The epidemiology of non-viral gastroenteritis in New Zealand children from 1997 to 2015: an observational study

Acute gastroenteritis is a common illness and a substantial cause of hospitalization in previously healthy young children. In their first three years of life, almost all children will experience at least one episode of acute gastroenteritis [1]. Most cases are self-resolving and do not require treatment, however, older people and young children are at an increased risk of complications. Morbidity due to gastroenteritis is greatest in children aged younger than five years [2].

A diverse range of pathogens are implicated in childhood gastroenteritis including viruses, bacteria and protozoa. Viral infections, and rotavirus in particular, account for the greatest burden of gastrointestinal disease in young children worldwide [3]. In December 2009, the World Health Organization (WHO) recommended that all infants should be routinely immunized to prevent rotavirus disease [4]. The rotavirus vaccination was introduced into the New Zealand (NZ) national schedule in 2014. This has led to a significant reduction in the incidence of viral gastroenteritis in NZ children [5]. Studies reporting the epidemiology of pediatric gastroenteritis in NZ have focused largely on rotavirus and other viral pathogens [5, 6]. There are no published studies reporting on the epidemiology of non-viral gastroenteritis in NZ children.

The total burden of disease due to foodborne and waterborne gastrointestinal infection in NZ is high. There are an estimated 4.17 to 5.16 million cases of acute gastroenteritis annually, and the incidence of disease in the community is estimated at 1.11 episodes per person per year [7, 8]. NZ has a notifiable disease monitoring system whereby certain communicable diseases for which investigation and public health action are required are notifiable to the local Medical Officer of Health. Diseases may be made notifiable by the Ministry of Health (MoH). This may be to allow prompt public health action, such as the provision of prophylaxis to contacts (eg. Meningococcal disease), to allow for environmental investigation of potential sources (eg. food and water borne diseases) or to monitor the incidence of vaccine preventable diseases (eg, mumps, measles, rubella). Some diseases are also notifiable as part of NZ’s commitment to implementation of the International Health Regulations (eg. Yellow Fever, Middle Eastern Respiratory Syndrome (MERS)).

Data on notifiable diseases are reported to The Institute of Environmental Science and Research (ESR) for disease surveillance and monitoring on behalf of the NZ MOH. ESR is one of ten NZ Crown Research Institutes (CRI) established in 1992, after the reorganisation of the Government-owned Department of Scientific and Industrial Research (DSIR) and science units from the Department of Health. As well as carrying out research, it is also responsible for surveillance and reporting of notifiable diseases in NZ. The list of notifiable disease in NZ can be found at https://​www.​health.​govt.​nz/​our-work/​diseases-and-conditions/​notifiable-diseases [9]. Notifiable bacterial pathogens include Campylobacter, Shigella, Salmonella, Yersinia and verotoxin-producing or shiga toxin-producing enterotoxigenic Escherichia coli (ETEC), and notifiable protozoal pathogens include Giardia and Cryptosporidium. Campylobacter has been notifiable since 1980, ETEC since 1993, and all other pathogens since at least 1996 (Table 1).

Surveillance data for NZ adults suggest the incidence of notifications for bacterial gastroenteritis is decreasing over time; a trend that has been particularly evident since the mid-2000s [10]. The incidence of protozoan illness has remained static over time [10]. Campylobacter is the most frequently identified gastrointestinal pathogen, followed by nontyphoidal Salmonella and Giardia [11]. Campylobacter is the most frequently notified gastroenteric disease in NZ and accounts for at least 35% of all notifiable disease reports (158.9 cases per 100,000 in the population in 2016) [10]. Campylobacter is also frequently implicated in outbreaks of disease, some of which have been large. For example, a recent outbreak of Campylobacter illness caused by contamination of drinking water occurred in Havelock North, NZ in August 2016, during which 5500 of the town’s 14,000 residents were estimated to have become ill with the disease [12].

The NZ health system is predominantly publicly-funded with services provided by public, private and nongovernmental sectors. The country is divided into twenty District Health Boards (DHB's) that are responsible for the planning and funding of health services for their geographical areas. Primary healthcare (including general practitioners) is free for all children aged 13 years and under and is subsidized for residents and citizens. Tertiary-level care (hospitals) is free-of-charge for all and there is no requirement for private healthcare insurance. The health status of the NZ population overall is high, however, there are significant inequalities in the health of Māori, the indigenous people [13].

Acute gastroenteritis affects children in greater numbers than adults [14], however, systematic analysis of the impact of non-viral gastroenteritis in NZ children has not been reported previously. The aim of this study was to determine the burden of disease due to non-viral gastroenteritis in NZ children by describing trends in hospital admissions and disease notifications from 1997 to 2015.

This is the first study in NZ to analyze longitudinal data on childhood gastroenteritis caused by non-viral pathogens. The trend towards a decline in both notifications and hospitalizations for most non-viral pathogens included in this study is reassuring. Most of these pathogens are predominantly foodborne, and the observed decline may have been contributed to by changes in food safety, such as food industry standards relating to food handling and general hygiene, as well as increased consumer awareness of food safety [24]. The decline may also have been contributed to by changes in the food production sector, including farming, such as increased mechanization and more stringent monitoring of food safety indicators.

Consistent with several other international studies [25‐27], Campylobacter was identified as the pathogen associated with the majority of notifications and hospitalizations. Hospitalization rates increased and decreased in parallel with notification rates, thus it is unlikely these results are artefactual. Our results are consistent with trends observed in the adult population in NZ, in which notification rates for Campylobacter peaked in 2006 (> 380 per 100,000) and were lowest in 2008 (161.5 per 100,000) [10].

Between 2004 and 2008, and most notably between 2006 and 2008, there was a reduction in Campylobacter notifications that was consistent across all age groups. This reduction coincided with the introduction of a range of voluntary and regulatory interventions to reduce Campylobacter contamination in poultry [28]. In late 2006, the NZ Food Safety Authority (formerly part of the Ministry of Agriculture and Fisheries - now the Ministry for Primary Industries) released guidance aimed at reducing the incidence of poultry-associated foodborne Campylobacter disease. This was in response to research that indicated poultry contributed disproportionately to the incidence of Campylobacter disease in NZ [28, 29]. Interventions included the development and implementation of microbiological surveillance activities and increased reporting. The observed reduction in Campylobacter incidence in children seen in this study provides evidence of the positive effects of a food safety measure on child health. Whilst these findings are encouraging, there is some suggestion from our analysis that Campylobacter notification rates may have plateaued since 2008. This may, in part, be attributable to recent outbreaks, which have been water, rather than food-borne, or other changes such as the increasing popularity of the consumption of raw milk. This observation warrants purposeful surveillance.

Nontyphoidal salmonellae are also common bacterial pathogens associated with acute gastroenteritis in children [26, 30] and the leading cause of childhood bacterial enterocolitis requiring hospitalisation [31]. Although the food safety interventions mentioned above were targeted predominantly at Campylobacter, they may also have served to reduce the incidence of disease due to nontyphoidal Salmonella, which is also commonly transmitted via poultry. The observed reduction in the incidence of nontyphoidal Salmonella between 1997 and 2016 (as for Campylobacter) supports this hypothesis.

Unlike for nontyphoidal Salmonella, the rates of notification and hospitalization for Salmonella typhi were very similar. This finding is not surprising given that infection with Salmonella typhi is more likely to present with severe disease requiring hospitalization.

The number of notifications of ETEC infection increased steadily after 1997, reaching a peak of 16 cases per 100,000 in the population across all age groups in 2016. This increase may, in part, be due to changes in laboratory testing practices over that period, with increasingly sensitive assays and algorithms used for the detection of Escherichia coli (E. coli) [32] It could also have been contributed to by improvements in surveillance due to increased public health concern [32]. However, the increased rates of notification and hospitalization in the under one and 1–4 year age groups compared to those > 5 years are notable. Jaros et al. (2014) reported that the highest rate of E. coli infections in their national prospective case-control study of confirmed cases of Shiga toxin-producing E. coli in NZ occurred in the 1–4 year age group. The risk to children was increased further if there was a family member in contact with animals other than household pets. That study provides some support for the contention that the higher rates of disease in babies and children under 5 years of age found in our study is unlikely to be accounted for by changes in laboratory testing practices in those ≤4 years of age.

Exposures to farming environments have been reported as risk factors of sporadic ETEC infections, particularly in young children [33, 34]. Sheep and, in particular, cattle, are considered an important reservoir for ETEC and are the primary source of foodborne and environmental outbreaks in humans [32]. Our study observed higher rates of ETEC infections in DHB regions with more intensive dairy farming compared to those DHB regions with less intensive dairy farming (Additional file 1: Figure S1).

Māori children had lower notification rates for disease when compared to non-Māori children. This is an unexpected finding. A previous study has reported that risk for morbidity due to infectious disease is higher in Māori compared to non-Māori, and also that infectious disease incidence in Māori has risen considerably over time, resulting in pronounced gradients of disease inequality [35]. However, a lower incidence of Campylobacter in Māori adults has been reported previously [8, 36]. Despite Māori people being more likely to live in farming regions [37], their incidence of notified Campylobacter disease does not correspond with the higher rates seen overall in these areas. Disparities in Māori access to health care are well documented and may be contributing to the lower rates of notification in this population [38]. In order for notification to occur, children must present to a health care provider and be tested. Hence, the results observed could be due to lower rates of both presentation and subsequent testing.