This article analyzes incidence data of acute intestinal infection among the population of Arkhangelsk oblast over a period of more than twenty years. The etiology of acute watery diarrhoea among hospitalized young children is presented and the role of noroviruses in the development of acute intestinal infections is established. Viral antigens are shown to persist in a proportion of children after the disappearance of the clinical symptoms and thus there might be a risk for infection transmission.
The most recent international studies addressing the etiology of diarrhoea confirm the leading role of viruses. The list of viruses causing intestinal disorders is continuously growing due to improved and more comprehensive diagnostic methods. To date the list includes rota-, noro-, astro-, adeno-, toro- and other viruses (1, 2). The most frequent manifestation of viral diarrhoea is the triad of symptoms: vomiting, watery stools and fever. These diseases are of special concern for practitioners and specialists practicing prophylactic medicine because often the diseases affect young children and are associated with dehydration requiring hospitalization for correction of fluid volume and water-salt metabolism. Rotaviruses are known to cause up to 80% of diarrhoea cases among young children (3-5) with an annual mortality of more than 500,000 children worldwide (6). Moreover, lactase insufficiency, intestinal dysbacteriosis and secondary digestive disorders are associated with rotavirus infection (RVI). Infected persons may also become long-term rotavirus carriers and risk transmitting the virus (7).
Laboratory confirmed cases of rotavirus infection in the Russian Federation have been notifiable since 1995. Since laboratory methods for rotavirus identification are not available in all health care institutions in Arkhangelsk oblast, the true rotavirus incidence in the region is not known.
Noroviruses belong to the Calicivirus family and cause approximately 30% of diarrhoea cases in developed countries (8,9). The role of noroviruses in the development of watery diarrhoea in the Russian Federation and Arkhangelsk oblast remains unknown.
The aim of this study was to describe the epidemiology of RVI in the Arkhangelsk oblast and establish the role of noroviruses in development of acute watery diarrhoea among hospitalised children less than 3 years of age.
Materials and methods
Epidemiological statistical data from an international collaboration, the “EpiNorth” project (10), and the Directorate of Rospotrebnadzor in Arkhangelsk oblast were used for analysis (11). In addition, the results of a 2007 pilot study including 68 children hospitalized with watery diarrhoea and tested for rota- and noroviruses by enzyme immunoassay (EIA) were included. The children’s parents provided written informed consent for participation in the study. The inclusion criteria were as follows: (a) age under 3 years, (b) hospitalization within first two days of onset of the symptoms, (c) signs of enteritis or gastroenteritis and (d) no sign of blood or pus in faeces. Faecal bacteriological testing was performed to rule out shigellosis, salmonellosis and enteritis caused by enteropathogenic E.coli. Faeces were collected in sterile bottles, assigned with an identification number and frozen at -700С prior to EIA testing in an independent laboratory. The laboratory staff was not aware of the course of disease among the patients.
Analysis of epidemiological data from Russia indicated that confirmed etiologic diagnosis is primarily due to rotavirus gastroenteritis and there is no official registration of noro-, astro-, adenovirus and other infections. In the city of Arkhangelsk and other large towns in Arkhangelsk oblast, testing for RVI has been actively implemented since 1994 and cases of RVI are officially registered.
A retrospective analysis of epidemiological data indicates that the increase in rotavirus gastroenteritis incidence since 1994 is probably due to improved and expanded RVI laboratory confirmation. The rotavirus gastroenteritis incidence in Arkhangelsk oblast (Figure 1) during the analyzed period was higher than in the Russian Federation. Since the beginning of RVI case registration the incidence has increased almost 20-fold (from 2.2 to 40.1 per 100,000 population).
Figure 1. Rotavirus infection incidence (per 100,000 population) among the general population of the Russian Federation and Arkhangelsk oblast, 1994 - 2007
*- The 2007 data on RVI incidence in the Russian Federation are absent because since 2007 RVI has been registered within the group of all acute intestinal infections of known (viral or bacterial) etiology
The highest incidence rate in children under 14 years was noted in 2005 (320.5 per 100,000 children). During 1994-2007 the incidence of rotavirus gastroenteritis among children was higher in Arkhangelsk oblast than in the Russian Federation (Figure 2). During the 14-years period the RVI incidence rate increased nearly 28-fold (from 9.2 in 1994 to 256.0 per 100,000 population in 2007).
Figure 2. RVI incidence among children under 14 years (per 100,000 children) in the Russian Federation and Arkhangelsk oblast, 1994-2007
* - The 2007 data on RVI incidence in the Russian Federation are absent because since 2007 RVI has been registered within the group of all acute intestinal infections of known (viral or bacterial) etiology.
Since 2005, RVI has been the most prevalent confirmed acute intestinal infection among children less than 14 years in Arkhangelsk oblast. Since 2001 there has been a drastic drop in incidence of dysentery. The incidence of salmonellosis and enteritis caused by enteropathogenic E.coli. was not high and varied insignificantly (Figure 3).
Figure 3. Incidence of acute intestinal infections among children less than 14 years (per 100,000 children) in Arkhangelsk oblast, 1994-2007
There was a high level of acute intestinal infections of unknown etiology through the years. The incidence was highest in 2007 (1763.8 per 100,000 children). We can not rule out the role of unknown viruses in the group of intestinal infections with unknown etiology.
Analysis of the monthly rotavirus gastroenteritis incidence data during the last 11 years indicates that this infection was registered throughout the year with an increase in incidence from November in Arkhangelsk oblast. The maximum number of cases was registered from December to April (82.3% of all patients). The number of patients declined in May.
Analysis of RVI patients’ age structure revealed a predominance of children less than 14 years with percentages ranging from 86.2% to 100%. Among children less than 14 years, the prevalence of RVI was greatest among children aged 1-3 years during 1999- 2007, comprising 42.7% to 58.5% of the patients. The percentage of infants less than one year ranged from 27.6% to 42.8%. Children from 3 to 14 years old were less prone to RVI.
The laboratory confirmation of other viral diarrhoeas in our region has previously not been performed.
From January through May 2007, a period with a high incidence of watery diarrhoeas, 68 children were simultaneously tested for rota- and noroviruses. Mono-infections with rotavirus and norovirus were detected among 50 and 11 children, respectively. Among 7 children coinfection with both rota- and noroviruses was detected (Table 1).
Table 1. Distribution of patients by age and by etiology of acute intestinal infection in Arkhangelsk oblast, 2007
Children < 1 year / Дети до 1 года
Children 1-3 years / Дети 1-3 лет
Total (%) / Итого, (%)
Number of patients / Количествобольных
RVI positive/ из них положительных на ротавирусную инфекцию
Norovirus positive / из них положительных на норовирусную инфекцию
Rota- and norovirus positive / из них положительных на рота- и норовирусную инфекцию (микстинфекция)
The largest number of children with confirmed norovirus and coinfection with both rota- and noroviruses (13 out of 18 subjects) was registered in January, at the peak of gastroenteritis incidence. In the following months the number of patients with these infections was sporadic.
Table 2. Frequency of major clinical symptoms in children with rotavirus, norovirus and rota-norovirus infections in Arkhangelsk oblast, 2007
Clinical symptoms / Клинические проявления
Norovirus infection (n=11) / Норовирусная инфекция (n=11)
Rota- norovirus co-infection
(n = 7) / Рота-норовирусная инфекция (n=7)
(n = 50) / Ротавируснаяинфекция (n=50)
Disease severity / Тяжесть:
Mild / Легкая
Moderate / Среднетяжелая
Severe / Тяжелая
Fever / Лихорадка:
absent / отсутствовала
Vomiting / Рвота:
absent / отсутствовала
1-5 times /раз
6-10 times / раз
11-15 times / раз
1-5 times / раз
6-10 times / раз
11-15 times / раз
No statistically significant differences in frequency and duration of main clinical symptoms were found. However, certain trends were noted. In contrast to other infections, high fever and severe diarrhoea (i.e. stool frequency and consistency) were more pronounced among RVI patients (Table 2). In approximately 90% of norovirus mono- and mixed infection cases diarrhoea was preceded by vomiting, as compared to 80% of RVI cases. In rotavirus and rota-norovirus coinfection the mean frequency of vomiting was higher than in norovirus infection alone. The hospital stay duration in children with norovirus, rota-norovirus and rotavirus infections was 8.9 ± 3.5 days, 10.1 ± 3.8 days and 7.6 ± 0.3 days, respectively.
Repeated tests were performed for 15 of the 18 norovirus-positive patients (including those 7 with rota-norovirus coinfection). In 8 (53.3%) of 15 tested patients norovirus was not found after the symptoms resolved (7.3 ± 0.7 days). The remained children shed norovirus after the symptoms resolved and were therefore discharged from the hospital with close follow-up by an outpatient paediatrician. No data regarding the time of viral elimination are available for those patients. Norovirus elimination was observed more often after moderate-to-severe compared to the severe form of the disease (62.5% and 42.9%, respectively).
Of the 7 patients with mixed rota- and norovirus infection, both viruses were eliminated in one child only by the same time (7.3 ± 0.7 days) as in two children only norovirus was eliminated and only rotavirus was eliminated in one other patient. At the time of clinical recovery (on average 8.6 ± 0.3 days) among patients with rotavirus mono-infection the virus was eliminated in only 10 (20.0%) of tested patients.
During 1994-2007 the incidence of acute intestinal infections in Arkhangelsk oblast was higher than in the Russian Federation. The incidence of intestinal infections of unknown etiology remained high. Simultaneously, a decrease in the incidence of shigellosis and salmonellosis and an increase in rotavirus gastroenteritis incidence were observed. The 2007 study indicated that rotavirus was the causative agent in 73.5% of diarrhoea cases and norovirus to be the cause of 26.5% of the gastroenteritis cases in the patient cohort. In more than a third of the patients a mixed infection of rota- and noroviruses was found. Virus elimination at the time of clinical recovery was observed in approximately half of the patients with norovirus infection, in only one patient with mixed rota- and norovirus infection and only 20% of the patients with the rotavirus mono-infection. Children that are virus carriers at the time of discharge from hospital may transmit the infection.
The data obtained indicate the need to expedite the implementation of novel diagnostic techniques for the simultaneous identification of intestinal pathogens. In addition, the surveillance of intestinal infections needs improvement.
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- EpiNorth, EpiNorthData (http://www.epinorth.org)
- Роспотребнадзор по Архангельской области (http://www.29rpn.ru)