Bacteremia in children at a regional hospital in Trinidad

Article Outline

• Summary
• Introduction
• Patients and methods
  • Study population
  • Case studies
  • Blood culture
• Results
• Discussion
• References
• Copyright

Summary 

Objective

The objective of this study was to provide a Trinidadian perspective on pediatric community-acquired and hospital-acquired bacteremia via the documentation of common etiologic agents, antimicrobial profiles of the isolated pathogens, and patient outcome.

Methods

This was a six-year retrospective study of children with bacteremia admitted to the pediatric wards of the San Fernando General Hospital, Trinidad.

Results

Seven hundred and four episodes of pediatric bacteremia were reviewed during the six-year study period. The predominant isolate was Staphylococcus aureus (23.9%), followed by Pseudomonas aeruginosa (15.5%), Klebsiella pneumoniae (12.5%), and Enterobacter spp (11.1%). The remaining isolates each accounted for less than 10% of total isolates. The mortality rate was highest for P. aeruginosa (39.4%), Streptococcus pneumoniae (22.5%), and Escherichia coli (19.2%). Of the six cases due to Neisseria meningitidis, only two survived. The overall mortality rate for the study period was 15.1%, but varied considerably according to age. All deaths due to P. aeruginosa and E. coli occurred in neonates. Almost 90% and about half of all S. aureus were resistant to ampicillin and erythromycin, respectively; nineteen (11.3%) were methicillin-resistant. More than 95% of K. pneumoniae and more than 87% of Haemophilus influenzae were resistant to ampicillin. Group B streptococci were fully susceptible to ampicillin and amoxicillin–clavulanic acid, but showed >90% and >70% resistance to tetracycline and trimethoprim-sulfamethoxazole, respectively. Of the 40 strains of S. pneumoniae isolated, 10.0% had a minimum inhibitory concentration (MIC) ≥4μg/mL (resistance) and 12.5% had a MIC=2.0μg/mL (intermediate resistance) to ceftriaxone, while 7.5% showed intermediate resistance (MIC between 0.12 and 1μg/mL) and 25.0% showed resistance (MIC ≥2μg/mL) to penicillin.

Conclusion

The bacteremia rate was found to be 8.4% among hospitalized children suspected of having sepsis and from whom a blood culture was positive. Bacteremia was also associated with a high mortality rate of 15.1%. An unusually high level of bacteremia with Gram-negative enteric bacteria was seen, which might indicate cross infection and reflect a breakdown in infection control measures. Relatively high-level resistance of S. pneumoniae to penicillin and ceftriaxone was not seen, even though the overall prevalence of resistance to other antibiotics among other pathogens was relatively low. The drugs that showed the greatest efficacy were imipenem, gentamicin, ciprofloxacin, and the cephalosporins ceftazidime and ceftriaxone.

Keywords: Bacteremia in children, Sepsis, Antibiotic resistance, Trinidad

Back to Article Outline

Introduction 

Bacterial isolation from blood specimens is often associated with high morbidity and mortality, particularly among children.¹, ², ³ Many studies on the incidence of blood stream infections have shown an increased occurrence over the past 15–20 years due to the increasingly vulnerable patient population being admitted to hospitals.¹, ⁴ Patients at particular risk for bacteremia include those less than five years of age,¹, ⁵ those with severe underlying disease,⁶, ⁷, ⁸, ⁹ the malnourished,¹⁰ and those with severe burns and admission to an intensive care unit.¹¹, ¹², ¹³ The majority of pediatric bacteremia cases are caused by a number of common pathogens that include Streptococcus pneumoniae, group B streptococci (GBS), Haemophilus influenzae, Escherichia coli, Pseudomonas aeruginosa, Klebsiella pneumoniae, Staphylococcus aureus, and Enterobacter spp,¹, ⁴, ⁷, ¹⁴ and the predominant etiologic agent may vary from one geographical area to another, and even within a given area.⁶, ⁷, ¹², ¹³ Different organisms may have different antimicrobial susceptibilities and successful treatment is dependent upon the prompt administration of the correct drug.⁸, ¹⁴ There is at present a scarcity of Trinidadian and regional data on bacteremia in pediatric patients.

The present study was undertaken to provide a Trinidadian perspective to bacteremia by documenting the distribution of organisms responsible for episodes of bacteremia in children admitted to the San Fernando General Hospital. Particular emphasis was placed on the underlying diagnosis of both community-acquired and hospital-acquired bacteremia, the suspected source of infection, risk factors, and outcome. Through the antimicrobial profile, the study provides a rational basis for empiric choices of drugs in suspected cases of bacteremia while awaiting results of blood culture.

Back to Article Outline

Patients and methods 

Study population 

All children from birth to 12 years of age, admitted to the pediatric wards of San Fernando General Hospital from January 1, 1997 to December 31, 2002 were eligible for the study. The San Fernando General Hospital is a 650-bed tertiary teaching hospital with a daily census of about 800 and a monthly admission rate of about 1800 patients. The hospital serves the southern area of the country that has a population of approximately 410000 people; the total population of the country is about 1.3 million. Trinidad is 4828 square kilometers in area and is the larger of the twin island republic, Trinidad and Tobago, located about 11kilometers off the northern coast of Venezuela in South America.

Case studies 

Case records of all hospitalized children whose blood cultures grew any organisms during the study period were reviewed retrospectively. There are four pediatric wards (two surgical and two medical) with 128 beds divided among them. The neonatal unit has 40 beds. Records were kept of patient age, sex, weight, duration of hospital stay, working diagnosis, and previously diagnosed underlying illness. Also recorded were the results of each positive blood culture and specimens taken from other body sites at the same time as the blood culture. White blood cell (WBC) and differential cell counts, highest body temperature on the day the blood culture was taken, and antimicrobial therapy before and after blood culture results were known, were also recorded.

Blood culture 

A positive blood culture was considered significant if the same organism was isolated from another specimen source from the same patient or if the blood isolate was compatible with the clinical diagnosis. Isolated organisms such as Neisseria meningitidis, H. influenzae, S. pneumoniae, GBS, E. coli and other Gram-negative bacilli of the Enterobacteriaceae family, viridans streptococci, S. aureus, and P. aeruginosa were considered significant. Organisms were considered contaminants if they were only isolated from a single blood culture and the patient recovered without being treated with any antimicrobial agents by the physician. Bacillus spp, diphtheroids, and coagulase-negative staphylococci were among organisms often considered as contaminants and these cases were not included in the study.

The pediatrician took blood specimens for culture after sterilizing the skin with 70% alcohol and then with 10% povidone iodine solution. One to three milliliters venous blood was taken from the patient and inoculated into an aerobic blood culture bottle (Bactec Peds Plus/F, Becton Dickinson, Microbiology Systems, Cockeysville, Maryland, USA). No note was taken as to whether the above aseptic measures were strictly adhered to in every sample taken. All cultures were checked daily for cloudiness, hemolysis, and gas production. Sepsis was defined according to the recommendations of Bone et al.¹⁵

Organisms were identified via standard microbiological techniques and susceptibility testing was evaluated using the disc diffusion methods according to the guidelines of the National Committee for Clinical Laboratory Standards (NCCLS).¹⁶ The following antibiotics and concentrations (in brackets) were used: ampicillin (10μg), amoxicillin–clavulanic acid (20/10μg), tetracycline (30μg), erythromycin (15μg), cefuroxime (30μg), imipenem (10μg), ceftriaxone (30μg), ceftazidime (30μg), vancomycin (30μg), gentamicin (10μg), ciprofloxacin (5μg), co-trimoxazole (trimethoprim–sulfamethoxazole) (1.25/23.75μg), penicillin (10U). Penicillin, oxacillin, and ceftriaxone were specifically tested against S. pneumoniae. Minimum inhibitory concentrations (MICs) were done by the local branch of PAHO, the Caribbean Epidemiological Center, according to NCCLS guidance and interpretative criteria.¹⁷ Penicillin resistance was defined as a MIC ≥2.0μg/mL, and relative or intermediate resistance as a MIC between 0.1 and 1.0μg/mL. For ceftriaxone, full resistance was defined as a MIC ≥4μg/mL, and a MIC=2μg/mL as intermediate resistance. Statistical analysis was done using the Chi-squared test.¹⁸ S. pneumoniae strain ATCC 49619 and S. aureus ATCC strain 25923 were used as control organisms.

Back to Article Outline

Results 

During the six-year study period, 63012 patients were admitted to the pediatric wards of the San Fernando General Hospital. We excluded 25583 who were admitted electively or for observation after minor trauma, and 12079 for whom complete data were missing. Of the remaining 25350 children included in the study, 14526 (57.3%) were under two years of age, 7478 (29.5%) were between two and five years, and 3346 (13.2%) were over five years old. The ratio of boys to girls was 1.6:1. A total of 8366 (33.0%) blood cultures from suspected cases of sepsis were processed, of which 957 (11.4%) were positive for bacterial growth. Organisms grown from 253 patients were considered as contaminants; the remaining 704 were documented to have true bacteremia. Repeated isolation of the same organism from the same patient was considered as one isolate. There was no polymicrobic bacteremia.

A variety of pathogens were isolated from the patients; Gram-negative organisms were responsible for 432 cases (61.4%) of bacteremia and Gram-positive bacteria for 272 cases (38.6%) (Table 1). P. aeruginosa and members of the Enterobacteriaceae were recovered primarily from neonates. Although S. pneumoniae, H. influenzae, and non-typhoidal salmonella were detected among all age groups, they were isolated predominantly from children within the >2–5 years age group. S. aureus was also seen among all age groups, but recovery was mainly within the >5–12 years age group. The main cause of bacteremia was S. aureus (23.9%) followed by P. aeruginosa (15.5%), and K. pneumoniae (12.5%). The remaining isolates each accounted for less than 10% of bacteremia cases.

Table 1. Distribution of bacterial species isolated from the blood of children at the San Fernando General Hospital, 1997–2002

Gram-negative organisms predominated in both hospital-acquired (65%) and community-acquired infections (55%) (Table 2), and the most common causes of bacteremia in community-acquired and hospital-acquired infections were H. influenzae and S. aureus, respectively. The highest mortality was due to P. aeruginosa (39.4%), S. pneumoniae (22.5%), and E. coli (19.2%). Although S. aureus was the most common cause of bacteremia its importance as a cause of death was clearly lower with a case fatality rate of 13.1%, when compared with P. aeruginosa (39.4%) (p<0.001). Of the six children with bacteremia due to N. meningitidis, only two survived.

Table 2. Case fatality ratio and distribution of bacterial species isolated from blood of children at the San Fernando General Hospital, 1997–2002

CFR, case fatality ratio.

The primary source of bacteremia among children is shown in Table 3. Most isolates were recovered from respiratory specimens of patients on ventilators, those with pneumonia, ear and sinus infections, and the nasal passageways in those infants being evaluated for sepsis; this was followed by infected wounds, urine, GIT and skin including intravascular lines. S. aureus was the only organism recovered from all sites, and was the most common isolate from surgical and burn wounds, decubitus ulcers, and boils. GBS, S. pneumoniae, H. influenzae, Acinetobacter spp, and Citrobacter spp were also primarily from the respiratory tract. The source of non-typhoidal salmonella was from stool of patients with chronic diarrhea. The source of 24 cases of bacteremia listed as ‘unknown’ could not be correctly identified.

Table 3. Primary sources of bacterial species isolated from blood of children at the San Fernando General Hospital, 1997–2002

RT, respiratory tract; GIT, gastrointestinal tract.

The antibiotic susceptibility patterns of bacterial isolates are shown in Table 4. Approximately 90% of, and almost half of all S. aureus were resistant to ampicillin and erythromycin, respectively, while resistance to the other drugs was variable. Only 19 (11.3%) methicillin-resistant S. aureus strains (MRSA) were isolated during the study period. More than 95% of all K. pneumoniae and >87% of H. influenzae were resistant to ampicillin. Almost 50% of E. coli were resistant to ampicillin and cefuroxime, two agents commonly used to treat uncomplicated urinary tract infections. Group B streptococci (GBS) were fully susceptible to ampicillin and amoxicillin–clavulanic acid, but showed 94.7% and 73.7% resistance to tetracycline and trimethoprim-sulfamethoxazole, respectively. Of the 40 strains of S. pneumoniae isolated, four (10.0%) had MIC of ≥4μg/mL (resistance) and five (12.5%) had MIC=2.0μg/mL (intermediate resistance) to ceftriaxone, while three (7.5%) showed intermediate resistance (MIC between 0.12 and 1μg/mL) and 10 (25.0%) showed resistance (≥2μg/mL) to penicillin.

Table 4. Susceptibility patterns of bacterial blood isolates from children at the San Fernando General Hospital, 1997–2002

N=total isolates. NT, not tested; AM, ampicillin; AMC, amoxicillin–clavulanic acid; E, erythromycin; TE, tetracycline; SXT, trimethoprim–sulfamethoxazole (co-trimoxazole); CXM, cefuroxime; CAZ, ceftazidime; IPM, imipenem; CiP, ciprofloxacin; GM, gentamicin; VA, vancomycin.

Back to Article Outline

Discussion 

Bacterial infections are common among all age groups, but have a higher morbidity and mortality in children.³, ⁶, ⁸, ¹⁴ This study examined the bacterial agents isolated from the blood of children admitted to the San Fernando General Hospital in southern Trinidad. Locally, regionally, and internationally, it is important to document the identity of pathogens and their susceptibility patterns as a means of monitoring resistance trends and spread, and to formulate infection control measures and develop antibiotic policies.¹, ⁵, ¹⁹

Agents of true bacteremia were recovered from 8.4% (704 of 8366) of suspected cases of sepsis, a prevalence rate of 2.8% (704/25300) of all hospitalized children included in the study. Data would suggest that no significant overlap occurred between pathogens and contaminants (non-pathogens). Those children from whom non-pathogens were isolated recovered without antibiotic therapy. However non-pathogens can cause infections in some children, especially those with compromised defenses. One notable example from a sister institution was the isolation of a diphtheroid from the superficial wound and blood of two children with acute lymphoblastic leukemia. Both isolates were multi-resistant with similar antibiogram and identified as Corynebacterium jeikeium.⁹

The most frequently isolated pathogen was S. aureus (23.9%) and this is consistent with the general increase in Gram-positive infections worldwide. This high prevalence of infections due to S. aureus is similar to the 28% reported from Australia,²⁰ but higher than the 7–16% observed in India and Ethiopia.²¹, ²² Among the Gram-negative isolates, P. aeruginosa, K. pneumoniae, and Enterobacter spp accounted for 63.7% of isolates. This trend showing Gram-negative bacteria as the major cause of pediatric bacteremia is in harmony with reports from China.²³ Lower recovery rates of other significant pathogens: H. influenzae (9.2%), GBS (8.1%), S. pneumoniae (5.7%), and E. coli (3.7%) further contradicts the findings of other studies that reported these organisms as the dominant cause of bacteremia in children.¹, ²¹ The carriage rates of GBS among third trimester women have remained relatively stable over the years, and infant mortality due to GBS was found to be <5%.²⁴, ²⁵ Two previous reports from this institution revealed that Gram-negative rods, in particular, P. aeruginosa have been the principal cause of bacteremia in neonates.¹³, ²⁶

One possible explanation for these findings may be a breakdown in infection control measures particularly in the nursery,²⁷ where the overwhelming majority of S. aureus, P. aeruginosa, K. pneumoniae, and Enterobacter spp infections were found. The thrust of the Public Health Authorities in this country, to educate, implement/enforce immunization policies aimed at preventable bacterial infections, such as those due to S. pneumoniae and H. influenzae, may be a possible explanation for the low levels of recovery of H. influenzae and S. pneumoniae. Despite this emphasis on immunization, it is of great concern that only 67.5% and 77.5% of S. pneumoniae strains were fully sensitive to penicillin and ceftriaxone, respectively. Because S. pneumoniae and H. influenzae are common causes of pediatric infections as reported in the literature, ceftriaxone or cefotaxime with an aminoglycoside (e.g. gentamicin) are the drugs empirically prescribed before culture reports become available, and are changed or continued when susceptibility profiles become available. Data from the pharmacy records showed that ceftriaxone is the most frequently prescribed antibiotic on the pediatric wards. All cases of bacteremia in children in this study were monomicrobic, although polymicrobic bacteremia has been reported by other investigators.²², ²⁸

The antibiotic susceptibility profile indicated multiple resistances of S. aureus to ampicillin, erythromycin, amoxicillin–clavulanic acid, and co-trimoxazole. Only 19 (11.3%) S. aureus strains were methicillin-resistant (MRSA). Methicillin resistance appears to be a growing problem in this country, increasing from 2% in 1995 to 9.8% in 1999.²⁹, ³⁰ The rate of 11.3% MRSA, though low when compared to high rates reported worldwide, reflects an increasing trend within the country. The incidence of MRSA is particularly high in Europe, Asia, and certain parts of the world. In Turkey it was shown to be between 25 and 80%,³¹ in Korea 64%,³² and in North America ³³, ³⁴ and the Middle East ³⁵, ³⁶ rates of 20–50% and 3–18% have been reported, respectively.

The study showed that the overall prevalence of resistance of significant pediatric blood isolates was very low. This may be due in part to the frequent communication between the pediatricians and the microbiologist, and the latter's close monitoring of antibiotic usage in the hospital and involvement in patient care. A previous report from this institution revealed that correlating culture and sensitivity reports with the clinicians’ empiric therapy showed that about 40% of prescribed antibiotics agreed with the antibiogram of the isolated pathogen, and that the pediatric wards ranked second (21%) in total antimicrobial consumption of all services.³⁷

In conclusion, the spectrum of pediatric bacteremia as seen in hospitalized children at the San Fernando General Hospital confirmed the importance of pathogens such as S. aureus, K. pneumoniae, Enterobacter spp, P. aeruginosa, GBS, and E. coli. The resistance profile showed that most antibiotics are still effective in the management of bacteremia and reiterate the need for continued constant monitoring of the antibiogram of bacterial blood isolates. It also indicates the need to document any change in the trend of resistance and the importance of instituting prompt selection of appropriate antibiotics.

Conflict of interest: No conflict of interest to declare.

Back to Article Outline

References 

1. Berkley JA, Lowe BS, Mwangi I, Williams T, Bauni E, Mwarumba S, et al. Bacteremia among children admitted to a rural hospital in Kenya. N Engl J Med. 2005;352:39–47
   • View In Article
   • CrossRef
2. Silverstein M, Bachur R, Harper MB. Clinical implications of penicillin and ceftriaxone resistance among children with pneumococcal bacteremia. Pediatr Infect Dis J. 1999;18:35–41
   • View In Article
   • MEDLINE
   • CrossRef
3. Walsh AL, Phiri AJ, Graham SM, Molyneux EM, Molyneux ME. Bacteremia in febrile Malawian children: clinical and microbiological features. Pediatr Infect Dis. 2000;19:312–318
   • View In Article
4. Jones ME, Karlowsky JA, Draghi DC, Thornsberry C, Sahm DF, Bradley JS. Rates of antimicrobial resistance among common bacterial pathogens causing respiratory, blood, urine and soft tissue infections in pediatric patients. Eur J Clin Microbiol Infect Dis. 2004;23:445–455
   • View In Article
   • MEDLINE
   • CrossRef
5. Shwe TN, Nyein MM, Yi W, Mon A. Blood culture isolates from children admitted to Medical Unit III, Yangon Children's Hospital. Southeast Asian J Trop Med Public Health. 2002;33:764–771
   • View In Article
   • MEDLINE
6. Berkley JA, Ross A, Mwangi I, Osier FH, Mohammed M, Shebbe M, et al. Prognostic indicators of early and late death in children admitted to district hospital in Kenya: cohort study. BMJ. 2003;326:361–365
   • View In Article
   • CrossRef
7. Siu LK, Lu PH, Hseuh PR, Lin FM, Chang SC, Luh KT, et al. Bacteremia due to extended-spectrum β-lactamase-producing Escherichia coli and Klebsiella pneumoniae in a pediatric oncology ward: clinical features and identification of differential plasmids carrying the SHV-5 and TEM-1 genes. J Clin Microbiol. 1999;37:4020–4027
   • View In Article
   • MEDLINE
8. Winchester D, Todd JK, Roe MH. Bacteremia in hospitalized children. Am J Dis Child. 1977;131:753–758
   • View In Article
   • MEDLINE
9. Fosi-Mbantenkhu J, Orrett FA. Predisposition to Corynebacterium jeikeium infection in acute lymphoblastic leukemia: a report of two cases in Trinidad. Med Pediatr Oncology. 1994;22:350–354
   • View In Article
10. Read RP, Wegerhoff FO, Rothberg AD. Bacteremia in malnourished African children. Ann Trop Paediatr. 1996;16:61–68
    • View In Article
    • MEDLINE
11. Morrow SE, Smith DL, Cairns BA, Howell PD, Nakayama DK, Peterson HD. Etiology and outcome of pediatric burns. J Pediatr Surg. 1996;31:329–333
    • View In Article
    • Abstract
    • Full-Text PDF (624 KB)
    • CrossRef
12. Wolf SE, Rose JK, Desai MH, Mileski JP, Barrow RE, Herdon DN. Mortality determinants in massive pediatric burns: an analysis of 103 children with > or=80% TBSA burns (> or=70% full-thickness). Ann Surg. 1997;225:554–565
    • View In Article
    • MEDLINE
    • CrossRef
13. Orrett FA, Shurland SM. Neonatal sepsis and mortality in a regional hospital in Trinidad: aetiology and risk factors. Ann Trop Paediatr. 2001;21:20–25
    • View In Article
    • MEDLINE
    • CrossRef
14. Cotton MF, Burger PJ, Bodenstein WJM. Bacteremia in children in the South-western Cape. S Afr Med J. 1992;81:87–90
    • View In Article
    • MEDLINE
15. Bone RC, Sprung CL, Sibbald WJ. Definitions for sepsis and organ failure. Crit Care Med. 1992;20:724–726
    • View In Article
    • MEDLINE
    • CrossRef
16. National Committee for Clinical Laboratory Standards. Performance standards for antimicrobial susceptibility tests. Approved standards. 7th ed. Vol. 20(1). Wayne, PA, USA: NCCLS M2-A7; 2000.
    • View In Article
17. National Committee for Clinical Laboratory Standards. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically. Approved standards. Wayne, PA, USA: NCCLS M7-A5; 2001.
    • View In Article
18. Daley LE, Burke GJ, McGilvray J. Interpretation and uses of medical statistics. 4th ed.. London: Blackwell Scientific Publications; 1991;p. 1–427
    • View In Article
19. Orrett FA. Pneumococcal infections in Trinidad: patterns of antimicrobial susceptibility: 1994–2002. Jpn J Infect Dis. 2005;58:20–24
    • View In Article
    • MEDLINE
20. Douglas MW, Lum G, Roy J, Fisher DA, Anstay NM, Currie BJ. Epidemiology of community-acquired and nosocomial bloodstream infections in tropical Australia: a 12-month prospective study. Trop Med Int Health. 2004;9:795–804
    • View In Article
    • MEDLINE
    • CrossRef
21. Sharma M, Goel N, Chaudhery U, Aggarwal R, Arora DR. Bacteremia in children. Indian J Pediatr. 2002;69:1029–1032
    • View In Article
    • MEDLINE
    • CrossRef
22. Ghiorghis B, Geyid A, Haile M. Bacteremia in febrile outpatient children. East Afr Med J. 1992;69:74–77
    • View In Article
    • MEDLINE
23. Xu Y, Shao J. Changes of pathogenic bacteria in pediatric patients of septicemia and drug resistance thereof in Zhejiang Children's Hospital 1991 approximately. Zhonghua Yi Xue Za Zhi. 2002;82:945–948
    • View In Article
    • MEDLINE
24. Orrett FA, Olagundoye V. Prevalence of group B streptococci colonization in pregnant third trimester women in Trinidad. J Hosp Infect. 1994;27:43–48
    • View In Article
    • Abstract
    • Full-Text PDF (424 KB)
    • CrossRef
25. Orrett FA. Colonization with group B streptococci in pregnancy and outcome of infected neonates in Trinidad. Pediatr Int. 2003;45:319–323
    • View In Article
    • MEDLINE
    • CrossRef
26. Orrett FA. Fatal multi-resistant Pseudomonas aeruginosa septicaemia outbreak in a neonatal intensive care unit in Trinidad. Ethiop Med J. 2000;38:85–91
    • View In Article
    • MEDLINE
27. Orrett FA, Brooks PJ, Richardson EG. Nosocomial infections in a rural regional hospital in a developing country: infection rates by site, service, cost, and infection control practices. Infect Control Hosp Epidemiol. 1998;19:136–140
    • View In Article
    • MEDLINE
28. Reuben AG, Musher DM, Hamill RJ, Breuche I. Polymicrobic bacteremia: clinical and microbiologic patterns. Rev Infect Dis. 1989;11:161–183
    • View In Article
    • MEDLINE
29. Adesiyun AA, Prabhakar P, Ali C, Lewis M. Characteristics of Staphylococcus aureus strains isolated from clinical and non-clinical sources in Trinidad: susceptibility to bacteriophages and antimicrobial agents, and toxigenicity. Zentralbl Bakteriol. 1995;282:519–532
    • View In Article
    • MEDLINE
    • CrossRef
30. Orrett FA. Methicillin resistance among Trinidadian isolates of community and hospital strains of Staphylococcus aureus and their patterns of resistance to non-β-lactam antibiotics. Jpn J Infect Dis. 1999;52:238–241
    • View In Article
    • MEDLINE
31. Erkmen O, Balci I, Gungor S. Staphylococci infections in a hospital. Turk J Med Sci. 1996;26:367–370
    • View In Article
32. Kim BH, Jang HC, Nam HJ, Lee YS, Kim BS, Park WB, et al. In vitro activities of 28 antimicrobial agents against Staphylococcus aureus isolates from tertiary-care hospitals in Korea: a nationwide survey. Antimicrob Agents Chemother. 2004;48:1124–1127
    • View In Article
    • MEDLINE
    • CrossRef
33. Panlilo AL, Culver DH, Gaynes RP, Banerjee S, Henderson TS, Tolson JS, et al. Methicillin-resistant Staphylococcus aureus in US hospitals, 1975–1991. Infect Control Hosp Epidemiol. 1992;13:582–586
    • View In Article
    • MEDLINE
34. Nath SK, Shea B, Jackson S, Rotstein C. Ribotyping of nosocomial methicillin-resistant Staphylococcus aureus isolates from a Canadian hospital. Infect Control Hosp Epidemiol. 1995;16:717–724
    • View In Article
    • MEDLINE
35. Araj GF, Uwaydah MM, Alami SY. Antimicrobial susceptibility patterns of bacterial isolates at the American University Medical Center in Lebanon. Diagn Microbiol Infect Dis. 1994;20:151–158
    • View In Article
    • MEDLINE
    • CrossRef
36. Bukharie HA, Abdelhadi MS. The epidemiology of methicillin-resistant Staphylococcus aureus at a Saudi University Hospital. Microbiol Drug Resist. 2001;7:413–416
    • View In Article
37. Orrett FA. Antimicrobial prescribing patterns at a rural hospital in Trinidad: evidence for intervention measures. Afr J Med Sci. 2001;30:161–164
    • View In Article