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ORIGINAL ARTICLE
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A 5-year retrospective study of antibiotic resistance pattern of Pseudomonas aeruginosa isolated from various clinical samples at a tertiary care hospital


1 Department of Microbiology, College of Medicine and Health Sciences, National University of Science and Technology, Sohar Campus, Sohar, Sultanate of Oman
2 Department of Community Medicine, All India Institute of Medical Sciences, Mangalagiri, Andhra Pradesh, India

Date of Submission30-Apr-2021
Date of Decision13-Jul-2021
Date of Acceptance28-Jul-2021

Correspondence Address:
Mohan Bilikallahalli Sannathimmappa,
Department of Microbiology, College of Medicine and Health Sciences, National University of Science and Technology, PO Box: 391, PC: 321, Al Tareef, Sohar
Sultanate of Oman
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/mjdrdypu.mjdrdypu_312_21

  Abstract 


Objective: Pseudomonas aeruginosa is a common cause of nosocomial infections worldwide. Increasing in the emergence and spread of multidrug-resistant (MDR) strains is a serious health concern. The aim of the present study was to determine the antibiotic resistance pattern of P. aeruginosa isolated from clinical samples. Materials and Methods: The current retrospective cross-sectional study was conducted at a tertiary-care hospital in Oman. The data of P. aeruginosa isolates identified during 2015–2019 at Sohar Hospital were retrieved from Al-Shifa computerized data system. The data were systematically analyzed using SPSS 22 software system, IBM Chicago. Descriptive statistics were applied to find frequencies and percentages. Trends were analyzed using a one-sample Chi-square test. Results: A total of 5865 P. aeruginosa strains identified in clinical samples of 4024 patients were studied. The frequency of isolation of P. aeruginosa was more among people aged >60 years (33%). The rate of isolation was significantly high (47%) in pus/wound swabs. The overall resistance of P. aeruginosa was low to moderate (10%–30%) to commonly used anti-pseudomonal drugs. Among, 10% were MDR strains. The lowest resistance (10%) was observed to piperacillin-tazobactam (TAZP), while significantly high resistance (29%–30%) was exhibited by carbapenems. Furthermore, strains isolated from respiratory secretions and urine samples have shown a significantly high percentage of resistance compared to others. Conclusions: Piperacillin-tazobactam is recommended as the drug of choice for treating especially severe Pseudomonas infections. Moderate resistance to carbapenems is an alarming sign. This pattern of resistance suggests the probable overuse of drugs. Therefore, it emphasizes strict antibiotic policy, rapid detection, and continuous monitoring of drug-resistant strains, and timely dissemination of the resistant report to clinicians.

Keywords: Antibiotic stewardship, carbapenem, nosocomial infections, Pseudomonas



How to cite this URL:
Sannathimmappa MB, Nambiar V, Aravindakshan R. A 5-year retrospective study of antibiotic resistance pattern of Pseudomonas aeruginosa isolated from various clinical samples at a tertiary care hospital. Med J DY Patil Vidyapeeth [Epub ahead of print] [cited 2022 Dec 6]. Available from: https://www.mjdrdypv.org/preprintarticle.asp?id=339181




  Introduction Top


Pseudomonas aeruginosa is a Gram-negative aerobic, oxidase-positive organism which is incapable of fermenting carbohydrates, hence categorized as nonfermentative Gram-negative bacilli. It is a ubiquitous organism widely distributed in hospital environment such as sinks, taps, drains, computer keyboards, bed rails, drinking water, physicians' and nurses' clothes, and various devices and equipment including heart-lung machines, ventilators, intravenous catheters, and others.[1],[2] Its ability to survive in dry and humid conditions, resistance to disinfectants and antibiotics has contributed immensely for their persistence in the hospital environment.[3] Currently, P. aeruginosa is one of the leading causes of wide variety of hospital-acquired infections with significant morbidity and mortality. The rapid emergence and spread of multidrug-resistant (MDR) strains in the hospital environment is a key factor for high mortality, especially among immunocompromised patients such as cystic fibrosis, neutropenia, cancer patients on chemotherapy, and other critically ill patients.[4],[5],[6] The infection may be transmitted through infected patients, hospital staff, or visitors apart from various medical and surgical interventions carried out in the hospital.[7]

Increasing resistance of P. aeruginosa to commonly used antibiotics and increase in the number of MDR strains is a major global health concern.[8] It develops drug resistance either due to chromosomal mutation or horizontal acquisition of resistance genes. The infections caused by these drug-resistant strains have had a significant impact on patients' health such as treatment failure, increased health care expenses, and high mortality. Inappropriate use of antibiotics and inadequate containment procedures practiced in hospitals creates a selective pressure on bacteria and drives the emergence of MDR strains.[8] P. aeruginosa possess array of virulence factors and displays various mechanisms to develop resistance to multiple classes of antibiotics.[8],[9] Biofilm formation, production of several drug inactivating enzymes such as extended-spectrum beta-lactamases, metallo-beta-lactamases, and carbapenemases, modification in outer membrane protein channels, and efflux pumps have enabled the P. aeruginosa strains to evade host defenses and antibiotic therapy efficiently.[10],[11],[12],[13]

Over the years, increasing in resistance of P. aeruginosa toward beta-lactams, fluoroquinolones, and aminoglycosides have been reported from around the world.[4] However, the resistance pattern of organisms including P. aeruginosa varies from one region to another which could be due to differences in antibiotic prescribing policies and infection control measures.[4] Therefore, a better understanding of local trends of antibiotic resistance through local and regional surveillance, periodic detection, and reporting of the pattern of antibiotic resistance among bacteria is critical for controlling the drug resistance menace. Furthermore, it would help immensely to local physicians to have an updated knowledge for the selection of appropriate antibiotics for empirical therapy. It would also help the infection control team to monitor and update regularly antibiotic policy and infection control measures. The current study looks at a 5-year antibiotic resistance pattern exhibited by P. aeruginosa isolated at a tertiary-care hospital in the North-Batinah region of Oman.


  Materials and Methods Top


This current retrospective single-center cross-sectional study was conducted at a 400-bed Sohar Hospital in the North-Batinah region of Oman. The study was approved by the Research and Ethics Committee, Ministry of Health, Oman (MH/DHSG/NBG/1923195718/2019). The data of P. aeruginosa isolates identified in various clinical samples of the patients during the period from January-2015 to December-2019 was retrieved systematically from Al-Shifa computerized system and microbiology laboratory records. The data included sociodemographic characteristics of the patients and antibiotic resistance patterns of P. aeruginosa.

Bacterial identification method and antibiotic susceptibility testing

Microbiological specimens such as wound swab, pus, blood, urine, respiratory secretions, and others received from different departments of the Sohar Hospital were processed at the Microbiology laboratory. Specimens were microscopically observed after staining with Gram stain and cultured by plating on MacConkey agar and nutrient agar (Oxoid, UK) and incubated at 37°C. The isolates were identified by the standard microbiological methods and the automated Vitek 2 system (Bio-Mérieux, France). Antimicrobial susceptibility testing was performed using Kirby-Bauers disc diffusion method on Muller-Hinton agar with the following antibiotic panel by using Oxoid antibiotic discs: Gentamicin (10 μg), ciprofloxacin (5 μg), piperacillin/tazobactam (100/10 μg), imipenem (10 μg), meropenem (10 μg), amikacin (10 μg), ceftazidime (CTAZ) (30 μg), and colistin (10 μg). For CTAZ, a minimum inhibitory concentration was determined by the Epsilometer (E) test, as recommended by Clinical Laboratory Standards Institute.[14] The strains that show resistance to at least one drug in three or more classes of antibiotics were categorized as MDR organisms. Quality control was performed using P. aeruginosa ATCC 27853.

Statistical analysis

The data were cleaned for duplicates and repeat samples. The data was systematically analyzed isolate-wise as well as patient-wise using SPSS 22 software, IBM, Chicago, IL, USA. Frequencies of gender and age groups were tallied both in total and year wise. One sample Chi-square test was done to find the significance of mode values among the classes. Sample wise isolates were classified for descriptive purposes and subjected to the Pearson Chi-square test. Year-wise antibiotic susceptibility pattern was tabulated and the trends plotted for the period 2015–2019. P < 0.05 was indicative of deviation from expected frequencies.


  Results Top


A total of 5865 P. aeruginosa isolates recovered from 4024 patients during 2015–2019 were included in the study. [Table 1] shows the characteristics of the patients and the isolates. The frequency of P. aeruginosa isolation was equal among males (51%) and females (49%) (P > 0.05). Among different age groups, P. aeruginosa was more frequently isolated from elderly people of age >60 years (33%) and younger people of age <20 years (28%) (P < 0.001). The percentage of isolation was gradually increased from 17% to 23% from 2015 to 2019 (P > 0.05). With respect to the source, P. aeruginosa was predominantly isolated from pus/wound swab (47%, n = 2766), followed by respiratory secretions (22%, n = 1288) and urine (17%, n = 1001) [Figure 1].
Table 1: Sociodemographic characteristics of patients

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Figure 1: Sample-wise distribution of Pseudomonas aeruginosa isolates

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A 5 year observation on the antimicrobial resistance pattern against the tested antibiotics is presented in [Figure 2]. Overall, the highest resistance was noticed to imipenem (30%), followed by meropenem (29%), amikacin (18%), gentamicin (15%), CTAZ (15%), ciprofloxacin (14%), and piperacillin-tazobactam (10%). The least resistance was shown to colistin (2%). With respect to year-wise change in resistance pattern, Amikacin resistance has been steadily decreased over the years. Ciprofloxacin resistance was somewhat steady at lower levels during the same period. Ceftazidime, Gentamicin, and piperacillin/tazobactam have also maintained similar levels of resistance. Imipenem/meropenem resistance also reduced during the same period after an interim rise in 2016. Colistin maintained single-digit percentage levels throughout. In the present study, 10% of P. aeruginosa were found to be MDR strains [Table 2]. Furthermore, resistant strains were more commonly isolated from respiratory (16%) and urine (15%) samples [Table 3].
Figure 2: Antibiotic resistance pattern of Pseudomonas aeruginosa isolates

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Table 2: Multidrug-resistant versus nonmultidrug-resistant isolates

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Table 3: Sample-wise antibiotic resistance pattern of Pseudomonas aeruginosa isolates

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  Discussion Top


P. aeruginosa exists naturally in the environment, especially in hospital settings. At present, it is a common nosocomial pathogen and causes a wide range of hospital-acquired infections often in immunocompromised individuals. In the current study, it is evident that there is a distinct variation in the frequency of isolation of P. aeruginosa from specimen to the specimen with maximal isolation from skin samples such as swab/pus (47%) followed by respiratory secretions (22%) and urine (17%). This is in line with the studies by Khan and Faiz and Hoque et al. in Pakistan and Bangladesh, respectively.[4],[15] Similar to our study, the gender distribution is more or less equal among males (52%) and females (48%) in a study by Badger-Emeka et al.[16] Furthermore, the frequency of isolation is highest among elderly people indicating to the waning of immunity at old age is a significant contributing factor.[16]

Fast-growing antibiotic resistance among P. aeruginosa strains is a serious concern of human health. Due to these facts, P. aeruginosa has received much attention in recent years.[16] Our study results revealed low-to-moderate rate of resistance (10% to 30%) of P aeruginosa to anti-pseudomonal drugs. The overall resistance of P. aeruginosa to first-line antibiotics such as piperacillin-tazobactam (10%), ciprofloxacin (14%), CTAZ (15%), aminoglycosides such as gentamicin (15%) and amikacin (18%) was low. The results obtained were consistent with studies by Khan and Faiz, and Hassan et al.[4],[17] However some studies from Nepal, Bangladesh, and Iran reported a high rate of resistance (50%–98%) of P. aeruginosa to these drugs.[18],[19],[20] Geographical variation in the resistance rates of P. aeruginosa is largely related to differences in antibiotic prescription policies, lack of awareness of the consequences of antimicrobial resistance, and inadequate infection control practices.[4],[21] Emergence and spread of resistant organisms is a worrisome fact.

In the current study, the highest overall mean resistance of P. aeruginosa was observed against carbapenems such as imipenem (30%) and meropenem (29%). Similar to our study, Badger-Emeka et al. have reported a 5 year mean percentage of resistance of P. aeruginosa to imipenem and meropenem as 32.3% and 34.9% respectively.[16] However, some studies have demonstrated an alarmingly high rate of carbapenem resistance; Hoque et al. demonstrated 68% meropenem resistance in P. aeruginosa, Khan et al. showed 60% resistance to both imipenem and meropenem, and Tam et al., reported 100% resistance against carbapenems.[15],[21],[22] Because carbapenems are the last line of antibiotics used for treating infections caused by P. aeruginosa, the high rate of resistance to carbapenems is frightening. The main mechanism associated with increased resistance to carbapenems is the reduction in the expression of outer membrane proteins (OprD).[21] Overuse or misuse of antibiotics is one of the reasons of growing resistance among pathogens. This warrants the need for careful monitoring of the use of antibiotics and encouraging culture-based antibiotic therapy. This would further benefit in preventing the emergence and spread of carbapenem resistance genes to other Gram-negative bacteria such as Enterobacteriaceae.[4] Another encouraging finding in our study was a decrease in carbapenem resistance from 2015 to 2019 after an interim increase in 2016.

The rise in ciprofloxacin resistance in P. aeruginosa is a growing concern worldwide. In our study, ciprofloxacin resistance was low (14%) which is comparable with the report of Khan and Faiz (16.5%) and Ahmad et al. (13.3%).[4],[23] However, a much higher rate of ciprofloxacin resistance ranging from 75% to 100% was reported from various studies across the world.[22],[24] Aminoglycosides, another commonly used group of anti-pseudomonal drugs have shown variable susceptibility against Pseudomonas. The resistance rate was reported to be high in studies by Angadi et al. (70%) and Hoque et al.(85%), while low resistance rate (7%) was noticed in the reports of Samad et al. and Raja and Singh.[25],[26] In the present study, amikacin (18%) and gentamicin (15%) resistance was low. The wide variations could be linked to the acquisition of resistant genes and patterns of antibiotic prescription in a particular region.[15]

The overall resistance to CTAZ in the current study was 15% which is comparable to the study report (14%) from Saudi Arabia.[4] But reports from Germany (23%), Nepal (90%), Bangladesh (81%), and the United States (10%) have shown varied patterns of resistance.[15],[18],[24],[27] The wide differences in CTAZ resistance were attributed to differences in antibiotic prescribing practices from region to region which has resulted in the acquisition of resistant determinants due to selective antibiotic pressure. Literature search recommends treatment of severe Pseudomonas infections by combination chemotherapy with at least two different anti-pseudomonal drugs. The rationale for combination therapy is to reduce the chances of emergence of mutants due to selective pressure during therapy in addition to capitalize on the potential synergistic activity of combination drugs. The most preferred combination remains aminoglycosides and beta-lactams.[28]

In the present study, piperacillin-tazobactam showed the lowest resistance (10%). In line with our study findings, the least resistance of P. aeruginosa (4.9% and 0%, respectively) towards piperacillin-tazobactam was also observed in studies of Khan and Faiz and Shidiki et al. Thus piperacillin-tazobactam synergy is still the most effective combination for anti-pseudomonal therapy as observed by us and many other researchers.[4],[18] Another encouraging finding in our study is steady declining or no increase in the resistance rate of P. aeruginosa to anti-pseudomonal drugs which contrasts with the study by Badger-Emeka et al. who observed a steady increase in resistance to beta-lactams, fluoroquinolones, and aminoglycosides.[16]

Concerning MDR strains, 11% of P. aeruginosa were found to be MDR in the present study, which is in line with the report (14%) from the United States.[25] Infections with MDR strains increasing worldwide and have become a serious threat as the therapeutic option is limited. Studies by Samad et al., and Farhan et al. reported a high rate of isolation of MDR Pseudomonas strains; 39% and 66% respectively.[29],[30] The emergence and continual spread of MDR P. aeruginosa is worrisome. The number of new therapeutic agents to treat Pseudomonas infections in the pipeline is scarce and these issues may result in catastrophic consequences on human health. Therefore strict laws on antibiotic policies need to be regulated to limit the unnecessary use of antibiotics and thus by to preserve currently available drugs and also to control the emergence and spread of drug-resistant strains.

Limitation of the study

The current study was single centered and the data included is of one hospital. Hence results cannot be generalized as the study did not include all tertiary hospitals in this region.


  Conclusions Top


P. aeruginosa is a leading cause of hospital-acquired infections. Unnecessary use of antibiotics is the most notable contributing factor for the emergence and spread of drug-resistant strains. In general, the present study has shown that first-line anti-pseudomonal antibiotics still useful for treating Pseudomonas infections. The combination of piperacillin-tazobactam was the most effective drug in our study, suggesting clinicians to consider this combination for treating especially severe Pseudomonas infections. However, P. aeruginosa have shown moderate resistance to carbapenems in our study. The increasing resistance to these drugs is a worrisome fact considering them to be a last line of antibiotics for treating Gram-negative bacterial infections such as P. aeruginosa. Furthermore, due to the limited number of new effective drugs in the pipeline, preserving the efficacy of the existing drugs is crucial. This can be achieved by emphasizing more restricted and rational use of antibiotics. Strict surveillance and control of hospital-acquired infections, antibiotic policy, regular monitoring of antibiotic susceptibility pattern, and timely dissemination of the results to guide physicians to prescribe antibiotics most appropriately is indispensable to control the emergence and spread of drug-resistant strains.

Acknowledgments

The authors express their sincere gratitude to the Microbiology and IT staff of Sohar Hospital for their kind-hearted support for data collection from the hospital microbiology and computerized records.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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