Introduction: This study compared the pattern of viral diarrhea in Yichang City, China, in 2022 and 2023 before and after the lifting of the COVID-19 restrictions. Methods: Stool samples were collected from outpatients and inpatients with diarrhea at three hospitals in Yichang from January to October 2022 and January to June 2023, before and after the lifting of COVID-19 restrictions, respectively. Samples were simultaneously tested for 13 types of enteric virus using a rapid multiplex assay that could simultaneously detect 13 types of five enteric viruses, including rotavirus (groups A, B, C, and H), norovirus (I, II, IV, VII, VIII, and IX), adenovirus, sapovirus, and astrovirus. Results: Testing of 458 samples showed variations in pathogen distribution by age group. Specifically, there was an increase in the number of viral infections among adults, a decrease among children, an increase in coinfection rates, and variability in virus positivity in 2023 compared to 2022. Conclusions: The multiplex assay method improved diagnostic efficiency and provided epidemiological insights. This study highlights the impact of public health transitions on viral diarrhea epidemiology, underscoring the need for ongoing surveillance and adaptable strategies in the post-COVID-19 pandemic era.

Journal Section:
Research Article
Keywords:
Viral diarrhea, China, Etiological distribution, Pathogen surveillance

Acute infectious diarrhea is a major public health problem worldwide owing to its high incidence and prevalence [1‒3]. Diarrheal diseases are the second leading cause of death among children aged under 5 years [4, 5]. The clinical manifestations include frequent bowel movements, abdominal pain, nausea, vomiting, fever, and dehydration [6]. Infectious diarrhea can be caused by bacteria, viruses, and parasites [7, 8]. Viral infections are the most common cause of acute diarrhea. Viral diarrhea is primarily caused by enteric viruses including rotavirus (RV), norovirus (NoV), adenovirus (AdV), sapovirus (SaV), and astrovirus (AstV) [5, 9].

On December 7, 2022, China officially introduced the “Ten New measures” to further optimize COVID-19 prevention and control efforts. This marked a major adjustment and the gradual easing of restrictions [10, 11]. Between December 2022 and January 2023, many parts of China, including the Yichang region, experienced the peak of COVID-19 infections [12, 13]. In order to further understand the change of diarrhea virus epidemic situation after policy adjustment, this study compared and analyzed the difference of diarrhea virus epidemic situation in Yichang region from 2022 to 2023. Yichang City is an important transportation hub in central China, with a population of approximately 4.15 million. We conducted virological surveillance of diarrhea cases using stool samples tested using a rapid multiplex assay.

Samples were collected from outpatients and inpatients at Yichang Central Hospital, Yichang Maternal and Child Health Hospital, and Yichang Third Hospital from January to October 2022 and January to June 2023. Patients with diarrhea were included in this study based on their defecation frequency, which was determined as more than three times a day, accompanied by notable alterations in fecal characteristics such as a watery or egg-like consistency, mucilaginous texture, or thin paste-like appearance.

The Diarrheal Viruses Detection Kits (XZK-P0000-46) and Nova HT flow cytometer (XZK-HT-001) were manufactured and provided by Hubei NewZongke Viral Disease Control Bio-Tech Ltd. The detection system utilize a bead-based flow cytometry to detect 13 different types of 5 enteric viruses, including RV groups A, B, C, and H; NoV groups I, II, IV, VII, VIII, and IX; AdV, SaV, and AstV. Briefly, nucleic acid was extracted and amplified by two rounds of polymerase chain reaction to obtain biotin-labeled polymerase chain reaction products, followed by microsphere hybridization. The hybridized products were then analyzed using a Nova HT flow cytometer and Liqchip V1.0 software, which measured the median fluorescence intensity of beads. Median fluorescence intensity values ≥20,000 were considered positive; otherwise, the sample was considered negative.

The data were analyzed using GraphPad Prism 8.0.1 (GraphPad Software, Inc., San Diego, CA, USA). The data obtained before (January to October 2022) and after (January to June 2023) the lifting of the pandemic restrictions were compared using the χ2 test to identify changes in viral detection rates and pathogen diversity. p values <0.05 were considered statistically significant.

A total of 458 diarrhea samples were collected, of which 317 were collected in 2022 and 141 were collected in 2023 (Table 1). In 2022, the age group with the greatest number of cases of diarrhea was children aged 0–5 years (52.4%), followed by adults aged 21–50 years (20.8%) and adults aged over 60 years (14.2%). In contrast, in 2023, the greatest number of cases was in adults aged 21–50 years (34.8%), followed by adults aged over 60 years (30.5%) and children aged 0–5 years (18.4%). The data show that there was a significant decrease in the proportion of diarrhea cases among children under 5 years old from 2022 to 2023, dropping from 52.4% to 18.4%. In contrast, there was a notable increase in the proportion of diarrhea cases among adults aged over 21 years, rising from 41.6% to 75.2%.

Table 1.

Prevalence of enteroviruses infected cases in Yichang in 2022 and 2023a

YearGroupCasesPositive casesbRVA-positive casesNV GI-positive casesNV GII-positive casesNV GIV-positive casesNV GIX-positive casesAdV-positive casesAstV-positive casesSaV-positive casesCoinfection cases
2022 Gender 
Male 160 64 (40) 14 (8.8) 1 (0.6) 2 (1.3) 1 (0.6) 0 33 (20.6) 32 (20) 1 (0.6) 16 (10) 
Female 157 42 (26.8) 10 (6.4) 2 (1.3) 4 (2.5) 1 (0.6) 1 (0.6) 19 (12.1) 18 (11.5) 1 (0.6) 10 (6.4) 
Age 
0–5 166 75 (45.2) 22 (13.3) 2 (1.2) 4 (2.4) 2 (1.2) 0 38 (22.9) 36 (21.7) 1 (0.6) 23 (13.9) 
6–20 19 4 (21.1) 0 0 0 0 0 2 (10.5) 3 (15.8) 0 0 
21–50 66 16 (24.2) 1 (1.5) 1 (1.5) 2 (3) 0 1 (1.5) 9 (13.6) 4 (6.1) 1 (1.5) 2 (3) 
51–60 21 4 (19) 1 (4.8) 0 0 0 0 2 (9.5) 2 (9.5) 0 1 (4.8) 
≥61 45 7 (15.6) 0 0 0 0 0 1 (2.2) 5 (11.1) 0 0 
Total 317 106 (33.4) 24 (7.6) 3 (0.9) 6 (1.9) 2 (0.6) 1 (0.3) 52 (16.4) 50 (15.8) 2 (0.6) 26 (8.2) 
2023 Gender 
Male 56 24 (42.9) 0 14 (58.3) 5 (8.9) 1 (1.8) 0 0 12 (21.4) 0 6 (10.7) 
Female 85 45 (52.9) 1 (1.2) 15 (33.3) 10 (11.8) 0 0 0 32 (37.6) 1 (1.2) 12 (14.1) 
Age 
0–5 26 16 (61.5) 0 9 (34.6) 5 (19.2) 1 (3.8) 0 0 9 (34.6) 1 (3.8) 6 (23.1) 
6–20 9 5 (55.6) 0 1 (11.1) 3 (33.3) 0 0 0 3 (33.3) 0 2 (22.2) 
21–50 49 30 (61.2) 0 12 (24.5) 6 (12.2) 0 0 0 21 (42.9) 0 8 (16.3) 
51–60 14 6 (42.9) 1 (7.1) 2 (14.3) 0 0 0 0 3 (21.4) 1 (7.1) 0 
≥61 43 12 (27.9) 0 5 (11.6) 1 (2.3) 0 0 0 8 (18.6) 0 2 (4.7) 
Total 141 69 (48.9) 1 (0.7) 29 (20.6) 15 (10.6) 1 (0.7) 0 0 44 (31.2) 2 (1.4) 18 (12.8) 
YearGroupCasesPositive casesbRVA-positive casesNV GI-positive casesNV GII-positive casesNV GIV-positive casesNV GIX-positive casesAdV-positive casesAstV-positive casesSaV-positive casesCoinfection cases
2022 Gender 
Male 160 64 (40) 14 (8.8) 1 (0.6) 2 (1.3) 1 (0.6) 0 33 (20.6) 32 (20) 1 (0.6) 16 (10) 
Female 157 42 (26.8) 10 (6.4) 2 (1.3) 4 (2.5) 1 (0.6) 1 (0.6) 19 (12.1) 18 (11.5) 1 (0.6) 10 (6.4) 
Age 
0–5 166 75 (45.2) 22 (13.3) 2 (1.2) 4 (2.4) 2 (1.2) 0 38 (22.9) 36 (21.7) 1 (0.6) 23 (13.9) 
6–20 19 4 (21.1) 0 0 0 0 0 2 (10.5) 3 (15.8) 0 0 
21–50 66 16 (24.2) 1 (1.5) 1 (1.5) 2 (3) 0 1 (1.5) 9 (13.6) 4 (6.1) 1 (1.5) 2 (3) 
51–60 21 4 (19) 1 (4.8) 0 0 0 0 2 (9.5) 2 (9.5) 0 1 (4.8) 
≥61 45 7 (15.6) 0 0 0 0 0 1 (2.2) 5 (11.1) 0 0 
Total 317 106 (33.4) 24 (7.6) 3 (0.9) 6 (1.9) 2 (0.6) 1 (0.3) 52 (16.4) 50 (15.8) 2 (0.6) 26 (8.2) 
2023 Gender 
Male 56 24 (42.9) 0 14 (58.3) 5 (8.9) 1 (1.8) 0 0 12 (21.4) 0 6 (10.7) 
Female 85 45 (52.9) 1 (1.2) 15 (33.3) 10 (11.8) 0 0 0 32 (37.6) 1 (1.2) 12 (14.1) 
Age 
0–5 26 16 (61.5) 0 9 (34.6) 5 (19.2) 1 (3.8) 0 0 9 (34.6) 1 (3.8) 6 (23.1) 
6–20 9 5 (55.6) 0 1 (11.1) 3 (33.3) 0 0 0 3 (33.3) 0 2 (22.2) 
21–50 49 30 (61.2) 0 12 (24.5) 6 (12.2) 0 0 0 21 (42.9) 0 8 (16.3) 
51–60 14 6 (42.9) 1 (7.1) 2 (14.3) 0 0 0 0 3 (21.4) 1 (7.1) 0 
≥61 43 12 (27.9) 0 5 (11.6) 1 (2.3) 0 0 0 8 (18.6) 0 2 (4.7) 
Total 141 69 (48.9) 1 (0.7) 29 (20.6) 15 (10.6) 1 (0.7) 0 0 44 (31.2) 2 (1.4) 18 (12.8) 

Data are presented as n (%).

AdV, adenovirus; AstV, astrovirus; NoV, norovirus; RV, rotavirus; SaV, sapovirus.

aThis table only shows the results of 8 detection targets, and no positive cases were detected in the remaining 5 targets.

bBecause of mixed infection, the total number of positive cases is not equal to the sum of the positive numbers of the 8 viral nucleic acids.

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Eight types of five viruses were detected in 2022, and six types of five viruses were detected in 2023. The positivity rates of the five viruses differed by age group (2022: p < 0.001, χ2 = 48.33; 2023: p < 0.01, χ2 = 37.63).

In children aged 0–5 years, the viruses most frequently identified were AdV, AstV, and RVA in 2022 and NoV-GI, ASV, and NoV-GII in 2023. The detection rates of RV, NoV, AdV, AstV, and SaV in samples from children aged 0–5 years differed significantly in 2022 and 2023 (p < 0.01, χ2 = 51.29). The positivity rate of NoV and AstV was significantly higher (NoV: p < 0.001, χ2 = 35.61; AstV: p < 0.001, χ2 = 23.93) and that of AdV was significantly lower (p < 0.05, χ2 = 4.05) in 2023 than in 2022 (Table 1).

In adults aged 21–50 years, the virus positivity rate increased from 24.2% in 2022 to 61.2% in 2023, and those for AstV and NoV-GI increased from 6.1% to 42.9% and 1.5% to 24.5%, respectively, whereas the positivity rate for AdV decreased from 13.6% in 2022 to 0% in 2023 (Table 1). The detection rates of RV, NoV, AdV, AstV, and SaV varied significantly by period (p < 0.001, χ2= 31.75). In adults aged over 60 years, the virus positivity rate increased from 15.6% in 2022 to 27.9% in 2023 (p < 0.05, χ2= 8.39).

In both 2022 and 2023, a high proportion of patients had coinfections with multiple enteric virus. In 2022, the coinfection cases exhibited greater diversity, involving multiple combinations of viruses. The most common combination was AdV + AstV, with a total of 12 cases. In 2023, the coinfection cases were mainly concentrated in NV and its combination with other viruses, with a total of 18 cases. In terms of gender and age distribution, in 2022, the infection ratio between males and females was similar, with 16 cases (10.0%) in males and 10 cases (6.4%) in females. The highest infection rate was observed in children aged 0–5, with a total of 23 cases (13.9%), while no cases were reported in the 6–20 age group. The number of cases in the age groups 21–50 and 51–60 was relatively low, with 2 cases (3%) and 1 case (4.8%), respectively. There were no reported cases in the age group 61 and above. In 2022, a total of 26 cases of coinfection of diarrheal viruses were recorded, accounting for 8.2% of the total cases. In 2023, the infection ratio of females (12 cases, 14.1%) was higher than that of males (6 cases, 10.7%). The infection rate in children aged 0–5 remained high, with 6 cases (23.1%), and the infection rate in the 6–20 age group was also relatively high with 2 cases (22.2%). The number of cases in the 21–50 age group was 8 (16.3%), while no cases were reported in the 51–60 age group. Two cases (4.7%) were reported in the 61 and above age group. In 2023, a total of 18 cases of coinfection of diarrheal viruses were recorded, accounting for 12.8% of the total cases.

The incidence of NoV and AstV infections increased in 2023, whereas the incidence of RV and AdV infections decreased. In 2022, RV and AdV mainly infected children aged 0–5 years, whereas no RV and AdV infections occurred in the first half of 2023.

Since only diarrhea patient data from January to July in 2023 were collected, a further analysis of differential virus prevalence was conducted by quarter. From 2022 to 2023, the infection rates of diarrhea viruses showed significant seasonal differences. In the first quarter of 2022, the main epidemic diarrhea viruses were RV, AdV, and AstV, with positivity rates of 44.0%, 37.8%, and 39.6%, respectively. In the first quarter of 2023, the main viruses shifted to NV and AstV, with positivity rates of 29.7% and 24.2%, respectively. For the second quarter of 2022, AstV was the main epidemic diarrhea virus with a positivity rate of 20.2%. In the second quarter of 2023, the main viruses became NV and AstV, with positivity rates of 36.0% and 44.0%, respectively (shown in Fig. 1, 2).

Fig. 1.
Difference in enterovirus detection rates between the first quarter of 2022 and the first quarter of 2023.
View largeDownload slide

Difference in enterovirus detection rates between the first quarter of 2022 and the first quarter of 2023.

Fig. 1.
Difference in enterovirus detection rates between the first quarter of 2022 and the first quarter of 2023.
View largeDownload slide

Difference in enterovirus detection rates between the first quarter of 2022 and the first quarter of 2023.

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Fig. 2.
Difference in enterovirus detection rates between the second quarter of 2022 and the second quarter of 2023.
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Difference in enterovirus detection rates between the second quarter of 2022 and the second quarter of 2023.

Fig. 2.
Difference in enterovirus detection rates between the second quarter of 2022 and the second quarter of 2023.
View largeDownload slide

Difference in enterovirus detection rates between the second quarter of 2022 and the second quarter of 2023.

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This study conducted in Yichang city revealed interesting findings regarding diarrheal viral infections before and after the lifting of China's stringent COVID-19 prevention and control measures. After the control measures were lifted, the positivity rate of NoV and AstV increased. In contrast, the positivity rate of RVA showed a decreasing trend. The positivity rate of AdV also decreased during this period. In 2022, the data indicated that RVA and AdV predominantly infected children aged 0–5 years. However, in the first half of 2023, no cases of infection were reported for these viruses in this age group. Instead, the infection rate of NoV and AstV significantly increased among adults in 2023. This suggests a shift in viral infection patterns from children to adults.

According to a study on the situation of diarrheal viruses in Hubei from 2017 to 2019 [14], the epidemic peak of NoV was occurred in March–April and October–December, prior to the emergence of COVID-19 pandemic. However, this study found a notable increase in the positive rate of NoV in the first and second quarters in Yichang in 2023, which may be related to the COVID-19 pandemic. Studies have shown that the epidemiology of infectious diseases has changed significantly due to changes in human lifestyles after the emergence of the COVID-19 pandemic. There have been reports of a decrease in infectious diseases as a result of the implementation of control measures for the COVID-19 pandemic and an increase in infections after the relaxation of control measures [15‒19]. Therefore, it is critical to conduct further examination and analysis to elucidate the specific details of these changes.

In the analysis of the coinfection of diarrheal viruses in 2022 and 2023, we have identified some significant trends and characteristics. In 2023, the infection rate among females was higher than that of males. This disparity may be attributed to the easing of COVID-19 restrictions, and females tend to stay at home to take care of their families, increasing their likelihood of getting infected with diarrheal viruses, while males are more likely to go out for work. The high infection rate among children aged 0–5 and the increase in the infection rate among the 6–20 age group in 2023 suggest that we may need to implement more targeted prevention and control measures for these specific groups.

These findings highlight the importance of continuous monitoring and adaptation of control measures after the lifting of the COVID-19 restrictions. Additionally, it is crucial to investigate the factors contributing to the changes in diarrheal viral infection patterns and prevalence to develop targeted prevention and control strategies.

A relatively new detection method was used in this study, allowing for the simultaneous detection of 13 types of five enteric viruses. The detection method included the identification of the RV and NoV group, which not only improved the detection efficiency but also provided useful epidemiological information. Coinfection can significantly worsen patient condition [20], and this new detection method can rapidly detect coinfection. Therefore, multiplex systems are useful for sensitive and comprehensive pathogen detection.

However, it is important to note the limitations of this study. First, the samples collected in this study only covered the periods January to October 2022 and January to June 2023. The number of patients with COVID-19 increased at the end of 2022, and due to the impact of the COVID-19 pandemic, samples were not tested for enteric viruses in November and December 2022. The limited sample size limited the depth of the analysis. Additionally, the samples were collected at only three hospitals in Yichang; therefore, the results are not representative of the epidemic situation regarding viral diarrhea in China before and after the lifting of the COVID-19 restrictions.

In conclusion, this study demonstrates a marked shift in the etiological profile and secular trends of viral diarrhea in Yichang following the end of China’s stringent COVID-19 prevention and control measures. Our findings provide critical insights into the influence of public health transitions on viral diarrhea and provide a scientific foundation for the prevention and control of viral diarrhea in the post-COVID-19 era. These findings underscore the importance of ongoing virological surveillance and adaptable public health strategies to address the evolving challenges of enteric viral diseases in the post-COVID-19 pandemic era.

Ethical approval is not required for this study in accordance with the “Viral Diarrhea Surveillance Program” of the Chinese Center for Disease Control and Prevention (Memorandum [2021]1006). Written informed consent from participants was not required for the study presented in this article in accordance with the “Viral Diarrhea Surveillance Program” of the Chinese Center for Disease Control and Prevention (Memorandum [2021]1006).

The authors declare no conflicts of interest related to this study.

This work was supported by grants from the Open Research Fund program of the State Key Laboratory of Virology of China (2022KF001) and Hubei Public Health Youth Talent Program (S2022JY22).

Z.S. and J.L. conducted the laboratory tests; A.M., J.Q., and D.Z. performed the statistical analysis; B.L., J.L., K.Z., and Y.L. were responsible for sample collection; K.C. and J.Y. participated in the conception and design; and J.Y. drafted the manuscript. All the authors approved the final manuscript.

Additional Information

Zhengyuan Su and Jing Li contributed equally to this work.

All data generated or analyzed during this study are included in this article. Further inquiries can be directed to the corresponding author.

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