Chest physiotherapy enhances detection of Pseudomonas aeruginosa in nonexpectorating children with cystic fibrosis

Christophe Marguet, Véronique Houdouin, Isabelle Pin, Philippe Reix, Frédéric Huet, Marie Mittaine, Sophie Ramel, Nathalie Wizla-Derambure, Michel Abely, Marie-Laure Dalphin, Michael Fayon, Tiphaine Bihouée, Muriel Le Bourgeois, Eric Deneuville, Harriet Corvol, Muriel Laurans, Laure Couderc, Evelyne Leroux, Ludovic Lémée
ERJ Open Research 2021 7: 00513-2020; DOI: 10.1183/23120541.00513-2020

Abstract

Lung damage in cystic fibrosis (CF) is strongly associated with lower airway infections. Early treatment of Pseudomonas aeruginosa is recommended. Pathogen detection requires sampling of lower airway secretions, which remains a challenge in nonexpectorating patients. Our hypothesis was that chest physiotherapy would improve the quality of airway secretion samples and increase the rates of pathogens detected in nonexpectorating patients.

This prospective multicentre study compared three successive methods for sampling airway secretions applied through the same session: 1) an oropharyngeal swab (OP), 2) a chest physiotherapy session followed by a provoked cough to obtain sputum (CP-SP) and 3) a second oropharyngeal swab collected after chest physiotherapy (CP-OP). Haemophilus influenzae, Staphylococcus aureus and P. aeruginosa growth cultures were assessed. Accuracy tests and an equivalence test were performed to compare the three successive methods of collection.

300 nonexpectorating children with CF were included. P. aeruginosa was detected cumulatively in 56 (18.9%) children, and according to the different collection methods in 28 (9.8%), 37 (12.4%) and 44 (14.7%) children by using OP, CP-OP and CP-SP, respectively. Compared with OP, the increased detection rate was +22% for CP-OP (p=0.029) and +57% for CP-SP (p=0.003). CP-SP had the best positive predictive value (86.3%) and negative predictive value (96.0%) for P. aeruginosa compared with the overall detection.

The results of this adequately powered study show differences in the rates of pathogens detected according to the sampling method used. Chest physiotherapy enhanced detection of P. aeruginosa in nonexpectorating children with CF.

Abstract

Sputum collection after a chest physiotherapy session strongly enhances the detection of P. aeruginosa in nonexpectorating CF children compared with the commonly used oropharyngeal swab method. Oropharyngeal swab after physiotherapy may be an acceptable alternative. https://bit.ly/3757ewq

Introduction

Cystic fibrosis (CF) is a genetic disease characterised by altered lower airway clearance and recurrent lower airway infections, which both lead to CF-related lung disease progression. Patient follow-up should target the early detection of lower airway colonisation by potentially pathogenic microorganisms. Thus, current guidelines recommend sampling airway secretions for microbiological culture and analysis at least four times per year and proposing adapted antibiotic treatment [1].

Early detection of Pseudomonas aeruginosa in CF is crucial as early treatment is a key to delaying P. aeruginosa-related chronic bronchial infection [2]. P. aeruginosa colonisation may be present in young children who are not yet able to expectorate spontaneously, i.e. 17% of children aged 4 years [3]. The accuracy of the evaluation of the microbiological status of CF patients depends on the quality of both airway samples and microbiological procedures. Thus, it is crucial to optimise sampling of lower airway secretions in CF. Currently, bronchoalveolar lavage (BAL) is considered as the gold standard; however, it cannot be performed repeatedly. Moreover, a 5-year BAL- versus oropharyngeal swab-directed therapy trial has been conducted for treating exacerbations in young CF children, showing similar clinical and radiological outcomes in both groups [4]. When patients are able to expectorate, results obtained in spontaneous sputum are considered to reflect the microbiological status of the lower airways. However, many children cannot expectorate as they are not able, do not want or do not have enough secretions to expectorate [5, 6].

Currently, oropharyngeal swab is a common sampling method. Nevertheless, available validation studies show notable differences in positive predictive values (PPVs) and, to a lesser extent, in negative predictive values (NPVs) compared with other methods [7–11]. Moreover, sputum cultures are likely to be better indicators of the bronchial microbiological flora than oropharyngeal swab samples, as reported by at least two studies in expectorating patients [10, 12] and one study in nonexpectorating patients [13]. Since these earlier studies, induced sputum collection by nebulised hypertonic saline solution has been proposed [13–21] with a good microbiological yield, but it is a time-consuming procedure. In contrast, chest physiotherapy has rarely been reported [16] as a reliable method for obtaining sputum in nonexpectorating children, although it is already used on a daily basis to improve airway clearance in CF.

In the present study, we focused on the methods used to sample airway secretions and formulated the hypothesis that sputum collected after a chest physiotherapy course provided more accurate samples than the oropharyngeal swab method in nonexpectorating children, as previously suggested in CF patients with productive cough [22].

Patients and methods

This prospective multicentre study was conducted in 16 French tertiary CF centres from January 1, 2006 to January 1, 2008. The included patients fulfilled the following criteria: 1) confirmed diagnosis of CF, 2) regularly followed up in a tertiary paediatric CF centre, 3) aged ≤18 years and 4) unable to spontaneously expectorate either routinely or during a pulmonary exacerbation. The study was approved by the Ethics Committee of Haute-Normandie (CCP-SPHN), and informed consent was obtained from all parents and children when relevant.

Study design

Data on demographics, history of microbiological status and ability to expectorate were collected. During the appointment at the CF centre, the chest physiotherapist collected three airway secretion samples during the dedicated session by using three successive methods: 1) an oropharyngeal swab (OP method), 2) a chest physiotherapy session followed by a provoked cough to obtain sputum (CP-SP method) and 3) a second oropharyngeal swab collected after chest physiotherapy (CP-OP method).

Airway secretion sampling

Chest physiotherapists applied a standardised operating procedure across all participating CF centres. The child was maintained in a sitting position and nasal lavage was first performed carefully by flushing 5 mL isotonic saline serum in each nostril until the liquid returned clear. The nasal fluid was evacuated either through the other nostril or was aspirated by introducing a suction catheter (6 Fr; Vygon, Ecouen, France) through each nostril as far as the nasopharynx. Oral lavage was performed in older children with sterile water. Oropharyngeal swabs were rubbed on the tonsils and pharynx without touching the buccal mucosa. Then, the chest physiotherapist applied at least four series of 15 expiratory flow ventilations to the child's chest with an empty stomach and drained the bronchial secretions to the lower pharynx. Cough at the end of chest physiotherapy was either spontaneous or gently provoked by pressing the thumb on the trachea in younger patients in order to collect samples for CP-SP spontaneously whenever possible or quickly suctioned into a sterile vial (catheter AM10610P; Cair LGL, Lissieu, France).

Microbiological analyses

The airway secretion samples were transported to the microbiology laboratory within 2 h and each sample was processed separately. A standardised operating procedure based on French Standard Operating Procedures was used in all CF centres [23]. Pure and diluted liquefied sputum samples as well as oropharyngeal swabs were inoculated and incubated onto several nonselective and selective isolation media, notably for Haemophilus influenzae, Staphylococcus aureus and P. aeruginosa detection and quantification. All media were incubated aerobically at 37°C for 5 days and monitored daily. All different morphotypes of bacterial colonies were identified. For sputum samples only, quantification was conducted based on the CFU·mL−1 counts and the dilution ratio of the plates. The study of antibiotic resistance was carried out according to Comité de l'Antibiogramme de la Société Française de Microbiologie/European Committee on Antimicrobial Susceptibility Testing guidelines [24]. Quantitative cultures were only done from sputum obtained after chest physiotherapy. Other identified bacteria were noted as recommended, but only H. influenzae, P. aeruginosa and S. aureus counts were determined for the comparison of the three methods.

The number of patients needed was calculated according to an expected prevalence of 20% of P. aeruginosa in the studied population, and a true detection of 87.5% of P. aeruginosa and S. aureus and 69.2% of H. influenzae [10]. The expected difference between the methods of sputum collection was set to 10% [14, 15]. In total, 300 nonexpectorating patients were required to achieve a power of 90% for equivalence between the studied methods.

Statistical analysis

The results of the three methods were compared using the McNemar test (Cochran–Mantel–Haenszel for dichotomous variables). An equivalence test was performed: the three methods for collecting secretions were considered as equivalent if the difference of true detection was ≤10%, i.e. the 90% confidence intervals were within −10% to +10%. The analyses were also displayed with 95% confidence intervals. Then, accuracy tests (predictive values, specificity and sensitivity) were performed with reference to sputum collection (CP-SP) and according to positive results (OP+CP-SP+CP-OP). All tests were performed at a bilateral risk of α=0.05 using SAS version 8.2 (SAS Institute, Cary, NC, USA).

Results

300 children were included, but the collection of secretions failed in one child. Therefore, data from 299 children were analysed (table 1). Nasal and oral lavage were performed prior to sampling in 216 (72.2%) and 198 (66.2%) children, respectively. The acceptability of the procedures is reported in table 2 and was comparable between the three methods. No respiratory distress occurred. The results for sampling airway secretions and microbiology cultures are displayed in table 2. S. aureus, H. influenzae and P. aeruginosa were detected in at least one sample in 188 (63.7%), 77 (26.1%) and 56 (19.0%) children, respectively. The results of growth cultures were concordant for the three methods in 176 (58.9%) patients (n=106 for positive cultures and n=70 for negative cultures).

View this table:
TABLE 1

Characteristics of the studied population

View this table:
TABLE 2

Collection of airway secretions and growth results by three different methods

Equivalence test for the three methods

The results for the three bacterial species are presented for both 90% confidence intervals (primary end-point) and 95% confidence intervals (table 3). Positive cultures obtained after CP-SP and CP-OP versus OP differed according to the studied bacteria. Although close to the 90% confidence intervals equivalence for P. aeruginosa, CP-SP appeared the most efficient method for the three bacteria. Conversely, OP and CP-OP as well as CP-SP and CP-OP appeared to be equivalent methods. The only difference was a better identification of S. aureus with CP-OP compared with OP. The results for 95% confidence intervals indicated that CP-SP is a better method than CP-OP, which is a better method than OP for detecting these three bacteria.

View this table:
TABLE 3

Equivalence test for the three methods and comparison of the paired results (McNemar test)

Accuracy of analyses of microbiological growth obtained by the three methods

CP-SP detected the three bacterial species more frequently than OP (p=0.013) (table 1). P. aeruginosa was detected in 56 (18.9%) children. Among those children, the use of CP-SP, CP-OP and OP contributed to detecting P. aeruginosa infection in 44 (78.6%), 37 (66%) and 28 (50%) children, respectively. Thus, the use of CP-SP and CP-OP augmented the overall detection of P. aeruginosa by +57% (p=0.003) and +22% (p=0.029), respectively, compared with OP. In detail, CP-SP and CP-OP enabled the additional identification of 22 and 13 infected children, respectively, who were not identified by OP (figure 1a). Conversely, CP-SP compared with OP or CP-OP failed to detect positive P. aeruginosa growth in 11 (19.6%) children. P. aeruginosa was detected with both OP and CP-OP in three samples, with OP only in three samples, and with CP-OP only in five samples. All P. aeruginosa strains detected by both OP and CP-SP had similar antibiotic susceptibilities.

FIGURE 1
FIGURE 1

Number of a) Pseudomonas aeruginosa, b) Haemophilus influenzae and c) Staphylococcus aureus detections in the airway secretions of 295 nonexpectorating cystic fibrosis patients using three methods: OP (oropharyngeal swab), CP-SP (a chest physiotherapy session followed by a provoked cough to obtain sputum) and CP-OP (a second oropharyngeal swab collected after chest physiotherapy). The results of positive airway secretion cultures collected by each method are compared by pairs. CP-SP and CP-OP significantly increased the detection of patients with P. aeruginosa compared with OP. CP-SP significantly increased the detection of patients with H. influenzae compared with OP.

H. influenzae was detected in 77 (26.1%) children. In samples collected after CP-SP and CP-OP, H. influenzae was cultured in 59 (20.0%) and 50 (17.1%) children, respectively, compared with 43 (14.6%) children with OP. Therefore, the use of CP-SP identified 75.3% of the infected children, leading to an additional detection rate of 34.9% (p=0.01) for H. influenzae compared with the use of OP. H. influenzae carriage was detected with only OP and only CP-OP sampling in 11 (14.2%) and 15 (19.4%) infected children, respectively (figure 1b).

S. aureus grew in 181 (61.1%) children and no significant difference was seen in the detection of additional patients irrespective of the chosen methods (figure 1c).

Sensitivity, specificity, predictive values and accuracy of OP and CP-OP were calculated by referring to the CP-SP results (table 4). OP and CP-OP had a weak sensitivity for P. aeruginosa identification compared with CP-SP. The predictive values of each method were then analysed by referring to all bacterial isolations obtained from all three sampling methods (table 5). CP-SP provided the best PPV and NPV for P. aeruginosa and S. aureus.

View this table:
TABLE 4

Accuracy of bacteria detection by the OP and CP-OP methods versus the CP-SP method

View this table:
TABLE 5

Predictive values of each method with reference to pooled positive cultures

Additional effects of age, cough/symptoms and current antibiotics were analysed. None of them had any relationship with the results of the current analyses.

Acceptability of chest physiotherapy and sampling was determined. Overall, chest physiotherapy was well accepted in 75.5% of in this young population, 55% were agitated and 86.1% cried mostly before starting the technique. The acceptability of sampling was also good (72.4%) and nausea was observed in 13 (16.7%) children. No respiratory worsening or distress was reported.

Discussion

In this present study, we focused on the methods used to sample airway secretions and two different statistical approaches were applied. The first considered equivalence testing at both 90% and 95% confidence intervals; the second tested the accuracy of the methods used and reflected the assessment at an individual level. Equivalence testings showed that oropharyngeal swab before chest physiotherapy (OP method) and sputum collected after chest physiotherapy (CP-SP method) provided different results. Our results clearly sustained the hypothesis that sputum provided a higher yield for the three studied bacteria. Considering P. aeruginosa results alone, one-third of the children infected with this pathogen would not have been identified by using oropharyngeal swab cultures alone.

Few studies have validated methods for sampling airway secretions in nonexpectorating children and those have mainly compared them with BAL, considered as the gold standard. Existing data in the literature present the results for the three common potentially pathogenic bacteria in CF [7–10]. Oropharyngeal swab sensitivity, specificity, PPV and NPV values varied widely between studies; the ranges for P. aeruginosa were 46–75%, 80–97%, 55–83% and 70–97%, respectively. The variations in these results might depend on various parameters, mainly on the size of the tested population for each bacteria and consequently on the relevant number of positive and negative growths for statistical analyses. For instance, an overwhelming number of negative culture growths will overestimate the NPV and consequently bias correct estimation of the PPV. The up-to-date largest Australian study compared 690 paired oropharyngeal swab and BAL sampling cultures in 181 young children with a prevalence of 7.8% P. aeruginosa infections [11]. Oropharyngeal swab compared with BAL had a very low sensitivity and PPV for detecting P. aeruginosa: 23.0% and 18.2%, respectively.

We powered our study to prevent any errors related to the size of the populations, according to the expected results of lower powered studies which compared sputum growth samples with samples obtained using other methods. Moreover, sputum analyses allowed quantification of pathogens and the detection limit of culture growth was 102 CFU·mL−1. In expectorating patients, BAL was better correlated with sputum than oropharyngeal swab culture growth [10] and sputum has been shown to provide more sensitive airway material for microbiological cultures than oropharyngeal swab [12]. Seven studies have explored the benefit of induced sputum cultures in smaller sized populations (19–125 children) with a range from 29 to 167 samples [13–15, 17, 18, 20, 21]. The additional yield of induced sputum compared with oropharyngeal swab or spontaneous sputum collection varied from 0% to +175% pathogen growths, and conversely enabled the identification of new pathogens in the seven studies. This underlined the risk of false-negative cultures from oropharyngeal swabs. The recent large study by Ronchetti et al. [21] compared the results of 169 paired samples of oropharyngeal swabs by coughing and induced sputum from 103 CF children. They identified at least one pathogen in 38% of induced sputum compared with 14% of swab samples. 92% of the pathogens were isolated from sputum compared with 31% from samples collected with oropharyngeal swabs by coughing. Their findings were independent of the presence of symptoms and age, as in our own study. In a molecular study, Zemanick et al. [25] observed a marked underestimation of the detected bacterial strains in oropharyngeal swab compared with sputum samples. Few studies focused on nonexpectorating children. In one study [14], 42% of 20 nonexpectorating children were shown to carry new bacteria. Zampoli et al. [20] reported a higher yield of induced sputum (+81%) than oropharyngeal swab growth cultures in infants. However, the low prevalence of positive growth samples in these previous studies prevented specific conclusions according to identified bacteria. The present study supports the use of the CP-SP method for detecting additional P. aeruginosa, which is known as a prognostic factor in CF. The benefit of induced sputum to detect additional P. aeruginosa was not found to be relevant in three cohorts [18, 20], although it increased the screening by 54% in another small study [19]. Our results also suggest that a swab applied after chest physiotherapy (CP-OP method) is an acceptable alternative method. The qualitative effect of chest physiotherapy on swab culture was previously suggested, with a two-fold increase achieved in the detection of P. aeruginosa [26] and doubling sensitivity of sputum compared with BAL [16].

Although microbiological analyses of collected sputum during a chest physiotherapy session allowed screening of 78.5% of the infected children with P. aeruginosa, the PPVs of sputum growths did not achieve 100%. In fact, 2% of P. aeruginosa-infected children were screened solely with oropharyngeal swabs. The lack of concomitant positive sputum growths has previously been underlined and remains a topic of discussion. With the growing interest in upper airway infection and the need to treat it [27], it is thought that isolated upper airway P. aeruginosa growths might reflect sinus infection [28], considered as a bacterial reservoir [29, 30]. Others defined them as false-positive results with no treatment necessary [11, 31].

This study has a number of strengths and limitations. The strengths are the adequately powered study on the number of detected P. aeruginosa for preventing bias in the measures of test accuracy. These results are those expected through the routine follow-up of a CF paediatric cohort, as 96% of the collections were performed during routine visits. Attention was given to providing training and guidelines in all CF centres for a similar application of identical physiotherapy practices and microbiological methods, with detection of bacteria at a low level of 102 CFU·mL−1. No centre effect was identified through the analyses. There are also some limitations. The techniques of chest physiotherapy for CF patients have progressed. The airway clearance technique currently used in France is autogenic drainage, or the concept of flow and breathing level modulation, as recommended by the European CF Society [32]. A similar acceptability was reported for each sampling method. Most crying started before the session in this young population. Thus, no specific adverse effect might be attributed to chest physiotherapy, a routine home care practice in CF. The aim of this study was to test the growth results in real life and, unfortunately, no molecular analysis of P. aeruginosa strains was performed. However, antibiotic susceptibility testing was constantly similar for an individual patient. This suggests that the same strains were found in the upper and lower airways, as previously demonstrated [33]. Not all of the study population benefitted from nasal lavage or oral washing, although no difference in the proportion of the identified pathogens was observed. Since this study, the matrix assisted laser desorption ionisation-time of flight mass spectrometry identification tool has become available, although this would not significantly improve the identification of P. aeruginosa, H. influenzae and S. aureus in CF compared with the usual phenotypic method [34].

In conclusion, this prospective, powered, multicentre study has demonstrated that sputum collected after chest physiotherapy in nonexpectorating CF children provides the most sensitive samples for P. aeruginosa screening. Oropharyngeal swab applied after chest physiotherapy remains an acceptable alternative. These results may enhance both patient care and end-points for research trials. A study using induced sputum, a method of a growing interest, and/or PCR diagnosis will be further clinically useful [21, 35, 36]. Given the microbial diversity and the emergence of other pathogenic species (i.e. Achromobacter spp. and Stenotrophomonas spp.) it would be interesting to extend the study to a larger panel of biomarker bacteria or even to make the comparison by metagenomics [21].

Acknowledgements

The authors are grateful to Nikki Sabourin-Gibbs (Rouen University Hospital, Rouen, France) for her help in editing the manuscript. The study was achieved with the full involvement of the chest physiotherapists and microbiologists of each participating centre.

Footnotes

  • Support statement: The study was fully funded by the French CF association “Vaincre la Mucoviscidose”. Funding information for this article has been deposited with the Crossref Funder Registry.

  • Conflict of interest: C. Marguet has nothing to disclose.

  • Conflict of interest: V. Houdouin has nothing to disclose.

  • Conflict of interest: I. Pin reports a presentation honorarium and travel grants from Novartis, and travel grants from AstraZeneca and AGIRadom, outside the submitted work.

  • Conflict of interest: P. Reix has nothing to disclose.

  • Conflict of interest: F. Huet has nothing to disclose.

  • Conflict of interest: M. Mittaine has nothing to disclose.

  • Conflict of interest: S. Ramel has nothing to disclose.

  • Conflict of interest: N. Wizla-Derambure has nothing to disclose.

  • Conflict of interest: M. Abely has nothing to disclose.

  • Conflict of interest: M-L. Dalphin has nothing to disclose.

  • Conflict of interest: M. Fayon has nothing to disclose.

  • Conflict of interest: T. Bihouée reports fees for a commercial article from Vertex, personal fees for speaker bureaus from Novartis and Mylan, and travel support and registration for a congress from Teva, outside the submitted work.

  • Conflict of interest: M. Le Bourgeois has nothing to disclose.

  • Conflict of interest: E. Deneuville has nothing to disclose.

  • Conflict of interest: H. Corvol has nothing to disclose.

  • Conflict of interest: M. Laurens has nothing to disclose.

  • Conflict of interest: L. Couderc has nothing to disclose.

  • Conflict of interest: L. Lémée has nothing to disclose.

  • Received October 2, 2020.
  • Accepted December 6, 2020.
http://creativecommons.org/licenses/by-nc/4.0/

This article is open access and distributed under the terms of the Creative Commons Attribution Non-Commercial Licence 4.0.

References

  1. ↵
    Haute Autorité de Santé. Mucoviscidose: Guide maladie chronique. [Cystic Fibrosis: Chronic Disease Guide.] 2017. www.has-sante.fr/jcms/c_2792719/fr/mucoviscidose Date last accessed: February 10, 2021.
  2. ↵
    1. Doring G
    . Editorial. J Cyst Fibros 2012; 11: 1. doi:10.1016/j.jcf.2011.11.011
    OpenUrlPubMed
  3. ↵
    Association Vaincre la Mucoviscidose. Registre Français de la Mucoviscidose. 2017. www.vaincrelamuco.org/registredelamuco Data last accessed: December 23, 2020.
  4. ↵
    1. Wainwright CE,
    2. Vidmar S,
    3. Armstrong DS, et al.
    Effect of bronchoalveolar lavage-directed therapy on Pseudomonas aeruginosa infection and structural lung injury in children with cystic fibrosis: a randomized trial. JAMA 2011; 306: 163–171.
    OpenUrlCrossRefPubMed
  5. ↵
    1. Radhakrishnan DK,
    2. Corey M,
    3. Dell SD
    . Realities of expectorated sputum collection in the pediatric cystic fibrosis clinic. Arch Pediatr Adolesc Med 2007; 161: 603–606. doi:10.1001/archpedi.161.6.603
    OpenUrlCrossRefPubMed
  6. ↵
    1. Sagel SD,
    2. Gibson RL,
    3. Emerson J, et al.
    Impact of Pseudomonas and Staphylococcus infection on inflammation and clinical status in young children with cystic fibrosis. J Pediatr 2009; 154: 183–188. doi:10.1016/j.jpeds.2008.08.001
    OpenUrlCrossRefPubMed
  7. ↵
    1. Armstrong DS,
    2. Grimwood K,
    3. Carlin JB, et al.
    Bronchoalveolar lavage or oropharyngeal cultures to identify lower respiratory pathogens in infants with cystic fibrosis. Pediatr Pulmonol 1996; 21: 267–275. doi:10.1002/(SICI)1099-0496(199605)21:5<267::AID-PPUL1>3.0.CO;2-K
    OpenUrlCrossRefPubMed
    1. Rosenfeld M,
    2. Emerson J,
    3. Accurso F, et al.
    Diagnostic accuracy of oropharyngeal cultures in infants and young children with cystic fibrosis. Pediatr Pulmonol 1999; 28: 321–328. doi:10.1002/(SICI)1099-0496(199911)28:5<321::AID-PPUL3>3.0.CO;2-V
    OpenUrlCrossRefPubMed
    1. Burns JL,
    2. Gibson RL,
    3. McNamara S, et al.
    Longitudinal assessment of Pseudomonas aeruginosa in young children with cystic fibrosis. J Infect Dis 2001; 183: 444–452. doi:10.1086/318075
    OpenUrlCrossRefPubMed
  10. ↵
    1. Ramsey BW,
    2. Wentz KR,
    3. Smith AL, et al.
    Predictive value of oropharyngeal cultures for identifying lower airway bacteria in cystic fibrosis patients. Am Rev Respir Dis 1991; 144: 331–337. doi:10.1164/ajrccm/144.2.331
    OpenUrlCrossRefPubMed
  11. ↵
    1. Breuer O,
    2. Caudri D,
    3. Akesson L, et al.
    The clinical significance of oropharyngeal cultures in young children with cystic fibrosis. Eur Respir J 2018; 51: 1800238. doi:10.1183/13993003.00238-2018
    OpenUrlAbstract/FREE Full Text
  12. ↵
    1. Equi AC,
    2. Pike SE,
    3. Davies J, et al.
    Use of cough swabs in a cystic fibrosis clinic. Arch Dis Child 2001; 85: 438–439. doi:10.1136/adc.85.5.438
    OpenUrlAbstract/FREE Full Text
  13. ↵
    1. Blau H,
    2. Linnane B,
    3. Carzino R, et al.
    Induced sputum compared to bronchoalveolar lavage in young, non-expectorating cystic fibrosis children. J Cyst Fibros 2014; 13: 106–110. doi:10.1016/j.jcf.2013.05.013
    OpenUrlCrossRef
  14. ↵
    1. Al-Saleh S,
    2. Dell SD,
    3. Grasemann H, et al.
    Sputum induction in routine clinical care of children with cystic fibrosis. J Pediatr 2010; 157: 1006–1011. doi:10.1016/j.jpeds.2010.06.001
    OpenUrlCrossRefPubMed
  15. ↵
    1. De Boeck K,
    2. Alifier M,
    3. Vandeputte S
    . Sputum induction in young cystic fibrosis patients. Eur Respir J 2000; 16: 91–94. doi:10.1034/j.1399-3003.2000.16a16.x
    OpenUrlAbstract/FREE Full Text
  16. ↵
    1. D'Sylva P,
    2. Caudri D,
    3. Shaw N, et al.
    Induced sputum to detect lung pathogens in young children with cystic fibrosis. Pediatr Pulmonol 2017; 52: 182–189. doi:10.1002/ppul.23636
    OpenUrl
  17. ↵
    1. Ho SA,
    2. Ball R,
    3. Morrison LJ, et al.
    Clinical value of obtaining sputum and cough swab samples following inhaled hypertonic saline in children with cystic fibrosis. Pediatr Pulmonol 2004; 38: 82–87. doi:10.1002/ppul.20035
    OpenUrlCrossRefPubMed
  18. ↵
    1. Hoppe JE,
    2. Towler E,
    3. Wagner BD, et al.
    Sputum induction improves detection of pathogens in children with cystic fibrosis. Pediatr Pulmonol 2015; 50: 638–646. doi:10.1002/ppul.23150
    OpenUrlCrossRef
  19. ↵
    1. Mussaffi H,
    2. Fireman EM,
    3. Mei-Zahav M, et al.
    Induced sputum in the very young: a new key to infection and inflammation. Chest 2008; 133: 176–182. doi:10.1378/chest.07-2259
    OpenUrlCrossRefPubMed
  20. ↵
    1. Zampoli M,
    2. Pillay K,
    3. Carrara H, et al.
    Microbiological yield from induced sputum compared to oropharyngeal swab in young children with cystic fibrosis. J Cyst Fibros 2016; 15: 605–610. doi:10.1016/j.jcf.2016.01.001
    OpenUrl
  21. ↵
    1. Ronchetti K,
    2. Tame JD,
    3. Paisey C, et al.
    The CF-Sputum Induction Trial (CF-SpIT) to assess lower airway bacterial sampling in young children with cystic fibrosis: a prospective internally controlled interventional trial. Lancet Respir Med 2018; 6: 461–471. doi:10.1016/S2213-2600(18)30171-1
    OpenUrl
  22. ↵
    1. Aaron SD,
    2. Kottachchi D,
    3. Ferris WJ, et al.
    Sputum versus bronchoscopy for diagnosis of Pseudomonas aeruginosa biofilms in cystic fibrosis. Eur Respir J 2004; 24: 631–637. doi:10.1183/09031936.04.00049104
    OpenUrlAbstract/FREE Full Text
  23. ↵
    Société Française de Microbiologie. Référentiel en Microbiologie Médicale. [Standard in Medical Microbiology.] Paris, SFM, 2007.
  24. ↵
    Société Française de Microbiologie. Comité de l'Antibiogramme de la Société Française de Microbiologie/European Committee on Antimicrobial Susceptibility Testing (CA-SFM/EUCAST Guidelines). Paris, SFM, 2008.
  25. ↵
    1. Zemanick ET,
    2. Wagner BD,
    3. Robertson CE, et al.
    Assessment of airway microbiota and inflammation in cystic fibrosis using multiple sampling methods. Ann Am Thorac Soc 2015; 12: 221–229. doi:10.1513/AnnalsATS.201407-310OC
    OpenUrlCrossRef
  26. ↵
    1. Kabra SK,
    2. Alok A,
    3. Kapil A, et al.
    Can throat swab after physiotherapy replace sputum for identification of microbial pathogens in children with cystic fibrosis? Indian J Pediatr 2004; 71: 21–23. doi:10.1007/BF02725650
    OpenUrlCrossRefPubMed
  27. ↵
    1. Berkhout MC,
    2. Rijntjes E,
    3. El Bouazzaoui LH, et al.
    Importance of bacteriology in upper airways of patients with cystic fibrosis. J Cyst Fibros 2013; 12: 525–529. doi:10.1016/j.jcf.2013.01.002
    OpenUrlCrossRefPubMed
  28. ↵
    1. Sakano E,
    2. Ribeiro AF,
    3. Barth L, et al.
    Nasal and paranasal sinus endoscopy, computed tomography and microbiology of upper airways and the correlations with genotype and severity of cystic fibrosis. Int J Pediatr Otorhinolaryngol 2007; 71: 41–50. doi:10.1016/j.ijporl.2006.08.015
    OpenUrlCrossRefPubMed
  29. ↵
    1. Bonestroo HJ,
    2. de Winter-de Groot KM,
    3. van der Ent CK, et al.
    Upper and lower airway cultures in children with cystic fibrosis: do not neglect the upper airways. J Cyst Fibros 2010; 9: 130–134. doi:10.1016/j.jcf.2010.01.001
    OpenUrlCrossRefPubMed
  30. ↵
    1. Whiteson KL,
    2. Bailey B,
    3. Bergkessel M, et al.
    The upper respiratory tract as a microbial source for pulmonary infections in cystic fibrosis. Parallels from island biogeography. Am J Respir Crit Care Med 2014; 189: 1309–1315. doi:10.1164/rccm.201312-2129PP
    OpenUrlCrossRefPubMed
  31. ↵
    1. Ranganathan SC,
    2. Skoric B,
    3. Ramsay KA, et al.
    Geographical differences in first acquisition of Pseudomonas aeruginosa in cystic fibrosis. Ann Am Thorac Soc 2013; 10: 108–114. doi:10.1513/AnnalsATS.201209-077OC
    OpenUrlCrossRefPubMed
  32. ↵
    International Physiotherapy Group for Cystic Fibrosis. Physiotherapy for People with Cystic Fibrosis: From Infant to Adult. IPG-CF Blue Booklet. 2019. www.ecfs.eu/ipg_cf/booklet Date last accessed: December 23, 2020.
  33. ↵
    1. Mainz JG,
    2. Naehrlich L,
    3. Schien M, et al.
    Concordant genotype of upper and lower airways P aeruginosa and S aureus isolates in cystic fibrosis. Thorax 2009; 64: 535–540. doi:10.1136/thx.2008.104711
    OpenUrlAbstract/FREE Full Text
  34. ↵
    1. Desai AP,
    2. Stanley T,
    3. Atuan M, et al.
    Use of matrix assisted laser desorption ionisation-time of flight mass spectrometry in a paediatric clinical laboratory for identification of bacteria commonly isolated from cystic fibrosis patients. J Clin Pathol 2012; 65: 835–838. doi:10.1136/jclinpath-2012-200772
    OpenUrlAbstract/FREE Full Text
  35. ↵
    1. Schultz A,
    2. Caudri D
    . Cough swabs less useful but induced sputum very useful in symptomatic older children with cystic fibrosis. Lancet Respir Med 2018; 6: 410–411. doi:10.1016/S2213-2600(18)30183-8
    OpenUrl
  36. ↵
    1. Stafler P,
    2. Mussaffi H,
    3. Gendler Y, et al.
    Induced sputum versus broncho-alveolar lavage for pathogen surveillance in young cystic fibrosis patients: low specificity is not necessarily a bad thing. Pediatr Pulmonol 2018; 53: 8. doi:10.1002/ppul.23887
    OpenUrl
Back to top
Email
Print
Citation Tools
Chest physiotherapy enhances detection of Pseudomonas aeruginosa in nonexpectorating children with cystic fibrosis
Christophe Marguet, Véronique Houdouin, Isabelle Pin, Philippe Reix, Frédéric Huet, Marie Mittaine, Sophie Ramel, Nathalie Wizla-Derambure, Michel Abely, Marie-Laure Dalphin, Michael Fayon, Tiphaine Bihouée, Muriel Le Bourgeois, Eric Deneuville, Harriet Corvol, Muriel Laurans, Laure Couderc, Evelyne Leroux, Ludovic Lémée
ERJ Open Research Jan 2021, 7 (1) 00513-2020; DOI: 10.1183/23120541.00513-2020
del.icio.us logo Digg logo Reddit logo Technorati logo Twitter logo CiteULike logo Connotea logo Facebook logo Google logo Mendeley logo
Full Text (PDF)

Jump To

Subjects