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Prevalence and associated factors of norovirus infections among patients with diarrhea in the Amhara national regional state, Ethiopia

BMC Infectious Diseases volume 24, Article number: 1053 (2024) Cite this article

Abstract

Background

Noroviruses (NoVs) are the leading cause of diarrheal disease among all age groups worldwide, with an increased burden in developing countries. As there is no surveillance, epidemiological data is limited in Ethiopia. Hence, this study aimed to investigate the prevalence and associated factors of NoV infection among patients with diarrhea in the Amhara National Regional State, Ethiopia.

Methods

A prospective health facility-based cross-sectional study was conducted from May 2021 to November 2021. A total of 550 study participants of all age groups with symptoms of diarrhea were proportionately assigned to the four study areas, area with three health facilities. Study participants were systematically sampled in each health facility. A fecal sample from each case was collected. The RNA was extracted and tested for NoV by one-step RT-PCR. Sociodemographic and other variables were gathered using a pre-tested questionnaire. A descriptive analysis was performed. Both binary and multiple logistic regressions were utilized to identify factors associated with NoV infection. Variables with a p-value < 0.05 in the final model were considered statistically significant.

Results

Five hundred nineteen out of 550 samples were analyzed (94.4% response rate). The overall prevalence of NoV was 8.9% (46/519). The positivity rates were higher among the elderly (33.3%) and under-5 children (12.5%). Both genogroup I and genogroup II (GII) were identified, with GII being the predominant, at 82.6% (38/46). Of all participants, only 20% reported a history of vomiting. Norovirus infection was more prevalent among participants from Debre Tabor (AOR = 4, 95%CI: 1.2–14) and Bahir Dar areas (AOR = 3.6, 95%CI: 1.04–11) compared to Debre Markos. Additionally, older adults (AOR = 7, 95% CI: 2–24) and under-5 children (AOR = 3.5, 95% CI: 2.8–12) were disproportionately affected compared to adults. The previous history of diarrhea (AOR = 3.6, 95% CI: 1.7–7) was a significant factor contributing to NoV infections. Moreover, the odds of NoV infection were higher among individuals with a high frequency of diarrhea (AOR = 15.3, 95%CI: 7.6–43) and vomiting (AOR = 3.5, 95%CI: 1.5-8).

Conclusions

The prevalence of NoV was considerably high, with the predominance of NoV-GII. The positivity rate was higher among the extreme age groups and varied across the study areas. To obtain a comprehensive understanding of the virus`s epidemiology and its genetic diversity, further research is warranted.

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Introduction

Diarrhea is defined as “the passage of three or more loose or liquid stools per day, or more frequently than is normal [1]. Acute gastroenteritis (AGE) often presents with the sudden development of diarrhea with or without vomiting, fever, nausea, and abdominal pain that is often associated with damage to the intestinal epithelium and causes fluid loss [2]. It usually lasts less than one week and not longer than two weeks [3]. Diarrheal disease ranks as the second leading cause of morbidity globally, only next to pneumonia [4]. This burden is particularly high in developing countries, including Ethiopia [5, 6].

Norovirus (NoV) is a major cause of acute gastroenteritis (AGE) and diarrhea, affecting individuals of all age groups, with an increased burden in under-5 children and the elderly (aged ≥ 65 years) [4, 7]. Globally, the overall prevalence of NoV among all age groups was 19% [8]. Specifically, among under-5 children, the prevalence is 17.7% [7]. Another global study also reported that the prevalence of NoV was 16%, with similar prevalence rates across contents except South America, which comprised 22% [9]. According to a recent study, NoV is responsible for about 18–58% of the cases of AGE in developing countries [8]. In Africa alone, the prevalence of NoV among all age groups of patients with gastroenteritis was 20.2% [10]. In the USA, 900 deaths, 109,000 hospitalizations, and 465,000 emergency department visits occurred annually due to NoV [11]. In Ethiopia, previous studies have reported that NoV is responsible for about 13% of the sporadic cases of gastroenteritis among under-5 children [12, 13], and 25.3% among all ages, as reported in Addis Ababa [14].

Noroviruses are a diverse group of non-enveloped viruses containing a positive-sense RNA genome and belong in the Caliciviridae family [15]. Noroviruses are categorized into 10 genogroups (GI-GX), with genogroups I (GI) and II (GII) being frequent causes of infection in humans [16], particularly with a predominance of GII [7, 10, 13].

Noroviruses are commonly transmitted through the fecal-oral route, primarily through contaminated food, water, or environmental surfaces, or directly via person-to-person contact [17, 18]. Their high contagiousness is attributed to a low infectious dose (18 particles) and a prolonged shedding period (8–60 days), often leading to large outbreaks [19, 20]. While these viruses typically cause mild and self-limiting acute infections, studies suggest that long-term infections are common among high-risk groups [21, 22]. Factors such as a history of contact with individuals with similar AGE, inadequate hand hygiene, lack of access to clean drinking water, consumption of raw food, absence of improved sanitation facilities, and poor environmental hygiene have been associated with an increased risk of NoV infection [18, 23].

There is a scarcity of comprehensive epidemiological data regarding viral gastroenteritis affecting individuals in all age groups in Ethiopia. Existing studies have focused on children under the age of five years, typically conducted during the dry seasons of the year and limited to specific geographic areas [13, 14]. The current study aimed to fill these gaps by investigating the prevalence of NoV across all age groups using specimens obtained during the rainy season, a period associated with increased prevalence due to the cold and rainy seasons. Additionally, our study tried to explore the roles of clinical characteristics and possible risk factors on the positivity rate of NoV infection. Therefore, this study aimed to assess the prevalence and associated risk factors of NoV infections among patients with diarrhea attending health institutions in the Amhara National Regional State (ANRS), Ethiopia.

Materials and methods

Study settings

A prospective health facility-based cross-sectional study was conducted from May 2021 to November 2021. The study was conducted in four cities located within the ANRS, namely, Bahir Dar, Gondar, Debre Tabor, and Debre Markos. Notably, the ANRS is the second-most populous region in Ethiopia [24, 25]. Variations in temperature, relative humidity, and rainfall could impact the prevalence and distribution of viral diarrheal diseases [26, 27]. The selected study areas comprise different levels of health facilities (primary health cares and comprehensive specialized hospitals). Bahir Dar, the regional capital, is situated 552 km away from Addis Ababa. The health institutions included in Bahir Dar were Felege Hiwot Comprehensive Specialized Hospital, Shimbit Health Center, and Abay Health Center. Gondar, located 727 km away from Addis Ababa, consists of the University of Gondar Comprehensive Specialized Hospital, Azezo Health Center, and Gondar Health Center. Debre Markos, located 298 km away from Addis Ababa, includes Debre Markos Comprehensive Specialized Hospital, Debre Markos Health Center, and Gozamen Health Center. Lastly, Debre Tabor, located 655 km away from Addis Ababa, includes Debre Tabor Comprehensive Specialized Hospital, Liul Alemayehu Health Center, and Debre Tabor Health Center (Fig. 1). These four sampling sites were primarily chosen for their diverse weather conditions, which could influence the prevalence and distribution of viral infections. Furthermore, the four Comprehensive Specialized Hospitals are the largest healthcare facilities in the region, experiencing high patient flow.

Fig. 1
figure 1

A map showing study sites for the study conducted from May 2021 to November 2021 on the prevalence and associated factors of NoV infections in the ANRS, Ethiopia: Each study site comprises of one comprehensive specialized hospital and two health centers

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Sample size determination

The sample size was determined by using a single population proportion formula (n = Z α/22*P (1-P)/d2). Assumptions: confidence level: 95%, critical value (Z): 1.96, precision (d): 0.03, P is the proportion taken from the previous study (13.3%) [13].

Calculations: (1.96) ² * 0.133 (1-0.133) / (0.03) ² by adding a 10% non-response rate, the total calculated sample size was 550.

Sampling technique

Four study areas, all found in the ANRS, were considered for this study. One comprehensive specialized hospital and two health centers were selected in each of the study areas by the lottery method. The sample size was assigned or proportionally allocated based on the previous year’s disease case flow. The study participants in each of the health facilities were selected by a systematic random sampling technique. The sampling frame was taken from the previous year’s average monthly record of patients with gastroenteritis (n = 1727 across all sites). The sampling fraction (K) was estimated by dividing the sampling frame by the allocated sample size (K = 1727/550 = 3.14). Accordingly, a sample was collected from every third patient who met the case definition of self-reported diarrhea in each health facility. The first study participant was selected by the lottery method from among the first three diarrheal patients at the facility (Fig. 2).

Fig. 2
figure 2

A schematic diagram showing the sampling technique for the selection of study participants in the Amhara National Regional State, Ethiopia

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Inclusion and exclusion criteria

All age groups visiting each of the health facilities in the given study area with self-reported gastroenteritis with at least diarrhea with or without vomiting, nausea, or abdominal pain were included. Individuals who were unable to defecate and provide fecal samples upon repeated requests were excluded.

Study variables

Dependent variables were NoV prevalence and its genogroups. Independent variables included sociodemographic variables (study area, age, sex, marital status, residence, occupation); clinical characteristics ((frequency of diarrhea, presence of vomiting, frequency of vomiting, fever, abdominal pain, nausea, generalized body weakness); risk factors (contact history with a related case of AGE, previous exposure for a related case of AGE, drinking water source, toilet status, hand washing practice, food consumption outside home, and comorbidity).

Operational definition

Acute gastroenteritis cases: A participant having at least diarrhea with or without vomiting, abdominal pain, nausea, fever, or generalized body weakness.

Previous history with AGE: A person experiencing a related AGE or diarrheal disease in the past two weeks.

Contact history: A person having contact history with another person having AGE in the past two weeks.

Uncooked food consumption history: A person consuming uncooked food in the past two weeks [28].

Comorbidity: A patient having one or more of the following underlying diseases: kidney, liver, and heart disease, hypertension, diabetes mellitus, tuberculosis, asthma, cancer and HIV/AIDS [29].

Data collection methods

Data were collected using pre-tested and semi-structured questionnaires that were adapted from previous literature [29, 30]. This questionnaire was used to assess the sociodemographic, exposure status, and clinical characteristics of study participants. All the data were collected by trained healthcare professionals for each of the health facilities. First, a clinical diagnosis was made based on the inclusion criteria. Second, the participants were selected based on the sampling technique and the inclusion criteria. Then, a pre-tested, semi-structured questionnaire was administered to assess associated factors.

Specimen collection and laboratory processing

Fecal sample collection

The study participants, parents, or guardians were instructed on how to collect fecal samples using clean and labeled containers. Five mL of diarrheic fecal samples were collected from each study participant. Following collection, the specimens were stored at -20 OC until transported to the Amhara Public Health Institute (APHI) for molecular tests and long-term storage at -70 OC.

RNA extraction

A 10% suspension of fecal samples was prepared with nuclease-free water. The suspension was vortexed and centrifuged at 12,000 g for 7 min. The supernatant was taken and subjected to a second-round centrifugation at 12,000 g for 7 min. Viral RNA was extracted from the 300 µL of the supernatant using MagaBio Plus Virus RNA Purification Kit II (Hangzhou, China). An automated extraction machine (BIOR) was employed, and the extraction was done according to the manufacturer’s instructions. The elution volume used for the real-time reverse transcription polymerase chain reaction (RT-PCR) was 50 µL.

Screening of norovirus

Screening of NoV was carried out by amplification of a portion of the viral protein 1 region using a one-step RT-PCR technique. Published primers and a probe were used for amplification of the target as previously done [13, 30]. The test was carried out in a 25 µL reaction mixture containing 15 µL of a one-step RT-PCR 2X enzyme mix (constituting buffer, enhancer, reverse transcriptase, Taq polymerase, dNTPs, MgCl2), 0.5 uL of a 10 µM probe working solution, 1 µL of 10 µM each of the forward and reverse primers, and 4.5 uL of nuclease-free water with an added 3 µL of RNA template. The amplification was done using Applied Biosystems™ Quant Studio™ 5 with a 7500 Real-Time PCR platform (Thermos Fisher). The cycling conditions and the temperature were adjusted based on the previously published articles [31, 32]. Targets with a Ct-value less than 40 were considered positive.

Data analysis

The data were entered into Epi data version 4.6 and transported to SPSS version 23 software for analysis. A descriptive analysis was performed to find the frequencies and percentages. Binary logistic regression analysis was done to check the association between dependent and independent variables. Those variables having a p-value < 0.25 in the binary logistic regression analysis were fitted into the multivariable logistic regression model. Finally, those variables with a p-value < 0.05, and an adjusted odds ratio (AOR) that did not cross 1 at the 95% CI in the multivariable logistic regression were considered statistically significant factors.

Results

Sociodemographic characteristics

Out of the 550 diarrheic patients approached, 519 were included in the analysis, with a response rate of 94.4%. Among these, the majority were females, constituting 266 participants (51.3%). The age of study participants ranged from 3 months to 85 years, with a mean age of 19.7 years. A substantial proportion of participants, 392 (75.5%), resided in urban areas, and the majority, 330 (63.6%), were married (Table 1).

Table 1 Sociodemographic characteristics of the study participants with diarrhea in the Amhara National Regional State, Ethiopia
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The prevalence of human norovirus

Among the 519 fecal samples screened, 46 (8.9%; 95% CI (6.6, 11.6)) tested positive for NoV. The average Ct-value for these positive samples was 30, ranging from 20.5 to 39. The positivity rate of NoV infection was notably high in samples collected from Debre Tabor, with 17 cases (17.2%), and Bahir Dar, with 15 cases (8.4%) (Fig. 3). Of the NoV-positive samples, GII was predominant, comprising 38 cases (82.6%; 95% CI (68.6, 92.2%)), while GI was found in 8 cases (17.4%; 95% CI (7.8, 31.4%)). Furthermore, the prevalence of NoV was higher among elderly individuals (33.3%) and children under the age of five years (12.5%). In Debre Tabor and Bahir Dar areas, the proportion of NoV GII compared to GI was notably high, with percentages of 94.1% and 93.3%, respectively. However, in samples obtained from Debre Markos, the proportion was equal, with both GII and GI accounting for 50% each (Fig. 4).

Fig. 3
figure 3

The geographic distribution of norovirus stratified by the study area, in the Amhara National Regional State, Ethiopia

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Fig. 4
figure 4

The proportional distribution of the two genogroups of NoV by study area, in the Amhara National Regional State, Ethiopia

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Clinical characteristics and exposure risk factors

While participants were recruited based on the presence of diarrhetic stools, 193 (37.2%) reported ≥ 3 episodes of diarrhea per day. The majority, 371 (71.5%) of the participants, had a normal body temperature. One-fifth of the study participants (20%) had a history of vomiting, among whom 51 (50%) reported vomiting three or more times per day. Additionally, two-thirds (67.2%) of participants complained of abdominal pain, while more than half (54.3%) reported generalized body weakness. Only one-third (34%) of participants had a previous history of AGE or diarrhea in the last two weeks. Similarly, 173 (33.3%) participants reported a history of consuming uncooked food with a similar time frame (two weeks). The majority (80.3%) used potable drinking water. Comorbidities including but not limited to kidney, liver, or heart disease, diabetes mellitus, HIV/AIDS, tuberculosis, cancer, hypertension, and asthma were reported by only 50 participants (9.6%). More than half (55.3%) of the study participants washed their hands before eating or preparing food, and 228 individuals (44%) had and used toilets (Table 2).

Table 2 Association of demographic, clinical, and other exposure factors with the prevalence of norovirus in the Amhara National Regional State, Ethiopia
Full size table

The association between sociodemographic, clinical, and exposure factors with norovirus infection

Variables with a cut of p-values of < 0.25 in the binary logistic regression analysis were fitted to the multivariable logistic regression analysis. These include study area, age group, frequency of diarrhea, duration of diarrhea, presence of vomiting, duration of vomiting, body temperature, generalized body weakness, nausea, previous history of diarrhea or AGE, family contact with a related case, and hand washing practice. Based on the outputs of multiple logistic regressions, the odds of NoV positivity were notably high among individuals living around Debre Tabor (AOR = 4, 95% CI: 1.2–14) and Bahir Dar area (AOR = 3.6, 95% CI: 1.04–11), compared to those in Debre Markos, and age < 5 years (AOR = 3.5, 95% CI: 2.8–12) and > 64 years (AOR = 7, 95% CI: 2–24) compared to those aged 18–64 years.

The odds of NoV infection were high among participants with previous history of AGE (AOR = 3.6, 95% CI: 1.7–7) and having a family contact history with related AGE cases (AOR = 5.4, 95% CI: 1.8–12.8). Conversely, participants who practiced good hand-washing habits before preparing or consuming food were less likely to be infected with NoV (AOR = 0.8, 95% CI: 0.4–0.85). The odds of NoV positivity were also high among individuals with a high frequency (≥ 3/day episodes) of diarrhea (AOR = 15.3, 95% CI: 7.6–43), acute phases (≤ 3 days) of diarrheal illness (AOR = 12, 95% CI: 6–33), vomiting (AOR = 3.5, 95% CI: 1.5–8), and acute phase of vomiting (≤ 3 days) (AOR = 7, 95% CI: 2–53) (Table 2).

Discussion

In the current study, NoV accounted for 8.9% of diarrhea cases. This prevalence was higher among under-5 children (12.5%) and the elderly participants (33.3%) compared to adults. This finding indicated the significance of NoV as a cause of AGE or diarrhea in the study areas. This finding is consistent with previous studies conducted in Ethiopia, 13.3% [13], and China, 9.5–11% [33, 34]. Conversely, lower prevalence rates were reported in Iraq at 6% [35] and Saudi Arabia at 3.6% [36], which could be attributed to various factors such as sample size, sociodemographic characteristics, and study period. On the other hand, the present finding was lower than studies done in Burkina Faso, 20% [37], and China, 38% [38]. The lower positivity rate of NoV infection in our study might be associated with the prevention and control strategies set for COVID-19 during the data collection period, which could reduce the transmission of NoV within the communities [17, 39]. In support of this, a rapid decrease in the incidence of viral gastroenteritis was reported during the COVID-19 pandemic [39,40,41].

The prevalence of NoV-GII among NoV positive AGE cases was notably higher compared to NoV-GI, accounting for 82.6% (95% CI (68.6, 92.2%)) of all cases across all age groups. Specifically, among under-5 children, the prevalence of NoV-GII was 80%. This finding is consistent with the previous report in Ethiopia, 98.3% [13], Cameron, 97.4% [42], Botswana, 93.9% [43], China, 95.67% [38], and the USA, 89% [44] indicating the predominance of NoV-GII on a global scale.

In a previous study conducted among under-5 children, the NoV positivity rate was not significantly different between the two sampling sites, Gondar and Bahir Dar [13]. However, in the present study, there was a significant difference in the positivity rates of NoV across the sampling sites. The possible explanation for the observed difference might be due to the differences in the data collection period. In the present study, samples were collected from May to November (including the rainy season), whereas the previous study was conducted from November to April (the dry season). Several studies reported that NoV infection has seasonality, in which the prevalence could be higher during the winter season [45,46,47]. The prevalence of NoV was higher in Debre Tabor as compared to the other study sites. The climate and weather conditions of Debre Tabor are characterized by an increase in altitude, winds, air pressure, and rainfall, which might have contributed to the spread of the infections [24, 25]. In support of this, the distribution of NoV is affected by the variability of climate changes and weather conditions, in which a lower temperature of less than 20 °C, relative humidity, and rainfall are considered as the environmental factors, that favor its prevalence [48, 49]. The socioeconomic status and access to potable water are also variable in the selected study areas, with better access in Bahir Dar, but lower access to potable water and low socioeconomic status in Debre Markos and Debre Tabor [50].

In the present study, a significantly higher positivity rate of NoV infection was found among under-5 children and the elderly compared to the adults. This implies that these extreme age groups are accompanied by increased disease severity, which is explained by factors such as underdeveloped or reduced immune function in these age groups [51]. In addition to this, increased environmental exposure to contaminated materials and surfaces found in their surrounding environment that is associated with low self-care capacity [17]. Moreover, NoV infection was associated with a self-reported previous history of AGE, family contact history with a related case of AGE in the past two weeks, and poor hand-washing practice, highlighting the highly contagious nature of the virus and its potential for transmission within households [20, 28]. This finding is in agreement with different studies [23, 28].

Limitation of the study

The present study was conducted over a short period of time (less than one year) and during the rainy season, which is expected to increase the prevalence of NoV and this might lead to an overestimation of the outcome. It was also better if asymptomatic cases were considered to evaluate the screening results and risk factors as a comparative study. Although co-infection with NoV is common, in the present study, we did not test for other pathogens. Furthermore, the lack of sequencing data affected the reporting of different NoV genotypes and strains. Despite these limitations, this study provided valuable insights on the prevalence, genogroup distributions, and associated factors of NoV in a diverse population across multiple sampling sites.

Conclusions

The prevalence of NoV among patients with gastroenteritis was considerably high. The predominant genogroup was GII. The prevalence of NoV was higher among under-5 children and the elderly. Previous history of diarrhea and family contact history with related cases of diarrhea were identified as statistically significant risk factors associated with NoV infections, while good handwashing practices had a preventive effect on NoV infection. Moreover, the positivity rate of NoV was associated with the duration and increased frequency of diarrhea, as well as the presence of vomiting. To obtain a comprehensive understanding of the virus`s epidemiology and its genetic diversity further research covering a broader geographical area is warranted. Moreover, the assessment of co-infections and asymptomatic infections in future studies might provide broader information.

 Availability of data and materials

The datasets supporting the conclusions are included within the article. However, upon reasonable and further inquiry they are available from the corresponding author [DT].

Abbreviations

AGE:

Acute gastroenteritis

ANRS:

Amhara national regional state

AOR:

Adjusted odds ratio

APHI:

Amhara Public Health Institute

COVID-19:

Coronavirus disease-19

Ct:

Cycle threshold

G :

Genogroup

NoV:

Norovirus

PCR:

Polymerase chain reaction

RNA:

Ribonucleic acid

RT-PCR:

Reverse transcription PCR

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Acknowledgements

We would like to thank the University of Gondar, the University of Gondar Post Graduate Strengthening Program, and Debre Tabor University for supporting this project. Amhara Public Health Institution is acknowledged for facilitating the data collection in the region and for allowing molecular detection and further storage of samples. Data collectors and study participants are also highly acknowledged as this project was not functional without the involvement of these individuals.

Funding

This research was partially supported by the University of Gondar, the University of Gondar Post-graduate Strengthening Program, the Debre Tabor University, and the Amhara Public Health Institution (partially for the molecular diagnosis part).

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Authors and Affiliations

  1. Department of Medical Microbiology, School of Biomedical and Laboratory Sciences, College of Medicine and Health Sciences, University of Gondar, Gondar, Ethiopia

    Dessie Tegegne, Aschalew Gelaw, Getachew Ferede & Baye Gelaw

  2. Department of Medical Laboratory Sciences, College of Health Sciences, Debre Tabor University, Debre Tabor, Ethiopia

    Dessie Tegegne

  3. Department of Molecular Biology, Amhara Public Health Institute, Bahir Dar, Ethiopia

    Girma Zerefaw

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  1. Dessie Tegegne
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  2. Aschalew Gelaw
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  4. Getachew Ferede
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  5. Baye Gelaw
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Contributions

DT, BG, AG, and GF all participated in the design and proposal development. DT and GZ conduct the laboratory analysis. DT analyzed the data and draft the manuscript. DT, BG, AG, and GF revised and edited the manuscript. All authors have read and agreed to publish this manuscript.

Corresponding author

Correspondence to Dessie Tegegne.

Ethics declarations

Ethics approval and consent to participate

An ethical approval letter was obtained from the University of Gondar institutional review board with a reference number V/P/RCS/05//765/2021. Permission was obtained from APHI to conduct the research in the region. A letter was written and given to each of the participating health facilities. The purpose of the research, risks, and benefits were explained. Written informed consent was obtained from study participants of age ≥ 18 years. For children under the age of 18, consent to participate was obtained from their parents or legal guardians prior to the initiation of study procedures. Moreover, for illiterate participants, the consent paper was read to them, and verbal consent was obtained. To maintain confidentiality, the data was recorded with a special code. The study participants were told that they had the right not to participate or withdraw at any time. Participants were managed as per the health facility protocol. The results obtained from each study participant were used only for research purposes.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Clinical trial number

Not applicable.

Key

*Variables with p−values < 0.25 (binary logistic regression) were fitted to the multivariable logistic regression model while p−value < 0.05 was the value considered for factors significantly associated with the prevalence of NoV.

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Tegegne, D., Gelaw, A., Zerefaw, G. et al. Prevalence and associated factors of norovirus infections among patients with diarrhea in the Amhara national regional state, Ethiopia. BMC Infect Dis 24, 1053 (2024). https://doi.org/10.1186/s12879-024-09988-5

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BMC Infectious Diseases

ISSN: 1471-2334

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