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ORIGINAL ARTICLE Table of Contents   
Year : 2009  |  Volume : 52  |  Issue : 4  |  Page : 509-513
Nosocomial cross-transmission of Pseudomonas aeruginosa between patients in a tertiary intensive care unit


1 Department of Microbiology, SGPGIMS, Lucknow, India
2 Department of Critical Care Medicine, SGPGIMS, Lucknow, India

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Date of Web Publication1-Oct-2009
 

   Abstract 

Background: Nosocomial infection caused by Pseudomonas aeruginosa (P. aeruginosa) is very common, despite the application of various preventive measures in intensive care units (ICUs) leading to increased morbidity, mortality, prolonged hospital stay, and increased treatment cost. Aim: The aim of the present study is to identify the source of P. aeruginosa infection in patients admitted to tertiary ICU. Materials and Methods: From 200 patients selected randomly, appropriate clinical specimens from different sites were collected and processed for the isolation and identification of the nosocomial pathogens. Surveillance samples from environmental sites and hands of nursing staff were also cultured. Results: P. aeruginosa was found to be the most common pathogen associated with nosocomial infections accounting for 23.3% of all bacterial isolates from different infection sites in the ICU. Serotyping of the clinical isolates and surveillance sample isolates from nurses' hands showed serotype E as the most common serotype. Other serotypes of P. aeruginosa were isolated from environmental cultures such as sinks, floors, walls, tap water, etc. Conclusion: Study revealed a high prevalence of P. aeruginosa infections in the ICU attributed to cross transmission from patient to patient via hands of the nursing staff. Strict enforcement of infection control protocols is essential to minimize the disease burden.

Keywords: Nosocomial infection, Pseudomonas aeruginosa, surveillance, cross transmission

How to cite this article:
Dwivedi M, Mishra A, Singh R K, Azim A, Baronia A K, Prasad K N. Nosocomial cross-transmission of Pseudomonas aeruginosa between patients in a tertiary intensive care unit. Indian J Pathol Microbiol 2009;52:509-13

How to cite this URL:
Dwivedi M, Mishra A, Singh R K, Azim A, Baronia A K, Prasad K N. Nosocomial cross-transmission of Pseudomonas aeruginosa between patients in a tertiary intensive care unit. Indian J Pathol Microbiol [serial online] 2009 [cited 2014 Apr 24];52:509-13. Available from: http://www.ijpmonline.org/text.asp?2009/52/4/509/56143



   Introduction Top


Infections in the intensive care unit (ICU) have been under intense study over the past few decades. Critically ill patients are at high risk for getting the hospital acquired (nosocomial) infections, as evidenced by several studies. [1],[2],[3],[4] The risk of acquiring nosocomial infection increases up to 5 to 10 times in ICU patients when compared to patients from general medical wards. [5],[6] Despite the advances in therapies available for treating critically ill patients, nosocomial infections and their complications still rank among the major causes of morbidity, mortality, and increased financial burden in ICUs worldwide.

P. aeruginosa is identified as one of the most common pathogen causing hospital acquired infections in ICUs. [4],[7],[8] Hospital-acquired infections caused by this organism are often associated with high morbidity and mortality because these microorganisms are virulent and have a limited susceptibility to antimicrobials. [9],[10] Although, several studies have presented overviews or specific aspects of the epidemiology of hospital-acquired infections caused by P. aeruginosa, a detailed epidemiological description for a particular hospital setting from India is still lacking. [11],[12]

In an earlier study, we have reported a very high prevalence of P. aeruginosa among the ICU patients (35% in ventilator associated pneumonia), despite the implementation of hospital infection control program. [13] The high prevalence of P. aeruginosa in our ICU prompted us to identify source of nosocomial pathogens, associated risk factors, as well as to characterize local epidemiology for P. aeruginosa colonization and infection.


   Materials and Methods Top


Hospital setting and study population

The study was conducted in 12 bedded general purpose ICU of a large tertiary care referral center. A total of 200 patients were admitted to the ICU during July 2005 to June 2007, with clinical features suggestive of nosocomial infections. They were randomly selected with the help of a random number table generated by SPSS 12.1 statistical software. The sample size was calculated under the guidance of a statistician.

Collection of data

For each patient the following data were collected before ICU admission: age, sex, date of admission, and discharge from the ICU, and location. Detailed information on invasive procedures, antibiotic treatment regimen before and after the onset of nosocomial infection, duration of mechanical ventilation, central venous catheterization, insertion sites, urinary catheterization, and surgical interventions were recorded.

Definitions

Infections were diagnosed according to the criteria for Centers for Disease Control and Prevention (CDC), Atlanta, US. [14] ICU-acquired infection was defined as infection documented after at least 48 hour in the ICU. Colonization was defined as the presence of P. aeruginosa in clinical specimens if the criteria of infection were not met. Pneumonia was diagnosed as per CDC criteria with little modifications. [15] The criterion for pneumonia was modified to include the isolation of pathogens from a barncheoalveolar lavage (BAL) fluid (≥104 cfu/ml), or endotracheal (ET) aspirate (≥105 cfu/ml) and/or upon direct examination, more than 5% of cells containing intracellular bacteria, in presence of characteristic signs/symptoms and radiological findings is considered diagnostic of bacterial pneumonia.

Sample collection and microbiological investigations

Microbiological specimens were collected on weekly basis as per the guidelines of the department or when the attending physician suspected infection based on systemic signs (unexplained fever, chills, and hypotension), and/or local signs (purulent tracheal aspirates in mechanically ventilated patients, purulent urinary drainage, or pus or pain at a vascular catheter insertion site). Microbiological specimens were collected and processed as per the standard guidelines. [16],[17] Specimens consisted of blood for bacteremia/septicemia, urine for urinary tract infection (UTI), a BAL fluid or ET aspirate for ventilator associated pneumonia (VAP) and purulent discharges, aspirated pus or drain fluid for surgical site infection. Duplicate isolates were excluded from the study. Bacteria isolated from clinical specimens were identified to species level by the standard laboratory techniques. [18]

Pseudomonas surveillance for nosocomial infection

During the study period following cultures were taken four times at the interval of six month: 1) From the staff of ICU: Hand impression cultures-hand impressions of the nursing staff working in the ICU were taken on Pseudomonas isolation agar, during their working hours; and 2) from environment: objects such as sinks, washing basins, floors, dressing trolley, door handles, O 2 bottles and suction bottle from ICU were cultured with a moist cotton swab on Pseudomonas isolation agar. Saline, tap water, O 2 tubing disinfectants, and medicated creams were cultured in trypticase soy broth (BBL and Difco, Mumbai, India) and sub cultured on Pseudomonas isolation agar. Air cultures were made on Pseudomonas isolation agar settle plates. [19].

Nonlactose fermenting colonies grown from different samples were subcultured on Pseudomonas isolation agar to isolate Pseudomonas. The isolates on Pseudomonas isolation agar were subjected to the standard biochemical tests for species differentiation. [20] Antimicrobial sensitivity testing was performed for all the isolates of Pseudomonas spp. using disk diffusion method as per Clinical and Laboratory Standards Institute (CLSI) (2006) guidelines. [21] Quality control was carried out using standard strain of P. aeruginosa (ATCC 10662). The following concentrations of drugs were used: Piperacillin (100 μg/disc), Piperacillin/Tazobactam (100/10 μg), Ceftazidime (30 μg), Gentamicin (10 μg), Amikacin (30 μg), Ciprofloxacin (5 μg), Meropenem (10 μg), and Polymyxin-B (300 units). Meropenem discs are provided by Oxoid, US. Rest all the discs were provided by Hi-media Laboratories Pvt. Ltd., Mumbai, India.

Serotyping was performed according to Homma [22] and Liu [23] by slide agglutination test using P. aeruginosa antisera kit (Denka Seiken Co. Ltd., Tokyo, Japan).

Statistical analysis

Statistical analyses was performed by Chi-square test using Graph pad Prism (version 2.0, Graph pad Software). P values less than <0.05 were considered statistically significant.


   Results Top


A total of 200 patients admitted in the ICU were included in the study; 142 males (71%), and 58 (29%) females. A total of 87% patients were hospitalized prior to ICU admission and 83% patients had already received antibiotic treatment. Most of the patients were referred from surgical disciplines (73%). On admission to ICU, infectious disease represented the primary diagnosis for 42 (21%) patients. A total of 79% patients received mechanical ventilation for a median period of 5.5 (range, 1-60) days. Median length of ICU stay was 10 days (range, 2-76), and 118 (59%) patients died during their ICU stay. The demographic data of study population is given in [Table 1].

Out of 200 ICU patients included in the study, 67 (33.5%) developed nosocomial infections during their ICU stay; VAP was the most common infection and occurred in 63 (31.5%) patients, UTI occurred in 48 (24%) patients, bloodstream infections (BSI) in 40 (20%) patients, and surgical site infections (SSI) documented in 24 (12%) patients. A total of 193 different bacteria were isolated from the four major infections. Overall, Gram negative organisms (59.1%) were more frequently isolated than the Gram positive cocci (40.9%) [Table 2]. P. aeruginosa was found to be the most frequent isolate. From various clinical specimens, a total of 45 isolates of Pseudomonas spp. were obtained [Table 2].

During the course of the surveillance study, cultures revealed 95 isolates of Pseudomonas spp (61 from environmental cultures and 34 from staffs' hands). Sixty-one isolates were obtained on different occasions from the following environmental sites: 12 from sinks, 14 from floors, 17 from walls, four from O 2 bottles, nine from O 2 tubes, and five from tap water.

Out of the 40 nursing staff enrolled in the study, hand cultures of 23 nursing staff yielded 34 isolates of Pseudomonas spp. on different occasions. From seven staffs, Pseudomonas spp. was isolated twice during the study, while from two staffs it was isolated thrice. Disinfectants, dressing trolleys, door handles, air, and saline never yielded any Pseudomonas spp. The results of surveillance cultures are summarized in [Table 3].

Among 45 clinical isolates of Pseudomonas spp., 44 (97.8%) were identified as P. aeruginosa by standard biochemical tests; only one clinical isolate from surgical site infection was identified as Pseudomonas spp. other than P. aeruginosa. All the isolates of surveillance cultures were biochemically identified as P. aeruginosa.

Among all isolates of P. aeruginosa, 46.7% were resistant to piperacillin, 51.7% to ceftazidime, 47.3% to gentamicin, 32.0% to amikacin, 47.3% to ciprofloxacin, 28.3% to piperacillin-tazobactam, 37.0% to meropenem, while 37.7% were resistant to imipenem. Colistin was uniformly sensitive against all the isolates. The maximum resistance was seen against ceftazidime (51.7%), while the minimum resistance was seen against piperacillin-tazobactam (28.3%). Resistance against amikacin was also less in comparison to other drugs. Similar resistance patterns were observed among clinical isolates and isolates from hand cultures. The environmental isolates were found to be less resistant. The resistance patterns of P. aeruginosa isolates are given in [Table 4].

On serotyping of 139 isolates (44 clinical isolates and 95 isolates from surveillance cultures) of P. aeruginosa, 52.3% (23/44) of clinical isolates were type E, with no other serotype (other than serotype I) exceeding 10 % of the total, and three (6.8%) of the clinical isolates were nontypable. Among the isolates from staffs' hands, 79.4% (27/34) of isolates were of serotype E. Among the environmental sites, majority of isolates (12/13) from oxygen tube and oxygen bottles shared the same serotype (serotype E), while a different serotype (serotype F) was shared by sinks, floors, walls, and tap water. Also, 16% (7/44) of clinical isolates were type as serotype I and this particular serotype was never isolated from any of the surveillance cultures. Comparison of results of serotyping is summarized in [Table 5].


   Discussion Top


In our study the prevalence of nosocomial infection was found to be very high. Gram negative bacteria, particularly P. aeruginosa, was the most common agent responsible for nosocomial infection. Most of the patients included in our study had history of previous hospitalization and were receiving antibiotics [Table 1] before admission to our ICU. These patients had prolonged ICU stay in addition to prolonged use of mechanical ventilation and surgical interventions. These factors may have contributed for the colonization and subsequent infection by multiresistant gram negative bacteria (including P. aeruginosa), as has also been reported previously by several studies. [15],[24]

The most common pathogen associated with nosocomial infection in our study was P. aeruginosa [Table 2], accounting for 23.3% (44/193) of all bacterial isolates from different nosocomial infections in the ICU. Among all bacterial isolates, P. aeruginosa was found to be the most common in nosocomial pneumonia (30.9%), followed by urinary tract infections (21.6%), and surgical site infections (12.9%), and the second most common pathogen isolated from bloodstream infections (18.6%). A total of 45 isolates of Pseudomonas spp. were cultured from the four major categories of infection.

In comparison to other studies, rates of nosocomial infections especially those caused by P. aeruginosa are higher in our study. [24],[25] These differences may be partly explained by heterogeneous nature of patient population. Our facility serves largely as a tertiary-care referral center, whereas the studies mentioned above mainly encompassed community or community-teaching hospitals [approximately 70% of the National Nosocomial Infections Study (NNIS) hospitals are categorized as community or community-teaching hospitals]. We probably have a larger proportion of patients who require intensive support therapies (respiratory assistance, invasive monitoring, etc.) than the community hospital patients and hence are more vulnerable to develop nosocomial P. aeruginosa infections.

In the present study, we found a clear tendency towards decreased susceptibility for all groups of antibiotics used against P. aeruginosa [Table 3]. In terms of percentage susceptibility, both piperacillin/tazobactam and amikacin scored the best percentage. In contrast to many other surveys, the carbapenem group of antibiotics (Meropenem and Imipenem) were not found to be much potent against P. aeruginosa. [26],[27] While OprD mutational inactivation alone is known to result in clinical imipenem resistance, the mutational mechanisms leading to clinical meropenem resistance are usually more complex and are thought to lie in the acquisition of additional mutations (beyond OprD inactivation), such as those leading to the hyperproduction of AmpC or the hyperexpression of the efflux pump MexAB-OprM. [28] Production of metallo-beta-lactamases may also be the reason behind the carbapenem resistance.

On serotyping of the isolates [Table 4], it was found that isolates from the patients and the nurses' hands shared serogroup E most frequently, which was also found to be the most prevalent serotype. This observation strongly suggests the occurrence of cross colonization with the direct handling by nursing personnel as the major means of cross-infection. The hands may have become contaminated during nursing care of patients. It was observed during the study that the nurse-patient contact was not always preceded by hand washing or hand hygiene measure.

The corresponding nomenclature of the serotype E with the International Antigenic Typing Scheme (IATS) serotypes designation is O11. Serotype O11 was recognized by several authors as an important hospital problem in recent years, principally in epidemic situations, because this microorganism presents multidrug resistance with different resistance phenotypes. [10],[29],[30],[31],[32]

In our study, the data showed that sinks, floors, and tap water were contaminated with P. aeruginosa, which is similar to other reports. [33],[34],[35] This contamination can not be contributory to the transmission of P. aeruginosa, because of the presence of different serotype of P. aeruginosa (serogroup F).

The possibility of endogenous infection cannot be ruled out because serogroup I, which was isolated from some of the patients, had not been isolated from any of the surveillance cultures. We believe that both endogenous and exogenous sources are likely, with cross-transmission through hands of nursing staff being the major mode of transmission of P. aeruginosa infection in the ICU.

In conclusion, cross transmission of P. aeruginosa from patients to patients through hands of nursing staff appears to be an important factor in the epidemiology of P. aeruginosa infection in our ICU. Strict enforcement of hand hygiene and infection control measures in ICUs are necessary to prevent nosocomial infections to reduce morbidity, mortality, and cost of hospital stay.

 
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R K Singh
Department of Critical Care Medicine, SGPGIMS, Lucknow
India
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DOI: 10.4103/0377-4929.56143

PMID: 19805958

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    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5]

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