Norovirus Infections and Disease in Lower-MiddleandLow-Income Countries, 1997⁻2018

Abstract

Noroviruses are a major cause of viral gastroenteritis. The burden of the norovirus in lowresourcesettings is not well-established due to limited data. This study reviews the norovirusprevalence, epidemiology, and genotype diversity in lower-middle-income countries (LMIC) andin low-income countries (LIC). PubMed was searched up to 14 January 2019 for norovirus studiesfrom all LIC and LMIC (World Bank Classification). Studies that tested gastroenteritis cases and/orasymptomatic controls for norovirus by reverse transcription-polymerase chain reaction (RT-PCR)were included. Sixty-four studies, the majority on children <5 years of age, were identified, and 14%(95% confidence interval; CI 14-15, 5158/36,288) of the gastroenteritis patients and 8% (95% CI 7-9,423/5310) of healthy controls tested positive for norovirus. In LMIC, norovirus was detected in 15%(95% CI 15-16) of cases and 8% (95% CI 8-10) of healthy controls. In LIC, 11% (95% CI 10-12) ofsymptomatic cases and 9% (95% CI 8-10) of asymptomatic controls were norovirus positive.Norovirus genogroup II predominated overall. GII.4 was the predominant genotype in all settings,followed by GII.3 and GII.6. The most prevalent GI strain was GI.3. Norovirus causes a significantamount of gastroenteritis in low-resource countries, albeit with high levels of asymptomaticinfection in LIC and a high prevalence of coinfections.

Keywords: GII.4; genotype diversity; lower‐middle‐income countries; low‐income countries; norovirus; systematic review.

Figure 1

The study selection flow diagram.

Figure 2

The world map indicating the low-income countries (LIC; dark blue) and lower-middle-income countries (LMIC; light blue) that are represented by the norovirus studies. The average norovirus prevalence and 95% confidence interval (95% CI) is indicated for each country. Countries are identified by two-letter International Organization for Standardization (ISO) codes, and the study references are indicated in brackets. AO, Angola [23]; BD, Bangladesh [28,29,37,38,39]; BO, Bolivia [40]; BT, Bhutan [41,42]; BF, Burkina Faso [20,27,43]; CI, Cote d’Ivoire [44]; CM, Cameroon [26]; KH, Cambodia [45]; EG, Egypt [46]; ET, Ethiopia [47,48]; GE, Georgia* [49]; GH, Ghana [50,51]; IN, India [52,53,54,55,56,57,58,59,60,61,62,63,64,65]; ID, Indonesia [66,67]; KE, Kenya [68]; MG, Madagascar [69]; MA, Morocco [70,71]; MW, Malawi [72,73]; MD, Republic of Moldova* [49]; NP, Nepal [22,74]; NG, Nigeria [75,76]; NI, Nicaragua [21,77]; PG, Papua New Guinea [78]; PK, Pakistan [79,80]; RW, Rwanda [81]; SD, Sudan [82]; TZ, Tanzania [83,84,85]; TN, Tunisia [86,87,88]; UA, Ukraine* [49]; VN, Vietnam [24,89,90,91,92,93,94]; YE, Yemen [95]; ZM, Zambia [96]. (https://d-maps.com/carte.php?num_car=13181&lang=en). *Includes data from studies that screened pathogen-negative stool specimens for norovirus.

Figure 3

An overview of the norovirus coinfections from 26 studies in 15 LMIC countries and six studies in four LIC countries: Twelve studies tested for norovirus and rotavirus; 12 studies tested for a range of enteric viruses; five studies tested for viruses and bacteria; and three studies tested for viruses, bacteria, and parasites.

Figure 4

(a) The distribution of norovirus capsid genotypes detected in six LIC between 1997 and 2013; (b) the distribution of norovirus capsid genotypes circulating in 14 LMIC between 1990 to 1994 and 1998 to 2015. The years in which the studies were conducted are indicated in parenthesis after each country. NA = not assigned a GI genotype.

Figure 5

The distribution of norovirus GII.4 variants in (a) LIC (5 countries, 9 studies, and 167 typed variants) and (b) LMIC (14 countries, 25 studies, and 945 typed variants) between 1997 and 2015. The GII.4 variant was determined based on partial capsid genotyping.