Open access peer-reviewed chapter

Non-Typhoidal Salmonellosis: A Major Concern for Poultry Industry

Written By

Mamta Pandey and Emmagouni Sharath Kumar Goud

Submitted: 16 October 2020 Reviewed: 03 February 2021 Published: 24 February 2021

DOI: 10.5772/intechopen.96400

From the Edited Volume

Salmonella spp. - A Global Challenge

Edited by Alexandre Lamas, Patricia Regal and Carlos Manuel Franco

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Abstract

Salmonella is the most important gastrointestinal pathogen distributed ubiquitously. The major serovars involved in Non-typhoidal salmonellosis are S. Typhimurium and S. Enteritidis. In the viewpoint of ban in the export and import of the Salmonella contaminated poultry food and poultry products, the need for rapid detection and mitigation of Salmonella has increased mani-folds. The major problem associated with its control is the growing incidence of antimicrobial resistance, which has been reported worldwide in the recent years. From causing self limiting gastroenteritis they have found to be responsible for several fatal diseases like endocarditis, meningitis, lung infestations, appendicitis, pneumonia, and cerebral abscess in human beings. Targeting several proteins such as adhesive proteins, lipoproteins, outer membrane proteins (Omps) etc. as vaccine candidates may pave a way in its control. So, continuous monitoring using one health approach and development of effective treatment and control strategies are critical.

Keywords

  • non typhoidal Salmonella
  • gastroenteritis
  • multiple drug resistance
  • poultry
  • vaccine

1. Introduction

Non-typhoidal Salmonellosis is caused by bacteria belonging to Enterobacteriaceae family. In poultry, Salmonella is known to be present in the gastrointestinal tract without showing any symptoms [1]. This leads to an undetected condition at farm level and after consumption of such poultry products like meat and eggs, humans gets infected at fork end. Domestic animals act as a reservoir for the food-borne spread of host-generalist serovars, which accounts for worldwide incidence of non-typhoidal Salmonella (NTS) infections. The range of symptoms varies from self limiting gastroenteritis to various dreadful diseases like endocarditis, meningitis etc. Generally condition becomes severe in children, geriatric and immunocompromised individuals [2]. NTS accounts for 93 million enteric infections and 155,000 deaths globally on annual basis [3]. The two factors contributing to majority of NTS infections are its broad host range and multiple drug resistance (MDR), which has been reported universally in recent years [4]. In developing countries, the situation is grimmer due to poor hygienic conditions. Near about 100 cells of virulent Salmonella are sufficient to cause infection in humans, which will further depend upon the health condition of an individual [5], hence it is critical to adopt multiple intervention strategies. Vaccination is considered as an effective tool to control the disease [6], but the available vaccines has their own restrictions such as short term immunity etc. which limits their applicability. So, there is a must requirement to develop a suitable vaccine against NTS. Several proteins such as lipoproteins, outer membrane proteins (Omps) and polysaccharides have been targeted to evaluate their potential as suitable vaccine candidates. This chapter aims to present a brief overview on some such valuable information on NTS.

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2. Non typhoidal Salmonella strains and its transmission

Till now, more than 2500 serotypes of Salmonella have been identified [7]. Non typhoidal salmonellosis is caused by all serotypes of Salmonella except for Typhi, Paratyphi A, Paratyphi B and Paratyphi C. Poultry can get infected either with host-specific Salmonella serovars, like S. Pullorum and S. Gallinarum, which cause a typhoid-like systemic disease or wide ranged NTS. Wide range NTS represents Salmonella enterica subspecies enterica serovar Enteritidis and Typhimurium together with serovars such as S. Newport, S. Heidelberg and S. Javiana etc. Broad host ranged S. serotypes get colonize [8] in host and carry infection asymptomatically. Salmonella enterica serotype Enteritidis and Typhimurium are the two most important NTS serotypes transmitted from animals to humans in most parts of the world [9].

NTS transmission usually occurs through consumption of contaminated food i.e. chicken, eggs, pork, beef, dairy products, and water contaminated with animal feces. However, contact with animals such as reptiles and animal environment are equally important sources [10]. Majority of reptiles are known to carry Salmonella as part of their natural intestinal flora. In poultry, mode of transmission can be vertical or horizontal. Vertical transmission occurs when parent poultry is suffering from systemic infection or transovarian infection which results in infection of infants. S. Enteritidis serovar have a particular preference to this mode of transmission. Polluted feed and drinking water, dirty cages, fomites etc. includes horizontal mode of transmission. Colonization of Salmonella in poultry without showing any sign and symptoms is common, hence, its transmission in layers (vertical) and broilers (horizontal) can occur at primary production level [11]. Transmission through eggs and meat from such healthy poultry with colonized NTS is common [12]. The degree of Salmonella colonization depends on parameters specific to Salmonella and effects of environmental stimuli on gene expression. Factors such as age, environmental and physiological stress, diet, and survival of Salmonella through gastric barrier, use of antimicrobials in the farm, chicken health, and genetic background of the chicks could possibly influence the colonization [13]. In poultry farms transmission can also occur through workers, vehicles, clothing, footwear, garbage, insects, rodents, wild birds, pets, equipment, and many other factors. In humans, factors contributing to susceptibility of NTS infections include pernicious anemia, any previous gastric surgery, excessive use of medications responsible for gastric barrier reduction etc. [14]. Other associated susceptibilities include homozygosity for sickle cell anemia [15], HIV [16], malaria [17], malnourished infants, and young adults [18].

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3. Global disease epidemiology

In many countries, over the past years, the incidence of NTS has increased markedly. In western countries, the predominant serotypes are S. Typhimurium and S. Enteritidis. In United States, each year NTS causes approximately 1.35 million illnesses, 26,500 hospitalizations, and 420 deaths [19]. As per the fact sheets of World Health Organization, NTS is 1 of 4 key global causes of diarrhea. The burden is so substantial that every year 33 millions of lives are lost. In Europe, NTS is the second most investigated zoonosis responsible for causing gastrointestinal infections in humans. As per the European Food Safety Authority (EFSA) and European Centre for Disease Prevention and Control (ECDPC) reports, the number of confirmed cases of salmonellosis in Europe still remains high, with a total of 91,857 cases reported in 2018 [20]. The estimation of the total number of NTS infections is a difficult task in developing and under-developed countries, a possible reason to this may be non-reporting of the diseased cases to hospitals. The epidemiological pattern has been variable over the past decade in African countries. Sub-Saharan African region is principally affected region in Africa. According to the hospital based studies of Africa, NTS is the second most frequently occurring pathogen in children and is leading cause of bacteremia in adults [21]. A population-based surveillance data reported the incidence to be between 0 and 54 cases per 100,000 person-years of observation in 13 surveillance sites [22]. The disease incidence ranged from 1.4/100,000 population/year in South Africa (all ages) to 2,520/100,000 population/year in Ghana (<5 years of age) [18]. The community acquired NTS bacteremia prevalence varied from 8% in Nigeria to 45% in Central African Republic [18]. From Kenya, documented incidences were found to be 4134/100,000 person-years [23]. According to the Statistical Committee of the Republic of Armenia, a total of 4,392 cases of salmonellosis were reported during the period 2010–2019, comprising at least 50% of patients below 6 years of age [24]. There is a scarcity in data related to NTS infections from several regions of Asia, limited reports are available from India [25], and Taiwan [26]. A hospital-based multicenter study from Indonesia, Thailand, and Vietnam, investigated NTS positivity rates of 27.5% and 11.7% in children and adults respectively from bacteremia cases [27]. From 2009 to 2013, the prevalence rate of NTS was found to be limited 20/12,940 in bacteremia patients with 25% case fatality report in Bangladesh [28]. In Malaysia, reported prevalence was 16.2%, among which most of the affected cases were from children below 1 year of age [29]. A variety of NTS serovars are known to be present in South-East Asia [30], even some less common serovars are also known to be prevalent such as occurrence of S. enterica Weltevreden from the farms of Vietnam [31].

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4. Clinical manifestations

NTS infections can cause several clinical symptoms depending on the type of serovar and host factors in humans. NTS symptoms are generally non-specific and hence their identification is a challenging task particularly in areas where laboratory diagnosis facilities are not accessible. Most commonly, Salmonella causes self limiting gastroenteritis in human beings. After an incubation period of 6–72 h (mean 24 h), there is sudden onset of nausea, vomiting, abdominal pain and tenderness, followed by mild to severe watery diarrhea and sometimes diarrhea may contain blood and mucus. The stool examination reveals a moderate number of polymorphonuclear leukocytes and blood. Fever is seen in about 70% of patients. Usually, symptoms subside within 2–7 days in healthy children. In certain high-risk groups, like in neonates, young infants, and immunodeficient individuals symptoms may persist for several weeks. As a complication of gastroenteritis, transient bacteremia may occur in some patients (reported incidences in approximately 5% of the patients) [32]. Certain serotypes i.e. S. Choleraesuis and S. Dublin show a higher predisposition for bacteremia in humans [33]. After gaining entry to the bloodstream, Salmonella get metastasize to different organs and cause focal suppurative infection. In sickle cell anemic patients a common finding as a result of NTS is osteomyelitis [34]. Less frequent occurrence of meningitis has been observed specially in infants [35]. Despite of antibiotic therapy, patients may develop rapid neurological deterioration. Other feared lethal complications include development of endarteritis [36], endocarditis [37], meningitis [38], lung infestations [39], appendicitis [40], pneumonia [41], bone and joint defects [15] and cerebral abscess [42].

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5. Multiple drug resistance

In current scenario, there has been an extensive increase in documentation of antimicrobial resistance in NTS. Multiple drug resistance (MDR) is the antimicrobial resistance shown by the microorganism to at least three different groups of antimicrobials. Some Salmonella strains are characterized by carrying several antimicrobial resistance. The possibility of having MDR in bacteria is due to the presence of several different resistance genes or a single resistance gene that shows resistance to more than one antibiotic. Some important factors that could cause MDR in microorganisms include selective pressures, proliferation of multiple resistant clones, and inability to detect emerging phenotypes. The overuse or misuse of antimicrobials for the treatment of human disease, in agriculture, and in-home disinfectants comes under selective pressure [43]. The development of the antimicrobial resistance in bacteria is as a result of the genetic modifications of a microorganism for its own survival either spontaneously or acquired. In spontaneous mutation, a genetic modification occurs naturally which helps to survive from the lethal effects of antimicrobials. The reason behind the occurrence of spontaneous mutations is unknown, but the exposure to the antimicrobials may provide selective pressure for antimicrobial resistance [44]. Acquired resistance eventuate from gene transfer from other bacteria [45]. High resistance rate have been reported from S. Typhimurium DT104, resistant to five antimicrobial agents i.e. ampicillin, chloramphenicol, streptomycin, sulphonamide, and tetracycline [46]. Resistance to some extended spectrum antibiotics like cephalosporins and fluoroquinolones have been increasingly reported [47]. The emergence of S. Choleraesuis resistance to multiple antibiotics including ciprofloxacin has posed serious public health concerns [48].

Bacteria develop MDR by three different mechanisms. In first mechanism of resistance, the bacteria are known to produce certain specific proteins such as hydrolytic enzymes, which destroy the antimicrobials present in their surroundings. An example to this is penicillin resistance, where Salmonella produces β-lactamases enzymes which cleave the β-lactam ring of active penicillin and convert it into its inactive form [49]. The second mechanism of resistance is the presence of an active efflux pump system in the cell which actively pumps out the antimicrobials before they become effective [45]. Salmonella have energy-dependent efflux pumps for tetracycline and chloramphenicol which inhibit protein synthesis in bacteria by binding to tRNA to the A-site of the 30S subunit of the ribosome [50]. The third mechanism of resistance is called as the receptor modification in which the bacteria tends to chemically modify or mutate the target of the antimicrobial agent. For example vancomycin is the antibiotic which binds with D-Ala-D-Ala on the cell wall and inhibits the peptidoglycan synthesis of the cell wall of bacteria. But vancomycin-resistant enterococcus mutates its terminal peptide to D-Ala-D-Lac that has a lower affinity for vancomycin [45]. The mechanism of action adopted by Salmonella for different antimicrobial classes has been enlisted in Table 1. Plasmid mediated resistance determinants (genes) to antimicrobials have been known to be responsible for the worldwide dissemination of several Salmonella serotypes i.e. Enteritidis, Heidelberg, Typhimurium, Infantis, Virchow, Kentucky. The most common genes found in poultry and its meat products are β-lactamases, CTX-M (CTX-M-1, −2, −9 and − 15), TEM-52, AmpC-type CMY-2. The transmission of these genes is associated with diverse plasmid families such as Incl l (blaCTX-M-1, blaTEM-52, blaCMY-2), Incl A/C (blaCMY-2), Incl H12 (blaCTX-M-2, blaCTX-M-9). Plasmid mediated quinolone resistance is governed by QnrB2, QnrB19, QnrS1 genes. The genes mediating R-type ACSSuT in NTS are commonly clustered together in Salmonella genomic island 1 (SGI-1), a chromosomal genetic element.

Antimicrobial classAntimicrobial mechanism of action by SalmonellaReference
AminoglycosidesDecreased drug uptake, drug modification, and modification of the ribosomal target of the drug[51]
Beta-lactamsSecretion of β-lactamase enzymes[50]
PhenicolsEnzymatic inactivation of the antibiotic by chloramphenicol O-acetyl-transferase and removal of the antibiotic by an efflux pump[52]
QuinolonesInducing mutations in the quinolone resistance determining region, increased efflux pumps expression and decreased outer membrane permeability.[53]
TetracyclineProduce energy dependent efflux pumps to remove tetracycline out from the bacterial cell[54]
Sulfonamides and trimethoprimExpression of sul genes i.e. sul1 or sul2 for sulfamethoxazole resistance and dihydrofolate reductase (dfr) genes for trimethoprim[55]

Table 1.

Antimicrobial mechanisms of Salmonella for different antimicrobial class.

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6. Antimicrobial resistance in poultry food chain

The practice of using antimicrobials in food animals is rigorous, it may be either for growth promotion, prophylactic, therapeutic or metaphylactic reasons and this results in MDR. In poultry sector, the use of antimicrobials as growth promoters, such as bambermycin, bacitracin, chlortetracycline, penicillin, tylosin, fluoroquinolones and cephalosporins is concerning [56]. Consumption of low doses of antibiotics in poultry feed for rapid poultry growth is a general practice. Use of antibiotics not only kill majority of the gut microbiota, but, some resilient bacteria survive and become resistant. Over time, these resistant bacteria transfer antibiotic resistant genes to other susceptible microbial population. The situation is crucial in developing countries where laws to control the sale and use of antibiotics are not strict. For therapy, antimicrobials like erythromycin, fluoroquinolones, gentamycin, neomycin, penicillin, spectinomycin, tetracyclines and tylosin are commonly used in poultry [56]. The minimum time period from administering the last dose of medication to the production of meat or other animal-derived products for consumption purpose is referred to as withdrawal period. The withdrawal period for antimicrobials should be followed strictly, in order to prevent the detrimental effects of drug residues in food. There are numerous programmes to reduce the flow of foodborne pathogens from animals to humans, for instance programs for meat and poultry inspection, Hazard Analysis Critical Control Point (HACCP) system and standard operating procedures for sanitation.

The drug-resistant bacteria can be present anywhere, in various environmental samples, farms, and retail meat products. S. Enteritidis (88%) isolated from hatching eggs, litter, feed, drinkers, bird rinse, and ceca, were reported to be resistant to drugs, ampicillin, nalidixic acid, and tetracycline [57]. There is a frequent isolation of Salmonella serovars such as S. Enteritidis, S. Infantis, S. Typhimurium, and S. Heidelberg from broiler carcasses. The antibiotic-resistant Salmonella isolates has been found from poultry chiller water and carcasses. The isolated Salmonella were resistant to antibiotics including tetracycline, ampicillin, amoxicillin-clavulanic acid, ceftiofur, streptomycin, and sulfisoxazole. Broiler farms with Salmonella isolates resistant to multiple antibiotics, i.e. streptomycin (30.9%), gentamicin (12.6%), sulfadimethoxine (20.9%), tetracycline (13.9%), and trimethoprim-sulfamethoxazole combination (8.6%) were recovered. Among these isolates, 67% of S. Heidelberg and 54% of S. Kentucky isolates showed resistance to five or more antibiotics [11]. These serovars have a high resistance towards ceftriaxone and ceftiofur antibiotics. It has been observed that conversion of conventional farms to organic farms can reduce the prevalence of antibiotic resistant Salmonella from 44% to 6% [58]. A comparison between the Salmonella isolates obtained from poultry samples of Maryland retail shop from conventional and organic farms revealed that conventional carcass samples were resistant for five to seven antimicrobials, whereas 79% of the isolates from organic carcass samples were susceptible to all 17 tested antimicrobials. Assessment of the status of poultry retail shops is necessary, as in many countries, people prefer to procure the freshly slaughtered chicken. In such retail shops, the likelihood of cross-contamination of poultry carcasses is high and MDR-Salmonella has been isolated from retail meat shops as well. The Food and Drug Administration (FDA) have reported the National Antimicrobial Resistance Monitoring System (NARMS), regarding retail meat interim report for Salmonella, which includes the antibiotic resistance profile of Salmonella sp. in retail poultry meat [59]. The retail meats show high resistance to the common antibiotics such as tetracycline, streptomycin, sulfamethoxazole, and ampicillin.

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7. Diagnosis

Salmonella diagnosis requires isolation of bacterium from the clinical samples and its culture in suitable culture media. The most common selective media used for Salmonella are SS agar, bismuth sulfite agar, Hektoen Enteric (HE) medium, Brilliant Green agar and Xylose-Lysine-Deoxycholate (XLD) agar. To further confirm diagnosis, biochemical, and serological tests are employed. The biochemical tests include sugar fermentation test, decarboxylation and dehydrogenation reactions, and hydrogen sulphide production. Serological examinations are usually carried out in outbreaks. Suffering from any other ailments makes diagnosis more cumbersome such as in cases of HIV-infected adults [60]. Hence, development of a rapid and sensitive diagnostic test is the need of the hour. A multiplex PCR has been found to be useful to identify NTS i.e. S. Typhimurium and variants, S. Enteritidis, S. Dublin and S. Stanleyville with 100% sensitivity and specificity [61]. Presence of low number of bacilli in clinical specimen is a limitation to this. So, to detect low infective loads of NTS, a microwave-accelerated metal-enhanced fluorescence (MAMEF) technique has been developed [62], which is well efficient enough to detect as little as 1 CFU/ml in less than 30 seconds. But, this still needs wider field applicability. A well defined ELISA with a definitive cut-off has not yet being commercialized for detection of NTS. But several researchers have suggested the use of lipopolysaccharide antigens from S. Enteritidis (serogroup D) and S. Typhimurium (serogroup B) for NTS detection [63].

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8. Prevention and control measures

The fundamental basis for the control of NTS is food safety at every step from farm to fork. Even antibiotic treatment is not recommended in uncomplicated gastroenteritis cases as this condition is self-limiting. The list for preventive and control measures include good sanitation practices, safer food, and water handling methods, vaccination, public awareness, malaria control, and antiretroviral therapy programmes. To limit the number of infections arising as a result of animal contact it is advisable to wash hands properly after each animal contact, as in many cases the organism is in colonized state in animals without showing any sign and symptoms. Proper food cooking contributes to limit infections. Although irradiation technology has been approved by several health agencies like WHO, CDC, and European commission’s Scientific Committee on Food, its use is partially implemented. Curtailment to the indiscriminate antibiotic usage in poultry feed along with better farm managerial practices leads to decreased multidrug resistant bacterial load. One health approach including multiple interventions is mandatory to enhance understanding, prevention, and control of NTS, as human health is completely related to the animal health and their environment. Adoption of different on-farm interventions strategies such as genetic selection of Salmonella-resistant birds, regular flock testing, use of natural antimicrobial products such as prebiotics or probiotics and egg washing on farms can reduce infection. The incidences of NTS infections have been observed more in individuals suffering from malaria and HIV because of immune-compromised health status in such individuals. So, adoption of strategies, such as malaria control, and antiretroviral therapy programmes, will not only lower the chances of primary sufferings but will greatly reduce NTS infections also.

Vaccination could be considered as a potential tool to control NTS, but currently no licensed vaccine is available for this in humans. The available typhoidal vaccine does not provide protection against NTS infections. Vaccination in animals may limit transmission of the micro-organism to humans. With this objective researchers are trying different vaccine strategies on livestock for NTS prevention. It includes live attenuated vaccines, killed vaccines, and a combination of both. Oral administration of live attenuated S. Gallinarum to chickens prevented not only wildtype infections by S. Gallinarum but also infections by S. Enteritidis [64]. Delivery of a killed vaccine comprising three different Salmonella serogroups i.e. Typhimurium, Mbandaka and Orion to chickens resulted in significant reduction in bacterial load when compared to the unvaccinated groups [65]. Administration of live attenuated S. Typhimurium vaccine followed by a killed Salmonella serovars Berta and Kentucky into chickens, showed a significant decrease in Salmonella sp. in the vaccinated animals when compared to the unvaccinated group [66].

Subunit vaccine development may pave a better way towards control scheme. Such vaccines come with an advantage of raising a protective immune response by using only a part of the infectious micro-organism. Common sub-cellular components of Salmonella used for development of vaccines are outer membrane proteins (Omps), porins, toxins and ribosomal fractions. Such vaccines have been tried in different animals and have variable success rates [67, 68, 69, 70]. Many of the cell surface carbohydrates of pathogenic bacteria like capsular polysaccharides are important antigenic determinants as in case of Vi-based vaccines against S.Typhi in humans. Omps are the surface exposed proteins which play a crucial role in pathogenic processes such as motility, adherence and colonization of the host cells, injection of toxins and cellular proteases, and formation of channels for the antibiotics removal [71]. Administration of Omps of S. Enteritidis can elicit high antibody responses and prevent bacterial shedding in chicken challenged with virulent Salmonella [72]. These functions make them attractive targets for the development of vaccines. Salmonella is an intracellular pathogen and generation of both B-cell and T-cell immune responses are essential. Live attenuated vaccines provide both humoral and cell mediated immune response; but, they may pose a risk in immunocompromised individuals. Whereas, inactivated vaccines induce only humoral immunity. Hence, the development of subunit vaccines after B-cell and T-cell epitope prediction and assessment of peptides with high affinity for class I and II MHC proteins are a better approach, and studies focussing this [73], increase the likelihood of developing a successful vaccine. Successful induction high levels of anti-porin antibodies and enhanced cell mediated immunity against Salmonella also have been demonstrated [74].

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9. Conclusion

The spread of non typhoidal salmonellosis is ubiquitous and persists in environment for a very long time duration. This poses difficulty in reducing the spread of infection. Infection from the poultry farm to fork level leads to severe complications in humans especially in immunocompromised individuals, children, and elderly. Moreover, the emergence of antimicrobial resistance in NTS is a major challenge in its effective treatment. Furthermore, till now no known vaccine is available which can control all the serotypes of NTS. Hence, in the present circumstances, implementation of one health approach could be a possible answer to prevent NTS infections.

References

  1. 1. Sexton M. Salmonella and Campylobacter in poultry in Australia. The Australian Poultry Science Symposium; 2016; Sydney: The Poultry Research Foundation, The University of Sydney
  2. 2. Kirk MD, Pires SM, Black RE, Caipo M, Crump JA, Devleesschauwer B, Dopfer D, Fazil A, Fischer-Walker CL, Hald T, Hall AJ. World Health Organization estimates of the global and regional disease burden of 22 foodborne bacterial, protozoal, and viral diseases. 2010:a data synthesis. PLoS medicine. 2015;12(12):e1001940. DOI:10.1371/journal.pmed.1001940
  3. 3. Majowicz SE, Musto J, Scallan E, Angulo FJ, Kirk M, O’Brien SJ, Jones TF, Fazil A, Hoekstra RM. The global burden of nontyphoidal Salmonella gastroenteritis. Clinical Infectious Diseases. 2010;50(6):882-889. DOI:10.1086/650733
  4. 4. Glenn LM, Lindsey RL, Frank JF, Meinersmann RJ, Englen MD, Fedorka-Cray PJ, Frye JG. Analysis of antimicrobial resistance genes detected in multidrug-resistant Salmonella enterica serovar Typhimurium isolated from food animals. Microbial Drug Resistance. 2011;17(3):407-418. DOI:10.1089/mdr.2010.0189
  5. 5. Crump JA, Sjolund-Karlsson M, Gordon MA, Parry CM. Epidemiology, clinical presentation, laboratory diagnosis, antimicrobial resistance, and antimicrobial management of invasive Salmonella infections. Clinical Microbiology Reviews. 2015;28:901-937. DOI: 10.1128/CMR.00002-15
  6. 6. Mastroeni P, Chabalgoity JA, Dunstan SJ, Maskell DJ, Dougan G. Salmonella: immune responses and vaccines. The Veterinary Journal. 2001;161(2):132-164. DOI:10.1053/tvjl.2000.0502
  7. 7. Grimont PA, Weill FX. Antigenic formulae of the Salmonella serovars. WHO collaborating centre for reference and research on Salmonella. 2007;9:1-66
  8. 8. Feasey NA, Dougan G, Kingsley RA, Heyderman RS, Gordon MA. Invasive non-typhoidal Salmonella disease: an emerging and neglected tropical disease in Africa. Lancet. 2012;379:2489-2499. DOI:10.1016/S0140-6736(11)61752-2
  9. 9. World Health Organization. [Internet] 2021. Available from: https://www.who.int/news-room/fact-sheets/detail/salmonella-(non-typhoidal). Accessed 2021-01-20
  10. 10. Centers for Disease Control and Prevention. 2011. Compendium of measures to prevent disease associated with animals in public settings. 2011. MMWR Morbidity Mortality Weekly Report 60:1-24
  11. 11. Liljebjelke KA, Hofacre CL, Liu T, White DG, Ayers S, Young S, Maurer JJ. Vertical and horizontal transmission of Salmonella within integrated broiler production system. Foodbourne Pathogens and Disease. 2005;2(1):90-102. DOI: 10.1089/fpd.2005.2.90
  12. 12. Hugas M, Beloeil PA. Controlling Salmonella along the food chain in the European Union-progress over the last ten years. Eurosurveillance. 2014;19(19):20804
  13. 13. Dunkley KD, Callaway TR, Chalova VI, Anderson RC, Kundinger MM, Dunkley CS, Nisbet DJ, Ricke SC. Growth and genetic responses of Salmonella Typhimurium to pH-shifts in an anaerobic continuous culture. Anaerobe. 2008;14(1):35-42. DOI: 10.1016/j.anaerobe.2007.10.001
  14. 14. Bavishi C, Dupont HL. Systematic review: the use of proton pump inhibitors and increased susceptibility to enteric infection. Alimentary Pharmacology and Therapeutics. 2011;34(11-12):1269-1281. DOI:10.1111/j.1365-2036.2011.04874.x
  15. 15. Jones TF, Ingram LA, Cieslak PR, Vugia DJ, Tobin-D'Angelo M, Hurd S, Medus C, Cronquist A, Angulo FJ. Salmonellosis outcomes differ substantially by serotype. The Journal of Infectious Diseases. 2008;198(1):109-114. DOI: 10.1086/588823
  16. 16. MacLennan CA, Gilchrist JJ, Gordon MA, Cunningham AF, Cobbold M, Goodall M, Kingsley RA, Van Oosterhout JJ, Msefula CL, Mandala WL, Leyton DL. Dysregulated humoral immunity to nontyphoidal Salmonella in HIV-infected African adults. Science. 2010;328(5977):508-512. DOI: 10.1126/science.1180346
  17. 17. Nyirenda TS, Mandala WL, Gordon MA, Mastroeni P. Immunological bases of increased susceptibility to invasive nontyphoidal Salmonella infection in children with malaria and anaemia. Microbes and Infection. 2018;20(9-10):589-598. DOI: 10.1016/j.micinf.2017.11.014
  18. 18. Uche IV, MacLennan CA, Saul A. A systematic review of the incidence, risk factors and case fatality rates of invasive nontyphoidal Salmonella (iNTS) disease in Africa (1966 to 2014). PLoS Neglected Tropical Diseases. 2017;11(1):e0005118. DOI: 10.1371/journal.pntd.0005118
  19. 19. CDC. Antibiotic Resistance Threats in the United States, 2019. Atlanta, GA: U.S. Department of Health and Human Services, CDC; 2019
  20. 20. European Food Safety Authority and European Centre for Disease Prevention and Control (EFSA and ECDC). The European Union one health 2018 zoonoses report. EFSA Journal. 2019;17(12):e05926. DOI:10.2903/j.efsa.2019.5926
  21. 21. Reddy EA, Shaw AV, Crump JA. Community-acquired bloodstream infections in Africa: a systematic review and meta-analysis. The Lancet Infectious Diseases. 2010;10(6):417-432. DOI: 10.1016/S1473-3099(10)70072-4
  22. 22. Marks F, Von Kalckreuth V, Aaby P, Adu-Sarkodie Y, El Tayeb MA, Ali M, Aseffa A, Baker S, Biggs HM, Bjerregaard-Andersen M, Breiman RF. Incidence of invasive salmonella disease in sub-Saharan Africa: a multicentre population-based surveillance study. The Lancet Global Health. 2017;5(3):e310-23. DOI: 10.1016/S2214-109X(17)30022-0
  23. 23. Oneko M, Kariuki S, Muturi-Kioi V, Otieno K, Otieno VO, Williamson JM, Folster J, Parsons MB, Slutsker L, Mahon BE, Hamel MJ. Emergence of community-acquired, multidrug-resistant invasive nontyphoidal Salmonella disease in rural Western Kenya, 2009-2013. Clinical Infectious Diseases. 2015;61(suppl_4):S310-6. DOI: 10.1093/cid/civ674
  24. 24. SCRA. [Internet]. Statistical Committee of the Republic of Armenia/Socio-Economic Situation of RA, January–December/Public Health. Available at: https://www.armstat.am/en/?nid=82. Accessed 2021-01-05
  25. 25. Menezes GA, Khan MA, Harish BN, Parija SC, Goessens W, Vidyalakshmi K, Baliga S, Hays JP. Molecular characterization of antimicrobial resistance in non-typhoidal salmonellae associated with systemic manifestations from India. Journal of Medical Microbiology. 2010;59(12):1477-1483. DOI: 10.1099/jmm.0.022319-0
  26. 26. Chen PL, Li CY, Hsieh TH, Chang CM, Lee HC, Lee NY, Wu CJ, Lee CC, Shih HI, Ko WC. Epidemiology, disease spectrum and economic burden of non-typhoidal Salmonella infections in Taiwan, 2006-2008. Epidemiology and Infection. 2012;140(12):2256-2263
  27. 27. Research SA. Causes and outcomes of sepsis in southeast Asia: a multinational multicentre cross-sectional study. The Lancet Global Health. 2017;5(2):e157-67. DOI: 10.1016/S2214-109X(17)30007-4
  28. 28. Shahunja KM, Leung DT, Ahmed T, Bardhan PK, Ahmed D, Qadri F, Ryan ET, Chisti MJ. Factors associated with non-typhoidal Salmonella bacteremia versus typhoidal Salmonella bacteremia in patients presenting for care in an urban diarrheal disease hospital in Bangladesh. PLoS Neglected Tropical Diseases. 2015;9(9):e0004066. DOI: 10.1371/journal.pntd.0004066
  29. 29. Kaur AA, Fadzilah MN, Mariam M, Abidin ASZ, Adnan, S, Nor, NSM. Community-acquired bacteremia in Paediatrics: epidemiology, aetiology and patterns of antimicrobial resistance in a tertiary care Centre, Malaysia. Medical Journal of Malaysia. 2016;71(3):117-121
  30. 30. Sinwat N, Angkittitrakul S, Coulson KF, Pilapil FM, Meunsene D, Chuanchuen R. High prevalence and molecular characteristics of multidrug-resistant Salmonella in pigs, pork and humans in Thailand and Laos provinces. Journal of Medical Microbiology. 2016;65(10):1182-1193. DOI: 10.1099/jmm.0.000339
  31. 31. Noor Uddin GM, Larsen MH, Barco L, Minh Phu T, Dalsgaard A. Clonal occurrence of Salmonella Weltevreden in cultured shrimp in the Mekong Delta, Vietnam. Plos one. 2015;10(7):e0134252. DOI: 10.1371/journal.pone.0134252
  32. 32. Chiu CH, Su LH. Salmonella, Non-Typhoidal Species (S. choleraesuis, S. enteritidis, S. hadar, S. typhimurium). Dostupno na http://www. antimicrobe. org/b258. asp. Zadnji pristup. 2019;21
  33. 33. Chen YH, Chen TP, Lu PL, Su YC, Hwang KP, Tsai JJ, Cheng HH, Peng CF. Salmonella choleraesuis bacteremia in southern Taiwan. The Kaohsiung Journal of Medical Sciences. 1999;15(4):202-208
  34. 34. Guery R, Habibi A, Arlet JB, Lionnet F, de Lastours V, Decousser JW, Mainardi JL, Razazi K, Baranes L, Bartolucci P, Godeau B. Severe, non specific symptoms in non-typhoidal Salmonella infections in adult patients with sickle cell disease: a retrospective multicentre study. Infectious Diseases. 2018;50(11-12):822-830. DOI: 10.1080/23744235.2018.1500706
  35. 35. Molyneux EM, Mankhambo LA, Phiri A, Graham SM, Forsyth H, Phiri A, Walsh AL, Wilson LK, Molyneux ME. The outcome of non-typhoidal salmonella meningitis in Malawian children, 1997-2006. Annals of Tropical Paediatrics. 2009;29(1):13-22. DOI: 10.1179/146532809X401980
  36. 36. Hsu RB, Tsay YG, Chen RJ, Chu SH. Risk factors for primary bacteremia and endovascular infection in patients without acquired immunodeficiency syndrome who have nontyphoid salmonellosis. Clinical Infectious Diseases. 2003;36(7):829-834. DOI:10.1086/367932
  37. 37. Di Bonaventura G, Di Girolamo A, Catamo G, Nicoletti M, Piccolomini R. Salmonella typhimurium-endocarditis secondary to an acquired environmental infection: a case report. Microbiologica-Bologna. 2001;24(1):85-90
  38. 38. Van Sorge NM, Zialcita PA, Browne SH, Quach D, Guiney DG, Doran KS. Penetration and activation of brain endothelium by Salmonella enterica serovar Typhimurium. Journal of Infectious Diseases. 2011;203(3):401-405. DOI:10.1093/infdis/jiq048
  39. 39. Genzen JR, Towle DM, Kravetz JD, Campbell SM. Salmonella typhimurium pulmonary infection in an immunocompetent patient. Connecticut medicine. 2008;72(3)
  40. 40. Arda IS, Ergin F, Varan B, Demirhan B, Aslan H, Ozyaylali İ. Acute abdomen caused by Salmonella typhimurium infection in children. Journal of Pediatric Surgery. 2001;36(12):1849-1852. DOI:10.1053/jpsu.2001.28867
  41. 41. Abdollahi A, Moradi-Tabriz H, Rasoulinejad M. Pneumonia due to Salmonella typhimuriumin an HIV-Infected Patient. Iranian Journal of Pathology. 2010;5(4):208-211
  42. 42. Samal B, Oommen S, Swami A, Maskey M, Shastri J. Salmonella brain abscess in an infant. Indian Journal of Pathology and Microbiology. 2009;52(2):269
  43. 43. Rybak MJ. Resistance to antimicrobial agents: an update. Pharmacotherapy: The Journal of Human Pharmacology and Drug Therapy. 2004;24(12P2):203S–15S
  44. 44. Alanis AJ. Resistance to antibiotics: are we in the post-antibiotic era? Archives of Medical Research. 2005;36(6):697-705. DOI:10.1016/j.arcmed.2005.06.009
  45. 45. Croft AC, D'Antoni AV, Terzulli SL. Update on the antibacterial resistance crisis. Medical Science Monitor. 2007;13(6):RA103-18
  46. 46. Molbak K, Baggesen DL, Aarestrup FM, Ebbesen JM, Engberg J, Frydendahl K, Gerner-Smidt P, Petersen AM, Wegener HC. An outbreak of multidrug-resistant, quinolone-resistant Salmonella enterica serotype Typhimurium DT104. New England Journal of Medicine. 1999;341(19):1420-1425. DOI: 10.1056/NEJM199911043411902
  47. 47. Su LH, Chiu CH, Chu C, Ou JT. Antimicrobial resistance in nontyphoid Salmonella serotypes: a global challenge. Clinical Infectious Diseases. 2004;39(4):546-551. DOI:10.1086/422726
  48. 48. Chiu CH, Su LH, Chu C, Chia JH, Wu TL, Lin TY, Lee YS, Ou JT. Isolation of Salmonella enterica serotype choleraesuis resistant to ceftriaxone and ciprofloxacin. The Lancet. 2004;363(9417):1285-1286. DOI:10.1016/S0140-6736(04)16003-0
  49. 49. Foley SL, Lynne AM. Food animal-associated Salmonella challenges: pathogenicity and antimicrobial resistance. Journal of Animal Science. 2008;86(suppl_14):E173-87. DOI:10.2527/jas.2007-0447
  50. 50. Mascaretti OA. Bacteria versus antibacterial agents: an integrated approach. American Society for Microbiology (ASM); 2003
  51. 51. Alcaine SD, Warnick LD, Wiedmann M. Antimicrobial resistance in nontyphoidal Salmonella. Journal of Food Protection. 2007;70(3):780-790. DOI:10.4315/0362-028X-70.3.780
  52. 52. Cannon M, Harford S, Davies J. A comparative study on the inhibitory actions of chloramphenicol, thiamphenicol and some fluorinated derivatives. Journal of Antimicrobial Chemotherapy. 1990;26(3):307-317. DOI:10.1093/jac/26.3.307
  53. 53. Cloeckaert A, Chaslus-Dancla E. Mechanisms of quinolone resistance in Salmonella. Veterinary Research. 2001;32(3-4):291-300
  54. 54. Chopra I, Roberts M. Tetracycline antibiotics: mode of action, applications, molecular biology, and epidemiology of bacterial resistance. Microbiology and Molecular Biology Reviews. 2001;65(2):232-260. DOI: 10.1128/MMBR.65.2.232-260.2001
  55. 55. Antunes P, Machado J, Sousa JC, Peixe L. Dissemination of sulfonamide resistance genes (sul1, sul2, and sul3) in Portuguese Salmonella enterica strains and relation with integrons. Antimicrobial agents and chemotherapy. 2005;49(2):836-839. DOI: 10.1128/AAC.49.2.836-839.2005
  56. 56. National Academy of Sciences Committee on Drug Use in Food Animals. The use of drugs in food animals: benefits and risks. Washington, DC: National Academy Press, 1999
  57. 57. Al-Zenki S, Al-Nasser A, Al-Safar A, Alomirah H, Al-Haddad A, Hendriksen RS, Aarestrup FM. Prevalence and antibiotic resistance of Salmonella isolated from a poultry farm and processing plant environment in the State of Kuwait. Foodborne pathogens and disease. 2007;4(3):367-373
  58. 58. Sapkota AR, Kinney EL, George A, Hulet RM, Cruz-Cano R, Schwab KJ, Zhang G, Joseph SW. Lower prevalence of antibiotic-resistant Salmonella on large-scale US conventional poultry farms that transitioned to organic practices. Science of the Total Environment. 2014;476:387-392
  59. 59. Food and Drug Administration (FDA). 2014-2015 Retail Meat Interim Report. 2017. Available online:https://www.fda.gov/downloads/AnimalVeterinary/SafetyHealth/AntimicrobialResistance/NationalAntimicrobialResistanceMonitoringSystem/UCM498134.pdf. Accessed 2018-06-15
  60. 60. Gordon MA, Banda HT, Gondwe M, Gordon SB, Boeree MJ, Walsh AL, Corkill JE, Hart CA, Gilks CF, Molyneux ME. Non-typhoidal salmonella bacteraemia among HIV-infected Malawian adults: high mortality and frequent recrudescence. Aids. 2002;16(12):1633-1641
  61. 61. Tennant SM, Diallo S, Levy H, Livio S, Sow SO, Tapia M, Fields PI, Mikoleit M, Tamboura B, Kotloff KL, Nataro JP. Identification by PCR of non-typhoidal Salmonella enterica serovars associated with invasive infections among febrile patients in Mali. PLoS Neglected Tropical Diseases. 2010;4(3):e621. DOI:10.1371/journal.pntd.0000621
  62. 62. Tennant SM, Zhang Y, Galen JE, Geddes CD, Levine MM. Ultra-fast and sensitive detection of non-typhoidal Salmonella using microwave-accelerated metal-enhanced fluorescence (“MAMEF”). PLoS One. 2011;6(4):e18700. DOI:10.1371/journal.pone.0018700
  63. 63. Kuhn KG, Falkenhorst G, Ceper TH, Dalby T, Ethelberg S, Mølbak K, Krogfelt KA. Detecting non-typhoid Salmonella in humans by ELISAs: a literature review. Journal of Medical Microbiology. 2012;61(1):1-7. DOI:10.1099/jmm.0.034447-0
  64. 64. Penha Filho RA, de Paiva JB, da Silva MD, de Almeida AM, Junior AB. Control of Salmonella Enteritidis and Salmonella Gallinarum in birds by using live vaccine candidate containing attenuated Salmonella Gallinarum mutant strain. Vaccine. 2010;28(16):2853-2859. DOI:10.1016/j.vaccine.2010.01.058
  65. 65. Pavic A, Groves PJ, Cox JM. Utilization of a novel autologous killed tri-vaccine (serogroups B [Typhimurium], C [Mbandaka] and E [Orion]) for Salmonella control in commercial poultry breeders. Avian Pathology. 2010;39(1):31-39. DOI:10.1080/03079450903454277
  66. 66. Dorea FC, Cole DJ, Hofacre C, Zamperini K, Mathis D, Doyle MP, Lee MD, Maurer JJ. Effect of Salmonella vaccination of breeder chickens on contamination of broiler chicken carcasses in integrated poultry operations. Applied and Environmental Microbiology. 2010;76(23):7820-7825. DOI: 10.1128/AEM.01320-10
  67. 67. Singh BR, Singh Y, Agarwal MC, Agarwal RK, Sharma VD. Salmonella vaccines for veterinary use: an overview. Haryana Vet. 2005;44:1-12
  68. 68. Vasava KA, Singh BR, Verma JC. Detection of cytotoxigenicity among strains of Salmonella enterica subspecies enterica serovar Abortusequi by an indirect ELISA. Indian Journal of Veterinary Research. 2004;13:31-34
  69. 69. Barman TK, Sharma VD, Kumar S. Optimization of dose of Salmonella toxoid vaccine in poultry. Indian Journal of Experimental Biology. 2002;79:106-110
  70. 70. Mishra RS, Sharma VD. Comparative efficacy of various toxoids against salmonellosis in poultry. Veterinary Research Communications. 2001;25(5):337-344
  71. 71. Cordwell SJ. Technologies for bacterial surface proteomics. Current Opinion in Microbiology. 2006;9(3):320-329. DOI:10.1016/j.mib.2006.04.008
  72. 72. Meenakshi M, Bakshi CS, Butchaiah G, Bansal MP, Siddiqui MZ, Singh VP. Adjuvanted outer membrane protein vaccine protects poultry against infection with Salmonella enteritidis. Veterinary Research Communications. 1999;23(2):81-90
  73. 73. Pandey M, Saxena MK. Cloning and immunopotential analysis of Omp 28 of Salmonella Typhimurium for the development of subunit vaccine for poultry salmonellosis. Indian Journal of Poultry Science. 2015;50(2):138-142
  74. 74. Lim E, Koh WH, Loh SF, Lam MS, Howe HS. Non-thyphoidal salmonellosis in patients with systemic lupus erythematosus. A study of fifty patients and a review of the literature. Lupus. 2001;10(2):87-92. DOI:10.1191/096120301675973164

Written By

Mamta Pandey and Emmagouni Sharath Kumar Goud

Submitted: 16 October 2020 Reviewed: 03 February 2021 Published: 24 February 2021