Does Listeria come from animals?

Listeriosis is an infectious and fatal disease of animals, birds, fish, crustaceans and humans. It is an important food-borne zoonosis caused by Listeria monocytogenes, an intracellular pathogen with unique potential to spread from cell to cell, thereby crossing blood–brain, intestinal and placental barriers. The organism possesses a pile of virulence factors that help to infect the host and evade from host immune machinery. Though disease occurrence is sporadic throughout the world, it can result in severe damage during an outbreak. Listeriosis is characterized by septicaemia, encephalitis, meningitis, meningoencephalitis, abortion, stillbirth, perinatal infections and gastroenteritis with the incubation period varying with the form of infection. L. monocytogenes has been isolated worldwide from humans, animals, poultry, environmental sources like soil, river, decaying plants, and food sources like milk, meat and their products, seafood and vegetables. Since appropriate vaccines are not available and infection is mainly transmitted through foods in humans and animals, hygienic practices can prevent its spread. The present review describes etiology, epidemiology, transmission, clinical signs, post-mortem lesions, pathogenesis, public health significance, and advances in diagnosis, vaccines and treatment of this disease. Special attention has been given to novel as well as prospective emerging therapies that include bacteriophage and cytokine therapy, avian egg yolk antibodies and herbal therapy. Various vaccines, including advances in recombinant and DNA vaccines and their modes of eliciting immune response, are also discussed. Due focus has also been given regarding appropriate prevention and control strategies to be adapted for better management of this zoonotic disease.

Listeriosis, also termed as silage disease, circling disease and meningoencephalitis, is caused by Listeria monocytogenes. It is an infectious and fatal disease of animals, birds, fish, crustaceans and humans where septicaemia and encephalitis are predominantly observed [Low & Donachie 1997; George 2002; Kahn 2005; Wesley 2007; Barbuddhe & Chakraborty 2009; Dhama, Verma, Rajagunalan, et al. 2013; OIE 2014]. Throughout the world, listeriosis occurs in a sporadic or epidemic form [Mitchell 1996; Barbuddhe, Malik, et al. 2008; Dhama, Verma, Rajagunalan, et al. 2013]. Most of the time, infection in animals is subclinical but severe forms can also occur [OIE 2014]. The disease is characterized by septicaemia, encephalitis, meningitis, meningoencephalitis, rhombencephalitis, abortion, stillbirth, perinatal infections and gastroenteritis [Brugere-Picoux 2008; Barbuddhe & Chakraborty 2009; Okada et al. 2011; Barbuddhe et al. 2012; Disson & Lecuit 2013; Limmahakhun & Chayakulkeeree 2013; Mateus et al. 2013; OIE 2014]. The organism has an intracellular life cycle that can pass from cell to cell without release from the cell. This ability presents its potential to cross placental barrier and blood–brain barrier, explaining its pathogenesis and clinical signs [Janakiraman 2008]. The organism can survive at varying temperatures ranging from 4 to 37 °C [Janakiraman 2008].

Due to poor measures of quality control during food processing/handling and packaging, contamination of L. monocytogenes may occur [Carpentier & Cerf 2011], raising concerns for public health [Rocourt & Bille 1997; Kaufmann 1988; Schelch & Acheson 2000; Oliver et al. 2005; Dhama, Verma, Rajagunalan, et al. 2013; Dhama, Rajagunalan, et al. 2013]. Ready-to-eat food-mediated listeriosis infection in humans has been documented by several workers over a timescale from different parts of the globe [Lianou & Sofos 2007; Meloni et al. 2009; Mengesha et al. 2009]. Furthermore, importance of L. monocytogenes cannot be underemphasized as it may lead to huge economic losses in livestock industries, may lead to abortion in pregnant mothers as well as in animals, and food poisoning leading to death in individuals who get infected. Good quality control strategies along with adequate prevention measures are suggested to effectively prevent and control this food-borne illness in health, agricultural as well as environmental systems [Oliver et al. 2005; Chukwu, Chukwu et al. 2006; Bhunia 2008; Li et al. 2014; Min et al. 2014; Nakari et al. 2014].

The present review discusses listeriosis in animals, its etiological agent [L. monocytogenes] and disease in general, its epidemiology, transmission and spread, clinical signs and post-mortem lesions, public health importance, trends and advances in diagnosis, vaccines and treatment, zoonotic aspects along with appropriate prevention and control strategies to be adapted to counter this important zoonotic disease of animals with high public health concerns.

In 1926, Murray, Webb and Swann discovered Listeria while investigating an epidemic in laboratory animals, rabbits and guinea pigs [Murray et al. 1926; Brugere-Picoux 2008; Mateus et al. 2013]. Later in the 1980s, its role as food-borne pathogen was recognized in humans due to consumption of contaminated food in Canada, USA and Europe [Mateus et al. 2013; McCollum et al. 2013]. Listeriosis is caused by members of the genus Listeria, which has now 17 species [Hage et al. 2014; Weller et al. 2015]. However, only two species are considered pathogenic. L. monocytogenes is considered pathogenic to human beings and several animal species, whereas L. ivanovii is pathogenic especially to ruminants but occasionally to humans [McLauchlin & Martin 2008]. There are four lineages in L. monocytogenes named as I, II, III and IV, and there exist several differences among these lineages [Orsi et al. 2011]. Lineage I comprising serotypes 1/2b and 4b is mostly concerned with human infections and a few subsets of this lineage code listeriolysin S which is not present in other lineages. Lineage II includes serotype 1/2a and other serotypes which are also involved in human infections, and carry several plasmids that are resistant to heavy metals [Orsi et al. 2011]. L. monocytogenes has been divided into 13 serotypes [namely 1/2a, 1/2b, 1/2c, 3a, 3b, 3c, 4a, 4ab, 4b, 4c, 4d, 4e, 7] on the basis of somatic and flagellar antigens [Muñoz 2012]. Serotypes 1/2a, 1/2b and 4b are commonly reported in humans, and serotypes 1/2a and 4b in animals [Low & Donachie 1997; Brugere-Picoux 2008; Paixao et al. 2008; Pontello et al. 2012; Datta et al. 2013; Mateus et al. 2013]. A few cases of human listeriosis have been attributed to L. seeligeri and L. welshimeri [Low & Donachie 1997; Hain et al. 2006]. A few phylogenetically distant species, viz., L. grayi, L. marthii and L. rocourtiae have also been reported, which are not pathogenic [Graves et al. 2010; Leclercq et al. 2010]. Recently, seven novel species have been added in the genus that include L. floridensis, L. aquatica, L. cornellensis, L. riparia, and L. grandensi [den Bakker et al. 2014], and L. booriae and L. newyorkensis [Weller et al. 2015]. Other non-pathogenic Listeria spp. include L. innocua, L. fleischmannii and L. weihenstephanensis.

L. monocytogenes is a Gram-positive, facultative intracellular and saprophytic bacterium, which is an ubiquitous, small, motile with flagella, nonspore forming, non-capsulated, pleomorphic, facultative anaerobic, rod-shaped cocco-bacillus with an ability to switch from an environmental saprophyte to a potentially fatal pathogen [Vazquez-Boland et al. 2001; Campero et al. 2002; Milillo et al. 2012; Mateus et al. 2013; Vera et al. 2013]. The organism contains important virulence factors, i.e. the internalins, haemolysin, listeriolysin O [LLO], fibronectin-binding protein, FbpA, ActA protein, two phospholipases, metalloprotease, Vip protein, a bile exclusion system [BilE] and a bile salt hydrolase that are necessary for adhesion, intracellular multiplication and pathogenicity, and are primarily regulated by PrfA protein [Cossart & Portnoy 2000; Dussurget et al. 2002; Cabanes et al. 2005; Sleator et al. 2005; Jahangir et al. 2011; Osanai et al. 2013; Vera et al. 2013]. The bacterium can tolerate a wide range of pH and temperatures. Optimum growth occurs at 30–37 °C but the organism can multiply at 4–45 °C. A typical tumbling motility is observed around 25 °C. It can grow at pH 4.5–9.6, although the growth is minimal at low pH and low temperatures [Juntilla et al. 1988; Huff et al. 2005; Radostits et al. 2008; Bhunia 2008; Barbuddhe & Chakraborty 2009; OIE 2014]. Pasteurization temperature of 72 °C for 10 seconds has been found to be effective against Listeria. Long filaments are seen in old bacterial cultures. The bacterium can stay alive outside the body of hosts in humid atmosphere for several years.

Listeria affects a list of species in the Kingdom Animalia, including sheep, goat, cattle, buffalo, horse, pig, camel, canine, rodent, wild animals, birds and also humans. Small ruminants, especially sheep, are mostly affected [OIE 2014]. L. monocytogenes has been isolated from meat and/or milk of goats, sheep, cattle, pig, chicken, quail, partridge, ostrich and buffaloes [Barbuddhe et al. 2002; Rahimi et al. 2012; Derra et al. 2013; Hasegawa et al. 2013; Kuan et al. 2013; Ndahi et al. 2014], fish and fishery products [Jayasekaran et al. 1996; Karunasagar & Karunasagar 2000; Parihar, Barbuddhe, et al. 2008], ice creams, vegetables, other ready-to-eat foods [Lambertz et al. 2012; Lambertz et al. 2013; Mateus et al. 2013; Poulsen & Czuprynski 2013], seafood [Ahmed et al. 2013] and mushroom production facility [Viswanath et al. 2013]. In the northern hemispheres, listeriosis has a distinct seasonal occurrence, probably associated with seasonal feeding of silage with the highest prevalence during December through May. Cases of abortions are more common during February and March due to late pregnancies among sheep population. Mortality due to listeriosis varies from 20% to 30% as per various reports in humans [Jahangir et al. 2011; Mateus et al. 2013].

Reports regarding outbreaks of listeriosis in humans and animals have been documented from different parts of the world at different timelines. In humans, listeriosis is caused by all the 13 serotypes, in particular 1/2a, 1/2b, and 4b, and the rate of annual endemic disease varies from 2 to 15 cases per million of population [Muñoz 2012; Mena et al. 2004]. L. monocytogenes isolates of human and food-borne origin, recovered during 20 years [1992–2012] from Argentina, corresponded to serotype 4b mostly [71%] and rest 29% to serotype 1/2b [Prieto et al. 2015]. Study in a Spanish meat processing plant concluded the predominance of serotype 1/2a [36.8%], 1/2c [34%], 1/2b [17.9%] and 4b [11.3%] by multilocus sequence typing [MLST] characterization [Martín et al. 2014]. Between particular forms of listeriosis, no direct links have been made but epidemiological association has been shown between perinatal listeriosis and serovars 1/2b, 3b and 4b [Zimmer et al. 1989; Bille 1990; Schuchat et al. 1991]. In Northern Italy, multi-virulence-locus sequence typing [MVLST] of L. monocytogenes isolates revealed ruminants to be hypothesized as the natural reservoirs of this pathogen which could transmit the organism to humans, as a few earlier outbreaks in the 1980s were related to manure of sheep and milk of cow [Rocha, Dalmasso, et al. 2013]. Persons with immunocompromised status such as pregnant women are more susceptible to listeriosis than others, around the world [Southwick & Purich 1996]. The gastrointestinal tract of humans serves as a major reservoir of the pathogen and it can be recovered from feaces of pregnant women and also normal human beings [Kampelmacher et al. 1972]. Incidence of listeriosis appears to be increasing in European countries, especially in elderly people [Goulet et al. 2008; Hernandez-Milian & Payeras-Cifre 2014]. About 19 outbreaks of an invasive form of listeriosis were reported during 1991–2001 from Europe [FAO 2004]. There were 299 invasive case reports in Denmark from 1994 to 2003 [Hernandez-Milian & Payeras-Cifre 2014], 110 in Barcelona [Spain] from 1991 to 2005 and 58 cases in Valencia [Spain] from 2008 to 2010 [Suarez et al. 2007; Muñoz et al. 2012]. In Sweden, 601 human isolates of Listeria have been documented [Parihar, Lopez-Valladares, et al. 2008]. Overall incidence of listeriosis in European Union was 0.32 cases/100,000 people during 2011 with a case fatality rate of about 12.7% [EFSA & ECDC 2013]. Compared to 1996–1998, approximately 37% decrease in incidence was seen in the USA during 1996–2001 [Lorber 2010], while Australia has seen a constant rate of incidence from 1991–2000, ranging from 0.2 to 0.4 cases/100,000 population [De Noordhout et al. 2014]. A few cases were reported from Asian countries, where 48 cases of listeriosis have been reported in Taiwan from 1996 to 2008 [Huang et al. 2011] and 479 isolates of Listeria in China from 1964 to 2010 [Feng et al. 2013]. In India, listeriosis has been reported in patients who had a history of genital problems [Krishna et al. 1966], abortion cases [Kaur et al. 2007], child with abdominal pain [Gomber et al. 1998] and from cerebro-spinal fluid [Pandit et al. 2005]. In animals, Vaissaire [2000] reported 428 outbreaks [of which sheep 25% and cattle 60%] in France during 1998–1999. Listeriosis outbreak in Nigeria affecting guinea pigs was documented to have almost 100% mortality [Chukwu, Ogo, et al. 2006]. A recent study in Iran reported isolation of Listeria spp. from milk samples originating from cattle, buffalo, goat, sheep and camel [Rahimi et al. 2014]. Incidence of animal listeriosis in India has been reported at varying time periods. The organism was first isolated in the 1950s by Vishwanathan and Iyer from an infected sheep [Sharma & Adlakha 1996]. The first case of listeric abortion in India was documented in an ewe in 1959 [Barbuddhe et al. 2012]. Experimental studies and field cases of Listeria infections in humans and animals in Indian subcontinent have been reviewed by Malik et al. [2002], usually documented as sporadic cases but occasionally as disease outbreaks. Chand and Sadana [1998] reported L. ivanovii-induced abortion in sheep. L. ivanovii and L. monocytogenes have also been recovered from mastitis cases in cattle and buffalo [Rawool et al. 2007]. Shakuntala et al. [2006] documented prevalence of L. monocytogenes and other Listeria spp. in buffaloes to be 4.4% and 7.4%, respectively. Elezebeth et al. [2007] reported isolation of L. ivanovii from aborted goats [7.5%], mastitic goats [5.6%] and healthy goats [14.5%]. There was also a rare report of L. monocytogenes isolation from buffalo brain in the state of Andhra Pradesh [Uppal et al. 1981]. Isolation of pathogenic Listeria spp. in faecal samples of captive wild animals [16%, 8/50 positive] has been reported by Kalorey et al. [2006].

Listeria spp. are widespread and truly ubiquitous in nature and commonly found in temperate zone. Rich sources include soil, manure/sewage, farm slurry, sludge, silage, animal feed, water and excreta/faeces of mammals and birds [Fenlon 1985]. They are also isolated from walls, floors, drains, decaying vegetation, rivers, pasture herbage, factory effluents, etc. of farms and other environments [Fieseler et al. 2014]. A study on listeriosis showed that, at 5 °C, the organism survives for 13, 16, 12 and 12 years in milk, brain, faeces and silage, respectively [Dijkstra 1975]. It may be present in poorly fermented silage [i.e. pH above 5.0–5.5] and in pockets of aerobic deterioration [Brugere-Picoux 2008]. Dairy cows usually represent a reservoir for the bacterium; and raw milk as well as beef serves as a major source of transmission from dairy farms to humans. Contaminated raw foods represent a vehicle for introduction of L. monocytogenes into food processing plants [Ferreira et al. 2014].

Listeria is widely distributed among birds, and the commonly affected species are chickens, turkeys, geese, ducks, pigeons, parrots, wood grouse, snowy owl, eagle, and canaries [Shivprasad et al. 2007; Ivanovic et al. 2010; Dhama, Verma, Rajagunalan, et al. 2013]. Chickens serve as carriers and prime reservoirs of Listeria and play a major role in its spread by contaminating the litter and environment in the poultry production systems [Njagi et al. 2004]. The opportunistic role of L. monocytogenes is reflected with observation of listeriosis concurrent with other diseases of poultry, viz., coccidiosis, salmonellosis, campylobacteriosis, infectious coryza, colibacillosis and parasitic infections [Uyttendale et al. 1999; Adzitey et al. 2012; Cook et al. 2012]. Intestinal colonization and presence of L. monocytogenes in faeces of poultry play a significant role in the spread of listeriosis in domestic animals/ruminants. Humans mostly get infected due to Listeria contamination of raw broiler meat and poor sanitation/hygienic conditions in processing premises instead of acquiring direct infection from poultry [Kosek-Paszkowska et al. 2005; Goh et al. 2012].

Listeriosis can be transmitted through the ingestion of food and water contaminated with saliva, faeces, nasal secretions and aborted material from infected animals [Brugere-Picoux 2008]. Potential source of infection transmission includes feed [poorly fermented silage] and food [unpasteurized milk or contaminated after pasteurization, milk by-products and raw vegetables [Brugere-Picoux 2008]], and inhalation of dust and soil infected with bacteria. Ready-to-eat foods play a crucial role in the transmission of listeriosis to humans. A study carried out with 384 food samples in Ethiopia showed a 25% prevalence of L. monocytogenes among which some isolates were multi-drug resistant [penicillin, nalidixic acid, tetracycline and chloramphenicol] emphasizing the need for adopting hygienic practices in food processing industries [Garedew et al. 2015]. Disease can also spread through carrier animals and rodents. Listeriosis is not vertically transmitted [Malik & Vaidya 2005; Raorane et al. 2014]. A recent study indicates that mutation in the inlA gene induces premature stop codon in the serotype 1/2c which could lead to potential transplacental transfer of the organism [Gelbíčová et al. 2015].

The organism survives acidic environments through glutamate decarboxylase and arginine deaminase systems [Gahan & Hill 2014]. The ability to form biofilms may assist its survival in the environment [Ammendolia et al. 2014]. However, the level of biofilm production depends upon strain, origin and environmental conditions [Barbosa et al. 2013; Lee, Chai, et al. 2013; Ochiai et al. 2014]. Though L. monocytogenes is not an established biofilm former than others [Kalmokoff et al. 2001], its persistence in the environment makes it as an emerging problem for the food processing industry and other food-associated environments [e.g., farms and retail establishments] [Gilbert et al. 2002; Galvao et al. 2012; da Silva & De Martinis 2013; Ferreira et al. 2014]. The organism is considered to employ mixed biofilm forming and subsequent antimicrobial resistance [Simões et al. 2009]. Growth of Listeria in non-nutrient saline is promoted by nutrients and other growth promoters released from Acanthamoeba [Fieseler et al. 2014]. Survival of this bacterium in Acanthamoeba spp. highlights potential impact of this interaction on food safety and human health.

Listeria possesses unique virulence factors to invade host, evade immune cells and to cause infection [Camejo et al. 2011]. Major virulence factors include LLO – a toxin having pore-forming activity; ActA – a factor responsible for polymerization of host actin; a group of internalin family proteins which play a major role in entry, namely, InlA and InlB; two phospholiphases, PlcA and PlcB; a metalloprotease, Mpl and UhpT, a system for uptake of sugars [Dussurget et al. 2004; Schnupf & Portnoy 2007]. UhpT helps bacteria to take up glucose-6-phosphate inside the cell, thus enhancing growth and multiplication [Camejo et al. 2011]. These virulence factors are under direct control of a transcriptional factor, PrfA [Lecuit 2007]. A thermosensor controls this PrfA and, based on environmental temperature, this sensor's 5' UTR can take up different secondary structures [de las Heras et al. 2011]. Hence, there is an optimal expression of PrfA at higher temperatures than at lower temperature where there is a downregulation of PrfA. As a result, all virulence genes are expressed to maximum at 37 °C compared to lower temperatures [Johansson et al. 2002] [Figure 1].

Internalin family proteins comprise InlA, InlB, InlC, InlJ, InlH and InlK. All these have different roles in virulence and pathogenesis of Listeria [Bierne et al. 2007]. InlA is mainly involved in entry inside the host cell through a receptor named E-cadherin. InlB, a signaling molecule, targets a wide range of cell compared to InlA [Cossart 2011] and is also involved in entry of the organism into the cell via the Met receptor. InlC is unique among these internalins as it occurs as secreted form. It is mostly expressed in higher amounts inside infected cells where it interacts with Tuba [a cytoskeletal protein that can bind various regulatory proteins of actin and IκB kinase [IKKα]] and blocks activation of NF-κB, thereby slowing down the innate immune system [Gouin et al. 2010; Polle et al. 2014]. Though InlJ also acts as an adhesion molecule, it cannot be detected inside the cell and is most likely expressed in the later stages of infection [Sabet et al. 2008]. Another internalin InlH is expressed as well to minimize the production of cytokine IL-6 [Personnic et al. 2010]. InlK helps Listeria to evade autophagy [Dortet et al. 2011].

L. monocytogenes has got the ability of crossing intestinal, blood–brain and fetoplacental barriers. Once the gastrointestinal tract is invaded, there is internalization of the bacterium within epithelial cells of the host [via phagocytosis] followed by multiplication and subsequent infection. Various stages are involved in harbouring and conquering of host cells by Listeria that includes adhesion, invasion, lysis of vacuoles, multiplication and evasion of the host defence mechanisms and cell-to-cell spread [Camejo et al. 2011]. Various bacterial surface proteins and host receptors are involved in the initial stage of adhesion [Jagadeesan et al. 2010]. Bacterial proteins like Lap, Ami, FbpA, DltA, LapB, InlJ, ActA, InlF and RecA are essential for adhesion of Listeria to the host cell [Sabet et al. 2008; Reis et al. 2010; Camejo et al. 2011]. All these proteins vary in their receptors and corresponding functions [Dramsi et al. 2004; Wampler et al. 2004]. Listeria can invade both phagocytic and non-phagocytic cells. In case of phagocytic cells like macrophages, bacterial entry is mediated by phagocytosis, while in non-phagocytic cells, the entry is mediated by invasive proteins of Listeria [Cossart 2011]. Internalins A and B are major proteins for invasion [Dramsi et al. 1995]. E-cadherin serves as a receptor for InlA and this interaction is species-specific as murine E-cadherin does not bind with InlA due to variation in their amino acid sequence [Mengaud et al. 1996; Smutny & Yap 2010]. More than 90% of human listerial strains possess InlA-mediated invasion [Jacquet et al. 2004]. Second, internalin InlB has a different receptor c-Met where gC1qR and glycosaminoglycans are co-receptors that help stabilizing interaction between InlB and c-Met [Marino et al. 2002] [Figure 1]. Apart from these two internalins, there are also other proteins like Vip, Auto, p60, GtcA and MprF involved in invasion [Camejo et al. 2011].

After adhesion to their respective receptors, the bacterium is covered by a phagocytic vacuole in macrophages and enters into cells [Cossart 2011]. Usually an organism inside phagocytic vacuoles is destroyed by the acidic environment. However, Listeria employs various ways to counteract this mechanism. LLO is the key factor responsible for degradation of the vacuole [Beauregard et al. 1997; Gedde et al. 2000]. LLO also regulates influx of calcium ions inside the host cell and plays a role in bacterium invasion [Dramsi & Cossart 2003], NFκB and MAP kinase pathway activation and limits the host immune system by suppressing the host cell protein SUMOylation [Ribet & Cossart 2010; Ribet et al. 2010] [Figure 1]. Once inside the cytoplasm after rupture of vacuoles, Listeria uses host sugars for its survival and multiplication. Besides relA, fri, pycA, and prsA2, various proteins are responsible for intracellular survival [Camejo et al. 2011]. A peptidoglycan N-deacetylase PgdA is one of the peptidoglycan-modifying enzymes reserved by Listeria to alter cell wall so as to escape the immune mechanism of the host [Boneca et al. 2007]. As a result of alteration of the cell wall, Listeria easily escapes lysozyme-mediated killing [Popowska et al. 2009; Burke et al. 2014]. The p60 also alters the host immune mechanism by activation of NK cells leading to release of proinflammatory cytokines [Humann et al. 2007]. Flagellin releases proinflammatory cytokines through TLR5 [Hayashi et al. 2001]. LLO, apart from its major role in the destruction of the vacuoles, also is of importance to downregulate the host immune system through dephosphorylation of H3 and deacetylation of H4 histones of the host cell [Hamon et al. 2007; Hamon & Cossart 2011]. LLO in secreted form can cause fission of the mitochondrial network [Stavru et al. 2011]. Listeria also possesses a superoxide dismutase enzyme which helps to fight against reactive oxygen species being generated by host cells [Archambaud et al. 2006]. The listerial immunity is primarily cell-mediated, explaining a greater association between listeriosis and conditions involving impairment of cell-mediated immunity that include pregnancy and organ transplantation along with Acquired Immunodeficiency Syndrome [AIDS] [Portnoy et al. 1992; Cossart & Lecuit 1998; Cossart et al. 2003; Seveau et al. 2007; Gekara et al. 2010]. Cell-to-cell spread is propelled by formation of an actin filament at one end of the bacterium that looks like the tail of a comet [Cameron et al. 1999]. This tail formation is facilitated by ActA that contains WASP-like domains which recruit host Arp2/3, an actin nucleator [Campellone & Welch 2011].

Three different forms of listeriosis are documented in animals, namely septicaemic, encephalitic and abortion form. Listeriosis causes encephalitis, abortion, mastitis, repeat breeding and endometriosis in animals [Malik et al. 2002]. It is primarily a disease of ruminants, particularly sheep, and causes encephalitis and abortion. In ruminants, it also produces syndromes of septicaemia, spinal myelitis, uveitis, gastroenteritis and mastitis [Rawool et al. 2007; Headley et al. 2014]. The encephalitic form is known as ‘circling disease’ due to movement of the animal in circles in one direction [OIE 2014]. Occasionally, septicaemic disease occurs in horses and pigs. Outbreaks of listeriosis are uncommon in birds and disease is observed occasionally in young chicks. The disease is sporadic/rare in poultry, usually seen as a septicaemia or localized encephalitis. Besides causing disease in domestic animals and birds, L. monocytogenes also affects rodents and wild animal population [OIE 2014].

Sheep can be severely affected by listeriosis and the signs include encephalitis [i.e. circling disease] with brainstem and cranial nerve dysfunction, abortion with placentitis in the last trimester [from 12 weeks on] and gastroenteritis with septicaemia [Rawool et al. 2007; OIE 2014]. Young lambs [under 5 weeks of age] might develop the septicaemic form while the encephalitic form is noticed in older lambs [4–8 months]. Signs vary between individual sheep; however, incoordination, head deviation sometimes with tilting of head, walking in circles, propelling themselves forward till getting a solid object like wall or gate and unilateral facial paralysis [causing drooling of saliva, drooping of eyelid and ear] are observed [Scott 2013]. Death occurs in 2–3 days due to respiratory failure. Goats and cattle exhibit similar signs like sheep [OIE 2014] [Figure 2]. However, in cattle, the disease course is long and takes about 1–2 weeks. Buffaloes are also susceptible to listeriosis where genital tract infections are common [Shakuntala et al. 2006]. The cerebral form of listeriosis also occurs in camels [Al-Swailem et al. 2010].

Less commonly, septicaemia in peri-parturient and neonatal sheep and goats, gastroenteritis in weaned sheep, spinal myelitis [fever, ataxia with initial knuckling of hindlimbs progressing to hindlimb weakness and paralysis], ophthalmitis and occasionally mastitis also occur [George 2002; Clark et al. 2004; Otter et al. 2004; Winter et al. 2004; Radostits et al. 2008]. Mastitis is a rare manifestation of listeriosis affecting only a single quarter of the udder and is not responsive to antibiotics [Rawool et al. 2007]. Unilateral uveitis and keratoconjunctivitis are also reported in cattle [Starič et al. 2008]. Infected sheep generally suffer from abortion storms that mostly occur after the 12th week of pregnancy. L. monocytogenes in cutaneous infection of canine has also been documented [Loncarevic et al. 2002]. Porcine listeriosis mainly concerns the septicaemic form; however, a few reports on the encephalitic form also exist [Rahman et al. 2009].

Very little gross lesions may be observed in aborted foetuses of ruminants but there may be presence of autolysis if the foetus is retained [Low & Donachie 1997; Walker 1999]. Aborted foetuses can demonstrate gross lesions which include small yellow foci of necrosis in liver and shallow abomasal erosions [Hamon et al. 2006; Painter & Slutsker 2007; Hoelzer et al. 2012]. Post-mortem findings and histopathology in affected animals depend upon clinical presentation. Changes in cerebrospinal fluid are noticed in the encephalitic form with cloudy fluid and congestion of meningeal vessels. No gross pathological lesions of the brain have been observed other than discolouration of the brain stem with softening and abscessation of the medulla noticed in some cases. Histopathology is pathognomonic of disease, consisting of micro-abscesses in the brainstem, spinal myelitis, perivascular lymphocytic cuffing, vasculitis, oedema and haemorrhages [Rocha, Lomonaco, et al. 2013]. Most commonly, there is involvement of medulla and pons. Multiple foci of necrosis in the liver and spleen are seen less frequently in the septicaemic form.

Pathognomonic signs of listeriosis are not observed in birds. Young birds are more susceptible with high mortality, upto 40% that show chronic infection. Septicaemia with occasional meningoencephalitis and sudden death is observed in adult birds. Predisposing factors include immunosuppression, wet/damp conditions, moist litters and cold [Kahn 2005]. Secretions and excretions of infected birds are rich sources of bacterium that play a main role in transmission and spread of Listeria via ingestion of contaminated feed, water, litter and soil. Recently, an outbreak in humans in British Coloumbia and Canada revealed that wild birds defaecating near water bodies to a cheese processing plant lead to L. monocytogenes infection in humans who consumed cheese from this plant [McIntyre et al. 2015]. Inhalation or wound contamination can also spread the bacterium. The incubation period is not defined in birds, and infection usually occurs subclinical [Kurazono et al. 2003]. Clinical signs include septicaemia, depression, listlessness, emaciation and diarrhoea with sudden/peracute death [Akanbi et al. 2008; Dhama, Verma, Rajagunalan, et al. 2013]. Salpingitis is observed in hens during the acute systemic phase [Kurazono et al. 2003]. Symptoms of encephalitis like spasms, opisthotonus and paralysis indicate subacute and chronic listeriosis. Lesions in the septicaemic form of disease are fibrinous pericarditis, hydropericardium, petechial haemorrhages in the proventriculus, heart and kidney, nephritis, lung oedema, thickening of air sac wall, enlargement of spleen and liver, retention of bile, liver and heart necrosis, enteritis and conjunctivitis [Kurazono et al. 2003; Kahn 2005]. The encephalitic form of listeriosis in birds is a rare occurrence. However, recently, an outbreak of listeriosis in red-legged patridges has been documented with the encephalitic form accounting for 30–40 mortalities/day over a period of 8 days out of 25,000 birds [Jeckel et al. 2015]. Myocardial degeneration, necrosis and inflammation are often extensive in nature. Whole carcass congestion and petechial haemorrhage on serosa are observed in the acute form of disease. The encephalitic form is seen with nervous signs of depression, incordination, ataxia, torticollis and opisthotonus condition. It shows no predominant gross lesions in the brain, except gliosis and satellitosis in the cerebellum, and microabscesses with presence of Gram-positive bacteria in the midbrain and medulla [Kurazono et al. 2003].

Many food-borne zoonoses are of serious public health concerns with long-term sequel to various organs [Batz et al. 2013; Dhama, Verma, Rajagunalan, et al. 2013; Dhama, Rajagunalan, et al. 2013]. Among these, listeriosis can cause severe and life-threatening complications [Dhama, Tiwari, et al. 2011; Ta et al. 2012; Asakura et al. 2013; Dhama, Verma, Rajagunalan, et al. 2013; Kudirkiene et al. 2013]. Owing to change in food habits towards ready-to-eat products, food production systems, processing and supply, refrigeration for food preservation, interest in organic and natural products, interest in free-range birds and awareness towards better health, listeriosis is now considered as an emerging food-borne zoonosis of increased public health significance [Kaufmann 1988; Low & Donachie 1997; Rocourt & Bille 1997; Farber & Losos 1998; Schelch & Acheson 2000; Barbuddhe et al. 2005; Kataria et al. 2005; Oliver et al. 2005; Barbuddhe, Malik, et al. 2008; Dhama, Tiwari, et al. 2011; Milillo et al. 2012; Zhu et al. 2012; Dhama, Verma, Rajagunalan, et al. 2013; Dhama, Rajagunalan, et al. 2013]. L. monocytogenes has also been isolated from seafoods, which poses a threat to human beings in the coastal areas too [Gawade et al. 2010].

Listeriosis may occur as sporadic, endemic and foodborne outbreak to induce septicaemic disease, meningoencephalitis, abortion and infection in other organs. The majority of risks involve contamination of foods during processing and the potential of the organism to grow at refrigeration temperature [Buzby & Roberts 2009; Zhu et al. 2012; Lambertz et al. 2013; Lamden et al. 2013; Viswanath et al. 2013]. Meningitis due to Listeria has been ranked at third position among the bacterial causes of meningitis in humans [Koopmans et al. 2014]. Young ones, especially newborns, elderly persons, pregnant women, immunocompromised and immunologically immature individuals are generally at higher risk to acquire listeriosis [Martínez-Montero et al. 2013; Poulsen & Czuprynski 2013; Sappenfield et al. 2013]. Serious implications such as septicaemia, meningitis and gastroenteritis occur in newborns/neonates, elderly and immunocompromised people with case fatality rates of 30%–40% [Barbuddhe, Malik, et al. 2008; Vera et al. 2013]. Recent studies from Australia and the USA have documented that elder age group of over 60 years more commonly succumb to listeriosis [CDC 2013; Popovic et al. 2014]. Food of animal origin including milk, meat and their products constitute the main sources of listerial infection [Mahmood et al. 2003; Goh et al. 2012; Klancnik et al. 2014; Osman et al. 2014].

In the USA, the annual cost of L. monocytogenes was estimated to be US$ 2.3–22 billion, and the annual benefit of Listeria food safety measures was $0.01–2.4 billion [Ivanek et al. 2004]. As per the latest estimates, in 2010, listeriosis was responsible for 23,150 illnesses, 5463 deaths and 172,823 disability-adjusted life-years [DALYs] globally [De Noordhout et al. 2014]. The proportion of perinatal cases was 20.7%. Several food-borne disease outbreaks of human listeriosis, particularly in developed countries, have been documented [Rocourt & Bille 1997; Schelch & Acheson 2000; Dhama, Tiwari, et al. 2011; Dhama, Verma, Rajagunalan, et al. 2013; OIE 2014]. Though incidences in these countries are low, mortality rate is higher [Gillespie et al. 2010]. In developed countries like the USA, England and Wales, approximately 20%–25% of infections have been reported to lead to abortion and still birth [McLauchlin et al. 2004; CDC 2005]. Fatal outbreak has been recorded in the USA during 2011, where 33 deaths were reported out of 147 infected persons [De Noordhout et al. 2014]. L. monocytogenes infection, therefore, stands third next to Clostridium botulinum and Vibrio vulnificus in the USA [Scharff 2012]. Epidemiological data regarding listeriosis infection in humans are not available from many developing countries [De Noordhout et al. 2014]. Genital listeriosis is very common in India. However, exact epidemiological data are not available due to under-reporting and poor diagnostic facilities. Studies regarding status of Listeria infection in various parts of developing countries are needed to know the exact status of disease throughout the world [De Noordhout et al. 2014]. L. monocytogenes has been isolated from cervical and vaginal discharges of women with a history of abortions, miscarriages, stillbirths or neonatal deaths [Krishna et al. 1966; Bhujwala & Hingorani 1975; Kaur et al. 2007]. It causes abortion and stillbirth in pregnant women with the potential to transmit it to neonates [Rocourt & Bille 1997; Swaminathan 2001; Kaur et al. 2007]. Opacity and discolouration of foetal membranes and abscess formation in between villous that can be seen during cross-sectional examination of placenta are observed. Affected foetuses may have small abscesses and granulomas in various organs like the lungs, the liver and the spleen [Drevets & Bronze 2008]. Microscopically, abscesses have a central area of necrosis which is infiltrated by polymorphonuclear leucocytic cells [Benirschke et al. 2006].

Occupational exposure to soil, vegetation and animals have also been reported, which may cause skin infections manifested by non-painful, non-pruritic, self-limited, localized, papulo-pustular or vesiculopustular eruptions [Godshall et al. 2013; Zelenik et al. 2014]. Humans can acquire listeric infections from contact with infected poultry/birds, consumption of contaminated poultry meat or meat products [pre-cooked and ready-to-eat products] and food-chain by faecal–oral route [Vivant et al. 2013] [Figure 2]. Improper/unhygienic food handling practices, contaminated water, flies and insects, and contaminated food materials are implicated in the spread of listeriosis [Dhama, Tiwari, et al. 2011; Dhama, Verma, Rajagunalan, et al. 2013; Vivant et al. 2013]. Direct contact with animals/birds is of lesser significance in the transmission/spread of Listeria, excluding highly susceptible individuals. Person-to-person transmission is not generally observed. Proper cooking of the food is valuable in terms of killing the organism.

The incubation period in humans varies from 1 day to 3 months based on the form of listeriosis [Goulet et al. 2013]. Clinical signs of listeriosis include fever, meningitis/encephalitis, neck stiffness, ataxia, tremors, seizures and erratic consciousness. L. monocytogenes causes endocarditis, brain abscess, lung infection, arthritis, and bone and gall bladder infection [CDC 2013]. Headache, nausea/vomiting, malaise, pneumonia and conjunctivitis may also occur [Rocourt & Bille 1997; Slutsker & Schuchat 1999]. Cases of conjunctivitis in poultry workers at processing plants have been documented while handling of apparently normal but Listeria-carrying chickens. Disease onset is rapid and death within 24–48 hours may occur. More recently, listeria has also been recovered from a patient who suffered from spontaneous bacterial peritonitis, which is a rare occurrence as listeria is not a common organism causing it [How et al. 2015].

It is important to note that a vast majority of cases of listeriosis result from consuming bacteria in high numbers and foods wherein pathogen level may be beyond 100 colony forming unit [cfu]/g. In some countries, absence of the pathogen in a 25 g sample and in others the pathogen load up to 100 cfu/g or even higher levels were permitted with the condition that growth would not be possible or be very slow [Todd & Notermans 2011]. Chance of illness is high when organisms are consumed in high numbers. It has, therefore, been seen that elimination of higher levels of L. monocytogenes has got a large impact on predicted number of cases of illness. Probability of illness by ingestion of L. monocytogenes is higher for a population which is susceptible. Between sub-groups of a susceptible population, probability of becoming ill has been shown to vary. Conditions compromising the immune system also effect susceptibility to extents that vary. There is an increase in risk of listeriosis at any given dose with immunocompromised nature of individual [Aureli et al. 2000; Goulet et al. 2008; Little et al. 2009; Fretz et al. 2010].

Listeric infections lead to gastrointestinal disease or systemic syndromes both in humans and animals, thereby causing meningitis and subsequently grave prognosis. Complications due to Listeria infection include meningitis, sepsis, miscarriage, pneumonia, shock, abscess formation, stillbirth and inflammation of the eye [Janakiraman 2008]. Mostly, humans recover from the gastrointestinal form of listeriosis but this form in animals may lead to meningitis. Overall case fatality rate is about 20%–30% in humans [Janakiraman 2008]. Death rate of immunocompromised persons and newborn is usually higher.

Diagnosis is based on history, clinical signs, pathological lesions and detection of the pathogen. Previous exposure of disease, feeding habits, grazing pasture and observation of signs and symptom are helpful for presumptive diagnosis. Definitive diagnosis can be made only after isolation and identification of the bacterium [Kahn 2005]. Isolation of Listeria is not much cumbersome as it can be readily isolated. However, difficulty may occur while recovering this pathogen from birds showing the encephalitic form of disease [OIE 2014]. The ubiquitous nature, wide distribution and ability to survive for long periods outside the host's body present difficulty in concluding the source and spread of infection. Conventional methods for isolation of L. monocytogenes, acceptable for international regulatory purposes, include the United States Food and Drug Administration [FDA] method, the Association of Official Analytical Chemists [AOAC] official method, the ISO 11290 Standards, the United States Department of Agriculture [USDA]-Food Safety and Inspection Service [FSIS] method and the French Standards [OIE 2014].

The preferred clinical samples for identification of the organism in culture include the brain tissue, lumbar cerebrospinal fluid [CSF], blood, liver, spleen, heart, aborted placenta and foetus, meconium of newborns, faeces, vomitus, and food/feed material [Brugere-Picoux 2008; Scott 2013; see also health.utah.gov/epi/diseases/listeria/plan/ListeriaPlan081610.pdf]. Samples should be chosen according to clinical presentation: materials from the lesions in the liver, kidneys and/or spleen in case of septicaemic form; the spinal fluid, pons and medulla in case of encephalitic form; the placenta [cotyledons], foetal abomasal contents and/or uterine discharges in case of abortion. Earlier methods included maceration of the materials and pre-incubation for months at 4 °C along with subculturing at intervals before isolation [Walker 1999]. For isolation purposes, blood/tryptose agar or brain heart infusion medium are the best media [Walker et al. 1990]. Traditional procedure for isolation of L. monocytogenes from animal tissues includes direct plating of specimens on sheep blood agar or other rich culture media along with concomitant use of ‘cold enrichment’ technique and subculturing upto 12 weeks. Listeria may need selective enrichment using University of Vermont Medium and Fraser's broth. Selective media include Dominguez–Rodriguez isolation agar, PALCAM agar and modified McBride Listeria agar. A number of beneficial selective chromogenic plating media replacing conventional media have been reviewed by Reissbrodt [2004] for isolation of pathogenic Listeria spp. particularly in food industries.

Organism can be identified on the basis of Gram-staining of smear/culture, motility, haemolysis, biochemical tests [catalase reaction], peroxide-anti-peroxide method, sugar utilization, immunofluorescence test [IFT], or DNA analysis [AOAC 2000; Dhama, Verma, Rajagunalan, et al. 2013; Jones & D'Orazio 2013; OIE 2014]. Anton test is also used for detecting Listeria where the infected material is dropped on the conjunctiva of an eye of a rabbit that produces conjunctivitis or kerato-conjunctivitis within 24–36 hours. Immunohistochemical testing is mainly employed in locating antigen in lesions having few bacteria and is particularly employed to detect encephalitic listeriosis. Demonstration of listerial antigen in fixed tissues with lesions of septicaemic disease confirms listeriosis where culturing of organism is not feasible.

Pathogenicity testing of Listeria isolates includes in vitro methods, viz., haemolysis on sheep blood agar, assay for PI-PLC [phosphatidylinositol-specific phospholipase C] activity, the CAMP test and in vivo tests, viz., inoculation of 3-week-old mice intra-peritoneally and 10-day-old chicken embryos via CAM [chorioallantoic membrane] route. Vero cell cytotoxicity assay [in vitro] can also be used for detection of haemolytic strains of L. monocytogenes [Khan et al. 2014]. Kaur et al. [2010] reported PI-PLC and polymerase chain reaction [PCR] as effective alternatives to in vivo pathogenicity test.

Useful serodiagnostic tests are serum agglutination test, complement fixation test [CFT], haemagglutination [HA], haemagglutination inhibition [HI], antibody precipitation, growth inhibition test and enzyme linked immuosorbent assay [ELISA] [Capita et al. 2001; Dhama, Verma, Rajagunalan, et al. 2013; OIE 2014; Benetti et al. 2014]. However, these tests exhibit considerable cross reactions if conventional antigens are used. Detection of anti-haemolysin [LLO] antibodies by ELISA is employed for detection of septicaemic as well as abortion status of listeriosis. An avidin–biotin-based ELISA was developed for detection of antibodies against LLO in milk samples of cattle with the assay showing potential as an epidemiological tool [Kalorey et al. 2007].

Different antigens of Listeria spp. like somatic [O], flagellar [H], outer membrane protein [OMP] have been used for development of serological tests but resulted in poor sensitivity and specificity [Berche et al. 1990; Chen & Chang 1996; Jadhav et al. 2012]. Therefore, virulent markers/protein antigen, such as LLO [Churchill et al. 2006], internalins [InlA, InlB, InlC, InlC2, InlJ] [Boerlin et al. 2003], actA protein [Jahangir et al. 2012], phospholipases C [Chaudhari, Malik, & Barbuddhe 2004; Chaudhari, Malik, Bhanu, et al. 2004] and autolysin p60 protein [Hess et al. 1996] have been studied. Among these, LLO has been extensively studied and found suitable for development of serological tests like ELISA in humans [Berche et al. 1990; Low & Donachie 1997; Barbuddhe et al. 1999; Kaur et al. 2006] and ELISA as well as immunoblotting in animals [Low & Donachie 1991; Miettinen & Husu 1991; Low et al. 1992; Lhopital et al. 1993; Barbuddhe et al. 2000; Chaudhari et al. 2001; Banu et al. 2006]. Recently, synthetic peptides of LLO and internalins have been used for diagnosing listeriosis caused by L. monocytogenes and L. ivanovii [Liu et al. 2007; Shoukat et al. 2013]. The MALDI-TOF MS approach has also been applied for detection of Listeria from food samples [Barbuddhe, Maier, et al. 2008; Jadhav et al. 2014]. Protocols including conventional and non-conventional commercially available tests, e.g. Vitek, API, MICRO-ID [on the basis of the CAMP test], ELISA and nucleic acid assay kits have been developed for identification of L. monocytogenes. For rapid detection of L. monocytogenes in food matrices, lateral flow enzyme immunochromatography together with an immunomagnetic separation has been developed recently [Cho & Irudayaraj 2013].

Molecular tools such as PCR, multiplex PCR and real-time PCR employing virulence-associated genes such as the mpl gene, prfA gene [Rossmanith et al. 2006] and ssrA gene [O'grady et al. 2008] have been found rapid, specific, reproducible and reliable [Portnoy et al. 2002; Gianfranceschi et al. 2013; Hage et al. 2014; Khan et al. 2014]. Several multiplex PCR assays have been developed for simultaneous detection of various food-borne pathogens like Salmonella, Escherichia coli, Staphylococcus and also Listeria [Park et al. 2006; Kawasaki et al. 2009; Lee et al. 2014]. Multiplex real-time PCR assay based on molecular beacon chemistry was developed recently which could detect eight food-borne pathogens [Salmonella enterica subsp. enterica, L. monocytogenes, E. coli O157, Vibrio parahaemolyticus, V. vulnificus, Campylobacter jejuni, Enterobacter sakazakii and Shigella spp.]. Sensitivity and specificity of this multiplex real-time PCR assay was near to 100% which suggest its promising potential for being used as a valuable diagnostic tool for food-borne pathogens, including Listeria, with high precision [Hu et al. 2014]. Targeting the hly gene in PCR has been found to be a sensitive and rapid method for confirmation of L. monocytogenes from selective/differential agar plates. Combined use of ELISA and PCR has been suggested for confirmatory diagnosis of listeriosis [Amagliani et al. 2006]. For studying epidemiological relatedness among Listeria isolates using various virulence genes such as the prfA, inlB, inlC, dal, clpP, and lisR, multi-virulence-locus sequence typing [MVLST] may be performed [Spratt 1999; Viswanath et al. 2013]. Pulsed-field gel electrophoresis [PFGE] using ApaI and AscI enzymes has been considered as ‘gold standard’ in subtyping Listeria for epidemiological purposes and disease outbreak investigations [Graves & Swaminathan 2001; Foerster et al. 2012]. However, World Health Organization recommended restriction endonuclease analysis [REA] of chromosomal DNA using HaeIII, HhaI and CfoI restriction endonucleases for serotyping [Graves et al. 1999; OIE 2014]. Other approaches for subtyping of L. monocytogenes include serotyping, phage typing, multilocus enzyme electrophoresis [MEE], nucleic acid sequencing-based typing, microarray analysis, amplified intergenic locus polymorphism [AILP], random amplification of polymorphic DNA [RAPD] [OIE 2014] and biosensor [Zhao et al. 2006; Suo et al. 2010]. Loop-mediated isothermal amplification [LAMP] has also been developed that is 100 fold more sensitive as compared to conventional PCR and could detect 2.0 cfu per reaction. Accuracy of the assay is also 100% in comparison to gold standard culture and biotechnological assays [Tang et al. 2011]. Immunoassay based on nanotechnology has also been developed that can detect minute quantities of Listeria in environmental samples [Jaakohuhta et al. 2007]. Recent progress in molecular detection techniques, comprising PCR, real-time PCR, multiplex PCR, LAMP, recombinant protein-based diagnostics, biosensors, biochips, microarrays, gene sequencing, phylogenetic analysis and nanodiagnostics, needs to be further exploited to their full practical potentials [Schmitt and Henderson 2005; Bollo 2007; Bergquist 2011; Deb and Chakraborty 2012; Dhama, Karthik, et al. 2014; Dhama, Chakraborty, et al. 2014; Verma et al. 2014].

Being an intracellular organism that requires effector T cells for effective immune response, it is very difficult to develop effective vaccines against L. monocytogenes. An in silico study based on sequences of LLO that plays a crucial role in pathogenicity has been used [Jahagir et al. 2011]. Experimental vaccines in laboratory animals [listerial antigens, IL-12, CD40 signalling along with heat-killed L. monocytogenes, plasmid DNA, LLO-deficient mutants inoculated along with liposome-encapsulated LLO, etc.] are being explored to confer protection against L. monocytogenes. However, efforts are still far away in availability for use [OIE 2014]. Type-1 polarized dendritic cells have been found to be effective in enhancing protective immunity against intracellular bacteria like L. monocytogenes [Kono et al. 2012].

For development of protective immunity against L. monocytogenes, recent advances in the field of biotechnology has greatly aided [Mohamed et al. 2012]. As the bacterium is found intracellular, it induces a long-lasting cellular immune response and as a consequence an attenuated vaccine may be a good candidate for vaccination. Live attenuated vaccine causes stimulation of the innate as well as adaptive immune response [Le et al. 2012]. Deletion of the frvA [Fur-regulated virulence factor A] leads to disruption of iron homeostasis and subsequent decrease in virulence of bacteria, thereby potentiating the use of this strain as live attenuated vaccine as well as a vehicle for vaccine delivery in future [McLaughlin et al. 2013]. Experiments on mice showed generation of high level of antibodies against L. monocytogenes using a combination of recombinant p60 and LLO [Luo & Cai 2012]. Development of recombinant listerial vaccine has led to induction of CD8[+] T-cell responses which are protective, antigen-specific and reduce CD4[+] T-cell mediated inflammation. For induction of the Th1 response, a DNA vaccine has been developed with a prime/boost vaccination schedule [Figure 3]. This causes induction of class-I restricted CD8[+] T cells that cause expression of cytotoxic T-lymphocyte activity [Ladel et al. 1994; Fensterle et al. 1999; Russman et al. 2001; Dhama et al. 2008; Chen et al. 2012]. Use of adenoviruses as vehicles for transferring foreign genes in a vaccine setting elicits strong cellular immune response involving both CD8[+] and CD4[+] T cells. This concept has been utilized for development of vaccines against L. monocytogenes, wherein adenoviral vector encodes soluble antigens derived from L. monocytogenes, i.e. listeriolysin and p60 [Darji et al. 2003; Jensen et al. 2013]. Apart from this, gas-filled microbubbles [MB] has also been successfully used as an antigen delivery system for L. monocytogenes in inducing specific effector CD8[+] T cell responses [Bioley et al. 2013, 2015].

There is certainly no need for a vaccine to be used in the general population, given the overall low incidence of the disease. However, vaccines for L. monocytogenes are especially required to tackle the infection in sheep. High-risk individuals also need to be protected by use of an effective vaccine. Hence, efforts to develop a vaccine against listeriosis need to be continued. In this regard, due emphasis should be given in exploring great potentials of new-generation vaccines, including DNA vaccines, plant-based vaccines, vector vaccines, protein/peptide vaccines, recombinant protein-based vaccines, along with improving vaccine delivery systems like nanovaccines, to combat listeriosis [Meeusen et al. 2007; Dhama et al. 2008; Dhama, Wani, et al. 2013; Koff et al. 2013].

Treatment of listeriosis may be a difficult task because L. monocytogenes can invade virtually all cell types. Time period of treatment may vary according to the level of infection. In livestock and human beings, antibiotics have been used since long time for treatment of listeriosis. Usually, treatment in sheep and goat has little value soon after the appearance of neurological signs or in the chronic form. Sulphonamides, penicillin and tetracycline may be used as prophylactics [Radostits et al. 2008]. However, the cure rate in the immunocompromised host is low. Drugs of choice for human listeriosis are erythromycin and ampicillin. Chlortetracycline at 10 mg/kg BW per day administered for 5 days intravenously is effective in encephalitis cases of cattle. Penicillin at 44,000 IU/kg BW IM can be given daily for 7 days along with supportive therapies such as rehydration with electrolytes. Treatment of listerial iritis involves systemic antibiotics in early stages coupled with subpalpebral corticosteroid and atropine to dilate the pupil [Starič et al. 2008]

Drug of choice for listeriosis was known to be ampicillin. However, in 1984, resistance towards this drug has been reported [Rapp et al. 1984; Rivero et al. 2003]. Irrational use of this antibiotic in animals has been suggested as one of the reasons for development of resistance against ampicillin in human listeriosis through animal-derived foods [Srinivasan et al. 2005; Mathew et al. 2007; Tiwari et al. 2013]. Gentamicin has been found effective in treatment of bovine genital listeriosis [Chopra et al. 2012]. Listeria isolates from food, environment, animal and human sources have been found to be resistant to commonly used antibiotics, including gentamicin, cotrimixazole and ofloxacin [Low & Donachie 1997; George 2002; Rahimi et al. 2012; Soni et al. 2013; Ndahi et al. 2014]. Since chemotherapy with antibiotics is the only available method for treatment of listeriosis, judicious use of these drugs in medical and veterinary practices along with monitoring of antibiotic susceptibility is very important [Okada et al. 2011; Barbosa et al. 2013].

During the current era where there are concerns for increased antibiotic resistance of bacterial pathogens along with issues related to food safety, use of bacteriophages is of major interest. Bacteriophage therapy has been found useful to control L. monocytogenes in poultry meat and meat products during processing and packaging of raw and ready-to-eat meat and its products [Leverentz et al. 2003; Carlton et al. 2005; Kim et al. 2008; Soni et al. 2010; Bigot et al. 2011; Tiwari et al. 2011; Dhama, Verma, Rajagunalan, et al. 2013; Klumpp & Loessner 2013]. Various phages that are specific for lysis of Listeria are used in the dairy and meat industry to prevent its entry into the human food chain. Listeriophages have been found abundantly in silages of dairy farms [Vongkamjan et al. 2012]. In dairy industry, Ply511 phage has been used successfully to control Listeria [Gaeng et al. 2000; Karthik et al. 2014]. FDA-approved commercial products of phages are presently available that can be used in poultry industries [Soni et al. 2010]. ListexP-100 [the Netherlands] and ListShield [USA] are two of the products used to control Listeria organisms [Chibeu et al. 2013; Karthik et al. 2014]. Bacteriocins such as nisin have been used in meat mince to inhibit L. monocytogenes [Pawar et al. 2000]. Synergistic action between listeriophages and the bacteriocin coagulin C23 demonstrated inhibition of L. monocytogenes in refrigerated milk [Rodríguez-Rubio et al. 2015].

Essential oils of plant origin also have potential antimicrobial properties and can reduce Listeria survival in various products [Gopi et al. 2014]. Essential oils like thyme, rosemary and oregano possess antilisterial action on stored vegetables [Scollard et al. 2009]. Essential oils from Cinnamomum cuspidatum and C. crassinervium showed a significant inhibitory effect against L. monocytogenes [Vairappan et al. 2014]. Bio-oil yielded from pyrolysis of pinewood sawdust when used at the concentration of 1000 μg/disc was found to produce 10.6–12.0-mm inhibition zone for L. monocytogenes [Patra et al. 2015]. Use of probiotics has also been suggested to significantly inhibit L. monocytogenes. Immunity is relatively enhanced by probiotics, thereby leading to prevention of infection due to the bacterium. Timely use of a multistrain probiotic is necessary for the best results [Dhama, Verma, et al. 2011; Dhama, Verma, Rajagunalan, et al. 2013; Dhama, Rajagunalan, et al. 2013].

In addition, use of Chinese and Japanese herbal remedies in animal studies has been suggested to be effective in Listeria-associated food poisoning [Thongson et al. 2005; Tosun et al. 2011; Lee, Kim, et al. 2013]. Several studies have been conducted with various plant extracts for their anti-listerial properties. Alcoholic extracts of plants like Allium vineale, Chaerophyllum macropodum and Prangos ferulacea [Sagun et al. 2006; Witkowska et al. 2013] as well as oregano, clove, rosemary, sage and celery have proved effective against L. monocytogenes [Witowska et al. 2013]. Yoon and Choi [2012] studied 69 herbal extracts against L. monocytogenes that showed two extracts, namely Psoraleae semen L. [Bogolji] and Sophorae radix L. [Gosam], as promising antilisterial agents. Computational approaches like docking were also used to predict herbal drug targets against Listeria, thereby evaluating herbal extracts in vitro. A docking study was carried out with 97 herbs where cinnamic aldehyde [[E]-3-phenylprop-2-enal]] and 1,2-epoxycyclododecane[13-oxabicyclo[10.1.0.0]tridecane] were found effective against Listeria. These two compounds were effective in inhibiting the general secretory pathway [SecA], thereby reducing virulence of the organism [Skariyachan et al. 2015].

Cytokines are used as adjunctive modulators in various infectious diseases. Endogenous cytokines like gamma-interferon [IFN-gamma], tumour necrosis factor – alpha [TNF-alpha], as well as interleukin-6, play protective roles in resistance of host against intracellular pathogens including Listeria [Nakane et al. 1995]. In mice, a non-lethal L. monocytogenes infection may result in induction of IL-4 and IL-10 which may lead to detrimental effects. It is, however, important to note that the bacterium causes modulation of cytokine responses in macrophages [Nakane et al. 1999; Stoiber et al. 2001]. Nanotechnology has also been used in the fight against Listeria in food industry such as Nanoclay [Hong & Rhim 2008].

To prevent gut-associated infections, chicken eggs are used nowadays as a source of valuable antibodies [Mine & Kovacs-Nolan 2002; Yin et al. 2011]. Avian egg yolk antibodies against Listeria have shown promising results by inhibiting Listeria in various samples tested [Sui et al. 2011] [Figure 3]. Enterocin CRL35, a peptide possessing bacteriocin property, when tested in a murine model was found to have anti-listerial activity [Salvucci et al. 2012]. Bacteriocin activity has been attributed to a 28-mer fragment of this enterocin, demanding further insights into the peptide for finding a novel area for preventing the food-borne listerial infections [Masias et al. 2015]. Another enterocin, namely AS-48, from Enterococcus has also revealed a good effect against various food-borne pathogens including Listeria when combined with essential oils and preservatives [Grande Burgos et al. 2014]. The use of Salmine, a peptide obtained from the milt of Salmon, which possesses antibacterial property, demonstrated inhibition of listerial growth in smoked salmon. However, its efficacy to prevent Listeria needs further exploitation for developing a commercial product [Cheng et al. 2015].

Novel and alternative/complementary immunomodulatory and therapeutic modules including immunotherapy, cytokines, avian egg antibodies, toll-like receptors, phages, enzybiotics, probiotics, nutritional immunomodulation, herbs and nanomedicines need proper attention for formulating effective prevention and control strategies against listeriosis and its public health concerns [Mahima et al. 2012; Dhama, Chakraborty, Mahima Wani, et al. 2013; Dhama, Chakraborty, et al. 2014; Tiwari et al. 2014].

Control of listeriosis is difficult because of the ubiquitous nature of the causative organism, lack of a simple method of identifying the presence of Listeria contamination in the environment and a poor understanding of risk factors other than silage. However, some of the control measures are as follows:

• Proper disposal of contaminated materials, beddings and litters, and infected carcasses should be done carefully by incineration or burning methods.

• Animals should not be fed with rotten vegetables.

• Proper hygiene and sanitation should be maintained at animal farms.

• In endemic areas, silage should not be fed to animals.

• Follow use of tetracyclines in ration of animals at risk as a preventive measure when there is a disease outbreak.

• Wear protecting cloth while handling infected animals, aborted material, or removing retained placenta.

• Spoiled silage should not be fed to animals.

• Immunocompromised hosts are more susceptible to listeric infections and, in these cases, appropriate and timely precautions need to be taken.

• Routine testing of raw milk or raw milk testing programme should be conducted to reduce the number of cases per year [Latorre et al. 2011].

Sweet buttermilk powder contains milk fat globule membrane [MFGM] which prevents adherence of pathogen to intestinal mucosa and protects against listeriosis infection [Sprong et al. 2012]. Bacteriocins, disinfectants, phages, proper processing and packaging practices in food processing industries can limit spread of Listeria to human population through the food chain. Bacteriocins including pediocin and nisin have been studied by various workers and found to be effective for use in food processing industries [Muriana 1996]. Enzymes like protease, lipase and cellulase were shown to inhibit biofilm formation [Longhi et al. 2008]. Crucial factors for disease prevention include timely detection, keeping away/eliminating possible sources of infection, maintaining high hygiene/sanitation standards and following good management practices in poultry farms and poultry processing units, discarding infected poultry at entry level of processing plants, adapting appropriate disinfection measures with proper culling and quarantine/isolation of affected birds [Swaminathan 2001; Cutter & Henning 2003; Kosek-Paszkowska et al. 2005; Malik & Vaidya 2005; Rossi et al. 2008; Dhama, Tiwari, et al. 2011; Dhama et al. 2012; Oh et al. 2014]. Control of listeriosis on a pre-harvest basis on farms should be based mainly on manure control, silage, health of herd and milking practices [Farber & Losos 1998; Borucki et al. 2004; Antognoli et al. 2009; Little et al. 2009; Buckley & Reid 2010; Santorum et al. 2012]. Antibiotics usage in feed is of prophylactic value for prevention of listeriosis in poultry. However, Listeria may survive non-stringent sanitation protocols in meat processing facilities [Tompkin et al. 1992; Slutsker & Schuchat 1999; Schelch & Acheson 2000]. Unusual growth and survival ability of L. monocytogenes along with adherance to various surfaces pose difficulties in its elimination. Practices of inadequate cooking or cross contamination after cooking may lead to the presence of Listeria in cooked foods Barbuddhe, Malik, et al. 2008]. To reduce contamination, control of pH and water activity, applying preservatives and checking shelf lives may be helpful. Refrigerated/frozen meat and meat products are more likely to be contaminated during their preparation and storage as compared to fresh meat, leading to higher incidences of Listeria in such situations [Tompkin et al. 1992; Cutter & Henning 2003]. Avoiding consumption of Listeria-contaminated foodstuffs prevents incidences of disease in human beings [Mateus et al. 2013]. The emerging era of antibiotic resistance among bacterial agents also poses high public health concerns for food-borne pathogens like Listeria [Tiwari et al. 2013]. Identification of high-risk foods and increased awareness of high-risk individuals [newborns, older and immunocompromised persons, pregnant women] as well as consumers regarding predisposing factors and risks of contracting listeriosis need proper attention [Rappaport et al. 1960; Rebagliati et al. 2009; Dhama, Verma, Rajagunalan, et al. 2013; Dhama, Rajagunalan, et al. 2013]. Practice of common usage of antibiotics in poultry feed as growth enhancers and prophylactics have significantly resulted into reduction of cases of listeriosis in poultry [Low & Donachie 1997; Dhama, Verma, Rajagunalan, et al. 2013]. Quaternary ammonium compounds can be used to disinfect food processing areas, but recently a transposon named Tn6188 has been identified in Listeria that cause tolerance to these disinfectants [Müller et al. 2013].

The present era of liberal globalization events and increasing trade options, changing food habbits, ecosystem and biodiversity changes and emerging microbial resistance to antibiotics warrant the quest for potent treatment options and prophylactics, implementation of strategic veterinary and medical networking, surveillance and monitoring programmes at national/international levels to prevent and control listeriosis in animals and humans [Kahn et al. 2007; Dhama, Verma, Tiwari et al. 2013; Dhama, Chakraborty, Kapoor, et al. 2013; Dhama, Chakraborty, et al. 2014; Verma et al. 2014]. Apart from these, sound implementation of good management practices, strict biosecurity measures, raising standards of hygiene and sanitation, timely follow-up of appropriate isolation and quarantine practices, and suitable trade restrictions need to be considered for effective prevention and control of Listeria and its public health implications.

Risk of cross-listerial contamination can be reduced by keeping uncooked meat away from other food substances. Hands along with knives and cutting boards must be washed after handling of uncooked meat. Organisms present in utensils can be killed by moist heat [121 °C for a minimum of 15 min] or dry heat [160–170 °C for 1 hour]. It is essential to practice cooking of raw meat thoroughly and properly [Schelch & Acheson 2000; Bremer et al. 2002; Rebagliati et al. 2009; Khen et al. 2015]. There is a need to store food properly and follow good kitchen hygiene practices [Khen et al. 2015]. Heating of packed as well as frozen meat products has to be further done according to instruction of manufacturers. Use of chlorine at 100 mg/kg along with UV radiations [300 mWs/cm2] has been found effective in inhibiting growth of L. monocytogenes in chicken meat [Oh et al. 2014]. For inactivation of organisms, disinfectants like 1% sodium hypochloride along with 70% ethanol must be used. Prevention of disease can be satisfactorily done by wearing protective clothing while handling infected animals, birds or their tissues. Efforts should also be made for applying control measures at fish ponds since fish products may serve as an important source of listeriosis [Nakari et al. 2014]. Tannin-rich fraction from pomegranate rind [TFPR] and acid-hydrolyzed Citrus unshiu peel extract have been found to be effective food preservatives in reducing chances of L. monocytogenes contamination in foods [Li et al. 2014; Min et al. 2014]. Food safety control measures must be implemented properly to limit listeriosis and to ensure consistent control strategies [Oyarzabal 2006; Adzitey & Huda 2010]. Good manufacturing practices [GMP], good hygiene and sanitation in operating procedures are the most appropriate strategies in operating procedures. This must be followed along with hazard analysis critical control point [HACCP] programmes, improved education about disease, its modes of transmission as well as suitable prevention measures [Mateus et al. 2013; McCollum et al. 2013]. To minimize environmental contamination by this organism, GMP will help thereby preventing cross-contamination in processing plants, packaging units as well as retail counters. Time as well as temperature controls must be appropriate during the entire distribution and storage period of packed meat and meat products. For destruction of L. monocytogenes in food products, there is a need of implementation of post-packaging treatments [USFDA 2001]. Several inert surfaces can be colonized by L. monocytogenes, thereby leading to the formation of biofilms on food processing surfaces [Roberts & Wiedman 2003]. At low temperature, this organism has the capacity to grow, for which thorough cooking along with prevention of cross-contamination and short-term refrigerated storage of cooked perishable foods is certainly a useful step to avoid disease [Oyarzabal 2006; Gillespie et al. 2006; Dhama, Verma, Rajagunalan, et al. 2013]. There must be provision for high-risk individuals for guidance on safe as well as healthy eating practices along with specific information on high-risk foods which must be avoided. Antenatal advice on prevention of listeriosis is essential as many mothers usually eat high-risk foods during their pregnancy [Wong et al. 2013].

Though listeric infections are zoonotic and cause havoc to humans and animals, these bacteria are also being studied for their potential usefulness in cancer treatment [Tangney & Gahan 2010]. Since Listeria is an intracellular pathogen, researchers have tried to use it as a potential carrier for developing cancer therapeutics [Barbuddhe & Chakraborty 2008]. Several workers have also tried both live and attenuated vaccines with Listeria as a carrier vector of tumour-associated antigens for immunotherapeutic purposes against human cancers [Paterson et al. 2010; Shahabi et al. 2011]. ActA of Listeria had been found to possess adjuvant property for primary and metastatic tumour immunotherapy [Wood et al. 2010].

Listeriosis caused by L. monocytogenes is a fatal infectious disease of mammals, birds and humans, characterized by septicaemia and encephalitis. It is a major problem in developing countries where there is scarcity of food as well as unhygienic conditions. As disease is under-rated in most countries and situations, extensive epidemiological investigations and data are required to know the current status and magnitude of infection to design and adapt an effective disease control programme at national and global level. Considering major food-borne zoonosis, due attention needs to be given towards rapid diagnosis and effective treatment/prevention. With advanced molecular tools like PCR, real-time PCR and multiplex PCR, diagnosis of disease has become much easier. Recently, documented food-borne outbreaks of listeriosis have highlighted the need for improvement in isolation as well as identification procedures of Listeria. Currently the need is better understanding about its persistence outside mammalian hosts, role of various virulence factors for survival over a wide range of temperature and materials needs to be elucidated well for sketching a better prevention programme. More studies from developing countries are required to take into account regional differences in clinical outcome of listeriosis. Considerable utility exists as a model to understand several aspects of host–pathogen interaction along with cell biology and host immunity. Novel and alternative therapeutic options such as bacteriophages, egg yolk antibodies, cytokines, herbs, essential oils and probiotics could pave way for generating valuable and effective treatment modules to combat listeriosis. Suspected silages, vegetables and foodstuffs should be appropriately disposed off so as to prevent and control incidences of listeriosis both in animals and humans. Consumption of unpasteurized milk or uncooked meat should be avoided. Currently, prevention is the only way to protect animals and humans from listeriosis which can be achieved by good managemental practices. Development of a good vaccine remains a lacuna and recent advances in vaccine technology like mutant vaccines, DNA vaccines or even RNAi technology can be studied for their efficacy against listeriosis. Though plasmid DNA or heat-killed organism-based vaccines have been developed, yet these are far from being valuable for human and animal use. However, development of such vaccines has helped in understanding the mode of immune responses against listeriosis.

All the authors of the manuscript thank and acknowledge their Institutes and Indian Council of Agriculture Research, Delhi, India.

The authors declare that they have no competing interests.

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