Recurrent environmental contamination in a centralized radiopharmacy unit by Achromobacter spp: Results of a large microbiological investigation


      • Old plastic containers present high risk of biocontamination if not changed regularly
      • To look for a reservoir, choosing the most adapted sampling method is essential
      • Finding the starting point of a biocontamination is a major help in controlling it
      • Achromobacter spp can survive in micro-cracks of plastic buckets



      Radiopharmaceuticals preparation unit, such as every aseptic preparation units, are strictly monitored in terms of microbiological contamination. Despite all biocontamination control procedures, our radiopharmacy unit faced repeated environmental contamination by Achromobacter spp which necessitated a large environmental investigation.


      Microbiological controls were carried out using Count Tact agars (Biomérieux) for flat surfaces, dry swabbing for hard to reach areas and containers were filled with a sterile water solution (then filtrated on 0.45 µm membrane and seeded). Microbiological identification was performed by mass spectrometry (MALDI-TOF-MS, Brucker) on each positive sample.


      Achromobacter spp was found in 10% of the 413 samples during the 8 months investigation period. The proportion of positive samples was stable among time but their location was unpredictable. The highest inoculum was finally found in the buckets used for biocleaning.


      Samples from cleaning buckets taken by dry swabbing were at first negative, but the use of a non-routinely used sampling method allowed to discover the reservoir of this persistent contamination.


      This investigation alerted us on the high microbiological risk associated with reusable plastic containers and the importance of a sampling method adapted to critical locations.

      Key Words

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'


      Subscribe to American Journal of Infection Control
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect


      1. European Direction for Quality of Medicines and Healthcare, European Pharmacopoeia, 9th Edition, 2018

      2. National Agency for Safety of Medicines and Health Products. Good Manufacturing Practices. Official bulletin. N2015/12:bis.

        • French Agency for Safety of Health Products
        Good Preparation Practices.
        Official Journal. 2007;
        • Ministry for employment and solidarity
        Good Hospital Pharmacy Practices.
        Official Journal. 2001;
      3. European Commission. EU guidelines to good manufacturing practice medicinal products for human and veterinary use. eudralex : the rules governing medicinal products in the European Union; 1989.

        • Elsinga P
        • Todde S
        • Penuelas I
        • et al.
        Guidance on current good radiopharmacy practice (cGRPP) for the small-scale preparation of radiopharmaceuticals.
        Eur J Nucl Med Mol Imaging. 2010; 37 (1 mai): 1049-1062
        • Bruel D
        • Duez C
        • Ebel-Lao S
        • Garrigue H
        • Le Meur C
        Guide de surveillance de l'environnement des unités de préparation des médicaments radiopharmaceutiques de la Société française de radiopharmacie.
        Pharm Hosp. 2011; 46 (1 mars): 45-52
        • Bador J.
        Résistance aux antibiotiques par mécanisme d’efflux chez Achromobacter xylosoxidans [Internet] [phdthesis].
        Université de Bourgogne, Dijon, France2013 ([cité 2 juill 2021]Disponible sur:)
        • Spear JB
        • Fuhrer J
        • Kirby BD.
        Achromobacter xylosoxidans (Alcaligenes xylosoxidans subsp. xylosoxidans) bacteremia associated with a well-water source: case report and review of the literature.
        J Clin Microbiol. 1988; 26 (mars): 598-599
        • Holmes B
        • Snell JJ
        • Lapage SP.
        Strains of Achromobacter xylosoxidans from clinical material.
        J Clin Pathol. 1977; 30 (juill): 595-601
        • Wu G
        • Liu J
        • Ye Z.
        Characterization of phosphobacteria isolated from eutrophic aquatic ecosystems.
        Mikrobiologiia. 2009; 78 (déc): 809-815
        • Ho YN
        • Mathew DC
        • Hsiao SC
        • et al.
        Selection and application of endophytic bacterium Achromobacter xylosoxidans strain F3B for improving phytoremediation of phenolic pollutants.
        J Hazard Mater. 2012; 219-220 (15 juin): 43-49
        • Lambiase A
        • Catania MR
        • Del Pezzo M
        • et al.
        Achromobacter xylosoxidans respiratory tract infection in cystic fibrosis patients.
        Eur J Clin Microbiol Infect Dis Off Publ Eur Soc Clin Microbiol. 2011; 30 (août): 973-980
        • Firmida MC
        • Pereira RHV
        • Silva EASR
        • Marques EA
        • Lopes AJ.
        Clinical impact of Achromobacter xylosoxidans colonization/infection in patients with cystic fibrosis.
        Braz J Med Biol Res [Internet]. 2016; 49 (23 févr[cité 5 déc 2018 ]Disponible sur)
        • Hugon E
        • Marchandin H
        • Poirée M
        • Fosse T
        • Sirvent N.
        Achromobacter bacteraemia outbreak in a paediatric onco-haematology department related to strain with high surviving ability in contaminated disinfectant atomizers.
        J Hosp Infect. févr. 2015; 89: 116-122
        • Dupont C
        • Michon AL
        • Jumas-Bilak E
        • Nørskov-Lauritsen N
        • Chiron R
        • Marchandin H.
        Intrapatient diversity of Achromobacter spp. involved in chronic colonization of Cystic Fibrosis airways.
        Infect Genet Evol J Mol Epidemiol Evol Genet Infect Dis. 2015; 32 (juin): 214-223
        • Reverdy ME
        • Freney J
        • Fleurette J
        • et al.
        Nosocomial colonization and infection by Achromobacter xylosoxidans.
        J Clin Microbiol. 1984; 19 (févr): 140-143
        • Turel O
        • Kavuncuoglu S
        • Hosaf E
        • et al.
        Bacteremia due to Achromobacter xylosoxidans in neonates: clinical features and outcome.
        Braz J Infect Dis. 2013; 17 (août): 450-454
        • Haviari S
        • Cassier P
        • Dananché C
        • et al.
        Outbreak of achromobacter xylosoxidans and ochrobactrum anthropi infections after prostate biopsies, France, 2014.
        Emerg Infect Dis. 2016; 22 (août): 1412-1419
        • Molina-Cabrillana J
        • Santana-Reyes C
        • González-García A
        • Bordes-Benítez A
        • Horcajada I.
        Outbreak of Achromobacter xylosoxidans pseudobacteremia in a neonatal care unit related to contaminated chlorhexidine solution.
        Eur J Clin Microbiol Infect Dis Off Publ Eur Soc Clin Microbiol. 2007; 26 (juin): 435-437
        • Tena D
        • Carranza R
        • Barberá J
        • et al.
        Outbreak of long-term intravascular catheter-related bacteremia due to Achromobacter xylosoxidans subspecies xylosoxidans in a hemodialysis unit.
        Eur J Clin Microbiol Infect Dis Off Publ Eur Soc Clin Microbiol. 2005; 24 (1 déc): 727-732
        • Günther F
        • Merle U
        • Frank U
        • Gaida MM
        • Mutters NT
        Pseudobacteremia outbreak of biofilm-forming Achromobacter xylosoxidans – environmental transmission.
        BMC Infect Dis. 2016; 16 (19 oct): 584
        • Amoureux L
        • Bador J
        • Fardeheb S
        • et al.
        Detection of achromobacter xylosoxidans in hospital, domestic, and outdoor environmental samples and comparison with human clinical isolates.
        Appl Environ Microbiol. 2013; 79 (13 sept): 7142-7149
        • Abdouchakour F
        • Dupont C
        • Grau D
        • et al.
        Pseudomonas aeruginosa and achromobacter sp. clonal selection leads to successive waves of contamination of water in dental care units. Schottel JL, éditeur.
        Appl Environ Microbiol. 2015; 81 (1 nov): 7509-7524
        • Marion-Sanchez K
        • Olive C
        • Platon MG
        • Cesarine M
        • Derancourt C
        • Pailla K.
        Achromobacter xylosoxidans in hospital environments: still waters run deep!.
        Trans R Soc Trop Med Hyg. 2020; 114 (1 juin): 470-472
        • Hugon E
        • Marchandin H
        • Poirée M
        • Fosse T
        • Sirvent N.
        Achromobacter bacteraemia outbreak in a paediatric onco-haematology department related to strain with high surviving ability in contaminated disinfectant atomizers.
        J Hosp Infect. 2015; 89 (févr): 116-122
        • Vu-Thien H
        • Darbord JC
        • Moissenet D
        • et al.
        Investigation of an outbreak of wound infections due to alcaligenes xylosoxidans transmitted by chlorhexidine in a Burns unit.
        Eur J Clin Microbiol Infect Dis. 1998; 17 (1 nov): 724-726
        • Reina J
        • Antich M
        • Siquier B
        • Alomar P.
        Nosocomial outbreak of Achromobacter xylosoxidans associated with a diagnostic contrast solution.
        J Clin Pathol. 1988; 41 (août): 920-921
        • Siebor E
        • Llanes C
        • Lafon I
        • et al.
        Presumed pseudobacteremia outbreak resulting from contamination of proportional disinfectant dispenser.
        Eur J Clin Microbiol Infect Dis. 2007; 26 (6 mars): 195-198
        • Shigeta S
        • Yasunaga Y
        • Honzumi K
        • Okamura H
        • Kumata R
        • Endo S.
        Cerebral ventriculitis associated with Achromobacter xylosoxidans.
        J Clin Pathol. 1978; 31 (févr): 156-161
        • Karen Olshtain-Pops
        • Colin Block
        • Violeta Temper
        • et al.
        An outbreak of achromobacter xylosoxidans associated with ultrasound gel used during transrectal ultrasound guided prostate biopsy.
        J Urol. 2011; 185 (1 janv): 144-147
        • Chang JML
        • McCanna DJ
        • Subbaraman LN
        • Jones LW.
        Efficacy of antimicrobials against biofilms of achromobacter and pseudomonas.
        Optom Vis Sci. 2015; 92 (avr): 506-513
        • Weber DJ
        • Rutala WA
        • Sickbert-Bennett EE.
        Outbreaks associated with contaminated antiseptics and disinfectants.
        Antimicrob Agents Chemother. 2007; 51 (déc): 4217-4224
        • Sauer K
        • Rickard A
        • Davies D.
        Biofilms and biocomplexity.
        Microbe Wash DC. 2007; 2 (1 juill): 347-353