data from 2016 to 2020

STHs prevalence

From 2016 to 2020, a total of 72,160 participants were involved in this study, including 34,525 males and 37,635 females (Additional file 1: Fig. S1). The result showed that the total prevalence rate of STHs was 1.13% (819/72,160), among which the prevalence rate of A. lumbricoides was 0.13% (92/72,160), hookworm was 0.03% (23/72,160) and T. trichiura was 0.99% (716/72,160). According to the intensity of infection, A. lumbricoides, hookworm, and T. trichiura were predominantly mildly infected, with proportion of 95.65%, 95.65% and 96.09%, respectively. In addition, 1.47% (12/819) of STHs infection were mixed infections, with predominant mixed infections of A. lumbricoides and T. trichiura (91.67%, 11/12), and the rest were mixed with T. trichiura and hookworms (8.33%, 1/12) (Table 1).

Table 1 Prevalence and infection intensity of STHs species in Shandong ProvinceEpidemiological characteristics

Data analysis showed that 62.90% of the surveillance counties had participants with STHs infection; among them, Yinan of Linyi City had the highest prevalence rate of 10.74% (109/1015), followed by Haiyang of Yantai City, Rongcheng of Weihai City and Lanshan of Rizhao City, with prevalence rates of 10.18% (102/1002), 8.76% (88/1004), 8.06% (82/1018), respectively. While the prevalence rates of other surveillance counties were below 5%, and the average rate was 0.98%, with the highest prevalence rate was 4.46% (45/1010) in Junan of Linyi City and the lowest prevalence rate was 0.09% (1/1089) in Yucheng of Dezhou City (Table 2).

Table 2 STHs prevalence of surveillance counties in Shandong Province

According to geographical location, the prevalence rate in the central, eastern, southern, and northern regions of Shandong Province was 0.25% (48/19,456), 2.02% (268/13,264), 1.45% (496/34,144) and 0.13% (7/5296), respectively, and the difference was statistically significant (χ2 = 307.675, P < 0.001). The two-pair comparison showed that the difference between the central and northern region was not statistically significant (χ2 = 2.463, P = 0.117), while the prevalence rate of eastern region was higher than other three regions and the prevalence rate of southern region was higher than central and northern region (all P < 0.001) (Additional file 1: Table S1).

The spatial scan analysis revealed one primary cluster and three secondary clusters. The primary cluster (a) was located at 35° 17′ N and 119° 11′ E with a radius of 76.35 km, covering eight counties of southern region of Shandong Province. This cluster had 6,152,451 exposed persons, with a risk of STHs infection 6.08 times of the surrounding areas (P < 0.001). The secondary cluster 1 (b) and secondary cluster 3 (d) demonstrated some overlap with the primary cluster and were also located in the southern region. Secondary cluster 2 (c) was located at 37° 22′ N and 122° 6′ E with a radius of 106.39 km, covering six counties of eastern region. This cluster included 4,170,756 exposed persons, and the RR of this cluster was 4.73 (P < 0.001) (Table 3).

Table 3 Spatial clusters of STHs prevalence in Shandong Province

The STHs prevalence rate among the male and the female was 1.10% (380/34,525) and 1.17% (439/37,635), respectively, and the difference was not statistically significant (χ2 = 0.695, P = 0.404).The prevalence rate of the ≥ 70-year age group was the highest (2.21%, 198/8968), followed by the 60–69-year age group (1.51%, 196/13,011). The differences among age groups were statistically significant (χ2 = 187.693, P < 0.001), and STHs prevalence rates increased as age increased (\(\chi_}}}^\) = 153.499, P < 0.001) (Fig. 1). The STHs prevalence rates differed among educational levels (χ2 = 90.088, P < 0.001). The illiterate/semi-illiterate group had the highest prevalence rate (1.99%, 159/7997) and the college/university or above group had the lowest rate (0.54%, 10/1838). STHs prevalence rates decreased as educational level increased (\(\chi_}}}^\) = 62.344, P < 0.001) (Fig. 2).

Fig. 1figure 1

Distribution of STHs prevalence according to sex and age. STHs Soil-transmitted helminths

Fig. 2figure 2

Distribution of STHs prevalence according to educational level. STHs Soil-transmitted helminths

As shown in Fig. 3, the prevalence rates of STHs from 2016 to 2020 were 2.09% (302/14,463), 1.31% (188/14,325), 20.67% (96/14,399), 0.87% (127/14,537) and 0.73% (106/14,436), respectively; the overall trend was linearly decreasing (\(\chi_}}}^\) = 127.600, P < 0.001), and the difference was statistically significant (χ2 = 178.749, P < 0.001). In terms of species, although the prevalence rates of A. lumbricoides, and hookworm were statistically different in different years (χ2 = 10.404, P = 0.034; χ2 = 16.167, P = 0.003), there was no linear trend (all P > 0.05). Fortunately, the prevalence rate of T. trichiura gradually decreased (\(\chi_}}}^\) = 144.323, P < 0.001).

Fig. 3figure 3

Temporal distribution of STHs prevalence. STHs Soil-transmitted helminths

Geographically, the prevalence rate of STHs in the eastern and southern region of Shandong Province showed a linear downward trend (\(\chi_}}}^\) = 127.515, 20.218, all P < 0.001), while the prevalence rate in the central region did not show a downward trend (\(\chi_}}}^\) = 0.023, P = 0.880). Notably, one site with a higher STHs prevalence rate (Haiyang > 10%) was included in the surveillance in 2017, and the prevalence rate in eastern region increased accordingly. Similarly, due to the relatively higher prevalence rates of two counties in central region in 2020, the STHs prevalence was higher than in previous years (Fig. 4).

Fig. 4figure 4

Temporal distribution of STHs prevalence in four regions of Shandong Province

Knowledge, attitude, and behaviour towards STHs prevention

A total of 1337 participants completed the questionnaire, including 635 males (47.49%) and 702 females (52.51%). The respondents were categorized into three age groups: 255 (19.07%) were in the 10–39 age group, 514 (38.44%) were in the 40–59 age group, and 568 (42.48%) were in the ≥ 60 age group. According to the geographical location, 553 respondents (41.36%) were in northern region, 361 (27.00%) in eastern region, and 423 (31.64%) in southern region of Shandong Province (Additional file 1: Fig. S1).

Five questions regarding prevention knowledge of STHs were investigated. The results showed that 61.78% (826/1337) had heard of STHs, of which 56.30% (465/826) knew the infection routes of roundworm/whipworm, 31.72% (262/826) knew the infection routes of hookworm, 82.20% (679/826) knew the harms of STHs, and 65.62% (542/826) knew the prevention measures for STHs. Through further analysis, the awareness rates of five knowledge in different age groups and different regions were significantly different (all P < 0.05), among which the awareness rates of people over 60 years old were the lowest, and the rates of southern region residents were the highest (Table 4).

Table 4 Comparison of STHs-related prevention knowledge, attitude, and behaviour in different groups

Among 1337 respondents, 95.96% washed hands before meals and after defecation, 88.78% did not consume raw water, 84.89% did not fertilize with fresh stool, 91.10% did not work on farms barefooted, 96.41% were willing to take deworming medicine, and 57.14% were willing to change dangerous behaviours. This survey showed that, the proportion of not working barefooted on farms (93.16%) and the proportion of willing to change dangerous behaviours (59.69%) in females were higher than that in males (all P < 0.05) (Table 4). The proportion of not fertilizing with fresh stool was highest in the 10–39 age group and lowest in the ≥ 60 age group (P < 0.05). Except for the behaviour of washing hands before meals and after defecation, the adoption rates of other behaviours and attitudes in the northern region residents were higher than that in eastern and southern regions (all P < 0.05).

Risk factors of STHs infections

Overall, survey on natural and social factors of STHs infection was conducted in 350 villages (Additional file 1: Fig. S1), and the terrains of the villages were predominantly flat (62.57%) or hilly (33.14%). The primary drinking water was tap water (92.29%, 323/350). The total number of toilets was 234,397, of which 155,640 (66.40%) were sanitary toilets, including biogas digesters, three-grid septic tanks, and double-urn funnel toilets, which could harmlessly treat faeces and reduce the spread of STHs.

From 2016 to 2020, the annual average temperatures were (13.83 ± 2.45) °C, (14.09 ± 1.52) °C, (14.79 ± 2.67) °C, (14.18 ± 2.61) °C, and (14.31 ± 1.36) °C in the respective 5 years. The annual average rainfall were (621.75 ± 247.77) mm, (674.70 ± 140.65) mm, (625.10 ± 214.29) mm, (697.29 ± 400.53) mm, and (631.16 ± 248.31) mm, respectively. The proportions of tap water as the primary drinking water were 91.43%, 91.43%, 88.57%, 91.43%, and 98.57%, respectively. The aforementioned differences were not significant (all P > 0.05). The proportions of sanitary toilets were 41.91% (15,121/36,081), 47.98% (18,121/37,770), 71.79% (39,115/54,482), 73.20% (31,489/43,020), and 82.16% (51,794/63,044), respectively. The differences were significant (χ2 = 24,062.161, P < 0.001), and the proportions showed linear upward trend (\(\chi_}}}^\) = 21,800.313, P < 0.001) (Additional file 1: Table S2).

As shown in Table 5, the differences in the annual average temperature, the annual average rainfall, the per capita gross national product (GNP), the annual net income per capita, and the proportion of sanitary toilets were all significant among the four regions of Shandong Province, with southern region demonstrating the highest temperature (14.69 ± 2.14 °C) and rainfall (738.93 ± 299.22 mm) and the lowest GNP (27,027.48 ± 15,258.81 RMB)and annual net income per capita (11,138.97 ± 6463.37 RMB), and eastern region having the greatest proportion of sanitary toilets (81.85%) (all P < 0.001).

Table 5 Comparison of STHs-related natural and social factors in four regions of Shandong Province

Classification function coefficients of two infection groups were generated by Bayes discriminant analysis (Table 6). The results showed that terrain was an important factor to both the low and the high infection groups. According to the prediction of the discriminant function, 259 villages (74.00%) in the original group were discriminated correctly, of which 238 villages (74.84%) in the low infection group were discriminated correctly. In the cross-validated group, 256 villages (73.14%) were discriminated into the right group, of which 236 villages (74.21%) in the low infection group were discriminated accurately (Table 7).

Table 6 Factors and classification function coefficients of low and high infection groupTable 7 Classification results of Bayes discriminant analysis

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