Trop Anim Health ProdDOI 10.1007/s11250-012-0334-7 Antimicrobial susceptibility and multi-drug resistanceof Salmonella enterica subspecies entericaserovars in Sudan Mayha Mohammed Ali Nor Elmadiena &Adil Ali El Hussein & Catherine Anne Muckle &Linda Cole & Elizabeth Wilkie & Ketna Mistry &Ann Perets # Springer Science+Business Media Dordrecht 2012 Abstract This study was undertaken to determine the anti- (98.4 %), ciprofloxacin (93.8 %), and norfloxacin (90.6 %).
microbial resistance patterns of Salmonella enterica subspe- Two chicken- and the two human-origin S. Kentucky iso- cies enterica recovered from human, food, water, and lates were resistant to both ciprofloxacin and norfloxacin.
animal samples collected in Khartoum State, Sudan. A total All S. Kentucky isolates and the one S. Rissen isolate of 64 Salmonella isolates belonging to 28 different serovars demonstrated multi-drug resistance. The results indicate were tested for their susceptibility to 13 antimicrobial the significance of multi-drug-resistant Salmonella serovars agents. The majority of isolates (98.4 %) were resistant to isolated from chickens and other animals and foods as at least one antimicrobial agent. Isolates were frequently sources for multi-drug-resistant Salmonella in humans in resistant to ampicillin (90.6 %), cephalexin (50.0 %), nali- dixic acid (25.0 %), streptomycin (21.9 %), kanamycin(18.8 %), gentamicin (17.2 %), and co-trimoxazole and Keywords Salmonella serovars . Multi-drug resistance .
trimethoprim (12.5 %). The most common pattern of multi- ple drug resistance included resistance to ampicillin andcephalexin. Most isolates were sensitive to chloramphenicol Emirates College of Technology, Millennium Tower Sheikh Hamdan Street, P.O. Box: 41009, Abu Dhabi, Department of Pathology and Microbiology, Atlantic Veterinary College, University of Prince Edward Island, Charlottetown, L. Cole : E. Wilkie : K. Mistry : A. Perets National Committee for Clinical Laboratory Laboratory for Salmonellosis, Laboratory for Foodborne Office International des Epizooties, Reference Zoonoses, Public Health Agency of Canada,Guelph, Ontario, Canada National Antimicrobial Resistance Monitoring participation in various surveillance programs, help monitor the development and spread of antimicrobial resistance in To date, few studies have analyzed the levels of resis- tance to antimicrobial agents in Salmonella serovars in Sudan (Yagoub et al. ). The present study was therefore Danish Integrated Antimicrobial Resistance undertaken to detect and monitor multi-drug resistance pro- files among Salmonella serovars isolated in Sudan.
Members of Salmonella enterica subspecies enterica are Isolation and identification of Salmonella widely distributed in the environment and in the intestinaltracts of animals. Most human infections are acquired Salmonella were isolated and identified as previously de- through consumption of contaminated food of animal origin scribed by El-Hussein et al. (). Salmonella isolates (Majowicz et al. ; Anjum et al. ). The progressive were recovered from a variety of sources: raw and cooked increase in multi-antimicrobial-resistant Salmonella strains food; chlorinated drinking water; livestock meat and feces; isolated from humans has been associated with the wide- and fish, chicken, and human fecal samples. Presumptive spread use of antimicrobial agents in food animal produc- Salmonella isolates were shipped to the Public Health tion. This spread of antimicrobial resistance through the Agency, Office International des Epizooties (OIE) food chain is regarded as a major public health issue Reference Laboratory for Salmonellosis, Guelph, Ontario, (Threlfall Lynch et al. ; Foley and Lynne Canada, for serotyping and phage typing as previously Le Hello et al. ). The appearance of both plasmid- described by El-Hussein et al. (Sixty-four mediated antibiotic resistant against conventional anti- Salmonella isolates identified into 28 different serovars Salmonella drugs and chromosomal resistance to quinolones and fluoroquinolones has reduced therapeutic options forSalmonella septicemia in humans (Foley and Lynne ).
Studies on antimicrobial resistance in Salmonella have primarily been undertaken in developed countries (van The antimicrobial resistance of the 64 Salmonella isolates Duijkeren et al. ), having launched large-scale surveil- was tested against 13 antimicrobial agents by the disk dif- lance systems to monitor the antimicrobial resistance of fusion method using Mueller Hinton agar (Oxoid, UK) and bacterial enteric pathogens (Jones et al. DANMAP antibiotic disks (Hi Media, India) following the guidelines ; Abdellah et al. ). In developing countries like of the Clinical and Laboratory Standards Institute (CLSI), Sudan, Salmonella and other zoonotic bacterial pathogens formerly the National Committee for Clinical Laboratory are not routinely cultured, and their resistance to commonly Standards (CLSI ). An isolate was defined as suscepti- employed antimicrobials both in public health and veteri- ble or resistant based on the critical points recommended by nary practices is rarely determined (Kariuki et al. National surveillance systems, ideally based on integra- The 13 antibiotics tested were those commonly used in tion of data for animals, food, and humans, are needed to humans or poultry flocks in Sudan, these being: ampicillin develop strategies for containing antimicrobial drug resis- (25 μg/disk), ceftazidime (30/10 μg), chloramphenicol tance. In several countries, these programmes are primarily (30 μg), ciprofloxacin (5 μg), gentamicin (10 μg), kanamy- based on a network of public or private clinical laboratories cin (30 μg), nalidixic acid (25 μg/disk), norfloxacin (10 μg), that refer Salmonella isolates to public health laboratories streptomycin (25 μg), trimethoprim (5 μg/disk), co- for identification. However, such laboratory-based surveil- trimoxazole (25 μg/disk), nitrofurantoin (100 μg/disk), and lance systems in developing countries are hampered by cost constraints and poor access to quality health facilities,resulting in a low rate of isolation of bacterial pathogensfrom patients having mild infections (Bouchrif et al. ).
These constraints account for the lack of data and underes-timation of the number of Salmonella infections in many The results of testing Salmonella isolates against 13 differ- countries, including Sudan. Clinical microbiology laborato- ent antimicrobial drugs are summarized in Tables and ries, through routine antimicrobial susceptibility testing and Isolates were mainly resistant to ampicillin (90.6 %), Table 1 Distribution by serovar and source of antimicrobial resistant Salmonella from samples collected in Khartoum State, Sudan Numbers in parentheses are the numbers of isolates. S. Typhimu- rium*1 : Phagetype 2, S. Enteritidis*1 : Phagetype 21a (from food) A1 ampicillin, C2 chloramphenicol, CAC3 ceftazidime, CIP4 cipro- floxacin, Cp5 cephalexin, Co6 co-trimoxazole, GM7 gentamicin, Ka8kanamycin, Na9 nalidixic acid, NF10 nitrofurantoin, NOR11 norflox- acin, S12 streptomycin, Tr13 trimethoprim cephalexin (50 %), nalidixic acid (25 %), streptomycin (21.9 %), and kanamycin (18.8 %). A total of 17.2 % iso- lates were resistant to gentamicin and 12.5 % to co- trimoxazole and trimethoprim. Isolates belonging to S.
Kentucky, S. Rissen, S. Muenster, S. I:4,12: r;-:enz15 were resistant to streptomycin. Two S. Livingstone isolates and one isolate each of S. Adelaide, S. Schwarzengrund, and S.
Typhimurium were also resistant to streptomycin. All iso- lates were sensitive to chloramphenicol with the exception of one S. Uganda isolate which showed intermediate sus- ceptibility. Only a low degree of resistance (3.1 %) to ceftazidime was detected, but 32.8 % of isolates demonstrat- ed only intermediate susceptibility to this drug. Most iso- lates were sensitive to ciprofloxacin (93.8 %) and norfloxacin (90.6 %). Two human S. Agona isolates were resistant to norfloxacin. The two human and two of the chicken S. Kentucky isolates were resistant to both norflox- Sixty three of 64 isolates (98.4 %) were resistant to at least one antimicrobial drug, and 71.9 % were resistant to more than one antimicrobial drug (Table ). Only the one Johannesburg isolate was sensitive to all antimicrobials tested (Table Twenty-six different patterns of antimicro- bial resistance were identified (Table ). The most common profiles were those which included resistance to ampicillin and cephalexin (20.3 %). The one S. Rissen isolate recov- ered was of chicken origin and was resistant to eight drugs.
All S. Kentucky isolates were resistant to at least four drugs, with the human isolates being resistant to seven.
Variations in resistance of different serovars to a particu- lar antibiotic can be seen in Tables and , with S. Rissen and S. Kentucky isolates being the most multi-drug resis- tant. Human and chicken isolates were most commonly chloramphenicol, and furazolidone in Sudan might have ledto the emergence of resistance, whereas ciprofloxacin has The majority (98.4 %) of 64 Salmonella isolates recovered been newly introduced in the medical field and is not used from human feces and a variety of animal, food, and water samples in Sudan were resistant to at least one antimicrobial Of particular concern, all eight S. Kentucky isolates were drug, this most commonly being ampicillin (90.6 %). Multi- multi-drug resistant. This serovar was common to both drug resistance was more frequent in chicken and animal source humans and chickens, suggesting that chicken and isolates than in humans. A similar small-scale survey of chicken-food products are a potential source of salmonello- Salmonella from food and humans conducted in Addis sis in the food chain (El-Hussein et al. ; Le Hello et al.
Ababa, Ethiopia, during 2003–2004 (Zewdu and Poppe Similar to our study, all three S. Kentucky isolates found 32.7 % of 98 isolates were resistant to one or more of 24 from chicken or beef origin isolated in Addis Ababa, antimicrobials tested, with resistance being most common to Ethiopia, were resistant to at least eight antimicrobials, streptomycin (75 %), followed by ampicillin (59.4 %). Another including ciprofloxacin (Zewdu and Poppe 2003 study of chicken carcass samples in Addis Ababa (Molla Emergence of this multi-resistant serovar undermines the et al. found that 63.7 % of 80 Salmonella isolates were value of relatively cheaper and commonly available antimi- resistant to one or more antimicrobials, with resistance to crobials as first-line drugs for human systemic salmonellosis sulfisoxazole being highest (51.2 %) and 45 % of isolates being for poor citizens of developing countries, as well as the less resistant to ampicillin. A 2003 study of Salmonella from beef available and more expensive cephalosporins and quinolone samples in Dakar, Senegal, found that 60 % of 247 isolates were resistant to at least one antimicrobial (Stevens et al. ).
The high proportion of Salmonella isolates in our study resistant to at least one antimicrobial is consistent with a 2001 study in the USA which found that 84 % of Salmonellaisolates from retail ground chicken, beef, turkey, and pork Our results are based on a relatively small number of were resistant to at least one antimicrobial. Recent national Salmonella isolates; however, these findings are consistent with antimicrobial resistance surveillance data for Salmonella the trends of Salmonella multi-drug resistance found in similar from animals collected in Canada (CIPARS ) showed small-scale surveillance research investigations conducted in that 52 % of Salmonella isolates from chicken samples and the same time period in other African countries (Fadlalla et al.
65 % of pigs abattoir samples were resistant to one or more ; Molla et al. Stevens et al. Zewdu and Poppe antimicrobials, and that 47 % of chicken and 69 % of ), as well as large-scale national surveillance programs in pig retail meat samples were resistant to one or more developed countries, such as DANMAP (DANMAP ), NARMS (Foley and Lynne ), CIPARS (CIPARS ), As previously noted (El-Hussein et al. ), it is difficult to make comparisons between Salmonella surveillance surveys This present study clearly demonstrates the need for con- conducted in different countries as the prevalence of tinued active surveillance to highlight the public health signif- Salmonella serovars varies regionally and isolation rates de- icance of multi-drug resistance among Salmonella in animals pend upon the country, sample plan, and methodology used.
and humans in Sudan. Salmonella surveillance can provide We speculate that the high level of multi-drug resistance of data to target interventions to most effectively treat and prevent Salmonella isolates in Sudan can be attributed to selective foodborne and zoonotic pathogens (Mangen et al. ).
pressure from the irrational use of antimicrobials in food ani-mals and humans which selects for certain Salmonella serovarsmore prone to develop resistance than others (WHO The authors gratefully acknowledge the support of the Office International des Epizooties (OIE) Reference Laboratory Our findings are comparable to a recently reported study on for Salmonellosis, Laboratory for Foodborne Zoonoses, Public Health antimicrobial susceptibility of Salmonella serotypes isolated Agency of Canada, Guelph, Ontario, Canada.
from the feces of humans, cattle, camels, and poultry in Sudan(Fadlalla et al. ). This survey demonstrated that 93.1 % of87 human isolates and 46.8 % of 32 animal isolates were resistant to at least one of the ten antimicrobial agents tested.
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