The South African 2017-18 human listeriosis outbreak is the deadliest in recorded history, tragically resulting in over 200 deaths with hundreds more made seriously ill. Sterling Crew reviews listeriosis, the epidemic and its management control measures.
Listeriosis
Listeriosis is an infectious disease caused by the intracellular pathogenic bacterium Listeria monocytogenes. The main route of acquisition of L. monocytogenes is through the ingestion of contaminated food. Most listeriosis cases are sporadic and infections are domestically acquired. Listeriosis can cause severe illness, including neonatal infection, severe sepsis and meningitis-type symptoms, sometimes resulting in lifelong ill-health and even, in 15-30% of cases, death[1]. In most people however, listeriosis has no symptoms – the clinical feature in healthy people has been described as asymptomatic carriage or it only causes mild symptoms, such as high temperature, nausea, vomiting and diarrhoea for a few days. Particularly vulnerable groups, such as neonates, pregnant women, the elderly and the immunocompromised, are advised to avoid high risk foods, which include ready-to-eat (RTE) delicatessen meat, ready-to-eat meat and other RTE products, such as soft (non-matured) cheeses and cold smoked fishery products[2].
Listeriosis is a relatively rare disease with 0.1 to 10 cases per million people per year, depending on the socioeconomic demographic and the region of the world. The average probability of a single L. monocytogenes CFU to cause illness in a host will reflect the host susceptibility and the virulence of the strain. Although the number of cases of listeriosis is relatively small compared to other food-borne pathogens, the high hospitalisation and mortality rates associated with the infection make it a significant public health problem. The Food Standards Agency has issued guidelines for consumers on how to avoid listeria (Figure 1).
L. monocytogenes grows and reproduces inside the host’s cells and is one of the most virulent food-borne pathogens. The infective dose varies with the strain and with the susceptibility of the host. The first documented case of listeriosis was in 1924 and its first link to transmission by food was as recent as 1981. The incubation period can vary from three to 91 days[3].
Although the number of cases of listeriosis is relatively small compared to other food-borne pathogens, the high hospitalisation and mortality rates associated with the infection make it a significant public health problem.
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The challenge
L. monocytogenes is a gram-positive, rod-shaped, facultative anaerobe, which does not produce endospores, i.e. it is vegetative. In food it is killed (6-log reduction) by thermal processing to an equivalent of 70°C for 2 minutes. L. monocytogenes is quite hardy and robust by comparison with other bacterial species. It has been widely recognised as a very important hazard in the food industry for more than 30 years. Its ability to grow at temperatures below 0°C permits multiplication at typical refrigeration temperatures. It also survives deep freezing at -18°C. It is tolerant to osmotic stress, acidic conditions and high concentrations of salt. It can be found widely distributed in the environment in soil, water, vegetation and the faeces of some animals.
Its ubiquity means L. monocytogenes has a multitude of potential environmental sources and routes to gain access to food facilities and subsequently to cross-contaminate products. It may be spread throughout a food site by personnel, inadequately controlled food flows and processs design, contaminated surfaces, improperly managed equipment, brines, cooling water, condensate and aerosols. It forms highly resistant biofilms on food contact surfaces and non-food contact environmental surfaces. L. monocytogenes can persist despite aggressive cleaning and sanitisation and be present for months and even years in some factories, harboured in cracks and crevices. In particular, it can become established and persist in drains[4]. Clearly normal cleaning and sanitisation practices are often not enough to eradicate L. monocytogenes. Persistence of L. monocytogenes in food processing facilities is generally accepted to be the major source of RTE food contamination. Therefore, RTE foods must be prepared to high care standards throughout the food supply chain[5]. This should include:
• Good Agricultural Practice (GAP) at the farms • Good Hygienic Practice (GHP)
• Good Manufacturing Practice (GMP)
• Hazard Analysis Critical Control Point (HACCP)
• Prerequisite programmes for processing and temperature control during distribution including retail stages
• Manufacturing standards coupled with an effective sampling programme to monitor efficacy of hygiene measures and provide feedback for improvement.
RTE food must carry appropriate clearly labelled usage instructions as storage conditions after retail are critical. Research in the European Union indicates that one third of listeriosis cases in the EU are due to:
• growth of L. monocytogenes in the consumer phase of a product’s life, including from cross-contamination by unpackaged foods in the refrigerator,
• inadequate storage temperatures,
• not following use-by dates, cooking or reheating instructions.
Due to the long incubation period for listeriosis, it can be difficult to retrospectively identify food which was the source of an infection or outbreak.
L. monocytogenes can persist despite aggressive cleaning and sanitisation and be present for months and even years in some factories, harboured in cracks and crevices.
July 2017
The South African National Institute for Communicable Diseases (NICD) noted an increase in laboratory-confirmed cases of listeriosis with an unusually high number of neonatal infections.
5th December 2017
A listeriosis outbreak was declared by the Minister of Health, Dr Aaron Motsoaledi.
4th March 2018
The Ministry of Health announced that the source of the outbreak was RTE-processed meat products manufactured at Enterprise Foods Polokwane, Limpopo production facility. The National Consumer Commission issued the implicated manufacturers with safety recall on polony and other RTE processed meats. Polony is often eaten by low income communities and sold by street vendors, making distribution difficult to track, trace and recall.
24th April 2018
The business confirmed that independent laboratory re-testing, which it had commissioned, had identified the presence of L. monocytogenes ST6 strain in its product and processing environment.
3rd July 2018
By this time a further 82 facilities producing RTE meat products had been inspected by NICD Incident Management Team members (IMT), who carried out site inspections and took environmental swabs. The number of laboratory-confirmed reported cases per week had declined since the implicated products were recalled (Figure 2) with a total of 87 cases reported since 5th March 2018, according to figures published on 26 July 2018.
Table 1 Timeline for establishing and responding to the South African listeriosis outbreak
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The South African outbreak
Cases of human listeriosis sporadically occur around the globe every year. The recent South African outbreak in 2017-18 is the world’s largest recorded human listeriosis incident and has tragically resulted in 216 deaths to date[6]. The outbreak has been running at a reported 28.6% fatality rate. At least 92 children have died since it began, more than 80 of whom were under two years of age. Neonates of 28 days and under are the most affected age group, followed by adults aged between 15 and 49 years. Most of the reported cases, as expected,
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Strain typing for epidemiology
Fera Science. fera.co.uk
are people who have higher risks for a severe disease outcome.
It is noted that 1060 laboratory-confirmed cases were reported from all provinces between 1st January 2017 to 26th July 2018. Previously on average there were 60 to 80 laboratory-confirmed listeriosis cases per year reported in South Africa. The majority of cases have come from three provinces: 59% from Gauteng, 13% from Western Cape and 77% from KwaZulu-Natal, with the remaining cases coming from the other provinces.
The timeline for establishing the listeriosis outbreak is shown in Table 1. The implicated polony was a popular, widely consumed RTE processed meat product, which had been exported to 15 countries: Angola, Botswana, Democratic Republic of the Congo, Ghana, Lesotho, Madagascar, Malawi, Mauritius, Mozambique, Namibia, Nigeria, Swaziland, Uganda, Zambia, and Zimbabwe. A number of these countries lack reliable disease surveillance systems and diagnostic tools, making it difficult to identify any subsequent listeriosis infections. Assistance with surveillance has been offered by the World Health Organization. Twelve of the countries have recalled the implicated processed meat products and banned further imports. The facility owned by Enterprise Foods, a subsidiary of Tiger Brands, the South African food giant, is now facing a class action lawsuit. Repairing the damage to the brand and rebuilding consumer trust and confidence will be challenging.
Despite the actions taken, cases could still persist due to the relatively long incubation period of listeriosis. Also, despite the public recall, some products might not have been totally removed from the supply chain and consumers’ homes. Subsequent cross-contamination from contaminated products could also pose a threat. Cross-contamination onto other processed meats could have occurred in shops and in homes. Consumers who stored recalled products in their fridges have been encouraged to disinfect them with diluted bleach.
The investigation
Whole genome sequencing (WGS) was carried out on isolates from infected patients. WGS allows more rapid identification of the food source of listeriosis outbreaks by linking L. monocytogenes strains isolated from patients with those isolated from implicated foods and production sites, thus, establishing stronger links between listeriosis patient cases and causative foods. WGS is a laboratory test that genetically fingerprints an organism by determining the complete DNA sequence. L. monocytogenes has a chromosome size of approximately 3 million base pairs. The genome of reference strain EGD-e has 2,944,528 base pairs with 39% GC (guanine-cytosine content)[7]. L. monocytogenes is notoriously hard to test for in the factory environment as it is not homogenously distributed in food and can also be hidden in the most obscure crannies and nooks in food factories.
The latest report by the South African National Listeria IMT concluded that 91% of the strains were identified as L. monocytogenes Sequence Type 6 (ST6) – the identical sequence type as was identified in the implicated RTE polony processed meat. This is also the same strain that was isolated at Enterprise Foods Polokwane production facility. Disturbingly, different strains of L. monocytogenes were also identified in the facilities of other food manufacturers during the countrywide food surveillance testing programme instigated by NCID. These businesses have also recalled products, which along with the 9% of different strains present in the infected patients might indicate that more than one outbreak is occurring.
Further actions and conclusions
Listeriosis was made a notifiable medical condition in South Africa in December 2017 and new regulations governing General Hygiene Requirements for Food premises, the Transport of Food and Related Matters were published. Measures to raise awareness amongst key stakeholders in the food chain, especially RTE suppliers, vulnerable groups, authorities and district environmental health practitioners, are being implemented. Education in safe food handling is a key measure for the prevention of listeriosis. A dedicated listeriosis website has been created. The World Health Organization has created a social media package in the 13 locally spoken languages to help raise overall awareness on listeriosis and to help tackle public concerns in relation to the ongoing outbreak.
The NICD has reiterated the World Health Organization’s core messages from its Five Keys to Safer Food Manual[8].
• Keep clean
• Separate raw and cooked
• Cook thoroughly
• Keep food at safe temperatures
• Use safe water and raw materials.
The NICD IMT has developed an emergency response plan to manage what is hopefully the end of this tragic listeriosis outbreak. It aims to reinforce systems to strengthen future prevention and to highlight early detection of any human listeriosis outbreaks. All clinical isolates received at NICD are undergoing WGS. The use of WGS has proved a key epidemiological diagnostic tool and the NICD is planning to use it for regular epidemiological surveillance to improve the prevention and detection of outbreaks.
Sterling Crew FIFST, FCIEH, FRSPH
Managing Director, SQS Ltd. Strategic Advisor, Shield Safety Group. Chair of the IFST Food Safety Group. Independent Scientific Advisor and Board member of Campden BRI. Audit Governance Board member Eurofins
Efsa-Ecdc (2014). The European Union Summary Report on Trends and Sources of Zoonosis, Zoonotic Agents and Food-borne Outbreaks in 2012. EFSA Journal 12, 3547-3312. doi: doi10.2903/j.efsa.2014.3547.
2. World Health Organization. Listeriosis. Fact sheet. February 2018.
3. Goulet, V., King, L.A., Vaillant, V., and De Valk, H. (2013). What is the incubation period for listeriosis? BMC Infect Dis 13, 11. doi: 10.1186/1471-2334-13-11.
4. Codex Alimentarius Commission. Guidelines on the application of general principals of food hygiene to the control of Listeria monocytogenes in foods. CAC/GL 61 – 2007.
5. USDA Food Safety and Inspection Service Compliance Guideline: Controlling Listeria monocytogenes in Post-lethality Exposed Ready-to-Eat Meat and Poultry Products January 2014.73.
