Recent emergence and outbreak of rotavirus gastroenteritis in Samoa: A scoping review of risk factors, containment measures and public health preparedness

Lawal Olatunde Olayemi, Vicky Yemoh, Alec Ekeroma

School of Medicine, Faculty of Health Sciences, National University of Samoa, Samoa

ABSTRACT

Diarrheal diseases have been known to cause death in many children below the age of five years, and rotavirus infection represents a major health problem in the world today, particularly in developing countries. The recent outbreak of rotavirus gastroenteritis in Samoa led to the introduction of her debut national immunization program on rotavirus vaccination for infants. Despite the introduction of anti-viral and anti-emetic drugs as of the containment approaches towards the virus, risk factors, preventive measures and public health preparedness against rotavirus infection are poorly understood in Samoa. This review aims to use available evidence on rotavirus literature to elucidate and map preventive strategies for the recently emerged rotavirus infections in Samoa. We conducted a search strategy using online medical literature databases and retrieval systems. A designated set of keywords such as rotavirus,gastroenteritis, outbreak, risk factors, containment measures,vaccination and Samoa were inserted in electronic databases to retrieve articles. The databases included PubMed, Google Scholar,MEDLINE, Scinapse, and EBSCO host. Findings from this review addressed the impact of rotavirus infection, associated threats and other preventive measures. Introducing useful health frameworks in pursuing possible methods such as improved water quality, exclusive breast feeding, improved laboratory diagnostics and outbreak surveillance, may be essential in addressing alternate approaches towards containment of the disease in Samoa and other Pacific Island Countries and Territories.

KEYWORDS: Rotavirus; Gastroenteritis; Outbreak; Risk factors;Containment measures; Vaccination; Pacific Island Countries and Territories; Samoa

1. Introduction

Acute gastroenteritis is a common infectious disease confronting people of all ages globally, especially the pediatric population[1].It represents a significant public health threat, particularly in developing countries. Enteric microbial pathogens, viruses,parasites, or bacteria remain the most frequent causative agents of acute gastroenteritis among children under the age of five[2]. Acute gastroenteritis is commonly acquired through the fecal-oral route,contaminated surfaces and from unhygienic water sources[3,4].Rotavirus gastroenteritis can be recurrently acquired in persons during childbirth and until old age, although infants in their early years are mostly affected[5]. The virus is extremely communicable and this can be assumed that after one year of age, about two-thirds of children would have experienced at least one rotavirus infection and one-third a second rotavirus infection[6]. Most infections could present as either asymptomatic or episodes of mild enteric symptoms, which may not be noticed in infected persons. Despite this, a large number of infections lead to severe disease sequelae with diarrhoea, need for hospitalization, and in rare cases death[7].There are also considerable disparities in the severity of disease amongst primary and successive infections[6]. Among the classical symptoms of rotavirus infections, the most alarming and critical include high fever, vomiting, diarrhoea and marked dehydration According to the Ministry of Health in Samoa, as of the 22nd of July 2021, rotavirus outbreak among children had resulted in over 31 rotavirus cases, which were confirmed by laboratory testing[8].Further investigations and contact tracing were still ongoing to ascertain the source of transmission of the virus in affected persons.Except for Fiji and the Philippines, the burden of rotavirus in the Asia-Pacific region is largely unknown[9,10]. With the growing and continuous drive towards vaccine-preventable disease and in achieving the World Health Organization (WHO) goal of global eradication of childhood infectious disease mortality, Pacific Island Countries and Territories (PICTs) may be the principal beneficiaries of rotavirus vaccination due to risks of severe disease outbreaks[11].In achieving such stride, urgent public health strategies and plans must be continuously introduced in mitigating the dangers associated with the spread of rotavirus infections in reducing the burden of the disease. Strengthening infectious disease diagnostics, introducing and consolidating emergency prevention and containment programs as well as socio-cultural networks in the PICTs may help in achieving this.

This paper briefly elucidates the current emergence of rotavirus infections in Samoa, including associated risk factors, improved containment measures and public health interventions. It further addresses the significance of rotavirus vaccination in Samoa and also the need for further research to identify post-vaccination effectiveness, acceptance rate measures and psychosocial levels amongst affected individuals.

2. Search strategy, study selection and eligibility

A search strategy was performed using online medical literature databases and retrieval systems. Databases included PubMed,Google Scholar, MEDLINE, Scinapse, and EBSCO host. A designated set of keywords from Medical Subject Heading (MESH)such as “Rotavirus”, “Gastroenteritis”, “Outbreak”, “Risk-factors”,“Containment measures”, “Vaccination” and “Samoa” were inserted in electronic databases to retrieve articles published between 1996 and 2021. Only articles in English were included in this review.Though no original research had been carried out on rotavirus in Samoa, studies that closely addressed the key entities, risk factors,containment measures and public health emergency preparedness towards rotavirus were included in this article to elucidate and map a conceptual public health framework for the prevention of rotavirus in Samoa.

3. Results

Findings from this review revealed various entities, which addressed the knowns and unknowns that characterized the outbreak of rotavirus gastroenteritis in Samoa. These ranged from risk factors of the rotavirus disease, importance of containment methods and diagnostics to the impact of rotavirus vaccination, public health emergency response and preparedness.

3.1. Associated risk factors for rotavirus infection

Significant risk factors attributed to rotavirus disease may predict the progression of rotavirus infection to severe illnesses, including hospitalization and death, due to debilitating the clinical effects of rotavirus in susceptible people. These could also contribute to the development of intussusception, autoimmunity, gastrointestinal disease, and immune deficiency[12]. There could be an upsurge in the severity of biological and social risk factors among affected populations, who are mostly young children, unimmunized teenagers and adults. These risk factors may range from nutritional status,malignancy, cardiac disease, and gastroparesis to breastfeeding,socio-economic levels, low gestational age and central nervous system complications. Previously available evidence indicated that the rate of hospitalizations due to childhood diarrhoea in Samoa decreased from 68% in 2009 to 62% in 2014[13]and 57.4% in 2019[14]. The reduction rate was largely attributed to the use of oral rehydration therapy (ORT) in syndromic case management of children who presented to a health facility[13]. However, in the recent rotavirus outbreak, children below the age of five years were the most affected with typical clinical manifestations as observed by attending clinicians at the emergency wards of the government hospital and following laboratory confirmations[8]. Moreover, studies have shown the highest burden of rotavirus infection amongst paediatric populations below the age of two years, where children below the age of six months experienced lower rates of infection and a decrease in the rate of infection was observed amid children above two years of age[15]. The disparity in the rates of rotavirus infection between the age groups may be explicated by the protective effect of maternal antibodies in newborns less than 6 months old, and the development of innate immunity after recurrent infections in children above two years of age[16]. These could largely be due to the peculiarity of individual risk factors for rotavirus gastroenteritis in at-risk age groups or populations in Samoa. Likewise, being malnourished, underweight, history of low-birth weight, drinking untreated water, and being born to an uneducated mother have also been shown to be identified as independent risk factors of rotavirus infection[15]. Infant feeding practices of using unboiled tap water to prepare formula milk also increases the risk of developing rotavirus infection[17]. These further explain the possibilities of the rotavirus outbreak and the spread of the infection in Samoa, where there may be lack of quality drinking water and poor hygiene practices,especially in rural and suburban areas. Despite the likelihood of government efforts in bridging the education gap and improving socio-economic living standards, there may still be challenges of poor health literacy and access to proper health education.

3.2. Role of containment measures

3.2.1. Rotavirus biology and genotype distribution

As an RNA virus, rotavirus belongs to the family Reoviridae. It is non-enveloped, measures 60-80 nm in diameter, and its genome length is approximately 18.5 kb. Its genome is made up of 11 segments of double-stranded RNA and encodes six structural proteins (VP1-7) and six nonstructural proteins (NSP1-6)[18,19].Rotavirus A is one of the main causative agents of diarrhea in young humans and animals[18,20]. It is ubiquitous in the environment and relatively resistant to disinfectants. Rotavirus exists in different genotypes and serotypes, and throughout the world, studies have identified common co-circulating rotavirus types, and G2P[21],G1P, G3P, and G4P are the predominant strains[22]. However, due to antigenic drift and variations in viral ecology, other less common genotypes, such as G9P, G5P[22]and G8P[23], are predominant in many countries. Molecular characterization of rotavirus genotypes could help underpin efficient global surveillance of rotavirus infections. There is a tremendous diversity amongst the human and animal strains of rotavirus, especially the human pathogenic rotavirus type A. The presence of such diversity among rotavirus isolates offers insight into the evolution of these strains which can occur based on point mutations, inherited reorganization and reassortment, and interspecies spread[24-26]. Despite the advent of rotavirus vaccination in most countries globally, circulating rotavirus strains tend to be more diverse, thereby enhancing the prevalence of non-vaccine strains. This eventually impairs vaccine effectiveness towards circulating strains, with much lower vaccine efficacy[27].Using the surveillance and distribution of predominant rotavirus genotypes in some Asia-Pacific countries (Table 1) may assist in understanding the pattern of spread and concentration of pathogenic rotavirus genotypes currently circulating in Samoa and other PICTs.This could further help explicate the efficacy and effectiveness of rotavirus vaccines during the pre- and post-vaccination periods.

Table 1. Distribution of predominant human rotavirus genotypes in some Asia-Pacific countries at pre- and post-vaccination era.

3.2.2. Significance of improved rapid diagnostic testing and surveillance networks against rotavirus infections

Laboratory diagnosis of rotavirus infection is achieved using various conventional and molecular techniques. Enzyme immunoassays(EIAs) are used as the standard diagnostic test for rotavirus infection in many parts of the world[55]. Numerous polymerase chain reaction(PCR)-based protocols for the uncovering of human enteric viruses with higher sensitivities have been published, but only a few allow simultaneous detection of most enteric viruses in one assay, especially during viral outbreak screening and surveillance activities[56,57]. This is essentially vital to understand the disease burden associated with viral gastroenteritis caused by rotavirus and other enteric viruses, which may be unknown and currently circulating in Samoa.

Furthermore, studies to solve hypotheses on diagnostic interventions and concerns surrounding their effectiveness in providing reliable and accurate data should be pursued. The potential benefits would help avail the challenges of misdiagnoses and under-diagnoses of diarrheagenic rotavirus infections in situations of outbreak cum community transmission. Clinical diagnoses and testing for rotavirus in Samoa are carried out at the major tertiary health centre-Tupua Tamasese Maeole Hospital (TTM Hospital), which is located in the center of the Capital City. Testing or baseline assessment for rotavirus infection is rarely done in remote regions, where laboratories have insufficient resources and limited human and medical capacities. In developing countries like Samoa, rapid serological EIAs may be the only available laboratory choice of investigation. Though reliable,this may not provide complete information on viral load, and will have low sensitivity and specificity, unlike molecular methods for rotavirus detection[58,59]. Molecular assays like rapid multiplex PCR,quantitative RT-PCR and RT-PCR platforms have been documented to have better performance than EIAs and conventional PCR, due to better detection of PCR products and reduced ambiguity in negative and positive samples[58,59]. Improved molecular and diagnostic techniques for virus’ genomic characterization and personal training are much needed in containment measures for the rotavirus epidemic in Samoa. Despite immunization against the rotavirus,future investigations into circulating rotavirus genotypes in Samoa is pertinent and will assist in evaluating post-vaccination outcomes and measuring vaccine effects. Provision of prompt diagnostic services is imperative in curbing the spread of the virus through laboratory surveillance, pathogen identification and confirmation. Hence,concerted efforts are required by all health stakeholders involved in public health prevention of enteric diarrheagenic diseases and rotavirus infections, to create functional systems and networks for syndromic and laboratory surveillance in specific locations in rural and suburban communities in Samoa, where there is little or nonexisting accessible screening facilities.

3.2.3. Upscaling and preventive role of rotavirus vaccination

Interventions with proven ability can only be effective when necessity warrants their accessibility. To maintain practical sustainability, aggregated efforts toward investment and ongoing acceptance of vaccination should be channelled to timely delivery of vaccination materials. Undoubtedly, the effectiveness of rotavirus vaccines has offered huge benefits in pediatric and adult populations susceptible to diarrheagenic rotavirus disease. In geographically isolated communities which are culturally diverse and sensitive such as Samoa, huge challenges face the surveillance, effectiveness and safety assessment of vaccine-preventable disease[60]. Sensitization on rotavirus vaccination for both adults and children could assist in preventing early infection transmission, early death, drastically reduce rotavirus morbidity and confer herd immunity within the communities. Certain studies had revealed that children who did not receive a second dose of the rotavirus vaccine suffered 3.96 times more from diarrheal morbidity compared to those in receipt of the second dose of the rotavirus vaccine[56]. Health regulations on child vaccination should be firm on compliance to avoid unwarranted complications from diarrhea morbidities. Thus, two-dose rotavirus vaccines (doses 1 and 2) should be given to children as part of a comprehensive approach to control diarrhea[61]. Studies on the safety and efficacy of rota-vaccines administered in Africa and Asia revealed the vaccines dramatically reduced severe diseases among infants in developing countries, where a majority of rotavirus-related deaths occurred[62,63], thereby overrating the effectiveness of RV1,RV5 and Rotavac vaccines to be safe at preventing diarrhea[64]. In Fiji, the introduction of rotavirus vaccines helped reduce confirmed gastroenteritis admissions at the main referral hospital by 87% amongst young infants[60]. There was an 81% reduction in case fatality from cause associated diarrheagenic patients and a decline of 89% of the outpatient burden of rotavirus gastroenteritis[60].Another study by Jenney et al. reported huge reductions in rotavirus confirmed diarrhoea in both hospital inpatients and outpatients in children below age of five years following the introduction of the rotavirus vaccine on a national scale. Likewise, there were demonstrable reductions in severity (81% fall in mortality), the total burden of rotavirus (above 80% decline) and all-cause diarrhoea(36% decline) amongst children. The mortality rate was further decreased from all cause-specific diarrhea admissions in those age groups, who were not eligible for vaccination[65]. This could be as a result of high, full-dose vaccine coverage and lower rates of malnutrition and gut enteropathy[57]. Replicating similar preventive interventional models in Samoa could help to halt the surge of a rotavirus outbreak and its absolute eradication. It may also rapidly reduce the incidence of community transmission and potential spread of the virus across borders of Samoa and neighbouring countries,as seen in other developed and developing regions of the world,with positive outcomes following the recommendation to introduce the rotavirus vaccines[66]. Although rotavirus-associated diarrhoea could be prevented with rotavirus vaccine or treated with lowosmolarity oral rehydration salt (ORS) and zinc, a lack of awareness of effective preparedness strategies towards diarrhoea prevention and management could lead to late presentation of ill children to the clinic and poor adherence to prescribed interventions[67].Additionally, low supply of rotavirus vaccines, under vaccination and challenges associated with lack of transparent government policies amongst others may come to bear in mitigating containment measures, awareness and upscaling vaccination towards the rotavirus disease in Samoa.

3.3. Public health preparedness: Public awareness and health education for communities

In Samoa, the rotavirus vaccination (Rotarix) for children is provided by the Ministry of Health at no cost, and the schedule includes two doses administered at 6 weeks and 10 weeks along with Penta 1, PCV1, PCV 2 and Penta 3. However, despite the vaccination implementation, there is a great need for public awareness via billboards, social media (TV, radio, Facebook, Instagram, etc.),community campaigns and education on the effects of the virus on infants and children. Low coverage rates are currently a public health challenge in Samoa, since vaccination was offered to children under five and half months, and parents had little information about the virus, thereby, resulting in vaccination hesitancy amongst parents.

A study on the knowledge of rotavirus conducted in Italy discovered that, though the majority of participants (89%) had agreed with the statement that the rota-vaccine was not harmful, among those who did not immunize their children, a large proportion reported they were not willing to obtain vaccination mainly due to lack of knowledge on the disease and concerns of side effects[68]. This emphasizes the importance of public health awareness and education towards at-risk populations, especially those with misconceptions regarding vaccinations, to eradicate their uncertainties about safety.Similarly, a mother’s lack of education may increase the risk for the development of diarrhea in her children, thus an educated mother is more likely to be empowered to take care of her offspring[69].Previous studies had also shown children of highly educated mothers were at low risk of cause-specific morbidity and mortality due to diarrhea because they had the necessary knowledge and observed good hygiene and sanitation practices[64,66,70]. This further explains the importance of health education in creating public awareness regarding disease prevention at both household and community levels. Moreover, improving sanitation and water quality provided a beneficial advantage for reducing diarrheal disease in low-income countries[67]. Different systematic analytic studies on the prevention of diarrheagenic rotavirus disease have shown campaigns on handwashing reduced the incidence of gastrointestinal infections by 30%(95% CI 19%-43%) [68].

Furthermore, studies had revealed positive associations between breast milk and the prevention of rotavirus disease. Breast milk contains special nutritious and bioactive compounds, which are known to boost immunity in infants. Exclusive breastfeeding for four months and partial breastfeeding thereafter are linked with lower rates of acute gastroenteritis in the first year of life[69]and decreased rates of hospitalization from the diarrheal disease[67]. A study by Shumetie et al. also depicted the odds of diarrheal morbidity were 2.69 times higher among under-five children who were not exclusively breastfed for six months[33]. Essentially, introducing health policies to tactically address vaccination challenges are germane in disease prevention and surveillance. A systematic and adoptable contextual framework could drastically help in reducing rotavirus epidemics in unvaccinated populations (Figure 1).This should be modeled to suit the population’s health literacy,communal way of living and socio-behavioural standards. Huge expectations bequeath on policymakers, including non-governmental and community-based organizations in creating support and efficient health systems to ensure enforcement, accountability and sustainability of preventive programs for collective health benefits.Implementation of strategies on rotavirus vaccination as discussed and previously studied may be pertinent in bridging the lapses,hitherto disease spread, case detection and management as well as surveillance of rotavirus in Samoa.

Figure 1. An adoptable conceptual framework for public health community and socio-preventive mechanism against the spread of rotavirus infection in a developing society.

4. Conclusions

The introduction of rotavirus vaccination in Samoa is a good achievement and has provided an opportunity for the government,community-based organizations and other stakeholders to reevaluate and address gaps in the health system. Implementing effective rotavirus vaccination programs, encouraging good sanitation and hygiene, hand-wash practice, exclusive breastfeeding and improving the quality of water would help to reduce childhood diarrheal morbidity in the country. However, due to the impact of environmental dynamics on virus antigenic variations or mutations and the resultant effects on the effectiveness of rotavirus vaccines,continuous monitoring of rotavirus disease burden and strain distribution in Samoa must be prioritized. Further scientific-based evidence should be carried out on the effectiveness of public health education and awareness of associated risk factors, safety and program preparedness on rotavirus infection in Samoa and other PICTs.

Conflict of interest statement

All authors have no conflict of interest to declare.

Authors’ contributions

L.O.O and V.Y conceptualized and wrote the initial version of the study. L.O.O, V.Y and A.E designed and coordinated the study.L.O.O, V.Y and A.E searched and designed the images. L.O.O, V.Y and A.E performed literature search, wrote the article and contributed to the final version of the manuscript.