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ORIGINAL ARTICLES

Pseudomonas aeruginosa
An Uncommon Cause of Diabetic Foot Infection
Heather Young, MD*
Bryan Knepper, MS, MPH†
Whitney Hernandez, NP‡
Asaf Shor, MD, MPH§
Merribeth Bruntz, DPM||
Chrystal Berg, DPM||
Connie S. Price, MD*
Background: Pseudomonas aeruginosa has traditionally been considered a common
pathogen in diabetic foot infection (DFI), yet the 2012 Infectious Diseases Society of
America guideline for DFI states that ‘‘empiric therapy directed at P aeruginosa is
usually unnecessary.’’ The objective of this study was to evaluate the frequency of P
aeruginosa isolated from bone or tissue cultures from patients with DFI.
Methods: This study is a cross-sectional survey of diabetic patients presenting with a
foot infection to an urban county hospital between July 1, 2012, and December 31, 2013.
All of the patients had at least one debridement procedure during which tissue or bone
cultures from operative or bedside debridements were obtained. The v2 test and the t
test of means were used to determine relationships between variables and the frequency
of P aeruginosa in culture.
Results: The median number of bacteria isolated from DFI was two. Streptococcus spp
and Staphylococcus aureus were the most commonly isolated organisms; P aeruginosa
was isolated in only five of 112 patients (4.5%). The presence of P aeruginosa was not
associated with the patient’s age, glycosylated hemoglobin level, tobacco abuse, the
presence of osteomyelitis, a prescription for antibiotic drugs in the preceding 3 months,
or the type of operative procedure.
Conclusions: Pseudomonas aeruginosa was an infrequent isolate from DFI in this
urban, underserved diabetic population. The presence of P aeruginosa was not
associated with any measured risk factors. By introducing a clinical practice guideline,
we hope to discourage frontline providers from using routine antipseudomonal antibiotic
drugs for DFI. (J Am Podiatr Med Assoc 105(2): 125-129, 2015)

Pseudomonas aeruginosa has traditionally been
considered a common pathogen in diabetic foot
infection (DFI), and it accounts for 9.3% to 31% of
DFI in the literature.1-12 However, the importance of
*Division of Infectious Diseases, Denver Health Medical
Center and University of Colorado Denver, Aurora, CO.
†Department of Patient Safety and Quality, Denver Health
Medical Center, Denver, CO.
‡Division of Infectious Diseases, Denver Health Medical
Center, Denver, CO.
§Division of Infectious Diseases, University of Colorado
Denver, Aurora, CO.
||Department of Orthopedic Surgery, Denver Health Medical Center and University of Colorado Denver, Aurora, CO.
Corresponding author: Heather Young, MD, Denver
Health Medical Center, 660 Bannock St, MC 4000, Denver,
CO 80204. (E-mail: Heather.Young2@dhha.org)

this pathogen has recently been questioned. The
2012 Infectious Diseases Society of America (IDSA)
guideline for DFIs states that ‘‘empiric therapy
directed at P aeruginosa is usually unnecessary
except for patients with risk factors for true
infection with this organism.’’13(p. e147) Risk factors
cited by the IDSA for P aeruginosa include a high
local prevalence of P aeruginosa infection, a warm
climate, and frequent exposure of the foot to
water.13
The IDSA recommendation is based on three
factors. First, the incidence of P aeruginosa as a
cause of DFI in developed countries outside of the
tropics seems to be low.1,2 Second, there is
increasing evidence that clinical cure of polymicro-

Journal of the American Podiatric Medical Association ! Vol 105 ! No 2 ! March/April 2015

125

2012. and antibiotic drugs prescribed in the 3 months before DFI culture.14-17 Third. erythema must be 0. erythema. The National Healthcare Safety Network defines osteomyelitis as 1) organisms cultured from bone.000 cells/lL. all of the wound swabs were excluded from the analyses. Definitions The IDSA infection severity criteria were used to classify DFIs in this study. Microbiological Methods Tissue or bone specimens were obtained by operative or bedside debridement. Methods Study Setting and Population This study is a cross-sectional survey of diabetic patients presenting with a foot infection to an urban county hospital in Denver.5 to 2 cm around the ulcer. Moderate infections are those involving structures deeper than the subcutaneous tissue or erythema greater than 2 cm. pathology results. In addition. Transmetatarsal amputation consisted of all five metatarsals transected at the midshaft or proximal. Aerobic media plates were incubated at 358C and checked daily for growth for 5 days.388C. a positive laboratory blood test result. Metatarsal amputation included a partial or full amputation of a digit plus a portion of the corresponding metatarsal. 2) evidence of osteomyelitis on direct examination of the bone during an invasive procedure or histopathologic examination. tenderness. Variables of interest included demographic information. between June 1.13 The National Healthcare Safety Network criteria were used to diagnose osteomyelitis.18 Toe amputation was defined as any partial or full amputation of a digit. Isolates were identified using biochemical testing. March/April 2015 ! Vol 105 ! No 2 ! Journal of the American Podiatric Medical Association . surgical management. Severe infections are defined as a local infection plus at least two signs of systemic inflammation. radiology results. The IDSA defines infections by the presence of at least two of the following items: local swelling or induration. local tenderness or pain. or drainage at the suspected site of bone infection) plus an organism cultured from blood. local warmth. Microbiological specimens included bone and tissue swabs. heart rate greater than 90/ min.000 or less than 4.13 Some patients presented with more than one distinct episode of DFI during the study period. Incision and debridement was a surgical procedure that did not include amputation of bone but may have included bone biopsy.bial skin and soft-tissue infections that include P aeruginosa can occur in the absence of antibiotic agents that cover this organism. medical and social history. localized swelling. to avoid sampling bias. or an imaging test with evidence of infection. and 126 leukocyte count greater than 12. Mild infections are defined as those including the skin and subcutaneous tissue without involvement of deeper tissues. Children younger than 18 years were excluded from the study. 2013. Colorado. and December 31. and were set up for both aerobic and anaerobic bacterial cultures. patients must have undergone at least one debridement procedure. Patients were eligible for inclusion if they were diabetic and were referred to the orthopedic infectious diseases consultation service or the outpatient musculoskeletal infections clinic for evaluation of a suspected foot infection. heat. either at the bedside or in the operating room. or 3) the presence of at least two signs of infection (fever . subsequent DFIs were excluded. and purulent discharge. microbiology specimen types and results. including temperature greater than 388C or less than 368C.19 Incomplete information was manually reconciled through review of the medical record. respiratory rate greater than 20/min. Specimens were transported to the clinical microbiology laboratory in sterile containers. P aeruginosa often is a colonizer of open wounds. as were patients who were found to have an uninfected foot wound according to the IDSA classification. The objective of this study was to determine the frequency with which P aeruginosa was isolated from patients hospitalized with DFI. Calcaneal debridement included partial or full resection of the calcaneus. This information may then be used to determine whether antipseudomonal antibiotic drug therapy is indicated for DFI at this facility. Anaerobic media plates were incubated at 358C in an anaerobic environment and checked daily for growth beginning on the second day for 5 days. Data Collection Data were prospectively entered into a research electronic data capture database developed for use in patient tracking and monitoring. were processed per routine laboratory protocol.

[%]) Streptococcus 54 (48.3%–9. North Carolina). or location of operative intervention (Table 2). 15. 112 patients were included in the analyses. glycosylated hemoglobin level. We hope that this guideline will assist frontline providers in minimizing unnecessary broad-spec- Journal of the American Podiatric Medical Association ! Vol 105 ! No 2 ! March/April 2015 127 . Authors from underdeveloped tropical countries report higher rates of P aeruginosa in DFIs (12%–31%)3-12 than authors in nontropical developed countries (9. and calcaneal debridement (n ¼ 3.7%). The v2 test was used to determine whether there were associations between categorical variables and outcomes of interest. Relatively few antibiotic drugs cover this organism.9) Enterococcus 16 (14. Enterobacteriaceae were present in 21.5) 41 (36.2%). Results One hundred thirty patients with suspected DFI were referred to the orthopedic infectious diseases consultation service or the musculoskeletal infections clinic during the study period. 25. and an additional five had only a wound swab. IDSA infection classification. and carbapenems. underserved diabetic population in the United States. transmetatarsal amputation (n ¼ 17.2) Staphylococcus aureus 48 (42. respectively.20 Our facility has developed a clinical practice guideline for DFI approved by a multidisciplinary group of physicians. Bacteria Isolated from Bone and Tissue Cultures of 112 Patients with a Diabetic Foot Infection Bacteria Patients (No. all of the P aeruginosa infections were polymicrobial.1) 1 organism 28 (25. Eighty patients (71. Twenty-seven patients (24. Substantial variation in the incidence of P aeruginosa is present in the literature.3) #5 organisms 5 (4. Pseudomonas aeruginosa can be a difficult bacterium to treat. metatarsal amputation (n ¼ 29.9 years and a mean glycosylated hemoglobin level of 9. and commonly used antipseudomonal antibiotic agents. the presence of osteomyelitis. 35.4% of DFIs.5) pathogens. Other Table 1. tobacco abuse.Statistical Analysis Descriptive statistics were used to determine the frequency of isolates present in DFIs. antibiotic drugs prescribed in the preceding 3 months. the rate of P aeruginosa in this study population is even lower than that in previous reports. fourth-generation cephalosporins. This study was unable to determine risk factors for P aeruginosa because the number of patients presenting with P aeruginosa DFI was insufficient to make statistical inferences.3 (SAS Institute Inc.0) 2 organisms 32 (28. Thirteen patients were found to be uninfected by IDSA classification.5%).1. The median number of isolates per patient with DFI was two.5) 4 organisms 16 (14.6) 3 organisms 23 (20. not tissue or bone.9) Coagulase-negative staphylococcus 48 (42.8%).1%) used tobacco. the t test of means was used to evaluate continuous variables and the outcomes of interest. such as fluoroquinolones.4) Pseudomonas aeruginosa Anaerobic bacteria 5 (4. whereas P aeruginosa was isolated from only five patients (4. Discussion Pseudomonas aeruginosa was a relatively uncommon cause of DFI in this urban. incision and drainage (n ¼ 23. Cary. present in 48. of organisms Culture negative 8 (7.4%) were diagnosed as having osteomyelitis.5%) with DFI (Table 1).2 Although the present data are more consistent with those of other authors from developed countries. With the low incidence of P aeruginosa and evidence that clinical cure of polymicrobial P aeruginosa DFI may not require antipseudomonal antibiotic drugs. Streptococcus spp and Staphylococcus aureus were the most commonly isolated organisms. Clinical practice guidelines standardize care for common conditions and have been shown to decrease unnecessary antibiotic drug use. Surgical procedures included toe amputation (n ¼ 40. are broad-spectrum agents. Thus.9% of DFIs. 28 infections (25.0%) were due to a single organism. 20. homelessness. The Colorado Multiple Institutional Review Board deemed this study exempt from human subjects review.14-17 we are faced with how to change the prescribing practices of frontline providers. such as Streptococcus and S aureus were more prevalent.2% and 42.6) No. All of the analyses were performed using SAS version 9.9%).7%). sent for microbiologic culture. 2. The presence of P aeruginosa was not associated with the patient’s age.3) Enterobacteriaceae 24 (21. Patients had a mean age of 55.5%.

9) Moderate 3 (60. By introducing a clinical practice guideline.3) Surgical procedure (No. 2010.0) 27 (25.5) 0.0 (9.4) Metatarsal amputation 2 (40. KHADKA PB. Conflict of Interest: None reported. multi-center study: factors related to the management of diabetic foot infections. Kathmandu Univ Med J (KUMJ) 4: 295.6 (2.35 3 (60. J Microbiol Immunol Infect 40: 39. 2005. 2000.Table 2.13 b trum antibiotic drug exposure while still ensuring optimal patient outcomes. 1.0) Calcaneal debridement 0 Soft-tissue debridement 1 (20. ABDULRAZAK A.0) 3 (2. AKBAY E. ONCUL O. KANDEMIR O.6) 0. J Infect 54: 439.13 3 (60. Saudi Med J 21: 344. [%]) 0. [%]) 2 (40. [%]) Osteomyelitis (No. 2009.2) 56. GARG A.0) 42 (39.0) 25 (23. CITRON DM. ET AL: Spectrum of microbial flora in diabetic foot ulcers. J Diabetes Complications 19: 138.0) Antibiotic drug use in the preceding 3 months (No. MARTINEZ-GOMEZ DDE A. SHARMA VK. ET AL: Bacteriology of moderate-to-severe diabetic foot infections and in 128 9. TABAK YP.[(%]) a Infection severity (No. ET AL: Common pathogens isolated in diabetic foot infection in Bir Hospital.0) 15 (14.95 Mild 0 2 (1. Patient Characteristics with and Without Pseudomonas aeruginosa Isolated from Deep Tissue Culture of Diabetic Foot Infection Variable Age (mean 6 SD [years]) Glycosylated hemoglobin (mean 6 SD [%]) Infections with P aeruginosa (n ¼ 5) Infections Without P aeruginosa (n ¼ 107) 54. 2007. ERTUGRUL BM. We are unable to determine whether P aeruginosa is a common pathogen in mild DFI.8) 22 (20. ET AL: A prospective. 5. 2. ET AL: Bacteriological study of diabetic foot infections. Diabetologia 53: 914. GOLDSTEIN EJ. AL-SHAMALI AA.0) 77 (72. Enferm Infecc Microbiol Clin 27: 317.2) Transmetatarsal amputation 2 (40. ET AL: Diabetic foot infections: prevalence and antibiotic sensitivity of the causative microorganisms [in Spanish]. 2012. Financial Disclosure: None reported.0) 63 (58. underserved diabetic population. CAMPILLOSOTO A.34 Toe amputation 0 40 (37. RAJA NS: Microbiology of diabetic foot infections in a teaching hospital in Malaysia: a retrospective study of 194 cases.18 Infectious Diseases Society of America classification. MERRIAM CV. ET AL: Risk factors for infection of the diabetic foot with multi-antibiotic resistant microorganisms.5) 0. J Clin Microbiol 45: 2819.7) 9. Limiting the use of antipseudomonal antibiotic drugs may also help prevent the emergence of resistant gram-negative bacteria at this facility.62 0. Eur J Clin Microbiol Infect Dis 31: 2345. ET AL: Skin and soft tissue infections in hospitalised patients with diabetes: culture isolates and risk factors associated with mortality. [%]) 2 (40. 7. length of stay and cost. 8.21. JOHANNES RS. Conclusions This study finds P aeruginosa to be a rare isolate from DFIs in an urban. References 10. LIPSKY BA. vitro activity of antimicrobial agents.4) 0.95 9. 2008. JOSHI A. we hope to discourage frontline providers from routinely prescribing antipseudomonal antibiotic agents for DFIs. 3. BITAR ZI.0) 38 (35.0) 13 (12.1) 0.1 (1.59 Homeless (No. BANSAL E. 6. 2006. 2007. TULEK N. EL-TAHAWY AT: Bacteriology of diabetic foot. Most cases included in this study were moderate and severe DFIs that required surgical intervention.6) a National Healthcare Safety Network definition. The presence of P aeruginosa was not associated with any measured risk factors.22 This study is limited by referral bias. SAHIN E. [%])b 0. RAMIREZ-ALMAGRO C.8 (9.69 P Value Tobacco abuse (No. BHATIA S. 4. March/April 2015 ! Vol 105 ! No 2 ! Journal of the American Podiatric Medical Association . 2007. Indian J Pathol Microbiol 51: 204.9) Severe 2 (40.

2008. 19. MOHAN V. LIPSKY BA. LUCASTI C. 2013. BOUTOILLE D. Clin Infect Dis 38: 17. 2005. SHANKAR EM. IRWIN A. double-blind multicenter study. Journal of the American Podiatric Medical Association ! Vol 105 ! No 2 ! March/April 2015 129 . ET AL: Ertapenem once daily versus piperacillin-tazobactam 4 times per day for treatment of complicated skin and skin-structure infections in adults: results of a prospective. Clin Infect Dis 34: 1460. CARMELI Y. 2012. Clin Infect Dis 46: 647. J Infect Public Health 5: 1. randomised. Lancet 366: 1695. HARRIS PA. Clin Infect Dis 54: e132. ROTIMI VO: A study of the microbiology of diabetic foot infections in a teaching hospital in Kuwait. Available at: http://www. BUSH K. Int J Infect Dis 17: e254. J Biomed Informatics 42: 377. 20. GOTTESMAN BS. 14.cdc. OLLIVIER F. LIPSKY BA. ET AL: Treating foot infections in diabetic patients: a randomized. PREMALATHA G. 18. NORDEN C. GRAHAM DR.gov/nhsn/PDFs/ pscManual/17pscNosInfDef_current. SHITRIT P. CORNIA PB. ET AL: Research electronic data capture (REDCap): a metadata-driven methodology and workflow process for providing translational research informatics support. doubleblind trial comparing ceftobiprole medocaril with vancomycin plus ceftazidime for the treatment of 17. JENKINS TC. 2012. CDC/NHSN surveillance definitions for specific types of infections. BERENDT AR. BAGCHI P. patients with complicated skin and skin-structure infections. 2013. Am J Med 126: 327. ARMSTRONG DG.11. 2009. 15. 13. controlled. Accessed October 10. 2002. 16. ET AL: Impact of quinolone restriction on resistance patterns of Escherichia coli isolated from urine by culture in a community setting. ET AL: A randomized. BATARD E. 2009. randomized. 2005. TAYLOR R. ET AL: Relationship between hospital antibiotic use and quinolone resistance in Escherichia coli. 12. Eur J Int Med 16: 567. 2004. double-blinded. ET AL: Bacterial etiology of diabetic foot infections in South India. ET AL: Ertapanem versus piperacillin/tazobactam for diabetic foot infections (SIDESTEP): prospective. AL MULLA A. multicentre trial. ET AL: 2012 Infectious Diseases Society of America clinical practice guideline for the diagnosis and treatment of diabetic foot infections. ET AL: Effects of clinical pathways for common outpatient infections on antibiotic prescribing. CITRON DM. AL BENWAN K.pdf. COOMBS L. THIELKE R. open-label trial of linezolid versus ampicillinsulbactam/amoxicillin-clavulanate. 21. 22. LIPSKY BA. ITANI K. NOEL GJ. multicenter. 2013. MALAFAIA O. Clin Infect Dis 49: 869.