MILITARY MEDICINE, 174, 9:899, 2009

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1 MILITARY MEDICINE, 174, 9:899, 2009 Association of Bacterial Colonization at the Time of Presentation to a Combat Support Hospital in a Combat Zone With Subsequent 30-Day Colonization or Infection COL Robert L. Kaspar, MC USA * ; MAJ Matthew E. Griffith, MC USA ; MAJ Paul B. Mann, MS USA ; CPT Devon J. Lehman, AN USA ; Lt Col Nicholas G. Conger, USAF MC ; COL Duane R. Hospenthal, MC USA ; LTC Clinton K. Murray, MC USA ABSTRACT U.S. casualties have developed multidrug-resistant (MDR) bacterial infections. A surveillance project to evaluate U.S. military patients for the presence of MDR pathogens from wounding through the first 30 days of care in the military healthcare system (MHS) was performed. U.S. military patients admitted to a single combat support hospital in Iraq during June July of 2007 had screening swabs obtained for the detection of MDR bacteria and a subsequent retrospective electronic medical records review for presence of colonization or infection in the subsequent 30 days. Screening of 74 U.S. military patients in Iraq found one colonized with methicillin-resistant Staphylococcus aureus. Fifty-six patients of these were screened for Acinetobacter in Germany and one found colonized. Of patients evacuated to the U.S., 9 developed infections. Carefully obtained screening cultures immediately after injury combined with look-back monitoring supports the role of nosocomial transmission. Consistent infection control strategies are needed for the entire MHS. * Department of Medicine, Darnall Army Medical Center, Fort Hood, TX. Infectious Disease Service, San Antonio Military Medical Center, Fort Sam Houston, TX. Uniformed Services University of the Health Sciences, Bethesda, MD. U.S. Army Medical Department Center and School, Fort Sam Houston, TX. Department of Nursing, Brooke Army Medical Center, Fort Sam Houston, TX. Infectious Disease Department, Landstuhl Regional Medical Center, Landstuhl, Germany. The opinions or assertions contained herein are the private views of the authors and are not to be construed as official or reflecting the views of the U.S. Department of the Air Force, the U.S. Department of the Army, the U.S. Department of Defense, or the U.S. government. The authors are employees of the U.S. government and this work was performed as part of their official duties. As such, there is no copyright to be transferred. This manuscript was received for review in Novermber The revised manuscript was accepted for publication in June INTRODUCTION Combat casualties returning from Iraq and Afghanistan during Operations Iraqi and Enduring Freedom (OIF/OEF) are developing multidrug-resistant (MDR) bacterial infections, especially with Acinetobacter baumannii-calcoaceticus complex (Abc), extended-spectrum b -lactamase (ESBL) producing Klebsiella pneumoniae, Pseudomonas aeruginosa, and methicillin-resistant Staphylococcus aureus (MRSA). 1 3 An assessment of the etiology of Abc has included screening both healthy personnel in Iraq and patients managed throughout the evacuation system. 3 7 Scott et al. showed the most definitive data on nosocomial transmission for Abc through collection of isolates within medical facilities in Iraq and matching those isolates genotypically with patients on the U.S. Naval Ship Comfort, in Germany, and in the U.S. (to include patients not deployed to Iraq). 5 A recent publication by Moran et al. provided more supporting data that non-u.s. personnel are the likely reservoir of these MDR bacterial infections. 8 In contrast to Abc being associated with nosocomial transmission, MRSA is associated with colonization at the time of injury as well as nosocomial infection. 1,7 Overall the data supports a primary role of nosocomial transmission for Abc, although the timing of the acquisition of this pathogen and the presence of other gram-negative bacteria has not been characterized. As patients transfer, on average, through 4 facilities in 7 days from point of injury to their final U.S. medical treatment facility, the entire military healthcare system (MHS) can be viewed as a series of facilities. Interventions such as antimicrobial therapy or infection control strategies at any one point could have substantial downstream impact in this large medical healthcare system. Currently there has not been a longitudinal assessment of colonization and infection among individual military personnel evacuated out of the combat zone. Information obtained from such an assessment could be used to educate the military medical command and enable the institution of standard management guidelines to improve overall patient care in and out of the combat theater in this system. Herein, we evaluate a performance improvement surveillance project involving U.S. military personnel who presented to one combat support hospital (CSH) for bacteria colonization using skin, orophyarnx, and perirectal cultures. Continued passive monitoring of routine patient care for 30 days was used to determine follow-on colonization or infection. SURVEILLANCE PROGRAM In Theater Colonization Screening was initiated on all U.S. patients who were admitted to the CSH in Baghdad, Iraq during June and July of The infrastructure and management strategies of the CSH has MILITARY MEDICINE, Vol. 174, September

2 been previously published. 1 All hospitalized patients at the CSH who required evacuation out of the combat zone were assessed for the presence of colonization with aerobic bacteria at the time of presentation to the hospital to direct isolation procedures and notify subsequent levels of medical care. Although all attempts were made to serially assess patients, times of rapid patient turnover or large fluctuations of arriving patients made this not universally possible. All patients were screened at the time of admission to the CSH or when the patient was deemed clinically stable, typically within hours of admission. Culture specimens underwent immediate processing. To identify the presence of bacterial colonization, samples were obtained from the axilla/groin, oropharynx, and perirectal area using separate BBL CultureSwab (Becton Dickinson, Sparks, MD) swabbing of each area for several seconds. These screening areas were chosen because of reports of higher colonization of these areas in other military treatment facilities (C.K.M., personal communication). Swabs were plated onto 5% sheep blood agar and MacConkey agar plates and were examined for growth after 24 and 48 hours incubation at 37 C. Colonies were subsequently identified using the MicroScanWalkAway-96 automated system (Dade Behring, West Sacramento, California). Pathogens of particular interest included MRSA, Enterobacter species, P. aeruginosa, K. pneumoniae, and Abc. Gramnegative bacteria were defined as MDR if they were resistant to 3 or more classes of antibiotics (classes that were evaluated included penicillins, cephalosporins, carbapenems, aminoglycosides, and quinolones). S. aureus isolates resistant to methicillin and Enterococcus isolates resistant to vancomycin were also considered MDR. 30-Day Outcomes All patients initially screened at the CSH in Iraq in this surveillance project underwent a review of the Department of Defense electronic medical records system records for the presence of subsequent cultures. This included screening or clinical cultures obtained in the subsequent 30 days after initial screening for the presence of isolates of interest. These cultures were obtained as part of standard clinical care indicated by their attending physicians or under the auspices of the admitting healthcare facility s infection control procedures for screening OIF/OEF casualties for MDR colonization upon admission. After evacuation from Iraq and Afghanistan, all patients pass through Germany with those admitted as inpatients to the U.S. military hospital undergoing screening for Abc colonization of the groin, axilla, and perirectal area. Those patients evacuated from Germany to the U.S. go to various military healthcare facilities. At the time of this project there was no standardized screening method across the various U.S. military healthcare facilities. Individual strategies at various institutions included no screening, screening for Abc only, screening for MRSA and Abc, and screening for all MDR pathogens. Of those facilities that screened inpatients for colonization, typically the nares, groin, and axilla were evaluated. Those patients transferred to Germany who were deemed appropriate for outpatient care did not receive screening cultures. FINDINGS Cultures were obtained from the skin, oropharynx, and perirectal area for analysis from 74 patients at the CSH in Iraq during the project period ( Fig. 1 ). Of the 74 patients who were admitted to the CSH, 20 (27%) had noncombat-related injuries. These patients had genitourinary problems, including hematuria or testicular abnormalities, appendicitis, or noncombat-related trauma. None of the skin samples or perirectal samples obtained in Iraq revealed MDR gram-negative bacteria or vancomycinresistant Enterococcus. Only 1 (1%) oropharyngeal sample demonstrated the presence of a MDR organism (MRSA). This patient was not found to have further colonization or infection with MRSA, but rather developed an infection with Abc in the U.S. during the 30-day follow-up period. Noncombat-Related Injuries Of the 20 patients admitted to the CSH without combat-related injuries ( Fig. 1 ), none were initially noted to be colonized by MDR bacteria in Iraq. Six underwent screening in Germany an average 2.5 (range, 2 3) days after admission in Iraq. Only 1 of the 5 patients admitted in the U.S. had a screening culture obtained in which no MDR bacteria were isolated and it was obtained 8 days after injury ( Table I ). This patient developed a MRSA infection of an open ankle fracture that was a result of a noncombat mechanical injury. Combat-Related Injuries Of the 54 patients with combat-related injuries occurring in Iraq, screening was performed on 50 in Germany, an average 2.8 days (range, 1 20) days after injury. One patient had a positive screen for Abc in Germany and again in the U.S. 3 days later. This patient developed evidence of Abc infection 1 day after admission to the U.S. military healthcare facility. A total of 32 patients of the 43 evacuated as inpatients to the U.S. underwent screening in the U.S., on average 7.2 (range, 2 23) days after injury. Six were colonized with MDR pathogens. Three patients screened positive for Abc (which includes the patient who screened positive in Germany), 2 patients tested positive for MRSA, and 1 patient was positive for ESBL-producing K. pneumoniae. A total of 8 of the 54 combat-related injured patients developed an infection in the 30 days following injury, on average 11.6 (range, 5 26) days after injury. Infections included 7 due to Abc (which includes the patient positive in Germany) and 1 due to ESBL-producing K. pneumoniae ( Table I ). The patient who was noted to be colonized with K. pneumoniae upon arrival to the U.S. developed an infection with ESBL-producing K. pneumoniae 3 days after the U.S. screening culture isolate was obtained. Isolates from patients 900 MILITARY MEDICINE, Vol. 174, September 2009

3 FIGURE 1. Colonization and infection rate of 74 patients over 30 days after screening for multidrug-resistant bacteria in Iraq. (Number in parenthesis indicates the average number of days from admission to the CSH in Iraq to obtaining the culture.) MDROs, multidrug-resistant organisms; MRSA, methicillin resistant Staphylococcus aureus ; ESBL, extended spectrum b-lactamase. TABLE I. Description of the 9 Patients That Developed an Infection in the U.S. Within 30 Days Following Injury in Iraq Iraq Screening Germany Screening U.S. Screening U.S. Infection Patient Admission Oropharynx Skin Rectal Days to Culture a Results Days to Culture a Results Days to Infection a Result 1 Non-BI NG NG NG 2 NG 8 NG 10 MRSA 2 BI NG NG NG 2 NG N/A N/A 7 Abc 3 BI NG NG NG 2 NG 5 NG 8 Abc 4 BI NG NG NG 2 NG 6 NG 6 Abc 5 BI NG NG NG 3 NG 7 NG 8 Abc 6 BI NG NG NG 1 Abc 4 Abc 5 Abc 7 BI NG NG NG 3 NG 7 Klebsiella 10 Klebsiella 8 BI NG NG NG 2 NG 5 NG 26 Abc 9 BI MRSA NG NG 2 NG 7 NG 23 Abc NG, no growth; N/A, not performed; BI, battle injury; non-bi, trauma, not battle injury; MRSA, methicillin resistant Staphylococcus aureus ; Abc, Acinetobacter baumannii-calcoaceticus complex; Klebsiella, extended spectrum b-lactamase-producing Klebsiella pneumoniae. a From injury. in the U.S. noted to have colonization and infections with the same bacteria had the same antimicrobial resistance profiles. DISCUSSION Infections are a major complication associated with injuries of war, and the presence of MDR bacteria increases the morbidity and mortality associated with these injuries. Determining the source of infections with MDR bacteria is paramount as this information can influence treatment and infection control strategies, not only in an individual hospital but also throughout a healthcare system as patients are transferred between facilities. This surveillance project is the first assessment of a MILITARY MEDICINE, Vol. 174, September

4 group of patients followed throughout their initial 30-day clinical course to determine when and if they developed subsequent colonization or infection. Colonization increased during evacuation through the various levels of the evacuation chain from Iraq, to Germany, and ultimately the U.S. This project lends further support to the proposition that infections with Abc are nosocomially related but also suggests that nosocomial transmission is possibly occurring for other MDR pathogens such as ESBL-producing K. pneumoniae, and MRSA. These infections are thus likely the result of hospital-acquired infection in facilities along the evacuation route. The project improves upon some aspects of previous studies. This is the first project actively sampling a consecutive cohort of patients admitted to a CSH. Further, the patient cohort was made up of patients injured in numerous areas across Iraq. There was prompt processing of the samples and samples were obtained from the oropharynx and perianal region as well as the skin, thus adding these important sites of potential colonization. This project also expands the evaluation to include non-abc bacteria. It should be noted that these findings deal with observable colonization and is limited by the sensitivity of swabbing as a screening method. It is still possible that the organisms could be present in very low numbers that are not apparent because they are obscured by more numerous resident flora. They likely grow to perceptible numbers when the normal flora is depressed by broad-spectrum antibiotic therapy during subsequent care. Despite attempts to standardize surveillance and infection control procedures, the prolonged nature of the war and the transition of healthcare providers make maintaining consistent infection control strategies challenging. Thus, these data were derived from documentation of routine clinical care. A deliberate, prospective study could confirm these observations. An important question is whether these MDR organisms are a problem resulting from some unique characteristics of the field hospital environment or of the type of wounding. The field hospital environment is a highly congested one. There is rapid turnover of patients, and preparation of beds and equipment between patients is often challenging. Such factors may make the control of nosocomially acquired infections difficult, and those patients not evacuated out of theater may become increasingly colonized with MDR pathogens. 8 Previous studies have shown that interventions are possible and effective in theater. It has been possible to not only modify the rates of ventilator-associated pneumonia, but also to eliminate successfully the MDR strains in the resident flora, and thereby, change the antimicrobial susceptibility profiles of the remaining bacteria, i.e., decreased minimum inhibitory concentrations.9 This study demonstrates that the use of surveillance cultures for U.S. personnel in theater is unlikely to predict subsequent infections. Given the findings of this project, further assessments are needed to evaluate the use of surveillance cultures out of theater and their role in guiding changes in theater to prevent nosocomial transmission. In the current wars in Iraq and Afghanistan, patients are managed at local treatment facilities such as battalion aid stations, then transported in theater to referral facilities with higher levels of medical care, such as CSHs, then to Landstuhl Regional Medical Center in Germany, and finally to a military hospital in the continental U.S., where definitive care is performed and rehabilitation is often completed. Patients are also transferred to the Veterans Administration system for completion of their rehabilitative care. The rapid movement of patients through this system mandates that the U.S. MHS be viewed as a system of facilities. The transfer of pathogens and patients within the U.S. MHS may be similar to prior reports documenting the transfer of resistant pathogens through international travel and patient transfers between local or regional healthcare facilities. 10,11 Therefore strategies to mitigate infections with MDR pathogens need to recognize the limitations and benefits of antibiotic control programs and infection control procedures throughout entire medical systems. Findings from this performance improvement surveillance project were provided to the military medical leadership. This included the consultant to the U.S. Army Surgeon General for Trauma, the U.S. Army and U.S. Navy Infectious Disease Surgeon General representatives, and physicians at the major healthcare facilities. The goals are to continue to make systemwide improvements in the care of patients in and out of a combat zone with standardization of processes across the MHS. 12 The results of this project support the conclusions that infections of combat-related injuries are likely the result of nosocomial infections rather than preexisting colonization, and that culturing casualties in theater is unlikely to predict subsequent infections. Continued efforts at aggressive infection control and minimizing the duration and spectrum of antibiotics are possible interventions applicable throughout the evacuation chain to reduce these infections. ACKNOWLEDGMENT The authors thank Stacey Young-McCaughan for editorial assistance. REFERENCES 1. Yun HC, Murray CK, Roop SA, Hospenthal DR, Gourdine E, Dooley DP : Bacteria recovered from patients admitted to a deployed U.S. military hospital in Baghdad, Iraq. Mil Med 2006 ; 171 : Petersen K, Riddle MS, Danko JR, et al : Trauma-related infections in battlefield casualties from Iraq. Ann Surg 2007 ; 245 : Ressner RA, Murray CK, Griffith ME, Rasnake MS, Hospenthal DR, Wolf SE : Outcomes of bacteremia in burn patients involved in combat operations overseas. J Am Coll Surg 2008 ; 206 : Griffith ME, Lazarus DR, Mann PB, Boger JA, Hospenthal DR, Murray CK : Acinetobacter skin carriage among US army soldiers deployed in Iraq. Infect Control Hosp Epidemiol 2007 ; 28 : Scott P, Deye G, Srinivasan A, et al : An outbreak of multi-drug resistant Acinetobacter baumannii-calcoaceticus complex infections in the U.S. military health-care system associated with military operations in Iraq. Clin Infect Dis 2007 ; 44 : Griffith ME, Ceremuga J, Ellis MW, Hospenthal DR, Murray CK : Acinetobacter skin colonization in US Army Soldiers. Infect Control Hosp Epidemiol 2006 ; 27 : MILITARY MEDICINE, Vol. 174, September 2009

5 7. Murray CK, Roop SA, Hospenthal DR, et al : Bacteriology of war wounds at the time of injury. Mil Med 2006 ; 171 : Moran KA, Murray CK, Anderson EL : Bacteriology of blood, wound and sputum cultures from non-us casualties treated in a US combat support hospital in Iraq. Infect Control Hosp Epidemiol 2009 ; 10: Landrum ML, Murray CK : Ventilator associated pneumonia in a military deployed setting: the impact of an aggressive infection control program. J Trauma 2008 ; 64 : S Fischer D, Veldman A, Diefenbach M, Schafer V : Bacterial colonization of patients undergoing international air transport: a prospective epidemiologic study. J Travel Med 2004 ; 11 : Naas T, Coignard B, Carbonne A, et al : VEB-1 extended-spectrum β-lactamase producing Acinetobacter baumannii, France. Emerg Infect Dis 2006 ; 12 : Hospenthal DR, Murray CK, Andersen RC, et al : Guidelines for the prevention of infection following combat-related injuries. J Trauma 2008 ; 64 (3 Suppl) : S MILITARY MEDICINE, Vol. 174, September