International Journal of Infectious Diseases
Volume 11, Issue 2 , Pages 109-114, March 2007

Occurrence and antimicrobial resistance pattern of inpatient and outpatient isolates of Pseudomonas aeruginosa in a Saudi Arabian hospital: 1998–2003

Internal Medicine Services Division, Room A-420B, Building 61, Dhahran Health Center, Saudi Aramco Medical Services Organization, Saudi Aramco, Dhahran 31311, Saudi Arabia

Received 25 July 2005; received in revised form 4 November 2005; accepted 11 November 2005.

Corresponding Editor: J. Peter Donnelly, Nijmegen, The Netherlands

Article Outline

Summary 

Objectives

The objective of this study was to describe the pattern and trends of antibiotic resistance of Pseudomonas aeruginosa over a six-year period in a Saudi Arabian hospital.

Methods

This was a retrospective study of the antibiotic resistance of outpatient and inpatient isolates of P. aeruginosa. Only one isolate per patient per year was included in the study.

Results

During the study period a total of 2679 isolates of P. aeruginosa were available for analysis. Outpatient isolates constituted 48% of the total number, and of these 23.4% were obtained from wound cultures. For the inpatient isolates, 33.6% and 30% were obtained from the respiratory tract and wounds, respectively. There was no significant increase in the resistance rates of outpatient isolates to the tested antibiotics over time. On the other hand, inpatient isolates showed a statistically significant increase in resistance rates to piperacillin, ceftazidime, imipenem, and ciprofloxacin (p<0.001). Over the study period, the resistance rates of outpatient and inpatient isolates to piperacillin, ceftazidime, imipenem, and ciprofloxacin were 4.6% and 11.5%, 2.4% and 10%, 2.6% and 5.8%, and 3% and 6%, respectively. Gentamicin demonstrated the highest resistance among all tested aminoglycosides for outpatient isolates (6%) and inpatient isolates (6.7%). Resistance to more than two classes of antibiotics was present in 1–2% of inpatient isolates and in 0% of outpatient isolates.

Conclusion

Antibiotic resistance continues to be a problem especially in inpatient isolates and is likely to be related to increased antibiotic use. Thus, continued monitoring of antibiotic resistance is of great importance to ensure the proper use of antibiotics and to detect any increasing trends in resistance.

Keywords: Pseudomonas aeruginosa, Antibiotic resistance, Surveillance, Saudi Arabia

 

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Introduction 

Bacterial resistance to commonly prescribed antibiotics is associated with increased morbidity, mortality, and healthcare costs.1, 2 The rate of antibiotic resistance to Pseudomonas aeruginosa is increasing in many parts of the world, in particular the rates of resistance to β-lactams, aminoglycosides, and fluoroquinolones.3 Regional variations in antibiotic resistance exist for different organisms, including P. aeruginosa, and this may be related to the difference in antibiotic prescribing habits.4

Local and regional surveillance of antibiotic resistance provides better understanding of the global trends in antibiotic resistance.5 Periodic testing and analysis of antibiotic resistance would enable physicians to detect trends in the resistance pattern to commonly prescribed antibiotics in a given organism.6 There are few data available in Saudi Arabia on the resistance of P. aeruginosa isolates.7 Moreover, there is only one study addressing the pattern of antibiotic resistance of P. aeruginosa in Saudi Arabia over an extended period of time.7 Thus, in this study we evaluated the trends of the susceptibility pattern of inpatient and outpatient isolates of P. aeruginosa in Saudi Aramco Medical Services Organization (SAMSO) in Dhahran, Saudi Arabia over a six-year period (1998–2003). SAMSO, which has five intensive care units, provides medical care to Saudi Aramco employees and their dependents, with >1000000 outpatient visits and >24000 admissions annually.

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Methods 

We analyzed, retrospectively, the in vitro antibiotic susceptibility of P. aeruginosa from 1998 to 2003. Only one isolate per patient per year was included in the analysis. There were no large intra-hospital P. aeruginosa outbreaks during the study period. Gram-negative bacilli were identified to the species level and antibiotic susceptibility testing was done by an automated system (Vitek Biomerieux, France). Results of the antibiotic susceptibility testing were interpreted according to guidelines of the National Committee for Clinical Laboratory Standards (NCCLS).8 P. aeruginosa American Type Culture Collection (ATCC) 27853 was used as a quality control strain. For the purpose of this study, percentage of resistance was calculated as the percent of intermediately susceptible and resistant organisms in relation to the total tested isolates. Multidrug resistance of P. aeruginosa was defined as resistance of isolates to three or more classes of antibiotics (imipenem, ceftazidime, ciprofloxacin, piperacillin, or an aminoglycoside). The bacterial isolates were considered as inpatient isolates if they were cultured more than 48hours after admission or within 30 days of hospital discharge. Otherwise, the isolates were considered as coming from outpatients.

Statistical analyses 

Statistical analyses were performed using the Statistical Package for the Social Sciences (SPSS version 10.0). The difference in resistance rates between inpatient and outpatient isolates was assessed by two sample proportion tests. The annual percentage of resistance of P. aeruginosa was calculated and analyzed for an increase or decrease in the trends over the study period using linear trend analysis. If the p value of the Chi-square test for association was significant (<0.05) then a trend existed. Furthermore, the Chi-square test for trends had to be significant, regardless of whether there was a departure from a linear trend. Whenever there was a significant trend in the resistance, the p value was given. The regression coefficient indicating a change in the y-axis (percentage of resistance), divided by the change in the x-axis (years) was calculated.9, 10 A negative slope (−) indicated a decrease in resistance, whereas a positive slope (+) confirmed an increase of resistance over time.

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Results 

A total of 3918 isolates of P. aeruginosa were identified in the study period. After excluding duplicate isolates, the remaining 2679 isolates constituted the sample of analysis in this study. Outpatient isolates constituted 48% of the total with the remaining isolates from inpatient cases. Of the outpatient isolates, 23.4% were obtained from wound cultures, 17.5% from urine, and 9.5% from respiratory cultures. Of the inpatient isolates, 33.6%, 30%, and 18.5% were obtained from respiratory, wound, and urine cultures, respectively. The resistance pattern of P. aeruginosa per site of isolation is shown in Table 1 (outpatients) and in Table 2 (inpatients). For the inpatient cases, isolates of P. aeruginosa from a respiratory source showed higher rates of resistance to piperacillin (p=0.01), ceftazidime (p<0.001), and imipenem (p=0.03) compared to other isolates (Table 1), whereas outpatient urinary isolates showed higher rates of resistance to ciprofloxacin (p<0.01) and amikacin (p=0.01) when compared to isolates from other sources (Table 2).

Table 1. Resistance pattern of inpatient isolates by site
BloodRespiratoryUrineWoundOther
Piperacillin10.1% (69)16.7% (258)10.9% (138)8.5% (234)2.2% (46)
Ceftazidime9.7% (93)13.4% (379)9.7% (174)0.8% (377)4.5% (66)
Imipenem4.4% (91)8.3% (359)6.5% (170)3.9% (331)0.0% (57)
Amikacin0.0% (93)2.7% (378)1.2% (173)2.6% (351)0.0% (62)
Gentamicin5.2% (97)8.2% (390)4.8% (248)7.3% (400)4.3% (69)
Tobramycin1.1% (88)3.4% (355)1.8% (223)2.6% (347)0.0% (62)
Ciprofloxacin2.2% (92)7.7% (387)6.5% (184)5.8% (398)1.5% (68)

The values in parentheses indicate the total tested isolates.

Table 2. Resistance pattern of outpatient isolates by site
BloodRespiratoryUrineWoundOther
Piperacillin0.0% (57)3.8% (342)6.2% (125)5.3% (169)7.0% (86)
Ceftazidime1.2% (84)2.2% (494)3.0% (165)2.9% (276)2.3% (132)
Imipenem3.9% (76)1.7% (462)3.3% (152)3.6% (250)2.5% (119)
Amikacin1.3% (79)3.8% (506)1.2% (165)0.7% (270)0.0% (133)
Gentamicin3.4% (88)7.3% (522)7.1% (225)4.3% (300)4.2% (146)
Tobramycin1.2% (81)1.7% (463)3.4% (204)1.5% (262)0.0% (121)
Ciprofloxacin1.2% (86)2.7% (519)6.3% (175)0.03% (296)2.1% (146)

The values in parentheses indicate the total tested isolates.

Annual trends in antimicrobial resistance of outpatient and inpatient isolates (1998–2003) 

The trends in resistance rates of outpatient isolates of P. aeruginosa are shown in Table 3. The overall resistance rates to the tested antibiotics showed no significant statistical increase over the study period. The resistance rate to ciprofloxacin ranged from 1.6% in 2001 and 4% in 1998 and 4.7% in 2003 (p=0.49) and ceftazidime resistance increased from 0.8% in 1998 to 2.4% in 2003 (p=0.203). Imipenem resistance remained relatively low over the study period and ranged from 2% in 1998 to 3.2% in 2003 (p=0.47).

Table 3. Trends in antibiotic resistance rates (%) of outpatient isolates of P. aeruginosa (1998–2003)
199819992000200120022003p ValueCRa
Piperacillin1% (97)3.2% (62)6.7% (30)7.7% (130)4.5% (332)4.6% (128)0.3040.509
Ceftazidime0.8% (124)0% (119)3% (167)3.8% (287)2.4% (328)2.4% (126)0.2030.606
Imipenem2% (96)2% (90)4% (148)2.3% (264)2.4% (335)3.2% (126)0.4740.37
Amikacin1% (99)0% (90)3% (194)3% (307)1.5% (335)2.3% (128)0.320.493
Gentamicin4.5% (156)4% (146)7% (202)7% (311)5.6% (338)6% (128)0.2840.526
Tobramycin0.6% (155)0.8% (132)4.4% (137)1.6% (258)1.2% (325)3.2% (124)0.4270.404
Ciprofloxacin4% (125)2.3% (194)2.6% (194)1.6% (309)4.2% (337)4.7% (127)0.490.355

The values in parentheses indicate the total tested isolates.

aCR denotes regression coefficient.

Table 4 shows the rates of antibiotic resistance of inpatient isolates to P. aeruginosa. Inpatient isolates showed increasing annual resistance rates to all tested antibiotics. In particular, the resistance rates to ciprofloxacin increased from 2.3% in 1998 to 10.7% in 2003 (p=0.026) and ceftazidime resistance increased from 6% in 1998 to 12.3% in 2003 (p=0.01). Imipenem resistance increased from 1.4% in 1998 to 11% in 2003 (p=0.042).

Table 4. Trends in antibiotic resistance rates (%) of inpatient isolates of P. aeruginosa (1998–2003)
199819992000200120022003p ValueCRa
Piperacillin3.5% (144)4.8% (104)7.4% (27)8.7% (112)14% (239)16% (119)0.0010.979
Ceftazidime6% (170)9% (178)10.4% (163)11.5% (225)11.2% (239)12.3% (114)0.010.917
Imipenem1.4% (143)5.6% (143)1.3% (153)7.7% (207)7% (243)11% (119)0.0420.828
Amikacin2% (144)2% (144)0% (172)1% (235)3.3% (243)4.2% (119)0.90.561
Gentamicin4% (213)7.6% (211)2% (177)7.6% (236)9% (246)11.6% (121)0.70.738
Tobramycin1.4% (212)1.5% (194)0.8% (131)2% (195)2.6% (232)8% (111)0.650.754
Ciprofloxacin2.3% (172)6.4% (188)4.7% (171)5.2% (230)7.7% (247)10.7% (121)0.0260.866

The values in parentheses indicate the total tested isolates.

aCR denotes regression coefficient.

Comparison of resistance rates between outpatient and inpatient isolates 

The resistance rates of inpatient isolates of P. aeruginosa were almost twice the rates of resistance of outpatient isolates to piperacillin, ceftazidime, imipenem, and ciprofloxacin (p<0.001) (Figure 1). There was, however, no significant statistical difference in resistance rates to amikacin, tobramycin, and gentamicin between outpatient and inpatient isolates (p>0.05). Piperacillin was the least effective antibiotic followed by ceftazidime in the inpatient isolates. Ceftazidime resistance, a predictive of derepression of the chromosomal AmpC β-lactamase gene or efflux pumps, was detected in 2.4% and 10% of outpatient and inpatient isolates, respectively. Ciprofloxacin resistance remained relatively low at 3% for outpatient isolates and 6% for inpatient isolates.

  • View full-size image.
  • Figure 1. 

    Comparison of the resistance rates of outpatient and inpatient isolates of P. aeruginosa. The clustered column graph shows the percentage of resistance of outpatient isolates (solid column) and inpatient isolates (dotted column). The numbers above each bar represent the total number of tested isolates.

Multidrug-resistant P. aeruginosa 

Multidrug-resistant (MDR) P. aeruginosa was rare among clinical isolates, ranging between 1% for ciprofloxacin, gentamicin, and ceftazidime, and 2% for piperacillin, gentamicin, and ceftazidime for inpatient isolates. However, there were no isolates with resistance to all classes of antibiotics. No MDR isolates were obtained from outpatient strains.

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Discussion 

Monitoring antibiotic resistance of bacterial agents and evaluating resistance rates for inpatient and outpatient bacterial isolates may assist in the appropriate selection of empiric antibiotic treatment in the proper setting. The few available studies on the resistance of P. aeruginosa in Saudi Arabia are limited to a small number of bacterial isolates.7 Moreover, these studies do not address the issue of annual trends in resistance to different antimicrobial agents. In this study, we analyzed the annual trends in antibiotic resistance of P. aeruginosa in SAMSO over a six-year period.

In this study, the resistance rate of P. aeruginosa to piperacillin was relatively low (4–11%). In a previous study from Saudi Arabia, the resistance rate to piperacillin/tazobactam was 18.2%.7 However, the study included only 704 isolates. In the Meropenem Yearly Susceptibility Test Information Collection (MYSTIC) program study (1999–2002) in the USA, the rate of resistance to piperacillin/tazobactam was 8.4–13.7% in 1999–200111 and 9.7% in 2003.12 A higher rate of resistance of P. aeruginosa to piperacillin was reported from Jamaica and had reached 25%.13 Similarly, 32% of P. aeruginosa in patients with cystic fibrosis in the UK were resistant to piperacillin.14

In this study, we demonstrated that the annual resistance rates of piperacillin had increased from 1 to 4.6% in the outpatient isolates and from 3.5 to 16% in the inpatient isolates in 1998 and 2003, respectively. Similarly, in a study from San Francisco the annual piperacillin resistance rates increased from 10% in 1996 to 30% in 1999.15 Thus, the resistance rate to piperacillin in the current study is similar or close to those reported from other parts of Saudi Arabia and those from the USA. However, the resistance rate was at least two-fold less than the reported rates from Jamaica and the UK.131,4 The differences in the resistance rates are probably related to differences in antibiotic use especially in selected groups of the population like cystic fibrosis patients in the UK study.14

Ceftazidime resistance in this study was 2.4% and 10% for outpatient and inpatient isolates, respectively. Similar to the resistance rates of the outpatient isolates in our study, the resistance rate to ceftazidime was 2.5% in a study from Trinidad16 and the resistance rate of inpatient isolates was similar to that reported from France (8.5%).17 However, the resistance rate was much less than that reported from Turkey where it reached 36%.18 In another study from Saudi Arabia, ceftazidime resistance was detected in 18.2% of clinical isolates.7 Ceftazidime resistance is usually due to selection of P. aeruginosa strains with derepression of the chromosomal AmpC β-lactamase gene or efflux pumps. Increased prevalence of ceftazidime-resistant P. aeruginosa is related to increased use of β-lactam antibiotics such as amoxicillin and ceftazidime. Thus, the differences in the resistance rates usually correlate with the prescribing habits of each hospital and the selective pressure of certain antibiotics. Unfortunately, figures on the amount of ceftazidime used in our hospital were not available for correlation with the resistance pattern.

Resistance of P. aeruginosa to ciprofloxacin is a major problem in many parts of the world. In our study, the resistance rate of inpatient isolates to ciprofloxacin increased from 2.6% in 1998 to 10.7% in 2003. A much higher rate of increase in the resistance of ciprofloxacin has been observed in intensive care unit (ICU) isolates in Denver, USA.19 In that study, ciprofloxacin resistance increased from 22% in 1998 to 54% in 2002.19 The difference in the rate of resistance between these studies is probably related to selective pressure of fluoroquinolones especially in a high-risk population in the ICU. The cumulative resistance rate of inpatient isolates of P. aeruginosa in our study was 6% and is similar to the rates reported from one study in Saudi Arabia.7 However, resistance rates of P. aeruginosa to ciprofloxacin are much higher in other parts of the world compared to those in our study. Ciprofloxacin resistance exceeds 50% in Italy20 and 30% in patients with cystic fibrosis in the UK.14 In a study of surgical site infections in the USA, the resistance rate of P. aeruginosa to ciprofloxacin was 16%.21 However, a lower rate of resistance was reported from Trinidad (2.6%).16 The difference in the rate of ciprofloxacin resistance is usually related to the intensity of the use of fluoroquinolones.

In our study, the resistance rate to imipenem was relatively low and accounted for 2.6% and 5.8% of outpatient and inpatient isolates, respectively. In a previous report from Saudi Arabia, the prevalence of imipenem resistance was 9.2%.7 This rate was comparable to the rate in the recent MYSTIC study (9.5%).12 A similar rate of resistance was obtained from blood isolates in France (6.4%).17 A much higher rate of imipenem resistance was reported from Croatia where resistance ranged from 10.2% to 31.6%.22 Geographical variation in the resistance rates of P. aeruginosa may be related to the antibiotic prescribing habits in different parts of the world.

The rate of MDR-P. aeruginosa is increasing in many parts of the world and poses a serious therapeutic dilemma. In some institutes, the treatment of MDR-P. aeruginosa is being limited to polymyxin B.23 In this study, the rate of MDR-P. aeruginosa from inpatient isolates was low (1–2%) compared to other studies from Saudi Arabia and the USA. In a study of resistance rates of P. aeruginosa in intensive care unit patients in the USA, the rate of MDR ranged between 4% in 1993 and 14% in 2002.19 In a study from Riyadh, Saudi Arabia, MDR-P. aeruginosa was detected in 6.4% of P. aeruginosa.7 However, in that particular study MDR was defined as resistance to ≥2 classes of antibiotics. The difference in the resistance rates between the two studies from Saudi Arabia may have been related to the difference in the definitions used (>2 classes vs. ≥2 classes). Thus, on-going surveillance of the rate of increase in antibiotic resistance and the presence of MDR at each institute is critical for the selection of appropriate antimicrobial therapy.

In this study, inpatient isolates were more resistant to ceftazidime, piperacillin, imipenem, and ciprofloxacin compared to outpatient isolates. Moreover, inpatient isolates of P. aeruginosa showed an increased rate of resistance to piperacillin, ceftazidime, and ciprofloxacin, whereas outpatient isolates showed no statistically significant increase in the resistance rate to the tested antibiotics over the study period. The differential increase in the rate of resistance between inpatient and outpatient isolates is interesting. This observation is probably related to the high exposure of inpatient isolates to more and broader spectrum antibiotics than outpatient isolates.24 A similar observation of a high rate of increase in the resistance of P. aeruginosa has been observed in ICU isolates in the USA.19 A pattern of significant stepwise increase in the frequency of antimicrobial resistance has also been observed in a study from Italy.24 The highest resistance rates occurred among isolates from ICU patients followed by isolates from non-ICU inpatients, and the least resistance was observed in outpatient isolates.24 However, we found no increase in the antibiotic resistance of outpatient isolates of P. aeruginosa over the study period. Other investigators have reported an increase in the resistance rate of outpatient urinary P. aeruginosa to some but not all antibiotics.25 However, that study did not address the trend in a statistical way.25

In conclusion, the finding in this study of the low resistance of outpatient isolates to P. aeruginosa is encouraging. The increase in resistance rates of inpatient isolates to some antibiotics such as ceftazidime, ciprofloxacin, and imipenem calls for judicious use of antibiotics to limit further increase in resistance rates. Antibiotic resistance is usually related to the amount of antibiotics being used in humans and non-humans. However, one limitation of this study is that we had no available data on antibiotic consumption for correlation with the resistance rates.

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Acknowledgments 

The author thanks Ms Angela J. Harwood for her help in editing the manuscript. The author acknowledges the use of Saudi Aramco Medical Services Organization (SAMSO) facilities for the research data utilized in this manuscript. Opinions expressed in this article are those of the author and not necessarily of SAMSO.

Conflict of interest: No conflict of interest to declare.

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PII: S1201-9712(06)00050-6

doi:10.1016/j.ijid.2005.11.004

International Journal of Infectious Diseases
Volume 11, Issue 2 , Pages 109-114, March 2007

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