Review Impact of sporadic reporting of poultry Salmonella serovars from selected developing countries Elie K Barbour1,2, Danielle B Ayyash1, Wafa Alturkistni3, Areej Alyahiby3, Soonham Yaghmoor3,4, Archana Iyer2,3,4, Jehad Yousef3,4,5, Taha Kumosani2,3,4, Steve Harakeh6 1 Department of Animal and Veterinary Sciences, Faculty of Agricultural and Food Sciences, American University of Beirut, Beirut, Lebanon 2 Biochemistry Department, King Abdulaziz University, Jeddah, Saudi Arabia 3 Experimental Biochemistry Unit, King Fahd Medical Research Center, King Abdulaziz University, Jeddah, Saudi Arabia 4 Production of Bioproducts for Industrial Applications Research Group, King Abdulaziz University, Jeddah, Saudi Arabia 5 Biochemistry Department, Faculty of Science for girls, King Abdulaziz University, Jeddah, Saudi Arabia 6 Special Infectious Agents Unit – Biosafety Level 3, King Fahd Medical Research Center, King Abdulaziz University, Jeddah, Saudi Arabia Abstract This review documents the sporadic reporting of poultry Salmonella serovars in South Africa, Egypt, Indonesia, India, and Romania, five countries selected based on the importance of their distribution in different regions of the world and their cumulative significant population size of 1.6 billion. South Africa reported contamination of its poultry carcasses by S. Hadar, S. Blockley, S. Irumu, and S. Anatum. Results from Egypt showed that S. Enteritidis and S. Typhimurium were predominant in poultry along with other non-typhoid strains, namely S. Infantis, S. Kentucky, S. Tsevie, S. Chiredzi, and S. Heidelberg. In Indonesia, the isolation of Salmonella Typhi was the main focus, while other serovars included S. Kentucky, S. Typhimurium, and S. Paratyhi C. In India, S. Bareilly was predominant compared to S. Enteritidis, S. Typhimurium, S. Paratyphi B, S. Cerro, S. Mbandaka, S. Molade, S. Kottbus, and S. Gallinarum. Romania reported two Salmonella serovars in poultry that affect humans, namely S. Enteritidis and S. Typhimurium, and other non-typhoid strains including S. Infantis, S. Derby, S. Colindale, S. Rissen, S. Ruzizi, S. Virchow, S. Brandenburg, S. Bredeney, S. Muenchen, S. Kortrijk, and S. Calabar. The results showed the spread of different serovars of Salmonella in those five developing countries, which is alarming and emphasizes the urgent need for the World Health Organization Global Foodborne Infections Network (WHO-GFN) to expand its activities to include more strategic participation and partnership with most developing countries in order to protect poultry and humans from the serious health impact of salmonellosis. Key words: Developing countries; poultry Salmonella serovars. J Infect Dev Ctries 2015; 9(1):001-007. doi:10.3855/jidc.5065 (Received 02 April 2014 – Accepted 17 November 2014) Copyright © 2015 Barbour et al. This is an open-access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Introduction Salmonella are the most common causes of foodborne illness worldwide [1]. The two foods that are most commonly associated with Salmonella food illness are eggs and poultry meat [2-4]. More than 2,500 serovars of Salmonella have been identified, with many commonly infecting poultry and humans. The frequency patterns of predominant serovars in each country is challenged with a shift in prevalence due to globalization, especially linked to livestock trade, international travel, and human migration [5-7]. Meager Salmonella control programs in most developing countries, and the presence of vigorous globalization, will challenge other countries with new serovars that could potentially be multidrug resistant [8] and could disseminate throughout the food chain [8,9]. The participation of different countries depends upon a number of factors, such as availability of financial and human resources, and also willingness to participate in and support initiatives of the Global Foodborne Infections Network (GFN). The World Health Organization (WHO) program is now known as the GFN [11,12]. The countries that are involved with national and regional projects of the WHO-GFN include fewer than 10 out of a total of 196 independent countries worldwide. The lack of active GFN projects Barbour et al. – Poultry Salmonella serovars in developing countries and initiatives in many developing countries has resulted in underreporting of Salmonella serovars in humans and other food sources that are supposed to be included in the web-based country data bank (CDB) [11]. This present global situation urges the need to build a hypothesis that compiling sporadic data on poultry Salmonella serovars from selected developing countries could highlight the importance of the chicken reservoir as a potential source of Salmonella infection to humans. The purpose of this review was to compile sporadic recent reports about the Salmonella serovars isolated from poultry and their derived products in five selected developing countries that represent, cumulatively, around 22.2% of the 7.2 billion people of the world. The global public health significance of the sporadic reporting of poultry Salmonella serovars, documented by developing countries, is highlighted. Methodology Significant inclusion of the five selected developing countries The significance of inclusion of the five selected developing countries in this study lies in their geographic distributions in different regions of the world that represent major trafficking of people and poultry products. The populations of the included developing countries range from 0.05–0.25 billion people, and cover countries in Africa, Asia, and Europe. Poultry contributes significantly as a major food source consumed by a total of 1.6 billion people inhabiting these five selected developing countries. The selected countries are South Africa (located at the southern tip of Africa), Egypt (with one part in Africa and the other part in Asia), Indonesia (located in the Asian continent), India (located in the southern region of Asia), and Romania (located in southeastern central Europe, and joined the European Union in 2007). Population and poultry product consumption The total egg and poultry meat production in the world is 65×103 and 103×106 tons, respectively. The highest consumption of eggs per capita per year is in Romania (13.6 kg) (population of 20 million), while the lowest is in Egypt and India (3.0 kg) (populations of 84 million and 1.2 billion, respectively). Indonesian and South African populations have a moderate consumption of eggs of 4.5 and 6.6 kg, respectively (populations of 246 and 53 million, respectively). The pattern of poultry meat consumption is different from that of eggs in the five countries. The highest consumption of poultry meat is in South Africa (24.5 J Infect Dev Ctries 2015; 9(1):001-007. kg/capita/year), while the lowest is in India (2.7 kg/capita/year). The data from the other three countries lie in between, with the following figures in a decreasing order of consumption: Romania (10.0 kg/capita), Indonesia (6.1 kg/capita), and Egypt (5.9 kg/capita) [13,14]. Sporadic reporting of Salmonella serovars The absence of controlled reporting of Salmonella serovars through the WHO-GFN program in these five selected developing countries [15] inspired the compilation of data on the sporadic reporting of Salmonella serovars in poultry. The 2014 regional centers of GFN are only present in six countries: Thailand (Faculty of Veterinary Science of Chulalongkorn University, Bangkok), Argentina (The National Institutes and Laboratories of Health, Buenos Aires), Mexico (The Autonomous University of Yucatan, represented by the Faculty of Veterinary Medicine, Merida, Yucatan), Poland (National Institute of Hygiene in Warsaw), Cameroon (Institute Pasteur Yaoundé), and Costa Rica (Costa Rica Nutrition and Health Research and Training Institute, San José). Unfortunately, none of these six centers of the WHO-GFN reported the serovar distribution in the five selected countries included in this study, due to the lack of routine national surveillance and scarcity of data in these countries. Results and Discussion The following is the compilation of reports related to Salmonella serovars present in poultry of the five developing countries. South Africa The presence of Salmonella in raw chicken carcasses in South Africa has not been extensively investigated. The first report from South Africa included an examination of fewer than 10 samples of raw poultry for isolation of Salmonella [16,17]. The results of such studies are not by any means considered representative of the overall situation of Salmonella prevalence in the poultry of South Africa. The other study by van Nierop et al. in 2005 [18] included a larger sample of 99 raw chicken carcasses (fresh and frozen) collected from butcheries, supermarkets, and street vendors. The percentages of Salmonella-contaminated chicken samples were found in chicken carcasses fresh from butcheries (53.3%), frozen from butcheries (64.7%), fresh from supermarkets (43.8%), and fresh from street vendors (50.0%). The level of contamination in the above2 Barbour et al. – Poultry Salmonella serovars in developing countries mentioned chicken carcasses is alarming, as it provides a potential reservoir for infecting human consumers. The four most commonly detected Salmonella serovars in the contaminated chicken carcasses in decreasing order of frequency were S. Hadar, S. Blockley, S. Irumu, and S. Anatum. The following serovars were also detected in equal frequency: S. Reading, S. Virchow, S. Schwarzengrund, S. Westhampton, S. Typhimurium, S. Derby, and S. Heidelberg. It is worth noting that the invasive non-typhi Salmonella (NTS) results in a case fatality percentage, among hospitalized patients in Africa, equivalent to 4.4%–27.0% for children [19-22] and 22%–47% for adults [23-25]. Unfortunately, a routine national surveillance of the distribution of Salmonella serovars in poultry of South Africa, and their potential effects on humans in this country, are absent. Egypt Egypt is another developing country that lacks routine Salmonella surveillance of chicken flocks. The sporadic cases of salmonellosis in Egypt were first reported by Ammar et al. in 2010 [26], who documented the isolation of Salmonella Enteritidis from chickens and other sources in Dakhlia governorate, and incriminated these sources as possible reservoirs for infection in hospitalized patients. Another report from Egypt described the development of a diagnostic-restriction enzyme and plasmid profile analysis of S. Typhimurium recovered from Egyptian poultry farms [27]. The numbers of plasmids in the tested poultry isolates of S. Typhimurium were one to six. One plasmid, with a molecular size of 11,425 bp, was common to all isolates. This study aimed to use a plasmid marker in future epidemiologic targeted surveillance of S. Typhimurium distribution in poultry farms. Another report by Rabie et al. in 2012 [28] documented a Salmonella food illness outbreak in humans, associated with Salmonella recovered from consumed poultry products. The samples included in this study were 50 chickens with diarrhea, 50 pieces of raw frozen chicken meat, and 30 patients with symptoms of food poisoning. The common Salmonella serovars isolated from different poultry samples and from the affected humans were S. Enteritidis and S. Typhimurium. This was confirmed by multiplex polymerase chain reaction (PCR) amplification of poultry and human Salmonella isolates, showing the same size of specific bands on the gel. J Infect Dev Ctries 2015; 9(1):001-007. An excellent report on Salmonella serovar distribution on broiler farms of Kalubia governate in Egypt was documented by Abd- El-Ghany et al. in 2012 [29]. This study included 1,073 samples collected from 293 broilers. The samples included cloacal swabs, gall bladders, yolk sacs, spleens, and livers. The frequency of Salmonella serovars recovered from the broiler flocks were S. Enteritidis (37.25%), S. Typhimurium (29.41%), S. Infantis (19.6%), S. Kentucky (7.84%), S. Tsevie (3.92%), and S. Chiredzi (1.96%). The prevalence of S. Enteritidis and S. Typhimurium in broiler flocks of Kalubia governate of Egypt requires drastic measures for their control, since the two serovars are known for their potential to cause severe foodborne illness in humans [30,31]. El- Safey in 2013 [32] focused on the isolation of S. Heidelberg from foods. A total of 200 samples were collected in Cairo and Assuit cities from chicken, beef, milk, kushary (traditional Egyptian food), and sausage. S. Heidelberg was recovered from 15% of chicken samples, 5% of beef samples, 2.5% of milk samples, 2.5% of kushary samples, and 10% of sausage samples. The chicken seemed to be the main source of this serovar. This is in agreement with what was reported by Hennessy et al. in 2004 [33], indicating that poultry is the main source of S. Heidelberg contamination. S. enterica serovar Heidelberg is the third most common cause of human infections in the USA, after S. Typhimurium, and it contributes to about 7% of all of the deaths caused by Salmonella [33-35]. Another work was performed in the vicinity of Assiut in Egypt, reporting the detection of S. Typhimurium in retail chicken meat and giblets [36]. This work included the examination of Salmonella in 100 samples of frozen raw chicken meat, livers, and hearts. S. Typhimurium was detected in 44% of chicken meat samples, 40% of liver samples, and 48% of heart samples. This high frequency of detection of S. Typhimurium in chicken carcasses and giblets is alarming, and is a threatening reservoir for this serovar that may have adverse effects on the health of Egyptian consumers. Indonesia The incidence of typhoid in Indonesia is high and alarming (148.7 per 100,000 persons/year) [37]. More than 90% of the world morbidity by typhoid occurs in Asia alone [38]. For this reason, the research work in Indonesia has been devoted towards the development of a rapid PCR technique to detect S. Typhi, avoiding 3 Barbour et al. – Poultry Salmonella serovars in developing countries the lengthy classical methods of isolation, biochemical testing, and serology [39]. In 2012, another targeted surveillance of Salmonella was documented in Indonesia; 125 samples were examined for Salmonella isolation and serovar typing [40]. The 125 samples included 40 samples of chicken cuts. The results indicated a high unacceptable percentage of Salmonella contamination in the examined chicken cuts collected from open markets (52.5%) as well as from supermarkets (50%). The identified serovars in the chicken cuts, collected from the open market, in decreasing order of frequency, were S. Kentucky, S. Typhimurium, and S. Paratyphi C. However, the only two serovars recovered from the chicken cuts collected from supermarkets were S. Kentucky and S. Typhimurium, in equal frequencies. These pilot studies in Indonesia indicated the significance of Salmonella presence in high frequencies in poultry products, which may act as possible reservoirs of these organisms to a large size of consumers in this country. The lack of routine surveillance of Salmonella serovar distribution in Indonesian poultry is a threat to the population’s health, and to visitors from different parts of the world. India This developing country is more aware of the Salmonella problem, as shown from its published articles in this area. The National Salmonella and Escherichia Center in India implemented routine monitoring of Salmonella serovars, and shares its isolates with different scientists in India for further investigations. An earlier study by Ganguli in 1958 [41] revealed the importance of S. Bareilly as a human pathogen. Majumdar and Singh in 1973 [42] pursued the work on this predominant serovar, developing a phage-typing system for it, helping later to implement an epidemiology for tracing this serovar across the country [43]. This system was further developed by Singh et al. in 1988 [44]; 637 strains of S. Bareilly were provided to these research works by the National Salmonella and Escherichia Center in Kasauli, India, collected from different parts of India between 1959 and 1989. This effective cooperation helped these researchers to study the distribution of the phage types of this serovar across India, including isolates recovered from poultry and sheep products. During the period 1990–1991, 3,222 Salmonella isolates were serotyped, revealing 53 different serovars. These isolates were recovered from humans, J Infect Dev Ctries 2015; 9(1):001-007. poultry, other animals, reptiles, birds, and other sources [45]. Another interesting study was conducted by Murugkar et al. in 2005 [46], analyzing poultry and human samples for Salmonella. The percent positive samples for Salmonella included human stool (20.5%) and poultry cloacal swabs (14.7%). Three Salmonella serovars were common between poultry and humans, resulting in same pattern of decreasing frequency; these serovars were S. Typhimurium, S. Enteritidis, and S. Paratyphi B. This work added more supporting evidence of poultry being the reservoir of Salmonella serovars that are shared by humans. Suresh et al. in 2011 [47] reported the prevalence and distribution of Salmonella serovars in marketed broiler chickens and processing environment in Coimbatore, a city in southern India. This work included 214 samples of broiler chickens and 311 environmental samples from cages. Salmonella was found in chicken cloacae (1.4%) and chicken crops (6.9%). The range of contamination of cage samples was between 0 and 16.67%. The predominant serovar was S. Enteritidis; the other less prevalent serovars were S. Bareilly, S. Cerro, S. Mbandaka, and S. Molade. Singh et al. in 2013 [48] reported the prevalence of Salmonella serovars in chickens from north India. One Salmonella serovar, S. Kottbus, was recovered from eggs, feces of chicken, and cloacae S. Kottbus. Another serovar, S. Typhimurium, was common to eggs and cloacae. Rajagopal and Mini in 2013 [49] reported an outbreak of salmonellosis in three different poultry farms in Kerala, India. The Salmonella serovar that caused the outbreak on all the surveyed farms was S. Gallinarum. Last but not least, a prevalence of Salmonella in pigs and chicken broilers in Tarai region of Uttarakh and in India was documented in correspondence by Kumar et al. in 2014 [50]. This work involved the isolation of Salmonella from a total of 343 fecal samples of poultry and pigs, and from 100 tissue samples of broilers. The study was performed between January 2011 and July 2012. The total prevalence of Salmonella in poultry was 12.28% (8.4% of cloacal samples and 22.0% of tissue samples). The detected poultry serovars, in decreasing order of frequency, were S. Typhimurium, S. Enteritidis, and S. Gallinarum. Romania Romania has a population of around 20 million, with the highest consumption of eggs per capita and the second-highest consumption of poultry meat per capita, compared to the four other developing 4 Barbour et al. – Poultry Salmonella serovars in developing countries countries included in this study. It is located in the southwestern central Europe, and became a member in the European Union (EU) in 2007. This merging with the EU presented a sensitive situation to food safety of Romania due to the pressure that the regulatory agencies in Romania were put under from the EU to permit Romanian poultry products to enter the whole EU market. The first study on Salmonella in poultry and pigs of all the regions of Romania was performed in 2011, four years after Romania joined the EU. Unfortunately, the publication came three years after the conclusion of the work [51]. The study was conducted on 650 samples of chicken and pork meat collected from production sites and retail markets. A total of 149 Salmonella isolates were recovered, of which 22.92% were contaminated with Salmonella: 48 pork isolates (32.21% of positive samples), and 101 chicken isolates (67.78% of positive samples). Thirteen serovars were identified in this surveillance, including, in decreasing order of frequency, S. Infantis (70.87%), S. Typhimurium (18.45%), S. Derby (14.56%), S. Colindale (13.59%), S. Rissen (5.83%), S. Ruzizi (4.85%), S. Virchow (4.85%), S. Brandenburg (3.88%), S. Bredeney (3.88%), S. Muenchen (0.97%), S. Hortrijk (0.97%), S. Enteritidis (0.97%), and S. Calabar (0.97%). The recovery of S. Typhimurium and S. Enteritidis, two serovars with known pathogenicity in human hosts, encourages the implementation of strict rules on poultry and pork products containing these two pathogenic serovars. In 2013, the president of the Union of Poultry Breeders in Romania declared that poultry flocks in this country are routinely monitored for Salmonella, and that all legal measures are taken in case of an outbreak. This regulation is enforced in all EU countries. At present, the Romanian Union of Poultry Breeders controls around 550 farms across the country; only 15 farms are the major producers of 60% of the country’s chicken meat [52]. The transformation of Romania from a developing country to a developed EU member country has helped it to build proper laboratories and to implement routine monitoring of Salmonella serovars, enabling it to take rapid action once Salmonella is detected in foods, before consumers are affected. The 2013 incident of Salmonella contamination of poultry products in Romania did not result in any food illness to consumers, due to the rapid intervention of the responsible Romanian authorities who adopted the EU food safety regulations. J Infect Dev Ctries 2015; 9(1):001-007. Conclusions This review focused on the sporadic nature of targeted surveillance for Salmonella serovars in poultry in South Africa, Egypt, Indonesia, and India, and the conversion towards EU regulations for routine Salmonella surveillance in Romania. Routine surveillance of poultry farms for Salmonella and rapid intervention will drastically improve global food safety and security, while the sporadic nature of targeted surveillance will miss the diagnosis of this zoonotic pathogen in many areas of the poultry sector, including breeders, hatcheries, commercial layers, broilers, slaughterhouses, and chicken processing plants. The absence of controlled routine reporting of Salmonella serovars in these five selected developing countries is expected to lead to more illness related to consumption of non-monitored poultry products that could be contaminated with Salmonella. It is recommended that the WHO-GFN expand its capacity-building program in the promotion of integrated, laboratory-based surveillance and intersectoral collaboration among the veterinary and food-related disciplines and human health worldwide. This indispensable expansion should include more strategic participation and partnership of developed countries in the WHO-GFN program, for the sake of improving the livelihood of animals and the safety of human consumers. Acknowledgements This work was funded by the EWABO Co., Germany, and the Deanship of Scientific Research (DSR), King Abdulaziz University, Jeddah, under grant no. 32/67459. The authors thankfully acknowledge the technical and financial support from DSR. References 1. 2. 3. 4. Majowicz SE, Musto J, Scallan E, Angulo FJ, Kirk M, O'Brien SJ, Jones TF, Fazil A, Hoekstra RM; International Collaboration on Enteric Disease 'Burden of Illness' Studies (2010) The global burden of nontyphoidal Salmonella gastroenteritis. Clin Infect Dis 50: 882-889. Cray PJF, Gray JT, Wray C (2000) Salmonella infections in pigs. In Wray C, Wray A, editors. Salmonella in Domestic Animals. Wallingford, United Kingdom: CABI Publishing. 191-208. Uzzau S, Brown DJ, Wallis T, Rubino S, Leori G, Bernard S, Casadesús J, Platt DJ, Olsen JE. (2000) Host adapted serotypes of Salmonella enterica. Epidemiol Infect 125: 229255. Pires SM, Evers EG, van Pelt W, Ayers T, Scallan E, Angulo FJ, Havelaar A, Hald T; Med-Vet-Net Workpackage 28 Working Group (2009) Attributing the human disease burden of foodborne infections to specific sources. Foodborne Pathog Dis 6: 417-424. 5 Barbour et al. – Poultry Salmonella serovars in developing countries 5. 6. 7. 8. 9. 10. 11. 12. 13. 14. 15. 16. 17. 18. Hendriksen RS, Bangtrakulnonth A, Pulsrikarn C, Pornreongwong S, Hasman H, Song SW, Aarestrup FM (2008) Antimicrobial resistance and molecular epidemiology of Salmonella Rissen from animals, food products and patients in Thailand and Denmark. Foodborne Pathog Dis 5: 605-619. Hendriksen RS, Vieira AR, Karlsmose S, Lo Fo Wong DM, Jensen AB, Wegener HC, Aarestrup FM (2011) Global monitoring of Salmonella serovar distribution from the World Health Organization Global Foodborne Infections Network Country Data Bank: results of quality assured laboratories from 2001 to 2007. Foodborne Pathog Dis 8: 887-900. Ethelberg S, Müller L, Mølbak K, Nielsen EM (2010) [Salmonella and Campylobacter infections in 2008]. Ugeskr Laeger 172: 1451-1455. Aarestrup FM, Hendriksen RS, Lockett J, Gay K, Teates K, McDermott PF, White DG, Hasman H, Sørensen G, Bangtrakulnonth A, Pornreongwong S, Pulsrikarn C, Angulo FJ, Gerner-Smidt P (2007) International spread of multidrugresistant Salmonella Schwarzengrund in food products. Emerg Infect Dis 13: 726-731. Clark GM, Kaufmann AF, Gangarosa EJ, Thompson MA (1973) Epidemiology of an international outbreak of Salmonella Agona. Lancet 1: 490-493. Hendriksen RS, Mikoleit M, Carlson VP, Karlsmose S, Vieira AR, Jensen AB, Seyfarth AM, DeLong SM, Weill FX, Lo Fo Wong DM, Angulo FJ, Wegener HC, Aarestrup FM (2009) WHO Global Salm-Surv external quality assurance system for serotyping of Salmonella isolates from 2000 to 2007. J Clin Microbiol 47: 2729-2736. Galanis E, Lo Fo Wong DMA, Patrick ME, Binsztein N, Cieslik A, Chalermchaikit T, Aidara-Kane A, Ellis A, Angulo FJ, Wegener HC, for World Health Organization Global Salm-Surv (2006) Web-based Surveillance and Global Salmonella Distribution, 2000–2002. Emerg Infect Dis 12: 381-388. Ayele M, DeLong SM, Lo Fo Wong DMA, Wagenaar JA, Karlsmose S, Maxwell N, Knope K, Chiller T, GFN Members (2011) WHO Global Foodborne Infections Network (GFN): Over 10 years of strengthening national capacities to detect and control foodborne and other enteric infections globally. International Meeting on Emerging Diseases and Surveillance (IMED 2011), February 4-7, Vienna, Austria. Population Reference Bureau (2014) Available: http://www.prb.org/DataFinder/Geography. FAOSTAT (2012) Food and Agriculture Organization of the United Nations. Available: http://faostat.fao.org/site/339/default.aspx. Accessed October 24, 2014. World Health Organization Global Foodborne Infections Network (WHO-GFN) (2014) Available: www.who.int/gfn/en. Mosupye FM, Von Holy A (1999) Microbiological quality and safety of ready-to-eat street-vended foods in Johannesburg, South Africa. J Food Prot 62: 1278 -1284. Mosupye FM, Von Holy A (2000) Microbiological hazard identification and exposure assessment of street food vending in Johannesburg, South Africa. Int J Food Microbiol 61: 137145. Van Nierop W, Duse AG, Marais E, Aithma N, Thothobolo N, Kassel M, Stewart R, Potgieter A, Fernandes B, Galpin JS, Bloomfield SF (2005) Contamination of chicken carcasses in Gauteng, South Africa, by Salmonella, Listeria J Infect Dev Ctries 2015; 9(1):001-007. 19. 20. 21. 22. 23. 24. 25. 26. 27. 28. 29. 30. 31. 32. monocytogenes, and Campylobacter. Int J Food Microbiol 99: 1-6. Enwere G, Biney E, Cheung YB, Zaman SM, Okoko B, Oluwalana C, Vaughan A, Greenwood B, Adegbola R, Cutts FT (2006) Epidemiologic and clinical characteristics of community-acquired invasive bacterial infections in children aged 2–29 months in the Gambia. Pediatr Infect Dis J 25: 700-705. Brent AJ, Oundo JO, Mwangi I, Ochola L, Lowe B, Berkley JA (2006) Salmonella bacteremia in Kenyan children. Pediatr Infect Dis J 25: 230-236. Walsh AL, Phiri AJ, Graham SM, Molyneux EM, Molyneux ME (2000) Bacteremia in febrile Malawian children: clinical and microbiologic features. Pediatr Infect Dis J 19: 312-318. Graham SM, Walsh AL, Molyneux EM, Phiri AJ, Molyneux ME (2000) Clinical presentation of non-typhoidal Salmonella bacteraemia in Malawian children. Trans R Soc Trop Med Hyg 94: 310-314. Gordon MA, Banda HT, Gondwe M, Gordon SB, Boeree MJ, Walsh AL, Corkill JE, Hart CA, Gilks CF, Molyneux ME (2002) Non-typhoidal Salmonella bacteraemia among HIVinfected Malawian adults: high mortality and frequent recrudescence. AIDS 16: 1633-1641. Gordon MA, Graham SM, Walsh AL, Wilson L, Phiri A, Molyneux E, Zijlstra EE, Heyderman RS, Hart CA, Molyneux ME (2008) Epidemics of invasive Salmonella enterica serovar Enteritidis and S. enterica serovar Typhimurium infection associated with multidrug resistance among adults and children in Malawi. Clin Infect Dis 46: 963969. Morpeth SC, Ramadhani HO, Crump JA (2009) Invasive Non-Typhi Salmonella Disease in Africa. Clin Infect Dis 49: 606-611. Ammar AMA, Ahmed YAE, Asawy AMI, Ibrahim AA (2010) Bacteriological studies on SalmonellaEntertidis isolated from different sources in Dakhlia governorate. Assiut Vet Med J 56: 125-135. El-Jakee, J, Abd El-Moez SI, Mohamed KF, Effat MM, Samy AA, El-Saaid WA (2010) Restriction enzyme, plasmid profile analysis and antibiotic resistance of Salmonella Typhimurium of poultry origin isolated from Egyptian farms. Int J Microbiol Res 1: 137-146. Rabie NS, Khalifa NO, Radwan MEI, Afify JSA (2012) Epidemiological and molecular studies of Salmonella isolates from chicken, chicken meat and human in Toukh, Egypt. Global Vet 8: 128-132. El-Ghany, WAA, El-Shafii SSA, Hatem ME (2012) A survey on Salmonella species isolated from chicken flocks in Egypt. Asian J Anim Vet Adv 7: 489-501. Carsiotis M, Weinstein DL, Karch H, Holder IA, O'Brien AD (1984) Flagella of Salmonella typhimurium are a virulence factor in infected C57BL/6J mice. Infect Immun 46: 814-818. Kimura AC, Reddy V, Marcus R, Cieslak PR, Mohle-Boetani JC, Kassenborg HD, Segler SD, Hardnett FP, Barrett T, Swerdlow DL; Emerging Infections Program FoodNet Working Group (2004) Chicken consumption is a newly identified risk factor for sporadic Salmonella enterica serotype Enteritidis infections in the United States: a casecontrol study in FoodNet sites. Clin Infect Dis 38 Suppl 3: 244-252. El-Safey EM (2013) Incidence of Salmonella heidelberg in some Egyptian food. Int J Microbiol Immunol Res 1: 16-25. 6 Barbour et al. – Poultry Salmonella serovars in developing countries 33. Hennessy TW, Cheng LH, Kassenborg H, Ahuja SD, MohleBoetani J, Marcus R, Shiferaw B, Angulo FJ; Emerging Infections Program FoodNet Working Group (2004) Egg consumption is the principal risk factor for sporadic Salmonella serotype Heidelberg infections: a case-control study in Food Net sites. Clin Infect Dis 38 Suppl 3: 237-243. 34. Kennedy M, Villar R, Vugia DJ, Rabatsky-Ehr T, Farley MM, Pass M, Smith K, Smith P, Cieslak PR, Imhoff B, Griffin PM; Emerging Infections Program FoodNet Working Group (2004) Hospitalizations and deaths due to Salmonella infections, FoodNet, 1996-1999. Clin Infect Dis 38 Suppl 3: 142-148. 35. Vugia DJ, Samuel M, Farley MM, Marcus R, Shiferaw B, Shallow S, Smith K, Angulo FJ; Emerging Infections Program FoodNet Working Group (2004) Invasive Salmonella infections in the United States, FoodNet, 19961999: incidence, serotype distribution, and outcome. Clin Infect Dis 38 Suppl 3: 149-156. 36. Abd El-Aziz DM (2013) Detection of Salmonella typhimurium in retail chicken meat and chicken giblets. Asian Pac J Trop Biomed 3: 678-681. 37. Ochiai, RL, Acosta CJ, Danovaro-Holliday MC, Baiqing D, Bhattacharya SK, Agtini MD, Bhutta ZA, Canh DG, Ali M, Shin S, Wain J, Page AL, Albert MJ, Farrar J, Abu-Elyazeed R, Pang T, Galindo CM, Seidlein LV, Clemens JD (2008) A study of typhoid fever in five Asian countries: Disease burden and implications for controls. Bull World Health Organ 86: 241-320. 38. Crump JA, Luby SP, Mintz ED (2004) The global burden of typhoid fever. Bull World Health Organ 82: 346-353. 39. Radji M, Malik A, Widyasmara A (2010) Rapid detection of Salmonella in food and beverage samples by polymerase chain reaction. Mal J Microbiol 6: 166-170. 40. Kusumaningrum, HD, Suliantari LN, Dewanti-Hariyadi R (2012) Multidrug resistance among different serotypes of Salmonella isolates from fresh products in Indonesia. Int Food Res J 19: 57-63. 41. Ganguli S (1958) Salmonella serotypes in India. Indian J Med Res 46: 637-642. 42. Majumdar AK, Singh SP (1973) A phage typing scheme for Salmonella bareilly. Indian Vet J 50: 1161-1166. 43. Saxena SN, Sharma NC, John PC, Mago ML (1985) A ten year study on the prevalence of geographical distribution of Salmonella bareilly phage types in India (1973-1982). Indian J Med Res 82: 486-491. J Infect Dev Ctries 2015; 9(1):001-007. 44. Singh G, Sharma NC, Jayasheela M, Saxena SN (1988) A study of the epidemiology of Salmonella bareilly in India using a new phage-typing system. Epidemiol Infect 100: 221225. 45. Mahajan R, Dhar Y, John PC, Sokhey J (1998) Prevalence and resistance pattern of Salmonella serotypes in India. J Commun Dis 30: 279-282. 46. Murugkar HV, Rahman H, Kumar A, Bhattacharyya D (2005) Isolation, phage typing and antibiogram of Salmonella from man and animals in northeastern India. Indian J Med Res 122: 237-242. 47. Suresh T, Hatha AAM, Harsha HT, Lakshmanaperumalsamy P (2011) Prevalence and distribution of Salmonella serotypes in marketed broiler chickens and processing environment in Coimbatore City of southern India. Food Res Int 44: 823-825. 48. Singh R, Yadav AS, Tripathi V, Singh RP (2013) Antimicrobial resistance profile of Salmonella present in poultry and poultry environment in India. Food Control 33: 545-548. 49. Rajagopal R, Mini M (2013) Outbreaks of salmonellosis in three different poultry farms of Kerala, India. Asian Pac J Trop Biomed 3: 496-500. 50. Kumar T, Rajora VR, Arora N (2014) Prevalence of Salmonella in pigs and broilers in the Tarai region of Uttarakhand, Indian J Med Microbiol 32: 99-101. 51. Mihaiu L, Lapusan A, Tanasuica R, Sobolu R, Mihaiu R, Oniga O, Mihaiu M (2014) First study of Salmonella in meat in Romania. J Infect Dev Ctries 8: 50-58. doi:10.3855/jidc.3715. 52. Xinhuanet (2013) Poultry products safe in Romania despite sporadic Salmonella outbreaks: breeders' representative. Available: http://news.xinhuanet.com/english/world/201303/09/c_132220735.htm. Accessed 9 March 2013. Corresponding author Steve Harakeh, Ph.D. Special Infectious Agents Unit – Biosafety Level 3 King Fahd Medical Research Center; King Abdulaziz University P.O.Box: 80216, Jeddah 21589, Saudi Arabia Mobile: 00966559392266 Fax: 0096626952076 Email: sharakeh@gmail.com Conflict of interests: No conflict of interests is declared. 7