- Email: [email protected]
Bacteriological profile and antimicrobial resistance patterns of clinical bacterial isolates in a University Hospital
Travel Medicine and Infectious Disease (2009) 7, 235e238
available at www.sciencedirect.com
journal homepage: www.elsevierhealth.com/journals/tmid
Bacteriological profile and antimicrobial resistance patterns of clinical bacterial isolates in a University Hospital Maimoonaa Mushtaq Ahmed*, Sami Bahlas Faculty of Medicine, King Abdul Aziz University, PO Box 80215, Jeddah 21589, Saudi Arabia Received 11 May 2009; received in revised form 23 July 2009; accepted 27 July 2009 Available online 22 August 2009
KEYWORDS Antimicrobial resistance; Bacteriological resistance; Bactermia
Summary The objective of this study was to determine the patterns of bacterial isolates found in blood culture of patients with bactermia in King Abdul Aziz University Hospital in addition to determination of antibiotic resistance. A retrospective analysis of the 672 positive samples collected over the period of December 2006eDecember 2008. The observed mean age was 40 years with comparable distribution in both genders. 65.2% of the population were Non-Saudi. 65.5% of isolates were Gram positive, mainly Staphylococcus epidermidis, on the other hand Klebsiella was the common Gram negative bacteria. Diabetes has been observed in 38.5%. Mortality was 32.4 (P-value 0.001) in diabetic patients versus non-diabetics. Benzyl penicillin, clindamycin, erythromycin, tetracycline, ciprofloxacin, oxacillin caused resistance to more than 50% of Gram positive organisms whereas antimicrobial resistance to ampicillin, nitrofurantoin, levofloxacin, piperacillin, cefuroxime and cefuroxime was found in Gram negative isolates. To conclude vancomycin, teicoplanin, linizolid, and piperacillin/tazobactam, were effective antimicrobial agents against the majority of bacterial isolates. Gram positive organisms are the common cause of bactermia. The highest risk of mortality is associated with Streptococcus pyogenes. ª 2009 Published by Elsevier Ltd.
Introduction Jeddah is a town located in the western province of Saudi Arabia. Millions of visitors coming to Holy Places Muslims in
* Corresponding author. Tel.: þ966 506525857. E-mail address: [email protected] (M.M. Ahmed). 1477-8939/$ - see front matter ª 2009 Published by Elsevier Ltd. doi:10.1016/j.tmaid.2009.07.004
Makkah and Madinah, pass through Jeddah airports and seaports. One of the Islamic events is so-called Hajj, the Islamic Pilgrimage. In 2006, Jeddah had received one million international pilgrims and eight hundreds national pilgrims during the 20e30 days of Hajj.1 The presence of airports and sea-ports in Jeddah, highlights the importance King Abdul Aziz University Hospital KAUH, as the only university hospital in Jeddah.
236
M.M. Ahmed, S. Bahlas
Table 1 Distribution of microorganism isolated from blood culture. Gram positive Medical Intensive care unit Peadiatric Surgical Gynecological wards Bactermia
152 128 100 54 6 440
Gram negative
(63.6%) 87 (66%) 66 (67.1%) 49 (65.1%) 29 (85.7%) 1 (65.5%) 232
(36.4%) (34%) (32.9%) (34.95) (14.3%) (35.5%)
Total number 239 (35.6%) 194 (28.9%) 149 (22.2%) 83 (12.4%) 7 (1%) 672
The transmission of bacterial infection and bacterial resistance is expected to be of interest in this region. Our objective was to determine the patterns of bacterial isolates from blood cultures of patients admitted with bactermia in KAUH and to determine their antibiotic resistance. Bactermia is a major contributor of morbidity and mortality.2e14
Methods This was a retrospective study of adult patients admitted with bactermia to KAUH from December 2006 to December 2008. Hospital charts were reviewed for age, sex, nationality, presence of Diabetes Mellitus DM, White Blood Cells (WBCs), days of positive culture from admission (more than three days from admission was considered as hospital acquired), mortality, bacterial isolates with their sensitivity and resistance to different antibiotics were studied. Blood cultures were performed on MacConkey agar or chocolate agar. Two bottles of culture media were used, one for
Table 2
aerobic and the other for anaerobic. Identification of bacteria was performed with standard diagnostic methods.
Results The mean age is of patients was 40.1 5.6 years. 65.2% of patients were Non-Saudis. 38.5% of study population were diabetics. 72.2% of cases had hospital acquired bactermia. The most common Gram positive isolate was Staphylococcus epidermidis 165 (24.6%) followed by Staphylococcus haemolyticus 75(11.2%) while in Gram negative was Klebsiella 57(9.7%), followed by Pseudomonas sp., Acinetobacter baumannii, Enterobacter cloacae and Salmonella, 46 (6.8%), 40 (6%), 28.4 (4.2%) and 15 (2.7%) respectively (Tables 1e5).
Discussion In 1991 the prevalence of bactermia in Saudi Arabia was 2.2%13 compared to 4.3% in this study. Gram positive bacteria have higher incidence of resistance to antibiotics. Prior to 1998 Gram negative bacilli were the predominant organisms associated with nosocomial blood stream infections in USA, now Gram positive aerobes (coagulase negative Staphylococci spp., Staphylococcus aureus, and Enterococci) have greater importance.9,12 Gram negative sepsis has a mortality rate of 30e50%. Such mortality is multifactorial depending on the use of appropriate antibiotic therapy and the timing of initiation of therapy.12e18 The 46.6% observed bactermia associated mortality was mainly in patients who had WBCs of more than 10 K/ml (43.3%, P-value 0.059). All Gram positive pathogens were completely sensitive to linizolid, similar to a relatively recent study from Italy.18 Ninety five percent of the tested
Resistance pattern of Gram positive isolates.
Penicillin Ampicillin Oxacillin Norfloxacillin Levofloxacin Clindamycin Vancomycin Teicoplanin Ciprofloxacin Augmentin Erythromycin Gentamycin Linizolid Piperacillin Cefuroxime Tetracycline
Staphylococcus aureus (%)
Streptococcus epidermidis (%)
Staphylococcus hominis (%)
Enterococcus faecalis (%)
Staphylococcus haemolyticus (%)
93.8 0.0 49.2 25 30.6 46 0.0 0.0 41.1 NT 48.4 26.2 0.0 0.0 0.0 31.9
98.1 NT 83.9 47.9 59.6 61.1 0.6 1.3 59.9 NT 75.3 57.1 0.0 0.0 100 10.8
95.2 0.0 65.1 38.5 29.8 41 0.0 1.6 30.4 0.0 68.3 13 0.0 NT NT 23.6
52.2 46.2 33.3 83.3 75 100 0.0 0.0 80 37.5 90.5 76 16.7 33.3 83.3 84.2
98.6 75 97.1 89.7 89.1 64.7 1.5 1.5 84.7 50 88.2 81 0.0 0.0 0.0 33.3
NT Z not tested, NA Z not applicable.
Bacteriological profile and antimicrobial resistance patterns Table 3
Resistance pattern of Gram negative isolates.
Meropenam Ciprofloxacin Gentamycin Sulpha-trimethoprim Cefuroxime Ceftriaxone Ceftazidime Piperacillin tazobactam Cefuroxime Amikacin Piperacillin Ampicillin Norfloxacin Levofloxacin Oxacillin Nitrofurantoin
Table 4
Klebsiella (%)
Pseudomonas (%)
E. coli (%)
E. cloacae (%)
A. baumannii (%)
Salmonella (%)
1.9 34 37.7 44.9 45.5 25 44.9 23.5 44.2 3.7 88.5 92.7 41.7 0.0 40 66.7
7.50 11.6 17.4 50 NT NT 17.95 6.7 100 9.3 14.3 0.0 17.6 100 20 NT
2.5 56.4 24.4 43.9 51.9 0.0 44.4 20.7 56 5.4 68.4 87.2 81.8 100 63.6 NT
0.0 8.7 15.4 30.8 62.5 0.0 37.5 8.0 36 0.0 32 88 0.0 0.0 20 66.7
32.4 44.4 35.9 38.9 93.3 100 53.1 40.5 86.7 25.6 54.3 88.9 56.2 50 55.6 100
0.0 0.0 100 35.7 100 NT 7.1 0.0 11.1 100 NT 40 0.0 0.0 0.0 100
Mortality versus WBC.
WBC
managing infections as well as in implementing hospital protocols.
Mortality
<10 mL >10 mL Total a
Ceasea
Alivea
45 (6.7%) 234 (34.9%) 279 (41.6%)
86 (12.8%) 305 (45.5%) 391 (58.4%)
c2-test, DF Z 1, P-value 0.059127.
Gram positive strains were sensitive to teicoplanin, vancomycin. Attention should be paid to the use of cefuroxime, ceftazidime, cefuroxime piperacillin and ampicillin which had recorded resistance more than 50% The risk of mortality was closely associated with Streptococcus pyogenes and this should be taken in consideration in Table 5
237
Conclusion Vancomycin, teicoplanin and linizolid, piperacillin/tazobactam, were effective antimicrobial agents against majority of the bacterial isolates. Gram positive organisms are common cause of bactermia. S. pyogenes is associated with higher risk of mortality.
Conflicts of interest The authors declare that there are no conflicts of interest.
Bacterial strains and mortality odds ratios.
Bacterial strain
Odds ratio
P-value (Wald’s test)
Confidence limit lower 95%
Confidence limit upper 95%
Staph. capitis E. coli Staph. aureus Staph. haemolyticus Klebsiella Pseudomonas Staph. hominis E. cloacae Enterococcus faecalis Bacteroides fragilis Acinetobacter baumannii Streptococcus pyogenes Haemophilus influenzae Salmonella Morganella morgani Streptococcus pneumonia Proteus
0.66667 0.60606 0.77778 1.11905 0.69048 0.61111 1.39683 1.03030 0.71111 0.66667 0.73684 8.66667 0.66667 4.33333 10,000þ 10,000þ 0.00002
0.41504 0.14948 0.39462 0.69490 0.23060 0.14180 0.27974 0.94311 0.38562 0.68883 0.38868 0.03969 0.77571 0.05881 0.95244 0.91772 0.94851
0.25146 0.30675 0.43607 0.63788 0.37685 0.31680 0.76201 0.45383 0.32919 0.09163 0.36798 1.10719 0.04098 0.94687 0.00000 0.00000 0.00000
1.76748 1.19743 1.38724 1.96317 1.26511 1.17886 2.56051 2.33902 1.53613 4.85055 1.47545 67.83943 10.84589 19.83144 10,000þ 10,000þ 10,000þ
238
M.M. Ahmed, S. Bahlas
References 1. Ministry of Hijj, Hajj and Umrah Statistics. Website: http:// www.hajinformation.com/main/l.htm [accessed 04.06.09]. 2. Richet Mohammed J, McDonald LC, Jarvis WB. Building communication networks, international network for the study and prevalence of emerging antimicrobial resistance. Emerg Infect Dis 2001;7(2):319e32. 3. Didier P, Wenzel RP. Nosocomial blood stream infections. Arch Intern Med 1995;115:1177e84. 4. Jamal WY, Eldin, Rolini V. Analysis of hospital acquired bactermia in ICU patients in a university hospital in Kuwait. J Hosp Infect 1999;43:49e56. 5. Ben JZ, Mahjoubi F, Ben HY, et al. Antimicrobial susceptibility and frequency of occurrence of clinically blood isolates in Tunisia. Pathol Biol 1993e1998;2004(52):52e8. 6. Qutub Mohammed, Akhtar Javed. Changing trends and etiology of bactermia in a referral hospital in Saudi Arabia. Saudi Med J 2001;22(2):178e9. 7. Gebre-Sealassie S. Patterns of isolation of common Gram positive bacterial pathogens and their susceptibility to antimicrobial agents in Jimma Hospital. Ethiop Med J 2002 April; 40(2):115e27. 8. Rahbor M, Gra Agaji R, Hashmi S. Nosocomial blood stream infection in Imam Khomeni Hospital, Urmia Islamic Republic of Iran. East Mediterr Health J 2005 May;11(3):478e84. 9. Wisplinghoff H, Bischoff T, Tallent SM. Nosocomial blood stream infections in US hospitals, analysis of 24,179 case from a prospective nationwide surveillance study. Clin Infect Dis 2004 August 1;39(3):309e17. 10. Lyytikainen O, Lumio J, Sarkkinen H. Nosocomial blood stream infection in Finnish hosp during 1999e2000. Clin Infect Dis 2002 July15;35(2):e14e9. 11. Baby Hanan A. Bacterial isolates from fatal cases of BSI at a university hosp in central Saudi Arabia. Saudi Med J 2007; 28(2):231e5. 12. Diekema DJ, Pfaller MA, Jones RN. Trends in antimicrobial susceptibility of bacterial pathogens isolated from patients
13. 14.
15.
16.
17.
18.
with blood stream infections in the USA, Canada, and Latin America. Int J Antimicrob Agents 2000;13:257e71. Abussaid MJI. Prevalence of nosocomial infection in a Saudi teaching hospital. J Hosp Infect March 1991;17(3):235e8. Gaynes R, Edwards JR. Overview of nosocomial infections caused by Gram negative bacilli. Clin. Infect. Dis. 2005;41: 848. Armstrong GL, Conn LA, Pinner RW. Trends in infectious disease, mortality in United States during the 20th century. J Am Med Assoc 1999;281:61e6. Elbashier AM, Malik AG, Khot AP. Blood stream infections, micro organisms, risk factors and mortality rate in Qatif central hospital. Ann Saudi Med 1997;17:143e8. Kang CI, Kim SH, Park WB. BSI caused by antibiotic resistance Gram negative bacilli, risk factor for mortality and impact of appropriate initial antimicrobial therapy on outcome. Antimicrob Agent Chemother 2005;49:760. Nicoletti G, Schito G, Boros S, et al. Bacterial isolates from severe infections and their antibiotic susceptibility patterns in Italy, a nationwide study in the hospital setting. J Chemother 2006 Dec;18(6):589e602. outcome Antimicrob Agent Chemother 2005;49:760.
Further reading 19. AlJasser AM, Elkhizzi NO. Antimicrobial susceptibility pattern of clinical isolates of Pseudomonas. Saudi Med J 2004 June; 25(6):780e4. 20. Yelkin G, Oluls Cicek A. Clinical microbiology and epidemiology, characteristics of Pseudomonas infections in a University Hospital e Malaya Turkey 21. Casellas JM, Blanca MG, Pinto ME. The sleeping giant, antimicrobial resistance. Infect Dis Clin North Am 1994;8:29e45. 22. CDC issues in health care setting. Antimicrobial resistance in hospitals, a growing threat to public health; June 1999 23. Staph aureus resistance to vancomycin in United States. CDC MMWR Weekly 2002;51:565e7.
available at www.sciencedirect.com
journal homepage: www.elsevierhealth.com/journals/tmid
Bacteriological profile and antimicrobial resistance patterns of clinical bacterial isolates in a University Hospital Maimoonaa Mushtaq Ahmed*, Sami Bahlas Faculty of Medicine, King Abdul Aziz University, PO Box 80215, Jeddah 21589, Saudi Arabia Received 11 May 2009; received in revised form 23 July 2009; accepted 27 July 2009 Available online 22 August 2009
KEYWORDS Antimicrobial resistance; Bacteriological resistance; Bactermia
Summary The objective of this study was to determine the patterns of bacterial isolates found in blood culture of patients with bactermia in King Abdul Aziz University Hospital in addition to determination of antibiotic resistance. A retrospective analysis of the 672 positive samples collected over the period of December 2006eDecember 2008. The observed mean age was 40 years with comparable distribution in both genders. 65.2% of the population were Non-Saudi. 65.5% of isolates were Gram positive, mainly Staphylococcus epidermidis, on the other hand Klebsiella was the common Gram negative bacteria. Diabetes has been observed in 38.5%. Mortality was 32.4 (P-value 0.001) in diabetic patients versus non-diabetics. Benzyl penicillin, clindamycin, erythromycin, tetracycline, ciprofloxacin, oxacillin caused resistance to more than 50% of Gram positive organisms whereas antimicrobial resistance to ampicillin, nitrofurantoin, levofloxacin, piperacillin, cefuroxime and cefuroxime was found in Gram negative isolates. To conclude vancomycin, teicoplanin, linizolid, and piperacillin/tazobactam, were effective antimicrobial agents against the majority of bacterial isolates. Gram positive organisms are the common cause of bactermia. The highest risk of mortality is associated with Streptococcus pyogenes. ª 2009 Published by Elsevier Ltd.
Introduction Jeddah is a town located in the western province of Saudi Arabia. Millions of visitors coming to Holy Places Muslims in
* Corresponding author. Tel.: þ966 506525857. E-mail address: [email protected] (M.M. Ahmed). 1477-8939/$ - see front matter ª 2009 Published by Elsevier Ltd. doi:10.1016/j.tmaid.2009.07.004
Makkah and Madinah, pass through Jeddah airports and seaports. One of the Islamic events is so-called Hajj, the Islamic Pilgrimage. In 2006, Jeddah had received one million international pilgrims and eight hundreds national pilgrims during the 20e30 days of Hajj.1 The presence of airports and sea-ports in Jeddah, highlights the importance King Abdul Aziz University Hospital KAUH, as the only university hospital in Jeddah.
236
M.M. Ahmed, S. Bahlas
Table 1 Distribution of microorganism isolated from blood culture. Gram positive Medical Intensive care unit Peadiatric Surgical Gynecological wards Bactermia
152 128 100 54 6 440
Gram negative
(63.6%) 87 (66%) 66 (67.1%) 49 (65.1%) 29 (85.7%) 1 (65.5%) 232
(36.4%) (34%) (32.9%) (34.95) (14.3%) (35.5%)
Total number 239 (35.6%) 194 (28.9%) 149 (22.2%) 83 (12.4%) 7 (1%) 672
The transmission of bacterial infection and bacterial resistance is expected to be of interest in this region. Our objective was to determine the patterns of bacterial isolates from blood cultures of patients admitted with bactermia in KAUH and to determine their antibiotic resistance. Bactermia is a major contributor of morbidity and mortality.2e14
Methods This was a retrospective study of adult patients admitted with bactermia to KAUH from December 2006 to December 2008. Hospital charts were reviewed for age, sex, nationality, presence of Diabetes Mellitus DM, White Blood Cells (WBCs), days of positive culture from admission (more than three days from admission was considered as hospital acquired), mortality, bacterial isolates with their sensitivity and resistance to different antibiotics were studied. Blood cultures were performed on MacConkey agar or chocolate agar. Two bottles of culture media were used, one for
Table 2
aerobic and the other for anaerobic. Identification of bacteria was performed with standard diagnostic methods.
Results The mean age is of patients was 40.1 5.6 years. 65.2% of patients were Non-Saudis. 38.5% of study population were diabetics. 72.2% of cases had hospital acquired bactermia. The most common Gram positive isolate was Staphylococcus epidermidis 165 (24.6%) followed by Staphylococcus haemolyticus 75(11.2%) while in Gram negative was Klebsiella 57(9.7%), followed by Pseudomonas sp., Acinetobacter baumannii, Enterobacter cloacae and Salmonella, 46 (6.8%), 40 (6%), 28.4 (4.2%) and 15 (2.7%) respectively (Tables 1e5).
Discussion In 1991 the prevalence of bactermia in Saudi Arabia was 2.2%13 compared to 4.3% in this study. Gram positive bacteria have higher incidence of resistance to antibiotics. Prior to 1998 Gram negative bacilli were the predominant organisms associated with nosocomial blood stream infections in USA, now Gram positive aerobes (coagulase negative Staphylococci spp., Staphylococcus aureus, and Enterococci) have greater importance.9,12 Gram negative sepsis has a mortality rate of 30e50%. Such mortality is multifactorial depending on the use of appropriate antibiotic therapy and the timing of initiation of therapy.12e18 The 46.6% observed bactermia associated mortality was mainly in patients who had WBCs of more than 10 K/ml (43.3%, P-value 0.059). All Gram positive pathogens were completely sensitive to linizolid, similar to a relatively recent study from Italy.18 Ninety five percent of the tested
Resistance pattern of Gram positive isolates.
Penicillin Ampicillin Oxacillin Norfloxacillin Levofloxacin Clindamycin Vancomycin Teicoplanin Ciprofloxacin Augmentin Erythromycin Gentamycin Linizolid Piperacillin Cefuroxime Tetracycline
Staphylococcus aureus (%)
Streptococcus epidermidis (%)
Staphylococcus hominis (%)
Enterococcus faecalis (%)
Staphylococcus haemolyticus (%)
93.8 0.0 49.2 25 30.6 46 0.0 0.0 41.1 NT 48.4 26.2 0.0 0.0 0.0 31.9
98.1 NT 83.9 47.9 59.6 61.1 0.6 1.3 59.9 NT 75.3 57.1 0.0 0.0 100 10.8
95.2 0.0 65.1 38.5 29.8 41 0.0 1.6 30.4 0.0 68.3 13 0.0 NT NT 23.6
52.2 46.2 33.3 83.3 75 100 0.0 0.0 80 37.5 90.5 76 16.7 33.3 83.3 84.2
98.6 75 97.1 89.7 89.1 64.7 1.5 1.5 84.7 50 88.2 81 0.0 0.0 0.0 33.3
NT Z not tested, NA Z not applicable.
Bacteriological profile and antimicrobial resistance patterns Table 3
Resistance pattern of Gram negative isolates.
Meropenam Ciprofloxacin Gentamycin Sulpha-trimethoprim Cefuroxime Ceftriaxone Ceftazidime Piperacillin tazobactam Cefuroxime Amikacin Piperacillin Ampicillin Norfloxacin Levofloxacin Oxacillin Nitrofurantoin
Table 4
Klebsiella (%)
Pseudomonas (%)
E. coli (%)
E. cloacae (%)
A. baumannii (%)
Salmonella (%)
1.9 34 37.7 44.9 45.5 25 44.9 23.5 44.2 3.7 88.5 92.7 41.7 0.0 40 66.7
7.50 11.6 17.4 50 NT NT 17.95 6.7 100 9.3 14.3 0.0 17.6 100 20 NT
2.5 56.4 24.4 43.9 51.9 0.0 44.4 20.7 56 5.4 68.4 87.2 81.8 100 63.6 NT
0.0 8.7 15.4 30.8 62.5 0.0 37.5 8.0 36 0.0 32 88 0.0 0.0 20 66.7
32.4 44.4 35.9 38.9 93.3 100 53.1 40.5 86.7 25.6 54.3 88.9 56.2 50 55.6 100
0.0 0.0 100 35.7 100 NT 7.1 0.0 11.1 100 NT 40 0.0 0.0 0.0 100
Mortality versus WBC.
WBC
managing infections as well as in implementing hospital protocols.
Mortality
<10 mL >10 mL Total a
Ceasea
Alivea
45 (6.7%) 234 (34.9%) 279 (41.6%)
86 (12.8%) 305 (45.5%) 391 (58.4%)
c2-test, DF Z 1, P-value 0.059127.
Gram positive strains were sensitive to teicoplanin, vancomycin. Attention should be paid to the use of cefuroxime, ceftazidime, cefuroxime piperacillin and ampicillin which had recorded resistance more than 50% The risk of mortality was closely associated with Streptococcus pyogenes and this should be taken in consideration in Table 5
237
Conclusion Vancomycin, teicoplanin and linizolid, piperacillin/tazobactam, were effective antimicrobial agents against majority of the bacterial isolates. Gram positive organisms are common cause of bactermia. S. pyogenes is associated with higher risk of mortality.
Conflicts of interest The authors declare that there are no conflicts of interest.
Bacterial strains and mortality odds ratios.
Bacterial strain
Odds ratio
P-value (Wald’s test)
Confidence limit lower 95%
Confidence limit upper 95%
Staph. capitis E. coli Staph. aureus Staph. haemolyticus Klebsiella Pseudomonas Staph. hominis E. cloacae Enterococcus faecalis Bacteroides fragilis Acinetobacter baumannii Streptococcus pyogenes Haemophilus influenzae Salmonella Morganella morgani Streptococcus pneumonia Proteus
0.66667 0.60606 0.77778 1.11905 0.69048 0.61111 1.39683 1.03030 0.71111 0.66667 0.73684 8.66667 0.66667 4.33333 10,000þ 10,000þ 0.00002
0.41504 0.14948 0.39462 0.69490 0.23060 0.14180 0.27974 0.94311 0.38562 0.68883 0.38868 0.03969 0.77571 0.05881 0.95244 0.91772 0.94851
0.25146 0.30675 0.43607 0.63788 0.37685 0.31680 0.76201 0.45383 0.32919 0.09163 0.36798 1.10719 0.04098 0.94687 0.00000 0.00000 0.00000
1.76748 1.19743 1.38724 1.96317 1.26511 1.17886 2.56051 2.33902 1.53613 4.85055 1.47545 67.83943 10.84589 19.83144 10,000þ 10,000þ 10,000þ
238
M.M. Ahmed, S. Bahlas
References 1. Ministry of Hijj, Hajj and Umrah Statistics. Website: http:// www.hajinformation.com/main/l.htm [accessed 04.06.09]. 2. Richet Mohammed J, McDonald LC, Jarvis WB. Building communication networks, international network for the study and prevalence of emerging antimicrobial resistance. Emerg Infect Dis 2001;7(2):319e32. 3. Didier P, Wenzel RP. Nosocomial blood stream infections. Arch Intern Med 1995;115:1177e84. 4. Jamal WY, Eldin, Rolini V. Analysis of hospital acquired bactermia in ICU patients in a university hospital in Kuwait. J Hosp Infect 1999;43:49e56. 5. Ben JZ, Mahjoubi F, Ben HY, et al. Antimicrobial susceptibility and frequency of occurrence of clinically blood isolates in Tunisia. Pathol Biol 1993e1998;2004(52):52e8. 6. Qutub Mohammed, Akhtar Javed. Changing trends and etiology of bactermia in a referral hospital in Saudi Arabia. Saudi Med J 2001;22(2):178e9. 7. Gebre-Sealassie S. Patterns of isolation of common Gram positive bacterial pathogens and their susceptibility to antimicrobial agents in Jimma Hospital. Ethiop Med J 2002 April; 40(2):115e27. 8. Rahbor M, Gra Agaji R, Hashmi S. Nosocomial blood stream infection in Imam Khomeni Hospital, Urmia Islamic Republic of Iran. East Mediterr Health J 2005 May;11(3):478e84. 9. Wisplinghoff H, Bischoff T, Tallent SM. Nosocomial blood stream infections in US hospitals, analysis of 24,179 case from a prospective nationwide surveillance study. Clin Infect Dis 2004 August 1;39(3):309e17. 10. Lyytikainen O, Lumio J, Sarkkinen H. Nosocomial blood stream infection in Finnish hosp during 1999e2000. Clin Infect Dis 2002 July15;35(2):e14e9. 11. Baby Hanan A. Bacterial isolates from fatal cases of BSI at a university hosp in central Saudi Arabia. Saudi Med J 2007; 28(2):231e5. 12. Diekema DJ, Pfaller MA, Jones RN. Trends in antimicrobial susceptibility of bacterial pathogens isolated from patients
13. 14.
15.
16.
17.
18.
with blood stream infections in the USA, Canada, and Latin America. Int J Antimicrob Agents 2000;13:257e71. Abussaid MJI. Prevalence of nosocomial infection in a Saudi teaching hospital. J Hosp Infect March 1991;17(3):235e8. Gaynes R, Edwards JR. Overview of nosocomial infections caused by Gram negative bacilli. Clin. Infect. Dis. 2005;41: 848. Armstrong GL, Conn LA, Pinner RW. Trends in infectious disease, mortality in United States during the 20th century. J Am Med Assoc 1999;281:61e6. Elbashier AM, Malik AG, Khot AP. Blood stream infections, micro organisms, risk factors and mortality rate in Qatif central hospital. Ann Saudi Med 1997;17:143e8. Kang CI, Kim SH, Park WB. BSI caused by antibiotic resistance Gram negative bacilli, risk factor for mortality and impact of appropriate initial antimicrobial therapy on outcome. Antimicrob Agent Chemother 2005;49:760. Nicoletti G, Schito G, Boros S, et al. Bacterial isolates from severe infections and their antibiotic susceptibility patterns in Italy, a nationwide study in the hospital setting. J Chemother 2006 Dec;18(6):589e602. outcome Antimicrob Agent Chemother 2005;49:760.
Further reading 19. AlJasser AM, Elkhizzi NO. Antimicrobial susceptibility pattern of clinical isolates of Pseudomonas. Saudi Med J 2004 June; 25(6):780e4. 20. Yelkin G, Oluls Cicek A. Clinical microbiology and epidemiology, characteristics of Pseudomonas infections in a University Hospital e Malaya Turkey 21. Casellas JM, Blanca MG, Pinto ME. The sleeping giant, antimicrobial resistance. Infect Dis Clin North Am 1994;8:29e45. 22. CDC issues in health care setting. Antimicrobial resistance in hospitals, a growing threat to public health; June 1999 23. Staph aureus resistance to vancomycin in United States. CDC MMWR Weekly 2002;51:565e7.