Received: 21 August 2019 Revised: 12 October 2019 Accepted: 19 October 2019 DOI: 10.1111/jfs.12732

ORIGINAL ARTICLE

Overview of listeriosis in the Southern African Hemisphere—Review

Adeoye J. Kayode1,2 | Etinosa O. Igbinosa3 | Anthony I. Okoh1,2

1Applied and Environmental Microbiology Research Group (AEMREG), Department of Abstract Biochemistry and Microbiology, University of Listeriosis is rarely reported in the Southern African Hemispheres in spite of the Fort Hare, Alice, South Africa increasing rate of Listeria in several foodborne outbreaks reported in advanced coun- 2SAMRC Microbial Water Quality Monitoring Center, University of Fort Hare, Alice, tries. This paper reviews the emerging trends in the spread, distribution, and epidemi- South Africa ology of Listeria species in foods, water, human, animals, and different environments 3Department of Microbiology, Faculty of Life Sciences, Private Mail Bag 1154, University of in Southern Africa based on the appraisal of scholarly articles. In this regard, informa- Benin, Benin City, Nigeria tion obtained from literatures from various online databases revealed that Listeria

Correspondence species are commonly recovered from food, water, and human samples. Fewer arti- Adeoye J. Kayode, Applied and Environmental cles provided information on Listeria recovered from animals (ruminants) and soil Microbiology Research Group (AEMREG), Department of Biochemistry and samples. Generally, reports of studies were more focused on Listeria monocytogenes Microbiology, University of Fort Hare, Private among other Listeria species. To this end, reports obtained from literature on the Mail Bag X1314, Alice 5700, South Africa. Email: [email protected] method of identification of Listeria were mostly based on serological, classical bio- chemical methods and the principle of aesculin hydrolysis, usually characterized by Funding information The World Academy of Sciences, Grant/Award black coloration on selective media for Listeria. These methods may not be reliable, Number: 110811; National Research as they could sometimes give a false positive report. Therefore, molecular methods Foundation of South Africa; South African Medical Research Council are more reliable, accurate, could show the genetic relationship between isolates, and at the same time capable of enabling tracking the source of this pathogen should be embraced as a better substitute for the identification of Listeria in Southern African sub-region.

1 | INTRODUCTION that they are catalase positive, oxidase negative, and ferment carbohydrates (Orsi & Wiedmann, 2016; Rods, 2014). Listeria is a bacterial genus, of the family Listeriaceae, made up of Listeria genus used to composed of six species which are: L. mono- gram-positive members that are short rods with a round end (Orsi & cytogenes, L. ivanovii, L. seeligeri, L. grayi, L. welshimeri, and L. innocua; Wiedmann, 2016). Usually, they appear as singular cells, short chains, all of which are mostly adapted to water, soil, and vegetation (Hawker and sometimes filamentous (Gelfand, 2012; Rods, 2014). They are fac- et al., 2018; Linke et al., 2014). Recently, a subspecies, and novel ultative anaerobes (Bortolussi, 2008), non-acid fast bacteria, non- species, usually isolated from foods, environmental niches in spore forming, and without capsule (Sleator, Watson, Hill, & Gahan, different parts of the world, as well as the natural and agricultural 2009). Listeria species possess peritrichous flagella, which are respon- milieu, were introduced to the genus, and includes: L. marthii, L. sible for their typical “tumbling” motility when grown at 20 to 25C weihenstephanensis, L. booriae, L. fleischmannii subsp. coloradonensis; (Rods, 2014). When cultivated on blood agar, the colonies are non- novel species such as L. floridensis, L. aquatica L. cornellensis, L. pigmented and may show resemblance to those of β-hemolytic strep- grandensis, L. riparia, L. fleischmannii, and L. newyorkensis (Abay et al., tococci (Gelfand, 2012). Their biochemical characteristics revealed 2019; Barre et al., 2016; Bertsch et al., 2013; Weller, Andrus,

This is an open access article under the terms of the Creative Commons Attribution-NonCommercial License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes. © 2019 The Authors. Journal of Food Safety published by Wiley Periodicals, Inc.

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Wiedmann, & Bakker, 2015). These 11 new Listeria species were et al., 2019; Ghanbari, Jami, Domig, & Kneifel, 2013; Jami et al., regarded to be non-pathogenic to humans on the basis of not having 2014). However, they can be easily destroyed at cooking tempera- major genetic traits in their genomic elements hence; Listeria genus tures (Chan & Wiedmann, 2008). currently has 17 species (Orsi & Wiedmann, 2016). In spite of the increasing listeriosis rate reported in several foodborne outbreaks globally (Desai, Anyoha, Madoff, & Lassmann, 1.2 | Transmission of Listeria 2019; Siegman-Igra et al., 2002) such as Europe, Germany, France, Japan, New Zealand, U.S.A. (Botsaris, Nikolaou, Liapi, & Pipis, 2016; Transmission of Listeria spp. (80–90%) is primarily by (fecal-oral route) Halbedel et al., 2019; Marus, 2019), China (Wang et al., 2013), consuming contaminated foods and water (den Bakker, Manuel, Canada (Hanson et al., 2019), it is not commonly reported in the Fortes, Wiedmann, & Nightingale, 2013; Jarvis, O'Bryan, Ricke, John- Southern African hemisphere. This study articulates an overview of son, & Crandall, 2016; Linke et al., 2014). However, they can also be emerging trends in the spread, distribution, and epidemiology of transmitted between humans (from mother to fetus both in per- Listeria species in foods, water, human, animals, and different environ- ipartum and utero following maternal bacteremia). Other uncommon ments in the Southern African countries. This review, evaluates schol- possible modes include infected animals to humans resulting in skin arly articles obtained from various online databases such as Google lesions among veterinarians and nosocomial transmission (Abay et al., Scholar, Pubmed, and Scopus. The search keywords used to access 2019; Goenka & Kneen, 2019; Nelson, Warren, Tomasi, Raju, & articles online includes phrases such as “isolation of Listeria species, Vidyasagar, 1985). Transmission of Listeria from animal to human and Listeria species in Southern Africa, Listeriosis and global outbreaks.” its circulation in the environment is presented in Figure 1. Search keywords like “Listeria species in South Africa” Listeria species The disease conditions associated with Listeria infection could be in Angola” and so on were also employed to source for articles for categorized into non-invasive (febrile listerial gastroenteritis) and inva- each of the Southern African countries (Angola, Botswana, Lesotho, sive (infection caused at sterile part of the body such as the blood, Malawi, Namibia, South Africa, Swaziland, Zambia, and Zimbabwe). liver, cerebral fluid) listeriosis (Bhat et al., 2013; Data, 2015; Zhu, Goo- Searches were extended to source for more articles on Google, due to neratne, & Hussain, 2017). Non-invasive listeriosis manifests less fewer articles indexed by the databases previously searched. There- severe symptoms like fever, diarrhea, headache, and muscle pain fore, this article further described the ecological distribution, transmis- (myalgia) which occur after a short incubation period and is often sion, treatment, control, and occurrence of Listeria of species in food, associated with ingestion of a high dose of the pathogenic Listeria food processing environment, water, animal, and human. species by healthy persons (FSAI, 2011; WHO, 2018) as reported in the case noninvasive listeriosis (Halbedel et al., 2019). Invasive listeri- osis affects immunosuppressed individual including cancer patients, 1.1 | Ecological distribution of Listeria pregnant women, acquired immunodeficiency syndrome (AIDS) patients, young and elderly persons (Desai et al., 2019). It is usually Species of Listeria have a wide distribution in the environment and have characterized by the severity of symptoms and high death rate com- been recovered from dust, vegetation, decaying materials, soil, water, monly associated with gastroenteritis, meningitis, pneumonia, septice- sewage, animal feeds, silage, and natural habitats (Barre et al., 2016; mia, and spontaneous abortion (Arslan & Baytur, 2019; Chersich, Sheng, Tsai, Zhu, & Zhu, 2019; Weller et al., 2015). They are often pre- Scorgie, Rees, & Wright, 2018; FSAI, 2011; Vázquez-Boland et al., sent in foods gotten from plant and animal sources, and are constantly 2001). The infectious dose of Listeria may vary with the susceptive found in environments where food is processed (Aalto-Araneda, host and the strain causing infection (FSAI, 2011; Pouillot et al., Lunden, Markkula, Hakola, & Korkeala, 2019; Kaczmarek, Avery, & Sin- 2016). The approximate value of 106–107 CFUs (colony forming units) gleton, 2019). Listeria may also be found in processed foods due to is considered as the infectious dose of L. monocytogenes in humans chances of contamination that may occur after processing or when and primates, however a lower dose of 104 can cause listeriosis in per- inadequate heat treatment is used (US FDA, 2019). Domestic as well as sons with compromised immune as in the case of the outbreak associ- wild mammals like: fowls, sheep, dog, and cattle are popularly known ated with butter in Finland (Drolia & Bhunia, 2019). On the other reservoirs of this pathogen (Abay et al., 2019). Humans most especially hand, FAO/WHO (2004) estimated 107–109 CFU as the infectious abattoir and laboratory workers may also be asymptomatic fecal carriers dose for healthy persons and 105–107 CFU for high risk individuals of these pathogens (Heymann, 2004). and the lethal dose value (LD50) derived from the animal model for Listeria has a unique ability to thrive within −7to45C tempera- human listeriosis is 1.9 × 106 CFU. Due to the lack of a uniform ture range (Ramaswamy et al., 2007; Sosnowski, Lachtara, benchmark on the exact value of infectious dose of this pathogen, the Wieczorek, & Osek, 2019). The most preferred temperature for FSANZ (2014) report stated that “Listeria monocytogenes should not growth is usually 37C but may also grow slowly at low temperatures be found in ready-to-eat food that support the growth of this Listeria around 0C (Jami, Ghanbari, Zunabovic, Domig, & Kneifel, 2014). Con- (not detected in 25 g) and a maximum value of 100 cfu/g for ready- sequently, they can proliferate in contaminated foods during refrigera- to-eat food that will not support its growth. This limit was aimed to tion (US FDA, 2019). Listeria can grow in diverse environments with remedy the high death rate among vulnerable groups often associated conditions like low pH, low water activity, and high salinity (Abay with listeriosis outbreak. KAYODE ET AL. 3of22

FIGURE 1 Circulation and disease conditions caused by Listeria

1.3 | Listeria pathogenicity Radoshevich & Cossart, 2018; Schmid et al., 2005; Vázquez-Boland et al., 2001). Figure 2 gives the illustration of the process of host cell Some Listeria species are pathogenic and are responsible for diseases invasion, and the virulent factors involved. called listeriosis - an infection that results from eating of foods that Furthermore, some other virulence genes apart from the viru- are contaminated with Listeria (Linke et al., 2014). The major virulence lence gene cluster were found distributed within the Listeria genome. factors commonly found to be responsible for Listeria main steps of These are an integral part of the multigene lineage called internalins intracellular infection/pathogenicity were found encoded on a six (Kim et al., 2018). These genes encode extracellular proteins con- gene cluster of about 9 kb long (Schmid et al., 2005; Vilchis-Rangel, sisting of a different fraction of 22 leucine-rich amino acid long del Rosario Espinoza-Mellado, Salinas-Jaramillo, Martinez- Peña, & repeats (LRRs). They were discovered in some Listeria species such as Rodas-Suárez, 2019). This gene cluster is also called LIPI-1 (Listeria Listeria monocytogenes (Kim et al., 2018; Lingnau et al., 1995; Pathogenicity Island) or the prfA gene cluster (Gouin, Mengaud, & Raffelsbauer et al., 1998), Listeria ivanovii (Engelbrecht et al., 1998a; Cossart, 1994; Johnson et al., 2004; Kreft, Vazquez-Boland, Altrock, Engelbrecht et al., 1998b) and L. innocua. A few of the internalins is Dominguez-Bernal, & Goebel, 2002; Linke et al., 2014). This same vir- required to invade the host cells of mammals (Dramsi, Dehoux, ulence gene cluster has been reported to be similar to those present Lebrun, Goossens, & Cossart, 1997; Kim et al., 2018). Among these, in L. ivanovii and L. monocytogenes but L. seeligeri possess a more com- is the invasion-associated protein gene (iap) responsible for retaining plex and detailed cluster containing about five extra virulence genes. the invasion phenotype in mouse fibroblast, macrophages and hepa- In most cases, Listeria contains genes which encode for: the transcrip- tocytes. This gene also acts as murein hydrolase essential for the tional or positive master regulator (prfA) of most known genes; two appropriate cell division (Hess et al., 1995; Johnson et al., 2004; phospholipases (plcA and plcB) which enhance lysis of the host cell Wuenscher, Köhler, Bubert, Gerike, & Goebel, 1993). Listeria seeligeri, membranes. Also, the hemolysin or pore-forming sulfhydryl-activated L. ivanovii,andL. monocytogenes harbor Listeria pathogenicity island listeriolysin (hly) required for bacterial evasion from the host cells' gene (LIPI-1) responsible for Listeria virulence (Gouin et al., 1994; phagosomes and into the host cytosol. In addition to this virulence Kim et al., 2018; Linke et al., 2014). Listeria ivanovii is most especially gene cluster, is the metalloprotease (mpl) gene needed for extracellu- pathogenic to ruminant animals (Linke et al., 2014). Nevertheless, this lar activation and proper maturation of plcB and a surface protein species was also reported to cause listeriosis in AIDS patients and (actin assembly capability) actA gene is responsible to power Listeria abortion case in sheep (Ryu et al., 2013). Listeria ivanovii has a unique movement within host cells. This gene (actA) in combination with the pathogenicity island (LIPI-2) that codes for phosphocholinesterases products of plcB and mpl enable Listeria cell to cell spread (Dramsi, for the efficient usage of phospholipids in the red blood cell of rumi- Lebrun, & Cossart, 1996; Pizarro-Cerdá, Kühbacher, & Cossart, 2012; nants (Linke et al., 2014) and may explain why they are susceptible to 4of22 KAYODE ET AL.

FIGURE 2 Listeria host cell invasion and intracellular cycle. Adapted and modified from Pizarro-Cerdá et al. (2012)

L. ivanovii infection (González-Zorn et al., 1999). Listeria mono- 1.4 | Epidemiological significance of Listeria cytogenes is a pathogen for both animal and human; it is usually the bacterium popularly known to cause listeriosis (Linke et al., 2014). The pattern of Listeria epidemiology is usually characterized by spo- Listeriosis can result in severe illness in pregnant women, infants, and radic cases of occasional or major invasive listeriosis outbreaks immunocompromised adults; it may cause gastroenteritis in severely (Reimer et al., 2019; Thomas, Strachan, Goodburn, Rotariu, & infected individuals (Buchanan, Gorris, Hayman, Jackson, & Whiting, Hutchison, 2012). These pathogens are of a serious public health 2017; Kim et al., 2018; Muchaamba, Eshwar, Stevens, von Ah, & threat because of their ubiquity, ability to survive diverse environmen- Tasara, 2019). However, L. ivanovii and L. seeligeri cause illnesses in tal conditions (FSAI, 2011), disease severity, and a high case of the human (Cocolin, Rantsiou, Iacumin, Cantoni, & Comi, 2002). L. fatality rate (Drolia & Bhunia, 2019; Vázquez-Boland et al., 2001). In innocua is sometimes found in encephalitis case in ruminant animals this regard, there is the need for a better knowledge of the link (Walker, Morgan, McLauchlin, Grant, & Shallcross, 1994). The results between the epidemiological patterns of Listeria from various sources, obtained from the histopathological studies using animal infection including the food processing environment (Jami et al., 2014). Source model, have usually been the basis of understanding the pathophysi- tracking of listeriosis has been enabled by employing phenotypic and ological process of human and animal listeriosis (Buchanan et al., genotypic characterization of Listeria (Wagner & Allerberger, 2003) to 2017; Vázquez-Boland et al., 2001). Regardless of the fact that con- their various serotypes for rapid detection of listeriosis outbreak dur- taminated food serves as the primary source of this pathogen in spo- ing epidemiological investigations (Graves & Swaminathan, 2001; radic and epidemic cases (Stratakos et al., 2019), the major entry Koudelka, Gelbícˇová, Procházková, & Karpíšková, 2019). This is partic- route of Listeria pathogen into the susceptible host is usually through ularly important during long-term surveillance of human listeriosis par- the gastrointestinal tract. The estimated period for the clinical mani- ticularly in the food industry where Listeria has become a cause of festation of gastroenteritic listeriosis begins at about 20 hr after con- concern within the food chain (Aalto-Araneda et al., 2019). This char- suming foods contaminated by the pathogen (Dalton et al., 1997; acterization has indeed provided a more reliable way of specifically Schlech III, 2006). However, longer incubation periods (ranging from identifying and tracing the strain(s) involved in an outbreak and others 1–67 days) were observed in human invasive listeriosis cases that were not involved. The basis for serotyping Listeria species is by (Buchanan et al., 2017; Halbedel et al., 2019). Similar duration of identification of the flagella (H) and somatic (O) antigen (Donnelly, incubation was described in cases of invasive and gastroenteric dis- Baigent, & Briggs, 1988). Listeria monocytogenes strains have more eases in animals (Buchanan et al., 2017). Considering the ubiquity of elaborate classification unlike strains of other Listeria species thus, Listeria in the environment which may impact the chance of a likely 12 serotypes/serotypes (½a, ½b, ½c, 3a, 3b, 3c, 4a, 4b, 4c, 4d, 4e, and increased rate of contaminating raw and processed foods, the annual 7) were described by (Seeliger & Höhne, 1979; Morobe, Obi, Nyila, incidence of human listeriosis is still at a minimum of about 2–8spo- Matsheka, & Gashe, 2012) and 13 serotypes described by some radic cases per million population (Jacquet et al., 1994; Rocourt, scholars, including serotype (4ab) in their classifications (FDA, 2011; Jacquet, & Reilly, 2000) and a 15.6% fatality rate in the EU Girgin & Çadirci, 2019; Graves, Swaminathan, & Hunter, 2007; (Buchanan et al., 2017). Nevertheless, a higher annual incidence of Jacquet, Gouin, Jeannel, Cossart, & Rocourt, 2002; Muchaamba et al., 10.9 and and 14.7 per million population were reported (Goulet & 2019). Three strains of Listeria innocua (4ab, 6a, and 6b); a strain of Brohier, 1989; Nolla-Salas et al., 1993). Listeria ivannovi; two strain of L. seeligeri (½b and 4ab) and three KAYODE ET AL. 5of22 strains of L. welshimeri (½b, 4c, and 6a) serovars were reported by clavulanic acid. However, the resistance of Listeria species to (Doumith et al., 2005; Jin et al., 2012; Shen et al., 2017; Zeinali, antibiotics such as ampicillin, cephalosporins trimethoprim, and Jamshidi, Bassami, & Rad, 2016). nitrofurantoin have also been reported (Olaniran, Nzimande, & Mkize, The virulence expressed by strains of this species may be depen- 2015). This may be attributed to the development of bacterial resis- dent on serotype, with serotypes ½a, ½c, ½b, and 4b in most cases tance to antimicrobials as a result of bacteria evolution or drug misuse implicated in cases of human listeriosis (Abay et al., 2019; Kathariou, by humans and in animal husbandry (Charpentier, Gerbaud, Jacquet, 2000) among these; serotypes ½a, ½b, and 4b are mostly clinical iso- Rocourt, & Courvalin, 1995). Multidrug-resistant strains of Listeria lates. Most strains of the serotype 4b (not commonly found in food) monocytogenes were recovered from the environment, food and have been reported in cases of major invasive listeriosis outbreaks human listeriosis cases (Charpentier et al., 1995). This pathogen was and serovar ½a strains in sporadic listeriosis outbreak (Kathariou, reported to be resistant to antibiotics such as ampicillin, erythromycin, 2000; Muchaamba et al., 2019). Strains of serovar ½c are commonly gentamicin, kanamycin, penicillin, sulfonamide, streptomycin, tetracy- found in food (Jacquet et al., 2002; Yildirim et al., 2004). In this regard, cline oxacillin, nalixidic acid, chloramphenicol, cefuroxime sodium, there tends to be appreciable evidence that epidemic serotypes 4b clindamycin, ceftriaxone, and trimethoprim-sulfa-methoxazole (Abay demonstrate specific virulence biomarkers and also possess unique et al., 2019; Charpentier & Courvalin, 1999; Jamali et al., 2015; Jiang genetic markers (Liu et al., 2006; Yildirim et al., 2004). So far, a few et al., 2017; Sosnowski et al., 2019). numbers of well-known L. monocytogenes strains were used for viru- lence study (Vázquez-Boland et al., 2001). Listeria monocytogenes were categorized into four distinct genetic 2 | OCCURRENCE OF LISTERIA IN WATER, lineages (I, II, III, and IV) based on phylogenetic investigations. Each FOOD, FOOD PROCESSING ENVIRONMENTS, lineage is made up of certain serotypes. Lineage I comprised of (½b, HUMAN, AND ANIMALS 3b, 4b, 4d, 4e, and 7); lineage II (½a, ½c, 3a, and 3c); lineage III (4b, ½a, 4a, and 4c); and lineage IV (4a, 4c) serotypes (Haase et al., 2014). Line- 2.1 | Water as a reservoir of Listeria species age I serotypes (½b and 4b) have been found in nearly all cases where human listeriosis outbreaks were described. Nevertheless, lineage II The relative abundance of Listeria in water could be attributed to run- serotype (½a) has also been reported in some listeriosis outbreaks off from land, vegetation, food-processing environments, dump sites, (Seeliger & Höhne, 1979; Cruz, Pitman, Harrow, & Fletcher, 2014; and sewage discharge into water bodies (Jami et al., 2014; Thomas Jami et al., 2014; Tamburro, Sammarco, Fanelli, & Ripabelli, 2019). et al., 2012) and animal droppings. These were characteristic of the South African Plankenburg Berg and Eerste rivers often used for irri- gation. The rivers were frequently polluted by sewage, refuse, poten- 1.5 | Treatment of Listeria infections tially pathogenic microorganisms from the river bank dwellers running off into the river from rainfall. The studies by Lotter (2010); Britz et al. Treating Listeria infections may be challenging as the pathogen is (2013) confirmed the presence of Listeria monocytogenes, Listeria capable of invading nearly all cell types (Dhama et al., 2015). In light ivanovii, Listeria grayi, Listeria innocua, and Listeria welshimeri isolated of this, effective treatment using appropriate antibiotics is essential. from these rivers. Likewise, Huisamen (2012) also isolated Listeria Only penicillin, amoxicillin, ampicillin in combination with gentamicin monocytogenes, Listeria ivanovii, Listeria grayi and Listeria seeligeri in his or aminoglycoside has been the common choice of treatment studies on these rivers and his report revealed a direct link in the inci- (Carvalho et al., 2019; Goenka & Kneen, 2019; Temple & dence of Listeria species and the pollution of the rivers. This, also, Nahata, 2000). Although, alternative Second-line agents such as sulfa- agrees with the argument of (Chigor, Sibanda, & Okoh, 2013; methoxazole or trimethoprim, vancomycin, erythromycin, and the Ijabadeniyi & Buys, 2012; WHO, 2004) that most farmers irrigate their fluoroquinolones may be administered to some patients at a certain crops using water from wells, close ponds, streams or rivers, and state of disease or those who are allergic to ampicillin and gentamicin dams; the majority of which are of poor quality for irrigation. The out- (Carvalho et al., 2019; Temple & Nahata, 2000). Generally, Listeria come of the investigations of Odjadjare, Igbinosa, and Okoh (2011); species isolates were described to be susceptible to wide varieties of Okoh et al. (2012) and Olaniran et al. (2015) on the microbial quality antibiotics but not cephalosporins, erythromycin, fosfomycin, strepto- of wastewater effluent also revealed the presence of Listeria mono- mycins, and tetracycline (Charpentier & Courvalin, 1999). Troxler, Von cytogenes and Listeria ivanovii. This agrees with the reports that Graevenitz, Funke, Wiedemann, and Stock (2000) in his experiment Listeria is able to survive disinfection and other processes of wastewa- also reported that all known Listeria species were sensitive against ter treatment Odjadjare et al. (2011). In this regard, this suggests that aminoglycosides, tetracycline, (except oxacillin), cefalor, cefazoline, effluents of wastewater treatment discharged into fresh water bodies cefotiam, carbapenems, cefoperazone, chloramphenicol, dalfopristin/ may compromise the water quality for human use. This may also play quinupristin, glycopeptides, lincosamides, and rifampicin. Abay et al. a crucial role in the epidemiology of this pathogen in the aquatic (2019) and Sosnowski et al. (2019) also observed that Listeria was sus- milieu (Czeszejko, Boguslawska-Was, Dabrowski, Kaban, & Umanski, ceptible to ampicillin, penicillin G, amoxicillin, erythromycin, gen- 2003; Odjadjare, Obi, & Okoh, 2010; Paillard et al., 2005) and may tamycin, streptomycin, vancomycin, sulfamethazole/trimethoprim and consequently result to severe public health consequences, most 6of22 KAYODE ET AL. especially in Southern African region where a larger number of the prepared salads (bean sprouts, coleslaw) and vegetables (FSAI, 2011). populace rely on natural water bodies for agricultural and domestic Listeria can thrive better than some other foodborne pathogens in purposes (Chigor et al., 2013; Venter et al., 2004; WHO, 2015). foods preserved under refrigeration that were initially contaminated during preparation (Abay et al., 2019; Heymann, 2004; US FDA, 2019). Soft cheese is often regarded as of high risk food for listeriosis 2.2 | Food and food processing environments as a owing to the fact that soft cheese are usually kept refrigerated and reservoir of Listeria species the pathogen may increase in number to a significant level during refrigeration (Buchholz and Mascola, 2001; FSAI, 2011). Also, this Listeria has been reported in various foodborne outbreaks (Table 1) in pathogen has also been found in ready-to-eat foods. Nyenje, advanced countries (Halbedel et al., 2019; Rocourt et al., 2000; Odjadjare, Tanih, Green, and Ndip (2012) described Listeria spp. as the Siegman-Igra et al., 2002) with little information on cases from devel- highest percentage of pathogens (22%) recovered from foods oping countries like the Southern African sub-region. This pathogen obtained in Alice, Eastern Cape Province, South Africa. Manani, Col- has constituted threat in the food industry and may pose serious pub- lison, and Mpuchane (2006); Lambrechts (2011); Shiningeni et al. lic health implications due to their capability of surviving most routine (2018) recovered Listeria monocytogenes from food samples in their food processing conditions (Law, Ab Mutalib, Chan, & Lee, 2015; studies, but the report of Mosupye and von Holy (1999) negates their Møretrø, Fanebust, Fagerlund, & Langsrud, 2019). Also, Listeria can observation as no Listeria species were found in his studies on street form biofilms, which are more resistant to sanitizing agents and disin- vendor ready-to-eat foods obtained in Johannesburg, South Africa. fectants on food processing contact surfaces such; as polystyrene and Furthermore, Strydom, Bester, Cameron, Franz, and Witthuhn (2013) stainless steels (Da Silva & De Martinis, 2013; Silva, Camargo, isolated Listeria monocytogenes from a South African avocado Todorov, & Nero, 2017; Skowron et al., 2019; Välimaa, Tilsala- processing facility; Christison, Lindsay, and Von Holy (2008) also iso- Timisjärvi, & Virtanen, 2015). However, cross contamination after pas- lated Listeria monocytogenes associated with food preparation plat- teurization or processing of food may also occur (Jadhav, Bhave, & forms in retail delicatessens shops in Johannesburg, South Africa. Palombo, 2012; US FDA, 2019). Reports from Christison et al. (2008) and Strydom et al. (2013) con- Foods often associated with human listeriosis comprised those firmed that cross contamination or biofilms formation after pasteuri- which have a long shelf-life under refrigeration; support the growth of zation or processing of food may also occur (Jadhav et al., 2012; US Listeria species and foods that are consumed without listericidal treat- FDA, 2019) in a food processing environment. Also, Lues, Theron, ments, like cooking (Aalto-Araneda et al., 2019; Bremer, Fletcher, & Venter, and Rasephei (2007) examined the microbial make-up of bio- Osborne, 2003; Desai et al., 2019; FSAI, 2011). Examples of impli- aerosols of a chicken-slaughtering facility in the Free State province, cated foods include poultry, meat, and fish products (frankfurters, fer- South Africa, and their report further confirmed the ubiquity of this mented raw meat sausages, smoked salmon, ready-to-eat meat); pathogen. However, products of dairy, vegetables, and some other products of dairy (raw milk, unpasteurized milk, soft cheeses); and ready to eat foods are not exempted from contamination of Listeria

TABLE 1 Foodborne outbreaks in some high resources countries

Number of cases Food type Country Year Listeria serovar(s) with deaths Reference Quargel Austria/Germany, 2009/2010 ½a strain 34 (8) Fretz et al., Czech Republic 2010 Cantaloupe US 2011–2012 Strains ½a and 146 (31) CDC, 2011 ½b Fresh cheese Spain 2012 ½a strain 2 de Castro et al., 2012 Ricotta salata cheeses 14 US states 2012 — 20 (4) CDC, 2012 Dairy products California and Maryland 2014 — 8 (1) CDC, 2014 Cured/cold-smoked salmon Denmark/France 2015–2017 — 1 (1) Schjørring et al., 2017 Caramel apple 12 US states 2014–January 4b 35 (7) CDC, 2015 2015 Frozen vegetables 4 US states 2012–2016 — 9 (3) CDC, 2016 Johnston County hams 2 US states 2018 — 4 (1) CDC, 2018 Deli-sliced meats and cheeses 4 US states 2019 — 8 (1) CDC, 2019 Rice pudding from a single local Germany 2015 Serogroup 4b, 163 (0) Halbedel et al., catering service ST2 clone 2019 KAYODE ET AL. 7of22 species. In addition, Morobe et al. (2012) reported the recovery of on March 4th, 2018 (National Institute for Communicable Diseases, Listeria monocytogenes while assessing the microbiological safety of 2019a). Following the 2017-2018 outbreak, 87 laboratory confirmed cheese, raw vegetables, salads, and raw milk obtained from Gaborone listeriosis cases and 21 deaths were also recorded from September Botswana. Similarly, Msalya (2017) also stated a higher percentage of 2018 to September 2019 (National Institute of Communicable Dis- L. monocytogenes, L. innocua, L. ivanovii above the required safety level eases, 2019b). This could suggest the presence and possible persis- for human consumption from a greater number of raw milk samples tence of Listeria species in the environment. Table 4 gives more obtained from three regions of Morogoro, in Tanzania. In order to jus- details of Listeria species in water food and food processing tify the potential of Listeria species to proliferate at low under refrig- environment. eration, Van Nierop et al. (2005) recovered L. monocytogenes from frozen chicken obtained from supermarkets and street vendors in Gauteng province, South Africa. Recently, the National Institute for 2.3 | Listeriosis in human Communicable Diseases reported about 1,060 cases confirmed by laboratories and 216 deaths, resulting from the listeriosis outbreak Human listeriosis in Southern African sub-region is gradually on the from all provinces across South Africa from January 1, 2017 to July increase. Sequence analysis of Listeria monocytogenes revealed that a 17, 2018 (Tables 2 and 3). The outbreak was traced to “Polony” predominant strain (ST6) was commonly found in an outbreak of (a South African ready-to-eat processed meat product) produced by a human listeriosis from 2017 to 2018 in South Africa (Smith et al., Polokwane food production facility. The number of weekly recorded 2019). Due to available information from literature, this cases declined drastically when the implicated product was recalled section focuses majorly on human listeriosis in South Africa. The first reported case of human listeriosis in this region was the case of a TABLE 2 Laboratory-confirmed listeriosis cases and deaths 55 year old European man from Swellendam, Western Cape province, available in all provinces at the end of listeriosis outbreak in South Africa in 1956. He was hospitalized and diagnosed with menin- South Africa from January 1 to July 17, 2018 (n = 1,060) gitis (Gant & McKenzie, 1956). Another death case of listeriosis attrib- Outcome available Number of No of uted to Listeria monocytogenes was reported in a newborn in (% of available deaths (% of cases (% of Zimbabwe (Nyati, 2000). Also, a 34 year HIV positive male patient Province(s) outcome) death) cases) was reportedly confirmed of dual infection of Streptococcus pneumo- Eastern 40 (4.96) 13 (6.02) 53 (5.0) nia and Listeria monocytogenes in Cape Town, South Africa Cape (Opperman & Bamford, 2018). In addition, Listeria monocytogenes Free State 32 (3.40) 9 (4.17) 36 (3.4) were found in blood samples of two neonates (a day old child) and a Gauteng 393 (57.93) 108 (50.00) 614 (57.93) 24 years old pregnant woman in 2015 during an increase in human Kwa-Zulu 76 (7.83) 21 (9.72) 83 (7.83) cases of this pathogen in the Western Cape of South Africa (Smith Natal et al., 2016a). Reports from scholars in the Southern African countries Limpopo 51 (5.19) 11 (5.09) 55 (5.19) justify that of others who had earlier reported the incidence of Listeria Mpumalanga 47 (4.53) 11 (5.09) 48 (4.53) species in humans from other parts of the world. In the same vein, Northern 6 (0.57) 3 (1.39) 6 (0.57) similar listeriosis disease conditions like fever, diarrhea, headache, and Cape muscle pain (myalgia), listeriosis in immunosuppressed persons, young North West 27 (2.74) 8 (3.70) 29 (2.74) and the elderly ones were reported by these scholars. The characteris- Western 134 (12.83) 32 (14.82) 136 (12.83) tic high death rate associated with gastroenteritis, meningitis, pneu- Cape monia, septicemia, and spontaneous abortion were also reported Total 806 216 1,060 (Buchholz and Mascola, 2001; Vázquez-Boland et al., 2001; Centre for Disease Protection, 2010; Food Safety Authority of Ireland, 2011;

TABLE 3 Age distribution and outcome of laboratory-conformed cases of listeriosis available at the end of listeriosis outbreak in South Africa from January1 to July 17, 2018 (n = 1,060)

Outcome pending available Number of deaths Age composition Discharge (% of death) (% of available outcome) (% of death) ≤28 days 242 (41.02) 108 (42.52) 93 (43.06) 1 month–14 years 44 (7.46) 16 (6.30) 9 (4.17) 15–49 years 201 (34.07) 81 (31.89) 52 (24.07) 50–64 years 48 (8.14) 23 (9.06) 30 (13.89) ≥65 years 47 (7.97) 16 (6.30) 29 (13.43) Age unknown 8 (1.36) 10 (3.94) 3 (1.39) TABLE 4 Occurrence of Listeria species in food, food processing environments and water in southern Africa 8of22

Prevalence of Listeria species by Food samples Country Isolation method sample type Overall prevalence Reference A total 99 samples of frozen Gauteng Province, USFDA, modified 19.2% L. monocytogenes 19.2% L. monocytogenes Van Nierop et al., 2005 chicken carcasses from South Africa supermarket and street vendors A total of 47 Vienna sausage, South Africa IDF Vienna sausage (4.3%) Ham 8.2% L. species: L. Vorster, Greebe, & Nortjé, 1993 43 ham, 44 Cervelat samples (14.0%) Cervelat (6.8%) welshimeri; L. grayi; L. innocua. A total of 140 environmental South Africa ND 64% L. monocytogenes 64% Strydom et al., 2013 samples from a food processing facility (conveyer belts, equipment, floors, food processor's hands, drains, boots, storage rooms, and cleaning facilities) A total of 25 floor mops and Johannesburg, South Africa ISO 11290-1 Plastic gloves (0%), cleaning 6% Christison, Lindsay, & Von Holy, 39 cleaning cloths, cloths (10.27%) and one floor 2007 20 disposable plastic gloves mop sample (4%) Listeria monocytogenes A total of 117 samples of Johannesburg, South Africa ISO 11290-1 L. monocytogenes found in RTE 4% Christison et al., 2008 assorted salads, filled food samples. 2 filled baguettes, serving utensils, baguettes and 1 salad. cutting boards and hands of handlers. Eighteen (18) L. monocytogenes Witwatersrand, AFLP reaction kit (PerkinElmer, L. monocytogenes, L. innocua ND Geornaras, De Jesus, Van Zyl, & 25 L. innocua isolates from South Africa Foster City, Calif.) Von Holy, 1995 poultry processing were recovered from carcasses, equipment surfaces and from the environment during the surveys of an abattoir A total of 17 soil samples Qwa-Qwa Region, Free Polymerase chain reaction, L. monocytogenes ND de Smidt, Smit, & Botes, 2015 State, South Africa sequencing (ABI Prism 3130 XL genetic analyzer) Vegetable samples and 55 Milk Bloemfontein, South Africa ISO 11290-1 (Milk) L. monocytogenes; (spinach, ND De Beer, 1998 lettuce, beans, and mushroom) L. monocytogenes, L. welshimeri, L. innocua, L. ivanovii KAYODE A total of 150 samples of dried Gauteng province, ISO 11290-1 1.33% L. monocytogenes 1.33% Naidoo, 2010 ready-to-eat meat (south South Africa African “biltong”) TAL ET

(Continues) . KAYODE TABLE 4 (Continued)

Prevalence of Listeria species by Food samples Country Isolation method sample type Overall prevalence Reference AL ET . A sum of 1,324 samples food Botswana Broth enrichment, cultured on Raw milk (1.08%), cheese 4.3% Morobe, Obi, Nyila, Gashe, & samples from street vendors modified Listeria agar (2.75%), frozen cabbage Matsheka, 2009 and Supermarkets (10.11%), meat (biltong) (0%), salad (7.41%) L. monocytogenes A total of 21samples of cheese, South Africa ISO 11290-1 Lean mince, Hamburger patty, 37% Gouws & Liedemann, 2005 ready-to-eat chicken and Salad, fish products, Cutting meat, raw meat/fish board L. monocytogenes products, dried fruit mixtures and spices A sum of 330 milk and cheese Rwanda ISO 11290-1 L. monocytogenes — Kamana, Ceuppens, Jacxsens, samples were obtained and Kimonyo, & Uyttendaele, 2014 investigated A total of 114 raw milk samples Tanga region, Northern ISO 11290-1 L. monocytogenes (42.1%), L. 55.1% Hyera et al., 2016 Tanzania innocua (11.4%), L. ivanovii (1.7%) A total of 45 samples from Gauteng Province, International Dairy Federation Dry powders, in 13% Listeria 13% Kunene, Hastings, & Von Holy, sorghum (dry powders, South Africa (IDF) 1995 monocytogenes 1999 fermented and cooked fermented porridge) A sum of 139 samples of food ISO 11290-1 23% Listeria species food 23% Lambrechts, 2011 contact surfaces at 8 food manufacturing plants. manufacturing plants. A sum of 396 samples of Gaborone, Botswana. FDA-BAM L monocytogenes 6(1.5%) and (15.2%) Letsholo, Loeto, Monthusi, & vendor ready-to-eat food 48(12.1%), 6(1.5%) recovered Wale, 2016 from protein, vegetable and starchy food samples respectively Samples of meats (ready-to-eat Windhoek, Namibia. ISO 11290-1: 1996 (Ready-to- 15% L. monocytogenes 15% Shiningeni, Chimwamurombe, beef and chicken) eat meats) Shilangale, & Misihairabgwi, 2019 Bioaerosol samples from Kroonstad, Free State Airborne microorganisms were L. Monocytogenes ND Lues et al., 2007 receiving, killing, province, South Africa. sampled by impaction on evisceration, defeathering, 55-mm Rodac agar plates packaging, air-chilling, and through a SAS super 90 air dispatch sampler (PBI Int., Milan, Italy) A total of 200 samples of Gaborone, Botswana ISO 11290-1 Corn, 4%, peas 2% and country 16% Manani et al., 2006 minimally processed frozen, crop, stir-fry 10% L. peas, corn, and a variety of monocytogenes

potato chips, of combined 9of22 vegetables (Continues) TABLE 4 (Continued) 22 of 10

Prevalence of Listeria species by Food samples Country Isolation method sample type Overall prevalence Reference RTE foodstuffs - apples, FDA-BAM L. monocytogenes ND Mogomotsi & Chinsembu, 2012 hotdogs, coleslaw, egg salads, meat salads, and polony

Raw vegetables (cabbage), Gaborone, Botswana FDA-BAM Out of 57 isolates, 3 cheese ND Morobe et al., 2012 meat (biltong), salads, (5.3%), 7 raw milk (12.4%), cheese, raw milk 20 (35.1%) and 27 biltong (47.4%), frozen cabbage (10.11%), and salads (coleslaw) 7.41% positive for L. monocytogenes respectively A total of 327 fresh milk Tanzania ISO 11290-1 28.6% L. monocytogenes, 17.2% L. 53.4% Msalya, 2017 samples obtained from innocua, 7.6% L. ivanovii Morogoro, coast, and Tanga region A total of 40 raw milk samples Kampala district, Uganda FDA-BAM 13% L. monocytogenes from raw 60% Mugampoza, Muyanja, Ogwok, milk and 3.0% locally Serunjogi, & Nasinyama, 2011 fermented dairy products A total of 50 of meat on Free State Province, Lovett et al., 1987, International 52% L. monocytogenes. 52% Nel, Lues, Buys, & Venter, 2004 conveyor belt before South Africa. Dairy Federation (IDF) 1995 vacuum-packaging Fresh-cut organic vegetables Zambia. IDF-14A, 1995 20% L. monocytogenes. 20% Nguz, Shindano, Samapundo, & produced in Zambia. Mixed Huyghebaert, 2005 vegetables (beans, carrots, baby corn, mangetout, chili Fresno, petty pan, peas and green beans) A sum of 180 spinach and Johannesburg, South Africa 24 hr enrichment at 37C, L. monocytogenes in 7.2% of 7.2% Plessis, Govender, Pillay, & cabbage samples and centrifuged cells extracted samples Korsten, 2017 9 street vendors food using the quick-g DNA Miniprep kit for presumptive confirmation by real-time PCRs using MALDI-TOF A total of 196 milk samples. Dar es Salaam and Lake ISO 11290-1 and 11290-2 L. seeligeri 1.8% (2 of 109) of raw 1.8% Schoder, Maichin, Lema, & Laffa, 109 raw milk, 46 samples of Victoria, northern milk samples. 2013 fermented products.4 Tanzania. KAYODE packed/open served heat- treated products, and

(Continues) AL ET . KAYODE TABLE 4 (Continued)

Prevalence of Listeria species by Food samples Country Isolation method sample type Overall prevalence Reference AL ET . A sum of 96 samples of street Windhoek, Namibia. ISO 11290-11996 Confirmation of presumptive L. 15% Shiningeni et al., 2018 vendors ready-to-eat chicken monocytogenes by gram (8) and beef (88) staining and biochemical tests Water final effluents East London, South Africa Method of Hitchins (2001) with From 56 presumptive, 1.8% L. 30% Odjadjare & Okoh, 2010 modifications. monocytogenes, 1.8% L. innocua, 19.6% L. ivanovii and 7.14% L. grayi Irrigation water from Cape Town, South Africa SABS ISO 11290-1 (1996) L. innocua, L. seeligeri, L. grayi and ND Alison, 2010 Plankenburg and Berg rivers L. ivanovii, L. monocytogenes, Plankenburg and Eerste Rivers Cape Town, South Africa SABS 11290-1 (1996) L. innocua, Listeria grayi, L. 83%, 67%, 92% at site Huisamen, 2012 welshimeri, L. monocytogenes 1, 2 and 3 respectively Plankenburg river Stellenbosch, Western Method of SANS 11290-1 L. monocytogenes, L. innocua, L. 56%, 51% 39% at site Britz et al., 2013 Cape (SANS, 2001) grayi, and L. ivanovii 1, 2 and 3 respectively Eerste River with the Stellenbosch, Western SABS 11290–1 L. grayi, L. ivanovii, L. ND Lotter, 2010 Plankenburg River Cape monocytogenes, L. seeligeri Berg River Stellenbosch region of the SABS 11290-1 L. grayi, Listeria ivanovii, L. ND Brand, 2012 Western Cape monocytogenes, Listeria innocua Irrigation canal from Mpumalanga, South Africa — L. monocytogenes not recovered Ijabadeniyi, Debusho, Loskopdam, vegetables from cauliflower Vanderlinde, & Buys, 2011 (broccoli and cauliflower Plankenburg and Eerste Rivers Stellenbosch, Western SABS ISO 11290-1, 1996) L. monocytogenes 53% Kikine, 2011 Cape Wastewater samples East London, Eastern Cape, The method of Hitchins (2001) L. monocytogenes, L. ivanovi ND Odjadjare et al., 2011 South Africa with modifications. Wastewater samples Nkonkobe Municipality The method of Hitchins (2001) L. ivanovii 60%, L. grayi 23%, L. ND Okoh et al., 2012 Eastern Cape, welshimeri 13%, L. seeligeri 3% South Africa Wastewater and river samples Durban KwaZulu-Natal, Standard membrane filtration L. monocytogenes 44% Olaniran et al., 2015 South Africa methods (incubate at 37C for 20 hr and 35C for 24–48 hr on Listeria chromogenic agar; Oxoid, UK 1o 22 of 11 TABLE 5 Occurrence of Listeria and human listeriosis cases in the southern African sub-region 22 of 12

Signs/length of Antibiotic used for Case prodrome Diagnosis Country Year Number of cases treatment Outcome Listeria species References

A 34-year-old HIV- Length of prodrome Gram-positive cocci and South Africa 2017 1 Ceftriaxone and Death within 7 days Listeria monocytogens Opperman & positive man with 3wks worsening small gram-positive azithromycin. Bamford, a bacteremia co- cough and dyspnea bacilli found in blood Ampicillin and 2018 infection of S. sample imipenem. Ampicillin pneumoniae and L. and cotrimoxazole monocytogenes with history of methamphetamine and cannabis

295 pregnant women Apparently healthy Cultured on 5% blood Mwanza, November Apparently healthy Ampicillin, penicillin, — 0.68% Listeria spp. Elawendy, sheep agar and Tanzania 2011– erythromycin, Abdelfattah, confirmed using May tetracycline and Nosier, & CAMP test 2012 clindamycin. One Gaber, 2011 isolate was resistant to cotrimoxazole

A 55 year old Meningitis Cultural methods and Swellendam, mid- November 1955 1 L. monocytogenes Patient was hospitalized L. European who animal bioassay. Western sensitive to on January 5, 1956 lived in Gram-positive bacilli province streptomycin, and recovery was Swellendam, found in the Cape, chloromycetin, uneventful cerebrospinal fluid South Africa ilotycin and culture terramycin but not to sulphatriad or penicillin

monocytogenes Gant & McKenzie, 1956 A newborn Source – Unknown — Zimbabwe 1990 Unknown — 100% mortality Listeria monocytogenes Nyati, 2000 Unknown

About 327 foodborne — Stool, water and food South Africa 2013–2017 Illness in 11, 155 — 49 (0.4%) deaths 1% Listeria Shonhiwa, outbreak samples were individuals; 8, 680 monocytogenes in Ntshoe, Essel, collected for analysis (78%), hospital visits stool samples (2/147) Thomas, & and 494 (4%) hospital and 3.0% Listeria McCarthy, admissions monocytogenes in 2019 food samples (4/132)

Two (2) neonates Bacteremia Blood culture. South Africa September 3 ——L. monocytogenes Smith et al., (1 day old) and a 2015 isolates 2016a 24 year old pregnant woman

Human cases of L. Listeriosis Whole-genome South Africa. 11 ——L. monocytogenes Smith et al., monocytogenes sequencing analysis 2016b involving 9 patients in Western cape 1Gauteng province and another 1 in eastern cape KAYODE (Continues) TAL ET . KAYODE TABLE 5 (Continued)

Signs/length of Antibiotic used for

Case prodrome Diagnosis Country Year Number of cases treatment Outcome Listeria species References AL ET

A 59 years old female Headache, dizziness, Test positive for blood Port Elizabeth, 2012 1 Telithromycin, Death L. monocytogenes Bateman, . having Listeria facial numbness, culture, cerebrospinal eastern moxifloxacin, Fredericks, brainstem hoarseness, fever fluid and brain biopsy cape, methylprednisolone Carr, & Britz, encephalitis (LBE) South Africa. 2015 with recent sinusitis

A 37 year old male Fever, ataxia, dizziness Test negative for blood Caledone, 2012 1 Amoxicillin, ceftriaxone, Alive L. monocytogenes Bateman et al., having Listeria culture, cerebrospinal Western ampicillin, acyclovir, 2015 brainstem fluid and brain biopsy Cape, rifampicin, isoniazid encephalitis with South Africa hypertension and diabetes mellitus

A 51 year old male Headache, nausea and Test negative for blood Paarl, Western 2012 1 Rifampicin, isoniazid, Alive L. monocytogenes Bateman et al., having Listeria vomiting, facial culture, cerebrospinal Cape ampicillin 2015 brainstem numbness, ataxia, fluid and brain biopsy encephalitis with worsening left HIV and ethanol dysmetria abuse

A 36 year old female Fever, dysphagia, Test positive for blood Kleinmond, 2012 1 Acyclovir, ceftriaxone, Death L. monocytogenes Bateman et al., having Listeria dysphagia, coma, culture, negative Western dexamethasone, 2015 brainstem quadriparesis cerebrospinal fluid Cape, ampicillin, gentamycin encephalitis with and negative brain South Africa. rheumatoid biopsy arthritis on immunosupp- ressant

A 25 year old male Headache, dizziness, Test negative for blood Villiersdorp, 2012 1 Ceftriaxone, Alive L. monocytogenes Bateman et al., having Listeria right facial palsy, culture, cerebrospinal Western dexamethasone, 2015 brainstem fever, drowsiness fluid and brain biopsy Cape, ampicillin encephalitis South Africa

A 32 year female Headache, dizziness, Test negative for blood Atlantis, 2012 1 Methylprednisolone, Alive L. monocytogenes Bateman et al., having Listeria hemisensory, right culture, cerebrospinal Western ceftriaxone, 2015 brainstem hemiplegia, gait ataxia fluid and brain biopsy Cape, trimethoprim/ encephalitis South Africa sulfamethoxazole, metronidazole, ampicillin

About 6 children and Pyrexial illness, focal Test positive for acute King Edward Over ten 9 Ampicillin, 8 deaths L. monocytogenes Lalloo, 3 adults neurological signs bacterial meningitis Hospital, 10 years chloramphenicol, Coovadia, and also positive for Durban, period trimethoprim/ Adhikari, & cerebrospinal fluid South Africa sulfamethoxazole, Poyiadji, blood cultures. gentamicin 1992 3o 22 of 13 14 of 22 KAYODE ET AL.

Zhangling, Jing, Yue, & Huanling, 2019). Furthermore, Listeria mono- identified due to their microscopic nature. Therefore, special skills and cytogenes was recovered from another 11 samples of human; 9 in the materials are required for the detection, identification, and control of Western Cape, 1 from the Eastern Cape and another 1 from Gauteng this pathogen in the environment. Province. The cluster of these cases initiated the use of whole- It is noteworthy to put several control measures into practice that genome sequencing for the studies of Listeria monocytogenes in would be effective for the control of this pathogen. Ensuring good South Africa (Smith et al., 2016b). Table 5 gives more information on sanitation practices in food processing industries is crucial to achiev- human Listeria cases in the Southern Africa region. ing this goal (Aalto-Araneda et al., 2019; Møretrø et al., 2019). Lack of extensive cleaning of food processing facilities may predispose food product to Listeria contamination (Aalto-Araneda et al., 2019). How- 2.4 | Listeriosis in animals ever, thorough regular cleaning at intervals, involving disassembling of food processing machines during cleaning was found to be more ade- Reports obtained on the occurrence of Listeria in animals from previ- quate to minimize the risk of Listeria contamination in food products ous studies in Southern African countries are few. According to Mur- than routing sanitation of processing machines after daily production. ray, Webb, and Swann (1926), the clinical manifestation of Listeria This is also applicable in food retail settings as it was found effective varies greatly and it occurs in a wide range of animals. He isolated in reducing the prevalence of Listeria in food facilities (Aalto-Araneda Gram-positive bacillus responsible for the death of a number of rab- et al., 2019; Etter et al., 2017; Hammons et al., 2017). Cleaning food bits and the same was confirmed after re-inoculating into rabbits, and processing areas during production may predispose food to contami- it produced dramatic symptoms characterized by mononuclear leuko- nation (Aalto-Araneda et al., 2019). Also, unhygienic movement of fac- cytosis. This microbe was named Bacterium monocytogenes due to no tory workers in food processing areas may increase the risk of available information in the literature similar to the microorganism. At contamination. Minimizing movements during production period the almost same time, Harvey Pirie in Johannesburg isolated a Gram- should be ensured at all times to prevent the risk of food contamina- positive bacterium while carrying out his studies on a fatal disease of tion especially in large food processing factories (Aalto-Araneda et al., veld rodents presenting necrosis as the major feature. This bacterium 2019; Clayton, Griffith, Price, & Peters, 2002; Hicks et al., 2004). Fur- Listerella hepatolytica was named in honor of Lord Lister (Gant & thermore, engaging several machines in food processing may increase McKenzie, 1956). Du Toit (1977) reported an outbreak of caprine lis- the risk of Listeria contamination in food products due to the fact that teriosis in 70 goats, 8 of the animals died in the darling District of the machines may harbor this pathogen (Aalto-Araneda et al., 2019; Western Cape, South Africa in 1975. Another outbreak of circling dis- Sheng et al., 2019). This, therefore, demands close monitoring of ease in ruminants (Listeria meningoencephalitis) credited to Listeria Listeria in such food industries. In addition, poor designs of food monocytogenes was reported in the Western Cape Province of processing facilities may hinder good hygiene practices (Vijayan, South Africa during winter and early spring where 10 deaths were Mork, & Giske, 2019). It is important to consider partitioning with the recorded in 275 sheep (Meredith, 1984). Reports from these scholars inclusion of appropriate access routes during design and construction indicated that the outbreak of listeriosis in ruminants may be more for the ease of possible control of Listeria pathogen in processing facil- pronounced during winter rainfall and early spring. This observation ities (Lunden, Autio, Sjöberg, & Korkeala, 2003; Rørvik, Skjerve, Knud- agrees with the reports of previous studies (Meredith & Schneider, sen, & Yndestad, 1997). 1984; Nightingale et al., 2005; Roels, Dobly, Sloovere, Geeroms, & Proper execution of disinfection is important for controlling Vanopdenbosch, 2009; Summers, 1995) that seasonal variation was Listeria in food processing facilities and in the environment. Moham- observed in the prevalence of Listeria monocytogenes (Chersich et al., med and Aziz (2019) found that upgrading the power of disinfectants 2018) on a cattle farm with most cases observed in late winter and such as quaternary ammonium compounds, Sodium hypochlorite, early spring. Although, Listeria ivanovii is mostly regarded as the spe- Virkon®S and hydrogen peroxide showed a strong bactericidal activity cies that causes listeriosis in ruminants while Listeria monocytogenes against Listeria. It is also necessary to put in place strategies tailored infect both animals and humans. This statement was not validated by to achieve the safety of foods and control of this pathogen when dis- the report of previous studies in Southern Africa as authors were not infectants are used. Likewise, some biologically active compounds able to isolate Listeria ivanovii in their studies. This may be due the (environmentally-friendly) from plants such as the essential oils (Gray fact that only the conventional (cultural and biochemical identification et al., 2018; Lloyd, Alvarado, McKee, & Berrang, 2010) of Lippia techniques) were used for their studies as it may be difficult to differ- sidoides, Pimenta pseudochariophyllus, and Thymus vulgaris were found entiate Listeria species by this method, unlike molecular methods. effective against Listeria. Lippia Sidiodes oil had complete bactericidal activity against Listeria biofilms at a high dosage, however a combina- tion of any two of the essential oils was found effective at a low dose 3 | PREVENTION AND CONTROL OF as the case of peracetic acid and Thymus vulgaris which was found the LISTERIA most potent among others (Vázquez-Sánchez, Galv~ao, Ambrosio, Glo- ria, & Oetterer, 2018). However the use of ultraviolet light, ultra-soni- Control of Listeria may be challenging due to their ubiquitous nature, cation, cold oxygen plasma and using organic acid under modified ability to survive stress, and their presence is usually not easily environment during packaging were found to be effective for KAYODE ET AL. 15 of 22 eliminating Listeria biofilms (Bhilwadikar, Pounraj, Manivannan, Gould, Hunter, Kucerova, & Jackson, 2018) are important measures for Rastogi, & Negi, 2019; Zhu et al., 2017). Bacteriocins (nisin and pedi- consideration to achieving excellent Listeria prevention and control. ocin) were studied by various scholars and were found to be active against Listeria in food processing industries (Castilho, Colombo, de Oliveira, Todorov, & Nero, 2019; Gray et al., 2018). Also, cellulase, 4 | FUTURE RESEARCH CONSIDERATIONS protease, and lipase enzymes possess the potential to stop biofilm for- mation (Galiè, García-Gutiérrez, Miguélez, Villar, & Lombó, 2018). The safety of food is becoming one of the major concerns in food Other methods like the use of enzymatic disruptors (organic macro- processing industries, society, and the government. In this regard, each molecules mostly polysaccharides and proteins), steel coatings using of the concerned party has their role to play in ensuring food safety nanotechnology agents, and using biosurfactants such as lichenysin such that it does not constitute health threats to the public. There (Galiè et al., 2018) may be effective in controlling Listeria in food should be more emphasis on ensuring good hygienic practices during processing facilities. food production processes, especially for ready-to-eat foods. Reports To control Listeria in the home, a good hand hygienic practice is obtained from literature in this work suggest the relative abundance of an essential tool to prevent food contamination/cross-contamination Listeria in the environment in the Southern African sub-region. This sug- of food in domestic kitchens. It is important to note that regular hand gests a likelihood of frequent contamination of food by this pathogen in washing before food preparation, eating after toileting, sneezing, han- the region. In this regard, more extensive investigations are needed to dling dirty laundry/rubbish, touching pets, and after handling raw provide information on the relationship between environmental compo- meat should be embraced (Evans & Redmond, 2017; Kennedy et al., nents and Listeria species for a better understanding of the transfer of 2011). Also, it is recommended that foods should be cooked under this pathogen between niches. Most of the individuals in developing sufficient heat that is capable of destroying foodborne pathogens. countries live in deprived conditions and this might probably be reasons Consumption of improperly cooked egg, seafood, and meat may result for the increased prevalence of Listeria among this group. The increase in foodborne infection (Evans & Redmond, 2017). Furthermore, foods in migration in recent years is said to have altered the vulnerable popu- that need refrigeration should be kept properly refrigerated as it is lation of neonatal listeriosis (Mook, Grant, Little, Kafatos, & Gillespie, vital in minimizing microbial growth in foods (Evans & Red- 2010). This is also a similar scenario in the Southern African countries mond, 2017). and this demands the need for appropriate immigration policies. Reports Detecting Listeria and maintaining regular surveillance on dairy, obtained from literature on the method of identification of Listeria in poultry, and crop farms and in the environments is an important mea- this article revealed that most of the information available was mostly sure to reduce its chances of getting into the food chain (Mohammed & based on cultural (primary) detection methods (Nwaiwu, 2015), serolog- Aziz, 2019). Listeria prevention on farm is necessary, because this path- ical, classical biochemical methods and the principle of aesculin hydroly- ogen may find its way to food processing facilities from farm produce. sis usually characterized by black coloration on selective media for Therefore, removing potential sources of infection, good personal Listeria. However, all Listeria species have the ability to hydrolyze hygienic practices, and proper sanitation of the environment may be aesculin. Fraser and Sperber (1988) proved that the identification of effective. Also, good management of husbandry operations on farms, Listeria based on aesculin hydrolysis could give a false positive result. destroying/disposal of infected crops and animals both on farms and at Devriese et al. (1999) also reported that subclinical isolate of Streptococ- processing points, proper disinfection, isolation and quarantine of cus pluranimalium of dairy cows has the ability to hydrolyze aesculin and infected animals should be considered (Dhama et al., 2015; Oh, Kang, cause brown coloration. In the meantime, molecular methods have Oh, & Ha, 2013). Notwithstanding, high quality feeds should be fed to proven to be more reliable, accurate and could also show the relation- animals, maintenance of good health status of animals, controlled ship between isolates genetically. Improved identification and accuracy milking, and controlled use of manure are important precautions to of multiplex PCR for serotyping Listeria monocytogenes was revealed by achieving proper control of Listeria on farms (Dhama et al., 2015; Nightingale, Bovell, Grajczyk, and Wiedmann (2007) and regarded PCR Santorum, Garcia, Lopez, & Martínez-Suárez, 2012). (polymerase chain reaction) as a better alternative for the replacement Proper management of pH, temperature, water activity control, of the previous classical serotyping procedures. This method is capable use of adequate preservatives, verifying food shelf lives (Dhama et al., of enabling the tracking and elimination of the source of contamination 2015) and ensuring that foods contaminated with Listeria are not con- in food processing industries. A recently developed technique for sumed (Mateus, Silva, Maia, & Teixeira, 2013). Similarly, concerned detecting foodborne pathogens is the Fourier transform infrared (FT- authorities should establish strategic networking programs for moni- IR), Raman and matrix-assisted laser desorption/ionization time-of-flight toring and surveillance across all levels to check listeriosis outbreaks mass spectroscopy (MALDI-TOF MS). This method is rapid, cost-effec- both in humans and animals. Enacting and enforcing good manage- tive, and reliable and requires less sample preparation (Janbu, Møretrø, ment practices, incorporating the hazard and critical control points Bertrand, & Kohler, 2008; Rodríguez-Sánchez, Cercenado, Coste, & into all stages of food processing, upholding good hygiene and sanita- Greub, 2019). It can identify the bacteria genus, species, and strains by tion, firm biosecurity procedures, timely isolation and quarantine targeting the bacterium's carbohydrate or nucleic acids, lipids, and pro- operations, appropriate trade policies, and creating public awareness teins (Al-Qadiri, Lin, Al-Holy, Cavinato, & Rasco, 2008). Another method about high-risk foods most especially to vulnerable groups, (Jackson, developed and implemented for the identification of Listeria is the 16 of 22 KAYODE ET AL.

Whole Genome Sequence (WGS) techniques. This method determines Abay, S., Bayram, L. Ç., Aydin, F., Müs¸tak, H. K., Diker, K. S., & Erol, I._ the complete nucleotide sequence of the bacterial genome and is also (2019). Pathogenicity, genotyping and antibacterial susceptibility of the Listeria spp. recovered from stray dogs. Microbial Pathogenesis, considered appropriate to use for routine epidemiological studies by 126, 123–133. CDC due to its reliability and specificity (Jackson et al., 2016). It Alison, A. (2010). Assessment of microbiological quality of the berg river as a employs the use of bioinformatics tools such as Single Nucleotide Poly- source of irrigation water for raw and minimally processed crops. Master morphism (SNP) and whole genome multilocus sequence typing of Science in Food Science In the Department of Food Science: Fac- ulty of AgriSciences University of Stellenbosch. (wgMLST) among others to analyze and compare the sequenced data. Al-Qadiri, H. M., Lin, M., Al-Holy, M. A., Cavinato, A. G., & Rasco, B. A. These methods were implemented by the U.S. Food and Drug Adminis- (2008). Detection of sublethal thermal injury in Salmonella enterica tration's (FDA) Center for Food Safety and Applied Nutrition (CFSAN) serotype Typhimurium and Listeria monocytogenes using fourier trans- − 1 and CDC, respectively. Next-generation genome sequencing will make form infrared (FT-IR) spectroscopy (4000 to 600 cm ). Journal of Food Science, 73(2), M54–M61. more information available on the genome of different Listeria species Arslan, S. and Baytur, S., 2019. Prevalence and antimicrobial resistance of and also enhance specificity in the detection of species and strains. Listeria species and subtyping and virulence factors of Listeria mono- cytogenes from retail meat. Journal of Food Safety, 39(1), 1–10. Barre, L., Angelidis, A. S., Boussaid, D., Brasseur, E. D., Manso, E., & 5 | CONCLUSION Besse, N. G. (2016). Applicability of the EN ISO 11290-1 standard method for Listeria monocytogenes detection in presence of new Listeria species. International Journal of Food Microbiology, 238, Food-borne disease is usually one of the causes of morbidity and mor- 281–287. tality globally, particularly among vulnerable groups such as immuno- Bateman, K. J., Fredericks, P., Carr, J. A., & Britz, M. (2015). Listerial compromised individuals, elderly and infants. There is a need to brainstem encephalitis- treatable, but easily missed: Forum-clinical alert. African Journal of Health Professions Education, 105(1), 17–20. minimize contamination in the processing environment as well as Bertsch, D., Rau, J., Eugster, M. R., Haug, M. C., Lawson, P. A., preventing contamination of water used for irrigating fresh agricul- Lacroix, C., & Meile, L. (2013). Listeria fleischmannii sp. nov., isolated tural produce and the ones for animal husbandry as these may be the from cheese. 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Decontamination of microorganisms and pesticides from fresh to intensify functional nationwide disease surveillance, food safety fruits and vegetables: A comprehensive review from common house- policies, and creating awareness on the risk of consuming improperly hold processes to modern techniques. Comprehensive Reviews in Food processed foods or foods that are usually of high risk of Listeria Science and Food Safety, 18(4), 1003–1038. pathogen. Bortolussi, R. (2008). Listeriosis: a primer. CMAJ, 179(8), 795–797. Botsaris, G., Nikolaou, K., Liapi, M., & Pipis, C. (2016). Prevalence of Listeria spp. and Listeria monocytogenes in cattle farms in Cyprus using bulk ACKNOWLEDGMENT tank milk samples. Journal of Food Safety, 36(4), 482–488. We are grateful to the South African Medical Research Council, the Brand, A.S., 2012. Critical evaluation of the accuracy of the enumeration World Academy of Sciences, and the National Research Foundation methodology of Coliforms and E. coli in water from rivers used for the of South Africa for financial support. irrigation of fresh produce (Doctoral dissertation, Stellenbosch: Stellen- bosch University). Bremer, P. J., Fletcher, G. C., & Osborne, C. (2003). Listeria monocytogenes CONFLICT OF INTEREST in seafood. New Zealand Institute for Crop and Food Research. The authors declare no potential conflict of interest. New Zealand: Auckland. Britz, T. J., Sigge, G. O., Huisamen, N., Kikine, T., Ackermann, A., Lötter, M., … Kidd, M. (2013). Fluctuations of indicator and index microbes as AUTHOR CONTRIBUTIONS indication of pollution over three years in the Plankenburg and Eerste Conceptualization: Adeoye J. K. and Okoh A. I.; Writing—original draft Rivers, Western cape, South Africa. Water South Africa, 39(4), preparation: Kayode J. 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