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Management of Initial Colonisations with Burkholderia Species in France

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Management of Initial Colonisations with Burkholderia Species in France Gruzelle et al. BMC Pulmonary Medicine (2020) 20:159 https://doi.org/10.1186/s12890-020-01190-y RESEARCH ARTICLE Open Access Management of initial colonisations with Burkholderia species in France, with retrospective analysis in five cystic fibrosis Centres: a pilot study Vianney Gruzelle1 , Hélène Guet-Revillet2,3, Christine Segonds3, Stéphanie Bui4, Julie Macey5, Raphaël Chiron6, Marine Michelet1, Marlène Murris-Espin7 and Marie Mittaine1* Abstract Background: Whereas Burkholderia infections are recognized to impair prognosis in cystic fibrosis (CF) patients, there is no recommendation to date for early eradication therapy. The aim of our study was to analyse the current management of initial colonisations with Burkholderia cepacia complex (BCC) or B. gladioli in French CF Centres and its impact on bacterial clearance and clinical outcome. Methods: We performed a retrospective review of the primary colonisations (PC), defined as newly positive sputum cultures, observed between 2010 and 2018 in five CF Centres. Treatment regimens, microbiological and clinical data were collected. Results: Seventeen patients (14 with BCC, and 3 with B. gladioli) were included. Eradication therapy, using heterogeneous combinations of intravenous, oral or nebulised antibiotics, was attempted in 11 patients. Six out of the 11 treated patients, and 4 out of the 6 untreated patients cleared the bacterium. Though not statistically significant, higher forced expiratory volume in 1 second and forced vital capacity at PC and consistency of treatment with in vitro antibiotic susceptibility tended to be associated with eradication. The management of PC was shown to be heterogeneous, thus impairing the statistical power of our study. Large prospective studies are needed to define whom to treat, when, and how. Conclusions: Pending these studies, we propose, due to possible spontaneous clearance, to check the presence of Burkholderia 1 month after PC before starting antibiotics, at least in the milder cases, and to evaluate a combination of intravenous beta-lactam + oral or intravenous fluoroquinolone + inhaled aminoglycoside. Keywords: Burkholderia cepacia complex, BCC, Burkholderia gladioli, Cystic fibrosis, Eradication * Correspondence: [email protected] 1CRCM pédiatrique, Service de Pneumo-Allergologie pédiatrique, Hôpital des Enfants, Centre Hospitalier Universitaire de Toulouse, 330 avenue de Grande-Bretagne - TSA 40031, 31059 Toulouse cedex 9, France Full list of author information is available at the end of the article © The Author(s). 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Gruzelle et al. BMC Pulmonary Medicine (2020) 20:159 Page 2 of 10 Background In this context, the aim of this preliminary study was The Burkholderia cepacia complex (BCC) is a group of to evaluate the current approach to new infections with 22 closely related species belonging to the Burkholderia Burkholderia in France, and the impact of potential genus, which are capable of colonising and infecting the eradication treatment on bacterial clearance and pul- respiratory epithelium of cystic fibrosis (CF) patients. monary outcomes. We present a 2010–2018 retrospect- Though asymptomatic carriage is possible, BCC organ- ive study in five CF Centres, including 17 patients. isms are associated with a marked increase in morbidity- mortality rates, due to rapid decline in lung function, ex- Methods tensive pneumopathy with life-threatening septicaemia Ethics statement (cepacia syndrome), as well as to poor lung transplant- The data collection process was reported to the Com- ation outcomes [1–3]. B. cenocepacia and B. multivorans mission Nationale Informatique et Liberté (French Data are the main species involved in North America and most Protection Authority) on 26/01/2018, under number European countries including France [3–6], whereas a 2146344v0. high prevalence of B. contaminans is observed in Ibero- American countries [7]. In the Iberian Peninsula,B.cepa- Patient recruitment and data collection cia and B. stabilis are more frequent than in other Euro- Five French CF Centres (3 paediatric and 2 adult Cen- pean countries [8, 9]. Several studies demonstrated faster tres), located in Toulouse, Montpellier and Bordeaux, as clinical deterioration, as well as lower survival after trans- well as the French OBC participated in the present pilot plantation in patients harbouring B. cenocepacia com- study. In all Centres, the microbiological analysis of spu- pared to those harbouring B. multivorans [2, 3, 10, 11]. tum samples was performed using a selective medium However, the spread of the ST180 strain of B. multivorans and a low detection level for Burkholderia species, ac- in a French CF Centre resulted in numerous cepacia syn- cording to the guidelines of the French Society for dromes and deaths (French Observatoire Burkholderia Microbiology [20]. Patients who acquired BCC or B. cepacia (OBC) data). The impact of other species of the gladioli between 01/01/2010 and 01/01/2018 were con- BCC is less documented, though adverse outcomes have sidered for retrospective analysis. The absence of Bur- also been reported [7, 12]. In the 1990s, highly transmis- kholderia from all sputum cultures during the two prior sible and often highly virulent strains were responsible for years was required for inclusion. The date of primary large outbreaks within CF communities [13–15]. Follow- colonisation (PC) was defined as the date of the first ing the implementation of infection control mea- positive sputum culture, and the primary isolate had to sures, patient-to-patient transmission decreased, and have been sent to the OBC for analysis. Patient data the distribution of BCC species was hence modified. were collected retrospectively from computerised re- Thus, in countries where B. cenocepacia was the gional registers and medical records in each CF Centre. most common species in the 1990s due to epidemic Baseline characteristics included gender, age, CFTR spread, B. multivorans currently outweighs B. cenoce- (Cystic Fibrosis Transmembrane conductance Regulator) pacia in new infections [3, 5, 6]. The impact of B. genotype, body mass index (BMI), best forced vital cap- gladioli colonisation is less clear, but abscesses and acity (FVC) and best forced expiratory volume in 1 sec- bacteraemia following lung transplantation have been ond (FEV1), as well as exocrine pancreatic insufficiency, reported [16, 17]. In Europe and the United States, insulin-dependent diabetes, nutritional support, liver cir- the current prevalence and incidence of BCC infec- rhosis, allergic broncho-pulmonary aspergillosis (ABPA), tions are about 2 and 0.5%, respectively, whereas the and need for systemic antibiotic treatment or corti- prevalence of B. gladioli is below 0.5% [4, 6]. cotherapy in the 3 months preceding PC. To assess lung Early eradication therapy of Pseudomonas aeruginosa function evolution, the FEV1 values 2 years after PC has been clearly proven to be a successful strategy to were recorded. postpone chronic infection. Conversely, studies evaluat- Microbiological data included the co-pathogens at PC ing the treatment of newly acquired BCC colonisations, (Pseudomonas aeruginosa, methicillin-susceptible and given their low incidence, are sparse and based on iso- methicillin-resistant Staphylococcus aureus, Achromo- lated case reports or small series, which are often incon- bacter spp., Stenotrophomonas maltophilia, Fungi and clusive [18]. There are no recommendations either Mycobacteria), the number of sputum cultures per- concerning the even rarer B. gladioli, though it is one of formed during the 2 years preceding and the 2 years fol- the most troublesome species during the peri- lowing PC, as well as the dates of the last positive and of transplantation period. Moreover, Burkholderia species the first negative cultures. The Burkholderia strains that are multi-drug resistant, which limits therapeutic op- were recovered only once (from the PC sputum), and tions, and in vitro susceptibility testing is considered to never during the follow-up period, were defined as single be poorly reliable [19]. isolates. Gruzelle et al. BMC Pulmonary Medicine (2020) 20:159 Page 3 of 10 When eradication therapy directed against Burkhol- using theoretical aspects for qualitative variables. deria was implemented, onset date, molecules used, Comparisons of quantitative variables were performed routes of administration, and duration were recorded. using the Student test, or the Mann-Whitney non- parametric test if the
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