In this study, we analyzed the molecular epidemiology of patients who acquired an IRPA strain by use of perianal surveillance cultures obtained over a 5-year period in a large ICU population. We found that, of the 149 patients who acquired colonization with IRPA, 46 (31%) had isolates with PFGE patterns that were similar to those of isolates obtained from other patients; 16 (11%) of 149 patients also had hospital stay overlap, and 28 (19%) acquired colonization by endogenous flora.
Our study is unique in that we are able to study the acquisition of antibiotic-susceptible and/or antibiotic-resistant organisms over a period of several years in a unique population of >7000 patients. Previous studies have generally studied drug-susceptible P. aeruginosa
and have disagreed on the amount of patient-to-patient transmission that occurs when patients acquire a P. aeruginosa
strain while in the ICU. These studies also included far fewer patients in their cohorts [8
]. Three major studies have found that cross-transmission played an important role in the acquisition of P. aeruginosa,
with cross-transmission accounting for >30% of cases of P. aeruginosa
acquisition. Olson et al [12
] found that cross-transmission accounted for 12 (32%) of 37 cases in which patients acquired a susceptible P. aeruginosa
strain. Pena et al [14
] studied the acquisition of carbapenem-resistant P. aeruginosa
using 2 serial incidence surveys that monitored colonization during two 1-month periods that were 1 year apart. The data showed that 9 (30%) of the patients in this study were found to have similar genotypes, but it was unclear whether these patients had hospital overlap. Bertrand et al [9
] found that 107 (51%) of 208 patients who acquired a P. aeruginosa
strain acquired that strain as a result of cross-transmission. Other studies, however, have indicated that cross-transmission does not play a major role in the acquisition of P. aeruginosa.
Bonten et al [11
] concluded from their study of 44 cases of acquisition that transmission of P. aeruginosa
was polyclonal; they found that endogenous acquisition played a major role and that patient-to- patient transmission was not significant (occurring in only 8% of cases). Two other studies agreed that endogenous sources played an important role and that clonal dissemination was not a significant factor in the acquisition of antibiotic-resistant P. aeruginosa
in an ICU population [10
]. Reuter et al [8
] concluded that faucets play an important role in the transmission of P. aeruginosa.
Their study analyzed a cohort of 45 patients colonized or infected with P. aeruginosa
in a surgical ICU and found that 33% of these patients had genotypes that were identical to those of isolates grown from the faucet of the patient's room.
The literature on the role of patient-to-patient transmission of drug-susceptible P. aeruginosa
is confusing, and there is even less data pertaining to IRPA. Therefore, we looked at a large cohort of patients over a 5-year period to determine the role of patient-to-patient transmission and antibiotic selective pressure on endogenous flora of IRPA colonization in the ICU population. In our study, we defined cases of patient-to-patient transmission on the basis of isolates with similar PFGE patterns and an overlap in hospital stay. We chose overlap in hospital stay, because other investigators have used a definition that extends beyond ICU stay, and we believe that this is an important variable in capturing all possible cases of patient-to-patient transmission [15
]. However, our data are puzzling, because 46 (31%) of 149 patients who acquired this organism had isolates with genotypes similar to those of isolates obtained from other patients, but when we combined this data with hospital overlap data, there were only 16 (11%) of 149 patients who fulfilled both criteria. When we used this same definition of patient-to-patient transmission for other antimicrobial-resistant gram-negative organisms, we did not see this discrepancy between hospital overlap and PFGE results [18
]. This finding could suggest that P. aeruginosa
has a reservoir that is undiscovered or that P. aeruginosa
can survive for many months in the environment. On the other hand, it could be possible that, in some of these patients, imipenem-susceptible strains were acquired through patient-to-patient transmission and then became resistant to imipenem as a result of selective antibiotic pressure.
Within this cohort, there is a population of patients for whom we did not determine the mode of IRPA acquisition. We believe that there are several possible explanations. Imipenem-susceptible P. aeruginosa
could have been transmitted by patient-to-patient spread and not determined in our study. Environmental contamination could have been a mode of transmission, because Pseudomonas
species are known to be an environmental pathogen found in water sources. Environmental sources were not evaluated in our prospective cohort study. Obtaining perianal cultures daily for each patient would have been laborious and time-consuming but could have increased the chance of obtaining more patients with drug-susceptible strains that became resistant to imipenem while the patient was hospitalized in the ICU or could have pinpointed more patients with culture results positive for an IRPA, possibly adding to the patient-to-patient transmission group. The use of swab samples from an infection-control intervention study for vancomycin-resistant enterococci could have decreased the recovery of IRPA within this cohort of patients. However, we performed a validation study of the swab samples after multiple cultures and freeze/thaw cycles and showed that we were able to recover all but 1 (5%) of the IRPA isolates [20
In conclusion, our study suggests that patient-to-patient transmission plays a role in the acquisition of IRPA colonization in the ICU at a tertiary-care hospital in a nonoutbreak setting. Our data also suggest that there is not a single mechanism of acquisition, and although patient-to-patient transmission is important, a patient's endogenous flora is also important. This suggests that a multifaceted approach is needed to control the emergence of IRPA.