EcoHealth 10, 348–351, 2013 DOI: 10.1007/s10393-013-0866-y
Ó 2013 International Association for Ecology and Health
Short Communication
Isolation of Salmonella Virchow from a Fruit Bat (Pteropus giganteus) Ausraful Islam,1 Andrea Mikolon,1 Matthew Mikoleit,2 Dilruba Ahmed,1 Salah Udddin Khan,1 M. A. Yushuf Sharker,1 M. Jahangir Hossain,1 Ariful Islam,3 Jonathan H. Epstein,3,4 Nord Zeidner,1 and Stephen P. Luby1 1
International Center for Diarrheal Diseases Research, Bangladesh (ICDDR,B), 68, Shaheed Tajuddin Ahmed Sharani, Mohakhali, Dhaka 1212, Bangladesh 2 Enteric Diseases Laboratory Branch, Centers for Disease Control and Prevention (CDC), 1600 Clifton RD MS C-03, Atlanta, GA 303333 3 EcoHealth Alliance, 460 West 34th Street, 17th Floor, New York, NY 10001-2320 4 School of Life Sciences, Kingston University, Kingston-upon-Thames, UK
Abstract: Detection of zoonotic pathogens carried by bats is important both for understanding disease ecology and for developing preventive measures. Pteropus fruit bats have been identified as potential carriers of Salmonella enterica serotype Typhi. A cross-sectional study was conducted to determine the prevalence of Salmonella Typhi and other Salmonella serotypes in Pteropus giganteus fruit bats in Bangladesh. Rectal swabs were collected from 302 bats and cultured for Salmonella species. The bats were trapped in three districts (Faridpur, Rajbari, and Cox’s Bazar). Salmonella Typhi was not found but one juvenile female bat from Faridpur district was positive for Salmonella Virchow. Close associations between frugivorous bats, humans, and livestock in rural Bangladesh make it likely that the bat was infected by consuming contaminated water. Keywords: fruit bats, Pteropus giganteus, Salmonella Typhi, Salmonella Virchow, Bangladesh
Each year, typhoid fever causes *21 million cases and 0.2 million deaths worldwide with the highest incidence in South-East Asia (Crump et al. 2004). The etiologic agent, Salmonella Typhi has been historically regarded as a hostadapted pathogen of humans (Miao and Miller 1999). Non-typhoidal Salmonella serotypes are a common cause of food-borne gastroenteritis in people, including Salmonella Virchow (Ispahani and Slack 2000), and have been found in a wide range of wild and domestic avian species (Craven et al. 2000; Epstein et al. 2006b). Shedding of salmonella in mammals and birds varies by species and serotype; duration and probability of shedding is affected by stressors Published online: October 18, 2013 Correspondence to: Ausraful Islam, e-mail: [email protected]
such as crowding and malnutrition (Hoelzer et al. 2011). Like wild birds, Pteropus fruit bats (family Pteropodidae) live in close proximity to humans and poultry and share their food resources (Luby et al. 2009; Luskin 2010). Fruit bats are common in the regions with the highest incidence of typhoid fever (Bates and Harrison 1997; Ram et al. 2007). In the early 1970s, Pteropus rufus or Madagascar flying fox was identified as a potential reservoir of Salmonella Typhi, after repeatedly isolating the bacteria from individuals in a colony in Madagascar through a crosssectional study (Brygoo 1973). The prevalence of Salmonella Typhi among these bats was 10% for first year and 14% for a second year (Brygoo 1973). P. giganteus is common throughout Bangladesh and is closely related to
Salmonellosis in a Fruit Bat
P. rufus, sharing the same dietary and ecological traits such as feeding, roosting, and breeding (Epstein et al., 2006a). P. giganteus lives very close to humans and has been associated with the zoonotic transmission of Nipah virus through consumption of fresh date palm sap presumably contaminated with bat saliva and excreta (Luby et al. 2009). It is likely that other fecally excreted pathogens (e.g., Salmonella) could be transmitted in a similar manner. Human infection with Salmonella Typhi in Bangladesh has been associated with eating papaya (Ram et al. 2007), a fruit known to be eaten by bats as well and which could similarly be contaminated with bat excreta during feeding activity. Our calculated sample size for this study was 302 bats (null hypothesis = 1%, against alternatives 3.5%) to get consistently more than 80% power. From February to June 2010, a cross-sectional study of 302 (70 juvenile and 232 adult; 148 male and 154 female) P. giganteus was conducted in three geographical regions of Bangladesh to determine whether these fruit bats may act as a potential source of human Salmonella infections. Capture techniques have been approved by IACUC (#04-08) and Animal Experimentation Ethics Committee of ICDDR,B. 178 bats were sampled from Faridpur district (23°360 03.800 N, 089°480 57.700 E), 89 from Rajbari district (23°350 38.800 N, 089°430 17.200 E), and 35 from Cox’s Bazar district (21°450 4000 N, 092°040 1000 E) (Fig. 1). After capture, the bats were brought to the field laboratory and anesthetized with isoflurane (Attane, Minrad INC., Bethlehem, NY, USA). Rectal swabs were collected using a sterile swab then placed in Cary Blair media (Becton, Dickinson and Company, Franklin Lakes, NJ, USA) and sent to the clinical microbiology laboratory of the International Centre for Diarrheal Disease Research, Bangladesh (ICDDR,B) within 48 h. Laboratory technicians used commercially available MacConkey agar, S–S agar (Salmonella Shigella agar), and selenite broth for bacterial culture and S–S agar (all from Becton, Dickinson and Company) for subculture. Standardized biochemical testing was performed by ICDDR,B to identify suspected colonies of Salmonella (Isenberg 1998) and serovar was determined at the US Centers for Disease Control and Prevention (CDC) using the method of Brenner and Murlin (1998). CDC used broth microdilution to determine minimum inhibitory concentrations to 15 antimicrobials (amikacin, amoxycillin/clavulanic acid, ampicillin, cefoxitin, ceftiofur, ceftriaxone, chloramphenicol, ciprofloxacin, gentamycin, kanamycin, nalidixic acid, streptomycin, sulfisoxazole, tetracycline, and trimethoprim/ sulphamethoxazole) based on the current
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Fig. 1. Study sites in different parts of Bangladesh. The study sites (Rajbari, Faridpur, Cox’s Bazar) from where we have captured and sampled P. giganteus fruit bats to detect salmonellosis among them. The one Salmonella Virchow positive bat was from Faridpur district.
CDC NARMS (National Antimicrobial Resistance Monitoring System) panel. Antimicrobial susceptibility was determined according to the interpretative criteria of the Clinical Laboratory Standards Institute (CLSI) and NARMS guidelines. Pulsed field gel electrophoresis (PFGE) and analysis following XbaI digestion was performed on this isolate utilizing PulseNet USA Standardized Protocols (Ribot et al. 2006). All rectal swabs from P. giganteus were negative for Salmonella Typhi, but Salmonella group C1 was isolated from a juvenile female bat (prevalence rate 0.33, 95% confidence interval 0.008, 1.83%) from Faridpur district. The bacterial isolate was identified as Salmonella serotype Virchow and was sensitive to all 15 antimicrobials. Although a previous investigation had reported salmonellosis among Pteropus fruit bats (Brygoo 1973), Salmonella Virchow has not been previously reported. Salmonella Virchow has been identified from several sources including powdered skimmed milk (Dziadkowiec et al. 1995), raw buffalo milk (Singh 2010), Asian house gecko (Hemidactylus frenatus) (Callaway et al. 2011), poultry,
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poultry and quail products (Aarestrup et al. 2005), and household dogs (Sato et al. 2000), and is known to cause disease in people. Though data on non-typhoidal salmonella (NTS) in South Asia are limited, a hospital-based surveillance from 1996–2011 shows that 1.3% diarrheal patients in Bangladesh are suffering from NTS (Leung et al. 2013). Villages in rural Bangladesh commonly include stagnant lagoons used for bathing and drinking by people and associated livestock and these water sources are often contaminated with sewage (Parveen et al. 2008). P. giganteus has been observed drinking from these water sources (Epstein, unpublished obs.); thus, contaminated water is a possible source of infection. Salmonella shedding can be sporadic and Salmonella is not equally distributed in the feces (e.g., a swab from one section of feces may be positive and another negative). We used a non-invasive sampling method and collected rectal swabs only; thus the way to improve on this would be to actually euthanize the bats and collect tissue and intestinal samples. Although the isolate produced a unique PFGE pattern, it did cluster with other isolates of Salmonella Virchow in the PulseNet USA database. Interpretation of PFGE data was precluded by a lack of Salmonella Virchow isolates from the region and the recovery of a single Salmonella Virchow isolate from this study. The PFGE profile of this strain has been archived in the PulseNet USA database and is readily available for retrospective comparison should additional Salmonella Virchow isolates be identified in future studies. Although it remains possible that P. giganteus bats can carry Salmonella Typhi in Bangladesh, this study of 302 bats in a setting where typhoid is common did not find any evidence of infection (prevalence 0, 97.5% exact binomial CI: 0–.012). With regard to close contacts between bats, humans, and livestock, the identification of zoonotic and anthropozoonotic agents carried by bats is critical for understanding the ecology of zoonotic pathogens and for developing appropriate preventive measures.
ACKNOWLEDGMENTS This research study was funded by the National Institute of Health (NIH) through EchoHealth Alliance, Grant Number 07-015-0712-52200. ICDDR,B acknowledges with gratitude the commitment of NIH to its research efforts. ICDDR,B is grateful to CDC for their laboratory support for the study.
REFERENCES Aarestrup FM, Hasman H, Jensen LB (2005) Resistant Salmonella Virchow in quail products. Emerging Infectious Diseases 11:1984–1985 Bates PJJ, Harrison DL (1997) Bats of the Indian Subcontinent, Sevenoaks, UK: Harrison Zoological Museum Brenner FW, McWhorter-Murlin AC (1998) Identification and serotyping of Salmonella. Atlanta: Department of Health and Human Services, Centers for Disease Control and Prevention. Brygoo ER (1973) Les chiropteres re´servoirs de virus d’ente´robacte´ries pathogenes pour l’homme. Archives de I’Institut Pasteur de Madagascar 42:239–252 Callaway Z, Thomas A, Melrose W, Buttner P, Speare R (2011) Salmonella Virchow and Salmonella Weltevreden in a random survey of the Asian house gecko, Hemidactylus frenatus, in houses in northern Australia. Vector-Borne Zoonotic Diseases 11:621–625 Craven SE, Stern NJ, Line E, Bailey JS, Cox NA, Fedorka-Cray P (2000) Determination of the incidence of Salmonella spp., Campylobacter jejuni, and Clostridium perfringens in wild birds near broiler chicken houses by sampling intestinal droppings. Avian Diseases 44:715–720 Crump JA, Luby SP, Mintz ED (2004) The global burden of typhoid fever. Bulletin of the World Health Organization 82:346– 353 Dziadkowiec D, Mansfield LP, Forsythe SJ (1995) The detection of Salmonella in skimmed milk powder enrichments using conventional methods and immunomagnetic separation. Applied Microbiology 20:361–364 Epstein JH, Field HE, Luby S, Pulliam JR, Daszak P (2006) Nipah virus: impact, origins, and causes of emergence. Current Infectious Disease Reports 8:59–65 Epstein JH, McKee J, Shaw P, Hicks V, Micalizzi G, Daszak P, et al. (2006) The Australian white ibis (Threskiornis molucca) as a reservoir of zoonotic and livestock pathogens. Ecohealth 3:290–298 Hoelzer K, Switt AIM, Wiedmann M (2011) Animal contact as a source of human non-typhoidal salmonellosis. Veterinary Research 42:34 . doi:10.1186/1297-9716-42-34 Isenberg HD (1998) Essential Procedures of Clinical Microbiology. Washington D.C.: American Society for Microbiologists Ispahani P, Slack RCB (2000) Enteric fever and other extraintestinal salmonellosis in University Hospital, Nottingham, UK, between 1980 and 1997. European Journal of Clinical Microbiology & Infectious Diseases 19:679–687 Leung DT, Das SK, Malek MA, Ahmed D, Khanam F, Qadri F, et al. (2013) Non-typhoidal Salmonella gastroenteritis at a diarrheal hospital in Dhaka, Bangladesh, 1996–2011. American Journal of Tropical Medicine and Hygiene 88:661–669 . doi:10.4269/ajtmh12-0672 Luby SP, Gurley ES, Hossain MJ (2009) Transmission of human infection with Nipah virus. Clinical Infectious Diseases 49:1743– 1748 Luskin MS (2010) Flying foxes prefer to forage in farmland in a tropical dry forest landscape mosaic in Fiji. Biotropica 42:246– 250 Miao EA, Miller SI (1999) Bacteriophages in the evolution of pathogen–host interactions. Proceedings of the National Academy of Sciences USA 96:9452–9454
Salmonellosis in a Fruit Bat
Parveen S, Ahmed MSU, Nasreen T (2008) Microbial contamination of water in around Dhaka city. Bangladesh Journal of Scientific and Industrial Research 43:273–276 Ram PK, Naheed A, Brooks WA, Hossain MA, Mintz ED, Breiman RF, et al. (2007) Risk factors for typhoid fever in a slum in Dhaka, Bangladesh. Epidemiology and Infection 135(3):458–465 Ribot EM, Fair MA, Gautom R, Cameron DN, Hunter SB, Swaminathan B, et al. (2006) Standardization of pulsed-field gel
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electrophoresis protocols for the subtyping of Escherichia coli O157:H7, Salmonella, and Shigella for PulseNet. Foodborne Pathogens and Disease 3:59–67 Sato Y, Mori T, Koyama T, Nagase H (2000) Salmonella Virchow infection in an infant transmitted by household dogs. Journal of Veterinary Medical Science 62:767–769 Singh BR (2010) Salmonella enterica serovar Virchow in raw milk of buffalo in Bareilly. Current Science 98:25
Ó 2013 International Association for Ecology and Health
Short Communication
Isolation of Salmonella Virchow from a Fruit Bat (Pteropus giganteus) Ausraful Islam,1 Andrea Mikolon,1 Matthew Mikoleit,2 Dilruba Ahmed,1 Salah Udddin Khan,1 M. A. Yushuf Sharker,1 M. Jahangir Hossain,1 Ariful Islam,3 Jonathan H. Epstein,3,4 Nord Zeidner,1 and Stephen P. Luby1 1
International Center for Diarrheal Diseases Research, Bangladesh (ICDDR,B), 68, Shaheed Tajuddin Ahmed Sharani, Mohakhali, Dhaka 1212, Bangladesh 2 Enteric Diseases Laboratory Branch, Centers for Disease Control and Prevention (CDC), 1600 Clifton RD MS C-03, Atlanta, GA 303333 3 EcoHealth Alliance, 460 West 34th Street, 17th Floor, New York, NY 10001-2320 4 School of Life Sciences, Kingston University, Kingston-upon-Thames, UK
Abstract: Detection of zoonotic pathogens carried by bats is important both for understanding disease ecology and for developing preventive measures. Pteropus fruit bats have been identified as potential carriers of Salmonella enterica serotype Typhi. A cross-sectional study was conducted to determine the prevalence of Salmonella Typhi and other Salmonella serotypes in Pteropus giganteus fruit bats in Bangladesh. Rectal swabs were collected from 302 bats and cultured for Salmonella species. The bats were trapped in three districts (Faridpur, Rajbari, and Cox’s Bazar). Salmonella Typhi was not found but one juvenile female bat from Faridpur district was positive for Salmonella Virchow. Close associations between frugivorous bats, humans, and livestock in rural Bangladesh make it likely that the bat was infected by consuming contaminated water. Keywords: fruit bats, Pteropus giganteus, Salmonella Typhi, Salmonella Virchow, Bangladesh
Each year, typhoid fever causes *21 million cases and 0.2 million deaths worldwide with the highest incidence in South-East Asia (Crump et al. 2004). The etiologic agent, Salmonella Typhi has been historically regarded as a hostadapted pathogen of humans (Miao and Miller 1999). Non-typhoidal Salmonella serotypes are a common cause of food-borne gastroenteritis in people, including Salmonella Virchow (Ispahani and Slack 2000), and have been found in a wide range of wild and domestic avian species (Craven et al. 2000; Epstein et al. 2006b). Shedding of salmonella in mammals and birds varies by species and serotype; duration and probability of shedding is affected by stressors Published online: October 18, 2013 Correspondence to: Ausraful Islam, e-mail: [email protected]
such as crowding and malnutrition (Hoelzer et al. 2011). Like wild birds, Pteropus fruit bats (family Pteropodidae) live in close proximity to humans and poultry and share their food resources (Luby et al. 2009; Luskin 2010). Fruit bats are common in the regions with the highest incidence of typhoid fever (Bates and Harrison 1997; Ram et al. 2007). In the early 1970s, Pteropus rufus or Madagascar flying fox was identified as a potential reservoir of Salmonella Typhi, after repeatedly isolating the bacteria from individuals in a colony in Madagascar through a crosssectional study (Brygoo 1973). The prevalence of Salmonella Typhi among these bats was 10% for first year and 14% for a second year (Brygoo 1973). P. giganteus is common throughout Bangladesh and is closely related to
Salmonellosis in a Fruit Bat
P. rufus, sharing the same dietary and ecological traits such as feeding, roosting, and breeding (Epstein et al., 2006a). P. giganteus lives very close to humans and has been associated with the zoonotic transmission of Nipah virus through consumption of fresh date palm sap presumably contaminated with bat saliva and excreta (Luby et al. 2009). It is likely that other fecally excreted pathogens (e.g., Salmonella) could be transmitted in a similar manner. Human infection with Salmonella Typhi in Bangladesh has been associated with eating papaya (Ram et al. 2007), a fruit known to be eaten by bats as well and which could similarly be contaminated with bat excreta during feeding activity. Our calculated sample size for this study was 302 bats (null hypothesis = 1%, against alternatives 3.5%) to get consistently more than 80% power. From February to June 2010, a cross-sectional study of 302 (70 juvenile and 232 adult; 148 male and 154 female) P. giganteus was conducted in three geographical regions of Bangladesh to determine whether these fruit bats may act as a potential source of human Salmonella infections. Capture techniques have been approved by IACUC (#04-08) and Animal Experimentation Ethics Committee of ICDDR,B. 178 bats were sampled from Faridpur district (23°360 03.800 N, 089°480 57.700 E), 89 from Rajbari district (23°350 38.800 N, 089°430 17.200 E), and 35 from Cox’s Bazar district (21°450 4000 N, 092°040 1000 E) (Fig. 1). After capture, the bats were brought to the field laboratory and anesthetized with isoflurane (Attane, Minrad INC., Bethlehem, NY, USA). Rectal swabs were collected using a sterile swab then placed in Cary Blair media (Becton, Dickinson and Company, Franklin Lakes, NJ, USA) and sent to the clinical microbiology laboratory of the International Centre for Diarrheal Disease Research, Bangladesh (ICDDR,B) within 48 h. Laboratory technicians used commercially available MacConkey agar, S–S agar (Salmonella Shigella agar), and selenite broth for bacterial culture and S–S agar (all from Becton, Dickinson and Company) for subculture. Standardized biochemical testing was performed by ICDDR,B to identify suspected colonies of Salmonella (Isenberg 1998) and serovar was determined at the US Centers for Disease Control and Prevention (CDC) using the method of Brenner and Murlin (1998). CDC used broth microdilution to determine minimum inhibitory concentrations to 15 antimicrobials (amikacin, amoxycillin/clavulanic acid, ampicillin, cefoxitin, ceftiofur, ceftriaxone, chloramphenicol, ciprofloxacin, gentamycin, kanamycin, nalidixic acid, streptomycin, sulfisoxazole, tetracycline, and trimethoprim/ sulphamethoxazole) based on the current
349
Fig. 1. Study sites in different parts of Bangladesh. The study sites (Rajbari, Faridpur, Cox’s Bazar) from where we have captured and sampled P. giganteus fruit bats to detect salmonellosis among them. The one Salmonella Virchow positive bat was from Faridpur district.
CDC NARMS (National Antimicrobial Resistance Monitoring System) panel. Antimicrobial susceptibility was determined according to the interpretative criteria of the Clinical Laboratory Standards Institute (CLSI) and NARMS guidelines. Pulsed field gel electrophoresis (PFGE) and analysis following XbaI digestion was performed on this isolate utilizing PulseNet USA Standardized Protocols (Ribot et al. 2006). All rectal swabs from P. giganteus were negative for Salmonella Typhi, but Salmonella group C1 was isolated from a juvenile female bat (prevalence rate 0.33, 95% confidence interval 0.008, 1.83%) from Faridpur district. The bacterial isolate was identified as Salmonella serotype Virchow and was sensitive to all 15 antimicrobials. Although a previous investigation had reported salmonellosis among Pteropus fruit bats (Brygoo 1973), Salmonella Virchow has not been previously reported. Salmonella Virchow has been identified from several sources including powdered skimmed milk (Dziadkowiec et al. 1995), raw buffalo milk (Singh 2010), Asian house gecko (Hemidactylus frenatus) (Callaway et al. 2011), poultry,
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A. Islam et al.
poultry and quail products (Aarestrup et al. 2005), and household dogs (Sato et al. 2000), and is known to cause disease in people. Though data on non-typhoidal salmonella (NTS) in South Asia are limited, a hospital-based surveillance from 1996–2011 shows that 1.3% diarrheal patients in Bangladesh are suffering from NTS (Leung et al. 2013). Villages in rural Bangladesh commonly include stagnant lagoons used for bathing and drinking by people and associated livestock and these water sources are often contaminated with sewage (Parveen et al. 2008). P. giganteus has been observed drinking from these water sources (Epstein, unpublished obs.); thus, contaminated water is a possible source of infection. Salmonella shedding can be sporadic and Salmonella is not equally distributed in the feces (e.g., a swab from one section of feces may be positive and another negative). We used a non-invasive sampling method and collected rectal swabs only; thus the way to improve on this would be to actually euthanize the bats and collect tissue and intestinal samples. Although the isolate produced a unique PFGE pattern, it did cluster with other isolates of Salmonella Virchow in the PulseNet USA database. Interpretation of PFGE data was precluded by a lack of Salmonella Virchow isolates from the region and the recovery of a single Salmonella Virchow isolate from this study. The PFGE profile of this strain has been archived in the PulseNet USA database and is readily available for retrospective comparison should additional Salmonella Virchow isolates be identified in future studies. Although it remains possible that P. giganteus bats can carry Salmonella Typhi in Bangladesh, this study of 302 bats in a setting where typhoid is common did not find any evidence of infection (prevalence 0, 97.5% exact binomial CI: 0–.012). With regard to close contacts between bats, humans, and livestock, the identification of zoonotic and anthropozoonotic agents carried by bats is critical for understanding the ecology of zoonotic pathogens and for developing appropriate preventive measures.
ACKNOWLEDGMENTS This research study was funded by the National Institute of Health (NIH) through EchoHealth Alliance, Grant Number 07-015-0712-52200. ICDDR,B acknowledges with gratitude the commitment of NIH to its research efforts. ICDDR,B is grateful to CDC for their laboratory support for the study.
REFERENCES Aarestrup FM, Hasman H, Jensen LB (2005) Resistant Salmonella Virchow in quail products. Emerging Infectious Diseases 11:1984–1985 Bates PJJ, Harrison DL (1997) Bats of the Indian Subcontinent, Sevenoaks, UK: Harrison Zoological Museum Brenner FW, McWhorter-Murlin AC (1998) Identification and serotyping of Salmonella. Atlanta: Department of Health and Human Services, Centers for Disease Control and Prevention. Brygoo ER (1973) Les chiropteres re´servoirs de virus d’ente´robacte´ries pathogenes pour l’homme. Archives de I’Institut Pasteur de Madagascar 42:239–252 Callaway Z, Thomas A, Melrose W, Buttner P, Speare R (2011) Salmonella Virchow and Salmonella Weltevreden in a random survey of the Asian house gecko, Hemidactylus frenatus, in houses in northern Australia. Vector-Borne Zoonotic Diseases 11:621–625 Craven SE, Stern NJ, Line E, Bailey JS, Cox NA, Fedorka-Cray P (2000) Determination of the incidence of Salmonella spp., Campylobacter jejuni, and Clostridium perfringens in wild birds near broiler chicken houses by sampling intestinal droppings. Avian Diseases 44:715–720 Crump JA, Luby SP, Mintz ED (2004) The global burden of typhoid fever. Bulletin of the World Health Organization 82:346– 353 Dziadkowiec D, Mansfield LP, Forsythe SJ (1995) The detection of Salmonella in skimmed milk powder enrichments using conventional methods and immunomagnetic separation. Applied Microbiology 20:361–364 Epstein JH, Field HE, Luby S, Pulliam JR, Daszak P (2006) Nipah virus: impact, origins, and causes of emergence. Current Infectious Disease Reports 8:59–65 Epstein JH, McKee J, Shaw P, Hicks V, Micalizzi G, Daszak P, et al. (2006) The Australian white ibis (Threskiornis molucca) as a reservoir of zoonotic and livestock pathogens. Ecohealth 3:290–298 Hoelzer K, Switt AIM, Wiedmann M (2011) Animal contact as a source of human non-typhoidal salmonellosis. Veterinary Research 42:34 . doi:10.1186/1297-9716-42-34 Isenberg HD (1998) Essential Procedures of Clinical Microbiology. Washington D.C.: American Society for Microbiologists Ispahani P, Slack RCB (2000) Enteric fever and other extraintestinal salmonellosis in University Hospital, Nottingham, UK, between 1980 and 1997. European Journal of Clinical Microbiology & Infectious Diseases 19:679–687 Leung DT, Das SK, Malek MA, Ahmed D, Khanam F, Qadri F, et al. (2013) Non-typhoidal Salmonella gastroenteritis at a diarrheal hospital in Dhaka, Bangladesh, 1996–2011. American Journal of Tropical Medicine and Hygiene 88:661–669 . doi:10.4269/ajtmh12-0672 Luby SP, Gurley ES, Hossain MJ (2009) Transmission of human infection with Nipah virus. Clinical Infectious Diseases 49:1743– 1748 Luskin MS (2010) Flying foxes prefer to forage in farmland in a tropical dry forest landscape mosaic in Fiji. Biotropica 42:246– 250 Miao EA, Miller SI (1999) Bacteriophages in the evolution of pathogen–host interactions. Proceedings of the National Academy of Sciences USA 96:9452–9454
Salmonellosis in a Fruit Bat
Parveen S, Ahmed MSU, Nasreen T (2008) Microbial contamination of water in around Dhaka city. Bangladesh Journal of Scientific and Industrial Research 43:273–276 Ram PK, Naheed A, Brooks WA, Hossain MA, Mintz ED, Breiman RF, et al. (2007) Risk factors for typhoid fever in a slum in Dhaka, Bangladesh. Epidemiology and Infection 135(3):458–465 Ribot EM, Fair MA, Gautom R, Cameron DN, Hunter SB, Swaminathan B, et al. (2006) Standardization of pulsed-field gel
351
electrophoresis protocols for the subtyping of Escherichia coli O157:H7, Salmonella, and Shigella for PulseNet. Foodborne Pathogens and Disease 3:59–67 Sato Y, Mori T, Koyama T, Nagase H (2000) Salmonella Virchow infection in an infant transmitted by household dogs. Journal of Veterinary Medical Science 62:767–769 Singh BR (2010) Salmonella enterica serovar Virchow in raw milk of buffalo in Bareilly. Current Science 98:25
