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Successful outbreak investigation of Burkholderia cepacia complex bacteremia in intensive care patients

Published:March 21, 2014DOI:https://doi.org/10.1016/j.ajic.2013.12.015
      To the Editor:
      Bulkholderia cepacia complex (Bcc) is a group of ubiquitous gram-negative aerobic bacilli found in plants, soil, and moist environments. Bcc is well described as a cause of respiratory infections in patients with cystic fibrosis and chronic granulomatous disease. Bcc bacteremia and nosocomial pneumonia have also been observed in intensive care patients as sporadic cases or during outbreaks.
      Here, we describe a small outbreak of nosocomial Bcc bacteremia in the 6-bed intensive care unit (ICU) of an 850-bed university-affiliated general hospital in Jerusalem, Israel. During July 2010, a patient admitted to our ICU because of congestive heart failure and pulmonary edema developed Burkholderia bacteremia. She was treated according to bacterial sensitivity with no attributable consequences. Several days later, a second patient in our ICU, hospitalized with severe immune thrombocytopenia and pulmonary hemorrhage, was found to have Burkholderia bacteremia. Repeated blood cultures were positive, and bacteremia resolved after an appropriate antibiotic was initiated. The patients had no known risk factors for Burkholderia infection and no obvious source for the bacteremia was found.
      After the second case an outbreak investigation was conducted. We detected 2 more patients who had bacteremia with Burkholderia in 2010; 1 of these was a third patient in the same ICU 3 months earlier, and the fourth was a patient in our thoracic heart surgery ICU. We concluded that we were facing an outbreak of Burkholderia bacteremia.
      Because Burkholderia is a waterborne and soilborne organism that can survive for a prolonged period in a moist environment, we sampled wet and humid products that had been used during care of the 2 index cases. We cultured inhalation solutions (ie, ipratropium bromide, albuterol, and water used in the nebulizer), insulin, heparin, erythromycin, piperacillin-tazobactam, water for injection, potassium chloride solution, hygiene products (eg, povidone, hand rub gel, chlorhexidine, and superoxide solution), and patient care products (eg, mouthwash and moisturizing cream).
      All items were sterile except for the moisturizing cream of both patients, which was contaminated with Burkholderia. Each patient in our ICU had an individual cream tube. We examined the cream tubes of 2 other patients residing in our ICU at the same time and found that their cream was also contaminated with Burkholderia. Subsequently, we cultured 6 new, sealed cream tubes from our ICU and other departments in our hospital, and found 3 were contaminated with the same bacteria.
      All clinical and environmental isolates of Burkholderia were isolated and identified by 16S ribosomal DNA sequencing at the Shaare Zedek Microbiology laboratory. For further identification, the specimens were sent to the Observatoire Cepacia, Laboratoire de Bactériologie-Hygiène Hôpital Purpan, Toulouse, France. Identification of the species level was performed by means of amplified 16S ribosomal DNA restriction analysis,
      • Segonds C.
      • Heulin T.
      • Marty N.
      • Chabanon G.
      Differentiation of Burkholderia species by PCR-restriction fragment length polymorphism analysis of the 16S rRNA gene and application to cystic fibrosis isolates.
      RecA species-specific polymerase chain reaction (PCR),
      • Mahenthiralingam E.
      • Bischof J.
      • Byrne S.
      • Radomski C.
      • Davies J.
      • Av-Gay Y.
      • et al.
      DNA-Based diagnostic approaches for identification of Burkholderia cepacia complex, Burkholderia vietnamiensis, Burkholderia multivorans, Burkholderia stabilis, and Burkholderia cepacia genomovars I and III.
      and/or RecA sequencing.
      • Baldwin A.
      • Mahenthiralingam E.
      • Thickett K.M.
      • Honeybourne D.
      • Maiden M.C.
      • Govan J.R.
      • et al.
      Multilocus sequence typing scheme that provides both species and strain differentiation for the Burkholderia cepacia complex.
      Genetic relatedness was assessed using PCR ribotyping.
      • Dasen S.E.
      • LiPuma J.J.
      • Kostman J.R.
      • Stull T.L.
      Characterization of PCR-ribotyping for Burkholderia (Pseudomonas) cepacia.
      Blood isolates were identified as B cenocepacia IIIB (patient 1) and B stabilis (patient 2) (Table 1). Twelve cream samples were found to be contaminated with Burkholderia species, 9 with the same strain of B contaminans, and 3 with the same strain of B cenocepacia IIIB, which harbored the same PCR ribotype as the isolate from the moisturizing cream of patient 1. The moisturizing cream was withdrawn from all hospital departments and notification was made to the manufacturer and to the Israeli Ministry of Health. No new cases occurred. The manufacturer identified lapses in the water filtration system as the cause of contamination. Two-year follow-up showed no additional Burkholderia bacteremia in our institution.
      Table 1Microbiology test results of patients' and moisturizing creams' samples with growth of Burkholderia
      DateSample16S rDNA identificationARDRA identificationRecA gene identificationRibotyping identification
      July 28, 2010Blood – patient 1B cepaciaB stabilis/pyrrociniaB stabilisND
      August 3, 2010Blood – patient 2B cepaciaB cepacia/cenocepaciaB cenocepacia IIIBJ1
      August 8, 2010Patient 1's creamNDB cepacia/cenocepaciaB cepacia complexJ2
      August 12, 2010Patient 2's creamNDB cepacia/cenocepaciaB cenocepacia IIIBJ1
      August 12, 2010Patient 3's creamNDB cepacia/cenocepaciaB cenocepacia IIIAJ2
      August 12, 2010Patient 4's creamNDB cepacia/cenocepaciaB cepacia complexJ2
      August 12, 2010Sealed cream - ICUNDB cepacia/cenocepaciaB cenocepacia IIIBJ1
      August 15, 2010Sealed cream - ICUNDNDB cepacia complexJ2
      August 15, 2010Sealed cream - orthopedic departmentNDB cepacia/cenocepaciaB cepacia complexJ2
      August 15, 2010Sealed cream - internal medicine A departmentNDB cepacia/cenocepaciaB cepacia complexJ2
      August 15, 2010Sealed cream - internal medicine B departmentNDB cepacia/cenocepaciaB cepacia complexJ2
      August 16, 2010Sealed cream - oncology departmentNDNDB cenocepacia IIIBJ1
      August 16, 2010Sealed cream - internal medicine A departmentNDNDB cepacia complexJ2
      August 16, 2010Sealed cream - pharmacyNDNDNDJ2
      ARDRA, amplified 16S rDNA restriction analysis; ICU, intensive care unit; ND, not done; rDNA, ribosomal DNA.
      We suspect the cause of the outbreak was moisturizing cream contaminated with at least 2-3 different B cepacia genomovars that had most probably occurred during manufacturing. Moisturizing cream was described once before as a cause of Burkholderia infections in an ICU.
      • Alvarez-Lerma F.
      • Maull E.
      • Terradas R.
      • Segura C.
      • Planells I.
      • Coll P.
      • et al.
      Moisturizing body milk as a reservoir of Burkholderia cepacia: outbreak of nosocomial infection in a multidisciplinary intensive care unit.
      The strain in the first patient with Burkholderia bacteremia was identified as B stabilis by amplified 16S ribosomal DNA restriction analysis and RecA gene methods. Although this genomovar was not found in the moisturizing creams, we believe this case was also caused by using contaminated cream because of polygenomovar contamination of the cream boxes.
      Although cosmetic products such as moisturizing cream are not required to be sterile if they are used solely topically, manufacturers are obligated to maintain high standards of control and are regulated by the Scientific Committee on Cosmetic Products and Non Food Products

      Scientific Committee on Cosmetic Products and Non Food Products' notes of guidance for the testing of cosmetic ingredients and their safety evaluation, 5th revision, 2003, SCCNFP/0690/03 final. http://ec.europa.eu/health/ph_risk/committees/sccp/documents/out242_en.pdf. Accessed January 13, 2014.

      (available online at http://ec.europa.eu/health/ph_risk/committees/sccp/documents/out242_en.pdf), and other national regulations. In the face of the numerous publications citing Burkholderia as a cause of outbreaks amongst vulnerable hospitalized patients, we believe that national and international regulations should require the absence of any Burkholderia species in products used for these patients. We also suggest avoiding the use of nonsterile cosmetics products in special populations, such as ICU patients and immune-compromised patients, while hospitalized.

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      1. Scientific Committee on Cosmetic Products and Non Food Products' notes of guidance for the testing of cosmetic ingredients and their safety evaluation, 5th revision, 2003, SCCNFP/0690/03 final. http://ec.europa.eu/health/ph_risk/committees/sccp/documents/out242_en.pdf. Accessed January 13, 2014.