Epidemiology of Group A Rotavirus in children under five years of age with gastroenteritis in N’Djamena, Chad

doi:10.21203/rs.3.rs-2214869/v1

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Epidemiology of Group A Rotavirus in children under five years of age with gastroenteritis in N’Djamena, Chad

https://doi.org/10.21203/rs.3.rs-2214869/v1

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published 22 Jan, 2024

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Background: Group A Rotaviruses (RVA) is one of the most common causes of severe diarrhoea in infants and children under 5 years of age. Unlike other African countries where RVA surveillance is active, with routine circulating strains check, in Chad there is not currently RVA surveillance and vaccine introduced in the routine vaccination program. The objective of this study was to determine the prevalence and associated risk factors of RVA gastroenteritis in N'Djamena in view show the impact of RVA on the health of children under five years of age.

Method: This study comprised two parts, (1) a cross-sectional study involving the detection of RVA VP6 protein by ELISA from stool samples collected in four hospitals in N'Djamena between August and November2019 from children aged five years and below, as well as a determination of risk factors through a questionnaire; and (2) a retrospective study consisting of analysing record of stool examinations to determine the frequency of diarrheic gastroenteritis among children aged five and below within the period from January 2016 to December 2018.

Results: For the cross-sectional study, 141 samples were collected and analysed. The percentage of infected individuals was 12.76% (18/141) with males (61.11 %) being the more affected (sex ratio: 1.57). Children under 12 months were the most infected age group (44.44 %) and 44.4% are malnourished. The mean Vesikari score shows that 38.8% of children are at summer of severity and 41.1% have moderate condition. For the retrospective study, 2’592 cases of gastroenteritis hospitalization were analysed and 980 (37.8%) positive cases (all germs combined) of diarrhoea recorded from January 2016 to December 2018. The pic was obtained during the dry seasons, and the age group the most affected was 0 to 11 months with 57.3%.

Conclusion: This study describes the evidence of RVA induced gastroenteritis among children below five years of age in N’Djamena, thus indicate a serious health burden. Malnourish and younger age children were found to be the most at risk of infection. Further studies are needed to determine the strains circulating for considering the introduction of RVA vaccine and establishing a routine surveillance of the disease in Chad.

Rotavirus

epidemiology

gastroenteritis

N'Djamena

Gastroenteritis of infectious origin is one of the most common human diseases with a particularly high morbidity in children under 5 years old. Among the microbial causes responsible for these infections, rotavirus (RV) is the primary aetiology and accounts for 80% of cases of all enteric viruses [1]. Rotavirus (RV) is considered to be the third pathogen associated with mortality in children, behind malaria (517000 deaths) and pneumonia (359000 deaths) [2]. Each year, it causes more than 128,500 deaths and more than 258 million episodes of diarrhoea in children under five [3]. RV is responsible for 34% of acute and severe diarrhoea cases in children under five years of age in countries without a vaccine [4] [5]

Rotavirus is a member of the Reoviridae family with a size of 70–75 nm and is classified into 10 serogroups (A-J) based on the structural intermediate capsid protein (VP6). Among these serogroups, rotavirus group A is responsible for most gastroenteritis cases in human populations [6] . Two structural outer capsid proteins, VP7 (G glycoprotein) and VP4 (P protein) deﬁne the G and P serotypes of the virus, respectively. These major antigens are involved in virus neutralisation, and hence elicit the production of neutralising antibodies in the host and are thought to be important for vaccine development. These antigens allow the classiﬁcation of rotaviruses into a dual nomenclature system, depending on the G–P antigen combination [7].

There is not yet a treatment against RVA infection [8], and vaccination remains the main intervention currently in use to reduce the disease burden as recommended by the World Health Organization [9] [13]. Studies have shown that with vaccination, rotavirus diarrhoea is significantly reduced in children under 5 years old [11] [12]. Early complimentary feeding, nutritional status, dehydration and age less than 2 years are important risk factors associated with rotavirus diarrhoea [13] [14].

In Africa, rotavirus is an important cause of severe diarrheal disease in children 5 years of age [15]. The prevalence of rotavirus infections is 30% and in 2016, Sub-Saharan Africa recorded 104,733 cases out of all death cases globally [3]. There is high genetic diversity of rotavirus strains circulating. The most common G types detected are G1, G2, G9 and G3. The most common P types detected are P[8], P[6] and P[4] [16] [17]. It shown a high proportion of unusual P/G combinations, suggesting viral reassortment, evidence for zoonotic rotavirus transmission, the emergence and spread across Africa of serotype G9 and a high prevalence of the P[6] VP4 genotype [18].

In Chad, 30 to 39% of deaths from diarrhoea in children under five may be attributable to RVA [3] and the prevalence was reported around 48% [19]. Despite this diarrhoea related high mortality among children, RVA vaccine has not yet been introduced to Chad, and few hospitals include RVA among the aetiologies of gastroenteritis sought in the laboratory in children of this age group. Therefore, this study aimed to determine prevalence and associated risk factors of RVA gastroenteritis in children under five years of age in N’Djamena. This study also intended to show what RVA represents in infantile gastroenteritis and evidence of its impact on health in children under five years of age.

Type of study, study population and sample collection

This study has two parts: cross-sectional and retrospective.

The first, cross-sectional study conducted between August and November 2019, was carried out in 4 hospitals in N'Djamena: “Centre Hospitalier Universitaire de la Mère et de l’Enfant” (CHUME), “Complexe Hospitalo-Universitaire le Bon Samaritain” (CHUBS), “Hôpital de l’Amitié Tchad-Chine” (HATC) and “Hôpital Notre Dame des Apôtres” (HNDA). The study population was constituted children under 5 years hospitalized or seen for acute non-bloody gastroenteritis. Only children with at least 3 watery or liquid stools, with or without vomiting were included in the study. In total, 141 samples were collected (table 1).

The other retrospective part of the study focused on hospital data from January 2016 to December 2018 from two health structures: CHUME and HNDA. A total of 2592 data on childhood diarrhoea analysis were considered (table 1). These data included the results of the stool culture and parasite research examinations for children under 5 years hospitalized or seen for acute non-bloody gastroenteritis. Although RVA was not researched, this result will make it possible to know if RVA could be involved in the aetiology of childhood gastroenteritis in these three years (Table 1).

Analysis procedures

Approximately 5 ml or 5 mg of faeces from each child were collected in a sterile stool container, labelled and transported in a cooler (2-8° C). The 141 samples collected were submitted to detection of the VP6 antigen of RVA on 10% Phosphate Buffered Saline suspension, at the virology laboratory of the “Institut de Recherche en Elévage pour le Développement” (IRED) using Enzyme-Immunoassay ELISA sandwich technique. According to manufacturer's instructions, Optical Density (OD) readings ranged ≥ Cut Off was considered positive and Optical Density (OD) value < Cut Off was considered negative [20].

The Vesikari scores of these children were determined for the severity of their gastroenteritis by analysing their clinical parameters (maximum number of stools and duration of diarrhoea per day, maximum number of vomiting and duration of vomiting per day, temperature, dehydration and treatment). Total score was obtained classing the severity level of gastroenteritis as mild for <7, moderate for 7-10 and severe for ≥ 11 for severe [21].

Statistical analysis

Statistical analyses were performed using SPSS 23 software. Statistical distributions were compared using Chi-square test with a 95% confidence interval and a p-value of 5%. The distribution of Vesikari clinical severity score was compared between children who tested positive for rotavirus versus those tested negative. The Vesikari clinical severity score was grouped into mild, moderate and severe.

Cross-sectional study

A total of 141 stool samples from children under 5 with gastroenteritis were collected (table 1). The mean age of the children was 17.12 months with a male predominance of 59% (83/141). Two cases of death were recorded whose one case of death of an 18-month-old child, following a digestive infection with the presence of persistent diarrhoea and dehydration, and one case of HIV infection were recorded.

Frequency and severity of rotavirus diarrhoea

RVA was detected in 12.76% (18/141) of the samples analysed and 61.11% (11/18) of child infected by RVA was male sex. The most affected age group was that of 0 to 11 months with 44.4% (8/18) and according to the hospitals, HNDA presented 44.4% (8/18) followed by CHUME hospital with 33.3% (6/18) as shown in Table 2. Among the positive cases, a case of death of a child suffering from gastroenteritis was noted.

Regarding nutritional status, out of all children who tested positive, 22.2% (4/18) had normal nutritional status while 44.5% (8/18) had severe acute malnutrition and 333% (6/18) moderate acute malnutrition. For exclusive breastfeeding, no child under exclusive breastfeeding was infected while all those infected were no while half (50%) of those early weaned were infected (Table 2).

The mean Vesikari score shows that 38.8% of children are at summer of severity and 41.1% have moderate condition (table 3).

Among children with rotavirus infection, 22.2% have diarrhoea lasting longer than six days and 38.9% of these diarrhoeas occur more than six times a day. Children with severe dehydration represent 44.5% (Table 3).

Retrospective study

In the retrospective study, in total 2’592 results of stool examination considering all microbial aetiologies in children under 5 years old collected between January 2016 and December 2018 were analysed of which 37.80% (980) were positive. That is, 62.20% of the examinations carried out were negative while all the children suffered from gastroenteritis.

It emerges that the male population has a slightly higher proportion with the test 54.5% (n= 534) with a sex ratio of 1.37. The most affected age is that of children under five with 57.3%, 562 cases (Table 4).

Among the parasites sought, Entamoeba histolytica (51%) followed by Gardia lamblia (14%) and Hymenolepus nana (14%) predominated in the stool ova and parasites test (Figure 1) while for stool culture, Escherichia coli (28%), Klebsiella oxytoca (24%), Candida albicans (19%) and Salmonella typhi (13%) were the most frequently identified (Figure 2).

Figure 3 above shows that the frequency of diarrheal infections, and therefore that of rotaviruses, is high between December and February. This corresponds to the dry season in the study area.

Rotavirus gastroenteritis in children under five in N’Djamena remains a public health problem in N’Djamena due to the fact that RVA are not taken into account in the laboratory diagnosis. This is why we conducted this study in two parts in order to know the place of RVA in the diagnosis.

For the cross-sectional study, previous research carried out in N’Djamena has highlighted the involvement of RVA in childhood gastroenteritis, with a prevalence of 8% [22] and a mortality rate ranging from 30% and 39% [3]. The results obtained during this study corroborate the endemicity of RVA diarrhoea with a frequency of 12.76% (18/141) and is close to that obtained by Muendo in 2018 in Kenya with 14.5% of positive cases [23]. However, it is lower than what obtained Fombotioh et al. in 2021 in N’Djamena which is 48.24% [24]. This can be explained by the fact that their study concerned all groups of rotaviruses, and their samples were analysed by immunochromatographic tests whereas we analysed ours by ELISA tests. Also, the most part of their study was conducted during the dry season when ours were conducted during the rainy season. This result is also lower compared to the 30% obtained in 2018 by Troeger for low-income countries in Africa [3]. This could also be due to the collection period corresponding to the rainy season considered as the period when there are fewer cases of rotavirus gastroenteritis [25] [26]. This result is lower than those obtained by Ekomi in 2016 in Central Africa [27], Ouedraogo in 2015 in Burkina Faso [28] and Eteme in 2015 in Cameroon [29] with high prevalence of 63.5%, 45% and 30% respectively.

Among the positive cases, the frequency was higher in boys (61.1%) than in girls (38.9%) with no statistical significance (p=0.83) (table 2). This high frequency could be explained by higher micronutrient requirements in boys than girls which suggests a greater susceptibility of male children to rotavirus gastroenteritis. In effect, it was shown that micronutrient deficiency, especially zinc and vitamin A constitute a factor favouring the occurrence of gastroenteritis [30] and the growth of boys is associated with development of muscle mass generally higher than that of girls. Therefore, micronutrient requirements may be higher in boys, more exposed to an imbalance diet including zinc deficiency and vitamin A [31]. This frequency is close to the 66.67% of males obtained by Eteme in Cameroon [29], but different from the 51.9% of females obtained by Sangaji in the Democratic Republic of the Congo [32].

RVA positive cases by age group analysis revealed differences in the infection rate with increasing age. RVA infection within the age group of 0-11 months has the highest RVA positive rate among the all age groups of infants less than 5 years of age with 44.4 % (p=0.03) (table 2). The other age groups, 12-23 and 24-59 months, accounted for 27.78% of positive cases each. This could be explained by the weak immunity of younger children exposing them to the disease and better developed natural immunity and repeated infections in older children promoting their immunization [33]. This result is similar to that of Tate presenting rotavirus as the leading cause of diarrhoea in infants (0-11 months) [1]. On the other hand, it is contradictory to that obtained in Mauritania, where children aged 12 to 24 months who were the most affected followed by those from 0 to 11 months [34]. This could be explained by the development natural immunity and repeated infections in older children promoting immunization [35].

According to the hospitals, more cases of gastroenteritis due to RVA were registered with HNDA and CHUME with respectively 44.4% and 33.3% (p=0.27) (table 2). This higher result could be justified by the fact that these two hospitals have the highest number of children sampled in the study. These two hospitals also have Nutritional and Therapeutic Units and take in more children because of their position in the most populous districts of N'Djamena.

Regarding nutritional status, out of all children who tested positive, 44.5% had severe acute malnutrition and 33.3% moderate acute malnutrition shows that the occurrence of the RVA infection is linked to the nutritional status at the risk of 5% (p=0.04) (table 2). This shows that the low nutritional intake favours the onset of infection. However, some studies show that nutritional status has no significant correlation with severity of rotavirus diarrhoea [35].

Among the exclusively breastfeeding children, none were infected with rotavirus while all those who were not had a positive result. The early weaning status presents half of the infection rate. This shows that exclusive breastfeeding has a very important contribution to the immunity of children and early weaning causes the onset of infection. However, these results are not statistically significant at the 5% risk. This could also be explained by the fact that exclusive breastfeeding provides natural immunity to infants through type A immunoglobulins [36].

The Vesikari Clinical Severity scoring system for gastroenteritis used in this study, elicited the distribution of severe diarrhoea as similar among those children who were rotavirus positive compared to those who were negative. The Vesikari Clinical Severity score among rotavirus infected children obtained shows 44.1% were rated moderate, 38.8% rated severe and 17.1% rated mild. This shows the severe level of rotavirus infection in these children with a fairly low nutritional status obtained. This can be explained by the young age of infected children 0-11 months (44.4%) exposing them more easily to the risks of severity. According to the World Health Organization scientific working group, most cases of rotavirus infections occur in children between 6 and 24 months with a peak incidence at 9 to 12 months [33]. It is postulated that younger children tend to be at an increased risk of developing severe dehydration due to their small body size, as they lose a greater portion of their total fluid volume during the illness [37].

For the retrospective study, 37.8% of stool examinations performed between January 2016 and December 2018 at the CHUME and HNDA were positive, while all the children diagnosed presented with gastroenteritis. That is, 62.20% of the examinations carried out were negative. This rate can be explained by the failure to consider viral aetiology in the laboratory diagnosis, particularly that of RVA. However, the RV is considered to be the leading cause of death associated with childhood gastroenteritis worldwide [1].

The male population predominated (54.5%) and could be explained by higher micronutrient requirements in boys than girls [32]. The most affected age is that of children under 12 months with (57.3%). This could be explained by the weak immunity of younger children exposing them to the disease and better developed natural immunity and repeated infections in older children promoting their immunization [33] (table 4).

Among the germs identified in the stool ova and parasites test, Entamoeba histolytica predominated with 51% while Escherichia coli predominated in the bacterial aetiology with 28% (fig. 1,2). However, by doing the statistical analysis and the difference in the margin between positive and negative cases, the RVA would be largely involved in the aetiology in this negative range (62.2%) at the risk of 5%.

Compared to seasonality, the frequency of RVA diarrhoea and gastroenteritis in children under (5) years of age was high in the dry season than in the rainy season (fig. 3). This result could be explained by the abundance of dust produced by the wind during this period, favouring the contamination of children. This observation is similar to those of Patel in 2013 [25] and Tsolenyanu in 2017 [26] but different from that of Bruno who rather observed high frequencies in the rainy season [22]. Godfrey and al. have also shown that seasonal peaks of rotavirus diarrhoea were between June–September [6]

Limitations

The major difficulty encountered was the difficulty in obtaining data from hospital structures with missing data. We did not obtain sufficient data on seasonality. The data presented is for only two hospitals (CHUME and HNDA). We also note the difficulty of pursuing molecular analysis of our samples to identify genotypes.

A viral frequency of 12.76% and a severe level of RVA gastroenteritis, and a significant rate of negativity (62.20%) of diarrhoea examined between 2016 and 2018 without testing for RVA demonstrate the need to take into account the viral aetiology in the diagnosis of gastroenteritis in children under 5 years of age and prefer exclusive breastfeeding. Also, it is necessary to carry out studies to identify the genotypes in order to introduce a vaccine in order to immunize children of this age group.

CHUBS : Centre Hospitalo-Universitaire le Bon Samaritain

CHUME : Centre Hospitalier Universitaire de la Mère et de l’Enfant

ELISA : Enzyme Linked ImmunoSorbent Assay

HATC : Hôpital de l’Amitié Tchad-Chine

HNDA : Hôpital Notre Dame des Apôtres

IRED : Institut de Recherche en Elévage pour le Développement

RVA: Group A Rotavirus

VP6: Viral Protein 6

Conflict of interest

The authors state that there is no conflict of interest.

Ethical clearance for this study was obtained from the National Ethics Committee of Chad (N°033/PR/MRDRI/DGM/CNBT/SG/2019). Research authorizations were obtained from the four hospitals CHUME, HNDA, HATC, CHUBS. Parents or legal guardians of sampled patients consented by signing the informed consent form. The study protocol conformed to the ethical guidelines of the 1975 declaration of Helsinki was approved by the Ministry of Public Health of Chad.

Consent for publication

Not applicable.

Availability of data and materials

The datasets used and analysed during the current study are available from the corresponding author.

Competing interests

No competing interests.

Funding

This study was supported by the personal funds of the authors.

Authors’ contributions

Bench and data analysis: BD, BM. Reagents/materials and analysis tools: BD, MFA, PK. Manuscript preparation: BD, MB, VNN. Study designed: MB, JPAA. Field work activities: BD, MB. Laboratory work: BD, MFA, RNG, CNE. Supervision: MB, VNN, JPAA, MFA. All the authors read and approved the final manuscript.

Acknowledgments

We hereby acknowledge the bench support for this work from IRED through the Virology Laboratory and the hospital HATC through the molecular biology laboratory N’Djamena, Chad. We would like also to thank parents or legal guardians for participating in the study, and doctors and nurses for their involvement in sample collection.

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Table 1 : Distribution of the number of samples per hospital in the two studies

Study type	Hospitals
Study type	CHUME	HNDA	HATC	CHUBS	Total
Cross-sectional	56	45	24	16	141
Retrospective	1250	1342	0	0	2592

Table 2: Frequency of RVA gastroenteritis according to the sex, age, hospitals, nutritional status, breastfeeding, and weaning (n=18)

	Positive RVA n (%)	Negative RVA n (%)	*p-value*
Sex
Male	11 (61.1)	72 (58.5)	0.83
Female	7 (38.9)	51 (41.5)
Age (month)
0-11	8 (44.4)	48 (39.0)
13-23	5 (27.8)	42 (34.2)	0.03
24-59	5 (27.8)	33 (26.8)
Hospitals
CHUME	6 (33.3)	50 (40.6)
CHUBS	1 (5.6)	15 (12.2)	0.27
HATC	3 (16.7)	21 (17.1)
HNDA	8 (44.4)	37 (30.1)
Nutritional status
Normal	4 (22.2)	55 (44.7)
Moderate	6 (33.3)	48 (39.0)	0.004
Severe	8 (44.5)	20 (16.3)
Exclusive breastfeeding
Yes	0 (0)	19 (21.8)	0.14
No	8 (100)	68 (78.2)
Weaning
Before 2 years	5 (50.0)	11 (30.6)	0.26
For 2 years	5 (50.0)	25 (69.4)

Table 3: Distribution of cases within the clinical parameters of the Vesikari scoring for severe gastroenteritis (n=18).

Risk factor	n (%)
Diarrhoea Duration (days)
1–4	8 (44.4)
5	6 (33.3)
≥ 6	4 (22.2)
Frequency of diarrhoea per day
3	1 (5.5)
4–5	10 (55.6)
≥ 6	7 (38.9)
Duration of vomiting (days)
0	6 (33.3)
1	2 (11.1)
2	5 (27.8)
≥ 3	5 (27.8)
Frequency of vomiting per day
0	6 (33.3)
1	1 (5.6)
2–4	6 (33.3)
≥ 5	5 (27.8)
Temperature (°C)
37.1–38.4	3 (20)
38.5–38.9	10 (66.7)
≥ 39.0	2 (13.3)
Dehydration status
None	4 (22.2)
Some dehydration	6 (33.3)
Severe dehydration/shock	8 (44.5)
Treatment
Rehydrated	6 (33.3)
Admitted	12 (66.7)
Severity Category
Mild	19 (17.1)
Moderate	49 (44.1)
Severe	43 (38.8)

Table 4: Frequency of gastroenteritis according to the sex, age and hospitals between 2016 and 2018

Risk Factor	Positive test n (%)	Negative test n (%)
Tests
Stool ova and parasite	901 (38.4)	1442 (61,6)
Stool culture	79 (31.7)	170 (68.3)
General frequency	980 (37.8)	1612 (62.2)
Sex
Male	534 (54.5)	966 (59.9)
Female	446 (45.5)	646 (40.1)
Age (month)
0-11	562 (57.3)	508 (51.8)
12-23	282 (28.8)	610 (62.2)
24-59	136 (13.9)	494 (50.4)
Hospitals
CHUME	472 (48.2)	778 (48.3)
HNDA	508 (51.8)	834 (51.7)

No competing interests reported.

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published 22 Jan, 2024

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Editorial decision: Major revision
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Epidemiology of Group A Rotavirus in children under five years of age with gastroenteritis in N’Djamena, Chad

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Introduction

Materials And Methods

Type of study, study population and sample collection

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Results

Cross-sectional study

Frequency and severity of rotavirus diarrhoea

Retrospective study

Discussion

Conclusion

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