Publications by authors named "Jean-Charles Dalphin"

103 Publications

Inflammatory and immunological profile in COPD secondary to organic dust exposure.

Clin Immunol 2021 08 17;229:108798. Epub 2021 Jul 17.

Service de Pneumologie, Oncologie Thoracique et Allergologie Respiratoire, CHRU de Besançon, France. Electronic address:

Inflammatory response in patients with COPD secondary to organic dust exposure (OD-COPD) is poorly understood. We therefore aimed to characterize inflammatory and immune profile from peripheral blood mononuclear cells (PBMC) in a group of patients with mild-to-moderate COPD secondary to organic dust exposure (OD-COPD), tobacco smoking (T-COPD), or both. We compared T, B and NK cells distribution and inflammatory (TNF-α, Il-1β, IL-6), type 1 (IFN-γ), type 2 (IL-4, IL-13) and type 3 (IL-17) immunity related cytokines at baseline, and after stimulation with LPS, flagellin and CD3/CD28 beads in all COPD groups. OD-COPD displayed significantly lower NK cells and CD8+ T cells compared with controls. After flagellin stimulation, T-COPD had significantly lower IL-13 levels than OD-COPD and controls (p < 0.05) whereas IFN-γ tended to be lower in OD-COPD. All COPD groups displayed higher IL-1β and IL-17 than controls after CD3/CD28 stimulation. Inflammatory responses in OD-COPD were different from T-COPD. OD-COPD displayed higher levels of type 2 immunity related cytokines.
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http://dx.doi.org/10.1016/j.clim.2021.108798DOI Listing
August 2021

Exposure Assessment Tools for Hypersensitivity Pneumonitis. An Official American Thoracic Society Workshop Report.

Ann Am Thorac Soc 2020 12;17(12):1501-1509

This report is based on proceedings from the Exposure Assessment Tools for Hypersensitivity Pneumonitis (HP) Workshop, sponsored by the American Thoracic Society, that took place on May 18, 2019, in Dallas, Texas. The workshop was initiated by members from the Environmental, Occupational, and Population Health and Clinical Problems Assemblies of the American Thoracic Society. Participants included international experts from pulmonary medicine, occupational medicine, radiology, pathology, and exposure science. The meeting objectives were to ) define currently available tools for exposure assessment in evaluation of HP, ) describe the evidence base supporting the role for these exposure assessment tools in HP evaluation, ) identify limitations and barriers to each tool's implementation in clinical practice, ) determine which exposure assessment tools demonstrate the best performance characteristics and applicability, and ) identify research needs for improving exposure assessment tools for HP. Specific discussion topics included history-taking and exposure questionnaires, antigen avoidance, environmental assessment, specific inhalational challenge, serum-specific IgG testing, skin testing, lymphocyte proliferation testing, and a multidisciplinary team approach. Priorities for research in this area were identified.
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http://dx.doi.org/10.1513/AnnalsATS.202008-942STDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7706597PMC
December 2020

A 35-Year-Old Man With Recurrent Pneumonia and Whitish Sputum.

Chest 2020 11;158(5):e229-e232

Service de Pneumologie, Oncologie thoracique et allergologie respiratoire, Centre Hospitalier Universitaire Besançon, Besançon, France.

Case Presentation: A 35-year-old man was admitted for recurrent episodes of pneumonia. He complained of a 2-month history of exertional dyspnea and productive cough with whitish and viscous sputum which was poorly responsive to antibiotic therapy. He also reported a weight loss of 5 kg since the first symptoms appeared. There was no dysphagia, fever, or chest pain. He currently did not use medication and did not have a relevant medical history except a current 10 pack-year smoking history. He did not report any history of trauma or respiratory exposure to fats.
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http://dx.doi.org/10.1016/j.chest.2020.06.016DOI Listing
November 2020

Maturation of the gut microbiome during the first year of life contributes to the protective farm effect on childhood asthma.

Nat Med 2020 11 2;26(11):1766-1775. Epub 2020 Nov 2.

German Center for Lung Research, .

Growing up on a farm is associated with an asthma-protective effect, but the mechanisms underlying this effect are largely unknown. In the Protection against Allergy: Study in Rural Environments (PASTURE) birth cohort, we modeled maturation using 16S rRNA sequence data of the human gut microbiome in infants from 2 to 12 months of age. The estimated microbiome age (EMA) in 12-month-old infants was associated with previous farm exposure (β = 0.27 (0.12-0.43), P = 0.001, n = 618) and reduced risk of asthma at school age (odds ratio (OR) = 0.72 (0.56-0.93), P = 0.011). EMA mediated the protective farm effect by 19%. In a nested case-control sample (n = 138), we found inverse associations of asthma with the measured level of fecal butyrate (OR = 0.28 (0.09-0.91), P = 0.034), bacterial taxa that predict butyrate production (OR = 0.38 (0.17-0.84), P = 0.017) and the relative abundance of the gene encoding butyryl-coenzyme A (CoA):acetate-CoA-transferase, a major enzyme in butyrate metabolism (OR = 0.43 (0.19-0.97), P = 0.042). The gut microbiome may contribute to asthma protection through metabolites, supporting the concept of a gut-lung axis in humans.
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http://dx.doi.org/10.1038/s41591-020-1095-xDOI Listing
November 2020

Never-smokers with occupational COPD have better exercise capacities and ventilatory efficiency than matched smokers with COPD.

J Appl Physiol (1985) 2020 12 1;129(6):1257-1266. Epub 2020 Oct 1.

Service Hospitalier Universitaire Pneumologie Physiologie, Pôle Thorax et Vaisseaux, CHU Grenoble Alpes, Grenoble, France.

Chronic obstructive pulmonary disease (COPD) in never-smokers exposed to organic dusts is still poorly characterized. Therapeutic strategies in COPD are only evaluated in smoking-related COPD. Understanding how never-smokers with COPD behave during exercise is an important prerequisite for optimal management. The objective of this study was to compare physiological parameters measured during exercise between never-smokers with COPD exposed to organic dusts and patients with smoking-related COPD matched for age, sex, and severity of airway obstruction. Healthy control subjects were also studied. Dyspnea (Borg scale), exercise tolerance, and ventilatory constraints were assessed during incremental cycle cardiopulmonary exercise testing in COPD patients at mild to moderate stages [22 exposed to organic dusts: postbronchodilator forced expiratory volume in 1 s (FEV)/forced vital capacity (FVC) score -2.44 ± 0.72 and FEV score -1.45 ± 0.78; 22 with smoking-related COPD: FEV/FVC score -2.45 ± 0.61 and FEV score -1.43 ± 0.69] and 44 healthy control subjects (including 22 never-smokers). Despite the occurrence of similar significant dynamic hyperinflation, never-smoker COPD patients exposed to organic dusts had lower dyspnea ratings than those with smoking-related COPD. They also had better ventilatory efficiency, higher peak oxygen consumption and peak power output than smoking-related COPD patients, all these parameters being similar to control subjects. Differences in exercise capacity between the two COPD groups were mainly driven by better ventilatory efficiency stemming from preserved diffusion capacity. Never-smokers exposed to organic dusts with mild to moderate COPD have better exercise capacities, better ventilatory efficiency, and better diffusion capacity than matched patients with smoking-related COPD. It is unknown whether or not never-smokers with chronic obstructive pulmonary disease (COPD) behave like their smoking counterparts during exercise. This is the first study showing that never-smokers with mild to moderate COPD [defined by a postbronchodilator forced expiratory volume in 1 s (FEV)/forced vital capacity (FVC) < lower limit of normal] have preserved exercise capacities. They also have lower exertional dyspnea than patients with smoking-related COPD. This suggests that the two COPD groups should not be managed in the same way.
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http://dx.doi.org/10.1152/japplphysiol.00306.2020DOI Listing
December 2020

Efficacy and safety of rituximab in patients with chronic hypersensitivity pneumonitis (cHP): A retrospective, multicentric, observational study.

Respir Med 2020 10 9;172:106146. Epub 2020 Sep 9.

Department of Pneumology and Respiratory Functional Exploration, University Hospital of Tours, Tours, France; INSERM U-1100, Faculty of Medicine of Tours, Tours, France.

Background: There are chronic forms of hypersensitivity pneumonitis (cHP) that can progress to pulmonary fibrosis. There is no recommended treatment for patients whose respiratory condition continues to deteriorate in spite of antigen avoidance. Whether rituximab may be beneficial to patients with cHP is unknown. The aim of this study was to describe the course of 20 patients with cHP under rituximab therapy.

Methods: This retrospective study was conducted from November 2018 to July 2019 in 7 French university hospitals. Forced Vital Capacity (FVC) was measured 6 months before rituximab therapy onset (M - 6), at rituximab onset (M0), and 6 months later (M+6).

Results: FVC decreased significantly in the 6 months preceding the introduction of rituximab (65% [44; 112%] at M - 6 versus 59% [39; 102%] at M0; p = 0.0001), but it did not differ significantly from that at 6 months after the introduction of rituximab (61% [38; 99%]). The decline in FVC between M0 and M+6 (-3% [-15; +19%]) was significantly less than between M - 6 and M0 (-8% [-21; 0%]) (p = 0.0002). Between M0 (37% [16; 73%]) and M + 6 (45% [15; 70%]), the median DLCO remained stable (p = 0.12). DLCO improved at M+6 in 5 of the 8 patients (63%) for whom a DLCO value was available at M+6 improved their DLCO.

Conclusion: Rituximab seems well tolerated, and may lead to stabilization or improvement of lung function in some patients.
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http://dx.doi.org/10.1016/j.rmed.2020.106146DOI Listing
October 2020

Functional assessment and phenotypic heterogeneity of and mutations in interstitial lung diseases and lung cancer.

Eur Respir J 2020 12 24;56(6). Epub 2020 Dec 24.

Pulmonology Dept, Pasteur Hospital, Nice, France.

Introduction: Interstitial lung diseases (ILDs) can be caused by mutations in the and genes, which encode the surfactant protein (SP) complex SP-A. Only 11 or mutations have so far been reported worldwide, of which five have been functionally assessed. In the framework of ILD molecular diagnosis, we identified 14 independent patients with pathogenic or mutations. The present study aimed to functionally assess the 11 different mutations identified and to accurately describe the disease phenotype of the patients and their affected relatives.

Methods: The consequences of the 11 or mutations were analysed both , by studying the production and secretion of the corresponding mutated proteins and , by analysing SP-A expression in lung tissue samples. The associated disease phenotypes were documented.

Results: For the 11 identified mutations, protein production was preserved but secretion was abolished. The expression pattern of lung SP-A available in six patients was altered and the family history reported ILD and/or lung adenocarcinoma in 13 out of 14 families (93%). Among the 28 mutation carriers, the mean age at ILD onset was 45 years (range 0.6-65 years) and 48% underwent lung transplantation (mean age 51 years). Seven carriers were asymptomatic.

Discussion: This study, which expands the molecular and clinical spectrum of SP-A disorders, shows that pathogenic or mutations share similar consequences for SP-A secretion in cell models and in lung tissue immunostaining, whereas they are associated with a highly variable phenotypic expression of disease, ranging from severe forms requiring lung transplantation to incomplete penetrance.
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http://dx.doi.org/10.1183/13993003.02806-2020DOI Listing
December 2020

Characterization of chronic obstructive pulmonary disease in dairy farmers.

Environ Res 2020 09 25;188:109847. Epub 2020 Jun 25.

Service de Pneumologie, Oncologie Thoracique et Allergologie Respiratoire, CHRU de Besançon, France; UMR CNRS Chrono Environnement, Université de Franche-Comté, Besançon, France.

Background: Although farming is often considered a risk factor for COPD, data regarding the burden and characteristics of COPD in dairy farmers are sparse and conflicting.

Objectives: To characterize COPD in dairy farmers.

Methods: 4788 subjects entered two parallel COPD screening programs, one in agricultural workers and one in general practice from 2011 to 2015. Subjects with COPD were invited to participate in the characterization phase of the study. Those who accepted were included in two subgroups: dairy farmers with COPD (DF-COPD) (n = 101) and non-farmers with COPD (NF-COPD) (n = 85). Patients with COPD were frequency-matched with subjects with normal spirometry for age, sex and tobacco smoking (pack-years and status) (DF-controls n = 98, NF-controls n = 89). All subjects from these four groups underwent lung function and exercise testing, questionnaires and blood analysis.

Results: The frequency of COPD in dairy farmers was 8.0% using the GOLD criterion and 6.2% using the lower limit of normal criterion and was similar in non-farming subjects (7.3% and 5.2%, respectively) although dairy farmers had lower tobacco consumption (screening phase). DF-COPD had better pulmonary function, exercise capacity and quality of life, fewer symptoms and comorbidities than NF-COPD, and higher levels of some Th2 biomarkers (MCP-2, periostin) (characterization phase). In farmers, COPD was not related to occupational exposure factors, supporting the role of host factors.

Conclusion: COPD secondary to organic dust exposure (dairy farming) appears less severe and associated with fewer comorbidities than COPD secondary to tobacco smoking.
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http://dx.doi.org/10.1016/j.envres.2020.109847DOI Listing
September 2020

Diagnosis of Hypersensitivity Pneumonitis in Adults. An Official ATS/JRS/ALAT Clinical Practice Guideline.

Am J Respir Crit Care Med 2020 08;202(3):e36-e69

This guideline addresses the diagnosis of hypersensitivity pneumonitis (HP). It represents a collaborative effort among the American Thoracic Society, Japanese Respiratory Society, and Asociación Latinoamericana del Tórax. Systematic reviews were performed for six questions. The evidence was discussed, and then recommendations were formulated by a multidisciplinary committee of experts in the field of interstitial lung disease and HP using the GRADE (Grading of Recommendations, Assessment, Development, and Evaluation) approach. The guideline committee defined HP, and clinical, radiographic, and pathological features were described. HP was classified into nonfibrotic and fibrotic phenotypes. There was limited evidence that was directly applicable to all questions. The need for a thorough history and a validated questionnaire to identify potential exposures was agreed on. Serum IgG testing against potential antigens associated with HP was suggested to identify potential exposures. For patients with nonfibrotic HP, a recommendation was made in favor of obtaining bronchoalveolar lavage (BAL) fluid for lymphocyte cellular analysis, and suggestions for transbronchial lung biopsy and surgical lung biopsy were also made. For patients with fibrotic HP, suggestions were made in favor of obtaining BAL for lymphocyte cellular analysis, transbronchial lung cryobiopsy, and surgical lung biopsy. Diagnostic criteria were established, and a diagnostic algorithm was created by expert consensus. Knowledge gaps were identified as future research directions. The guideline committee developed a systematic approach to the diagnosis of HP. The approach should be reevaluated as new evidence accumulates.
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http://dx.doi.org/10.1164/rccm.202005-2032STDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7397797PMC
August 2020

Short term association between air pollution (PM, NO and O) and secondary spontaneous pneumothorax.

Sci Rep 2020 07 16;10(1):11823. Epub 2020 Jul 16.

Emergency Department, CHU Besançon, 3 boulevard Alexandre Fleming, 25030, Besançon, France.

Secondary spontaneous pneumothorax (SSP) occurs in the context of underlying pulmonary disease. Our objectives were to estimate the relationship between SSP and short term air pollution exposure with nitrogen dioxide (NO), ozone (O) and particulate matter with a diameter ≤ 10 μm (PM). Patients with SSP were included between June 1, 2009 and May 31, 2013, in 14 Emergency Departments in France. In this case-crossover design study, PM NO, and O data were collected hourly from monitoring stations. Quantitative values, fast increase in air pollutant concentration, and air quality threshold exceedance were retained. These assessments were calculated for each of the 4 days prior to the event (Lag 1-Lag 4) for all case and control period, and for the entire exposure period. A total of 135 patients with SSP were included, with a mean age of 55.56 (SD 18.54) years. For short term exposure of PM, NO and O, no differences were observed between case and control periods in terms of quantitative values of air pollutant exposure (P > 0.68), fast increase in concentration (P > 0.12) or air quality threshold exceedance (P > 0.68). An association between O exposures cannot be ruled out, especially when considering the Lag 2 prior to the event and in warm seasons.
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http://dx.doi.org/10.1038/s41598-020-68831-4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7366720PMC
July 2020

In Patients with Mild-to-Moderate COPD, Tobacco Smoking, and Not COPD, Is Associated with a Higher Risk of Cardiovascular Comorbidity.

Int J Chron Obstruct Pulmon Dis 2020 1;15:1545-1555. Epub 2020 Jul 1.

Service Hospitalier Universitaire Pneumologie Physiologie, Pôle Thorax et Vaisseaux, CHU Grenoble, Alpes, France.

Background: Comorbidities including cardiovascular diseases are very common in chronic obstructive pulmonary disease (COPD) secondary to tobacco smoking and contribute to the overall severity of the disease. In non-smoking COPD, which accounts for about 25% of COPD cases worldwide, current knowledge on the frequency and determinants of comorbidities remains scarce. The aims of the current study were to assess the frequency of major comorbidities and to evaluate their determinants in a group of non-selected patients with mild-to-moderate COPD who were exposed to organic dust (dairy farmers), to tobacco smoking, or to both, and in controls without COPD who were exposed to organic dust (dairy farmers), or to tobacco smoking, or to both, or who were without exposure.

Patients And Methods: A total of 4665 subjects (2323 dairy farmers and 2342 non-farmers) including 355 patients with COPD and 4310 controls with normal spirometry were recruited through a large COPD screening program. Self-reported physician-diagnosed diseases with plausible links to COPD were recorded in this cross-sectional study.

Results: Whatever the exposure, cardiovascular comorbidities were not more frequent in patients with COPD than their counterparts without airflow limitation. A higher risk of major cardiovascular comorbidities was associated with tobacco smoking and a lower risk was associated with exposure to organic dusts.

Conclusion: Tobacco smoking (but not COPD) is associated with higher frequency of cardiovascular comorbidities. By contrast, being a dairy farmer exposed to organic dusts is associated with a lower frequency of the same comorbidities. This reinforces the crucial need for controlling established cardiovascular risk factors even in patients with mild-to-moderate COPD.
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http://dx.doi.org/10.2147/COPD.S253417DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7335866PMC
June 2021

Gender differences in respiratory health outcomes among farming cohorts around the globe: findings from the AGRICOH consortium.

J Agromedicine 2021 04 17;26(2):97-108. Epub 2020 Mar 17.

Monash Centre for Occupational and Environmental Health (MonCOEH), Department of Epidemiology and Preventive Medicine, Faculty of Medicine, Nursing and Health Sciences, Monash University, Melbourne, VIC, Australia.

: Respiratory hazards of farming have been identified for centuries, with little focus on gender differences. We used data from the AGRICOH consortium, a collective of prospective cohorts of agricultural workers, to assess respiratory disease prevalence among adults in 18 cohorts representing over 200,000 farmers, farm workers, and their spouses from six continents.: Cohorts collected data between 1992 and 2016 and ranged in size from 200 to >128,000 individuals; 44% of participants were female. Farming practices varied from subsistence farming to large-scale industrial agriculture. All cohorts provided respiratory outcome information for their cohort based on their study definitions. The majority of outcomes were based on self-report using standard respiratory questionnaires; the greatest variability in assessment methods was associated with chronic obstructive pulmonary disease (COPD).: For all three respiratory symptoms (cough, phlegm, and wheeze), the median prevalence in men was higher than in women, with the greatest difference for phlegm (17% vs. 10%). For asthma, women had a higher prevalence (7.8% vs 6.5%), with the difference associated with allergic asthma. The relative proportion of allergic asthma varied among cohorts. In two of eight cohorts for women and two of seven cohorts for men, allergic asthma was more common than non-allergic asthma.: These findings indicate that respiratory outcomes are common among farmers around the world despite differences in agricultural production. As women in the general population are at higher risk of asthma, exploring gender differences in occupational studies is critical for a deeper understanding of respiratory disease among agricultural workers.
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http://dx.doi.org/10.1080/1059924X.2020.1713274DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7494561PMC
April 2021

Cardiovascular Risk in COPD: Deciphering the Contribution of Tobacco Smoking.

Chest 2020 04 22;157(4):834-845. Epub 2019 Nov 22.

Service Hospitalier Universitaire Pneumologie Physiologie, Pôle Thorax et Vaisseaux, Centre Hospitalier Universitaire Grenoble-Alpes, Grenoble, France; Université Grenoble Alpes, Grenoble, France.

Background: The observation that COPD is an independent risk factor for cardiovascular disease (CVDs) comes from comparisons between smokers with COPD and smokers without COPD. The mechanisms that explain increased risk of CVD in patients with COPD are still unclear.

Objectives: The goal of this study was to assess systemic arterial stiffness (a predictor of CVD mortality) and to evaluate its determinants in a group of patients with mild to moderate COPD secondary to organic dust exposure, tobacco smoking, or both.

Methods: Systemic arterial stiffness was assessed by using aortic pulse wave velocity (aPWV). Measurements were made in 142 patients with COPD and 155 healthy control subjects matched for age, sex, BMI, and tobacco smoking, exposed to tobacco smoking (n = 56/70 for COPD/control subjects, respectively), organic dusts (n = 44/48), or both (n = 42/37).

Results: aPWV was higher in COPD than in healthy controls in subjects exposed to tobacco smoking and to both organic dusts and tobacco smoking. By contrast, among never smokers exposed to organic dusts, patients with COPD and matched control subjects had similar aPWV. Multivariate analysis of the 142 patients with COPD (exposed to tobacco smoking and/or to organic dusts) showed that tobacco smoking was associated with high aPWV. Moreover, soluble suppression of tumorigenicity 2, a marker of major cardiovascular events, was correlated with aPWV in these patients.

Conclusions: Analysis of an unselected group of patients with COPD with different causes suggests that: (1) COPD by itself is not sufficient to explain increased aPWV; and (2) tobacco smoking is a risk factor for elevated aPWV in COPD.
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http://dx.doi.org/10.1016/j.chest.2019.11.002DOI Listing
April 2020

Parents know it best: Prediction of asthma and lung function by parental perception of early wheezing episodes.

Pediatr Allergy Immunol 2019 12 2;30(8):795-802. Epub 2019 Oct 2.

Dr von Hauner Children's Hospital, Ludwig Maximilians University of Munich, Munich, Germany.

Background: Childhood asthma is often preceded by early wheeze. Usually, wheezing episodes are recorded retrospectively, which may induce recall bias.

Aims And Objectives: The aim of this study was to investigate true-positive recall of parent-reported wheeze at 1 year of age, its determinants, and its implications for asthma and lung function at 6 years of age.

Methods: The PASTURE (Protection Against Allergy-Study in Rural Environments) study followed 880 children from rural areas in 5 European countries from birth to age 6 years. Wheeze symptoms in the first year were asked weekly. At age 6, parent-reported asthma diagnosis was ascertained and lung function measurements were conducted. Correct parental recall of wheeze episodes at the end of the first year was assessed for associations with lung function, asthma, and the asthma risk locus on chromosome 17q21.

Results: Parents correctly recalled wheeze after the first year in 54% of wheezers. This true-positive recall was determined by number of episodes, timing of the last wheeze episode, and parental asthma. Independently from these determinants, true-positive recall predicted asthma at age 6 years (odds ratio 4.54, 95% confidence interval (CI) [1.75-14.16]) and impaired lung function (β = -0.62, 95% CI [-1.12; -0.13], P-value = .02). Associations were stronger in children with asthma risk SNPs on chromosome 17q21.

Conclusion: Correct parental recall of wheezing episodes may reflect clinical relevance of early wheeze and its impact on subsequent asthma and lung function impairment. Questions tailored to parental perception of wheezing episodes may further enhance asthma prediction.
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http://dx.doi.org/10.1111/pai.13118DOI Listing
December 2019

TNF-α-induced protein 3 is a key player in childhood asthma development and environment-mediated protection.

J Allergy Clin Immunol 2019 12 2;144(6):1684-1696.e12. Epub 2019 Aug 2.

Pediatric Allergology, Department of Pediatrics, Dr von Hauner Children's Hospital, University Hospital, LMU Munich, Munich, Germany; Member of the German Center for Lung Research-DZL, LMU Munich, Munich, Germany. Electronic address:

Background: Childhood asthma prevalence is significantly greater in urban areas compared with rural/farm environments. Murine studies have shown that TNF-α-induced protein 3 (TNFAIP3; A20), an anti-inflammatory regulator of nuclear factor kappa-light-chain-enhancer of activated B cells (NF-κB) signaling, mediates environmentally induced asthma protection.

Objective: We aimed to determine the role of TNFAIP3 for asthma development in childhood and the immunomodulatory effects of environmental factors.

Methods: In a representative selection of 250 of 2168 children from 2 prospective birth cohorts and 2 cross-sectional studies, we analyzed blood cells of healthy and asthmatic children from urban and rural/farm environments from Europe and China. PBMCs were stimulated ex vivo with dust from "asthma-protective" farms or LPS. NF-κB signaling-related gene and protein expression was assessed in PBMCs and multiplex gene expression assays (NanoString Technologies) in isolated dendritic cells of schoolchildren and in cord blood mononuclear cells from newborns.

Results: Anti-inflammatory TNFAIP3 gene and protein expression was consistently decreased, whereas proinflammatory Toll-like receptor 4 expression was increased in urban asthmatic patients (P < .05), reflecting their increased inflammatory status. Ex vivo farm dust or LPS stimulation restored TNFAIP3 expression to healthy levels in asthmatic patients and shifted NF-κB signaling-associated gene expression toward an anti-inflammatory state (P < .001). Farm/rural children had lower expression, indicating tolerance induction by continuous environmental exposure. Newborns with asthma at school age had reduced TNFAIP3 expression at birth, suggesting TNFAIP3 as a possible biomarker predicting subsequent asthma.

Conclusion: Our data indicate TNFAIP3 as a key regulator during childhood asthma development and its environmentally mediated protection. Because environmental dust exposure conferred the anti-inflammatory effects, it might represent a promising future agent for asthma prevention and treatment.
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http://dx.doi.org/10.1016/j.jaci.2019.07.029DOI Listing
December 2019

Dietary Patterns and Prevalence of Post-bronchodilator Airway Obstruction in Dairy Farmers Exposed to Organic Dusts.

COPD 2019 04 12;16(2):118-125. Epub 2019 Jul 12.

i Service Hospitalier Universitaire Pneumologie Physiologie, Pôle Thorax et Vaisseaux, CHU Grenoble Alpes , Grenoble , France.

Exposure to organic dusts is an independent causative factor of chronic obstructive pulmonary disease (COPD). Unhealthy dietary patterns have been associated with poor lung function in smokers. This study investigated whether dietary patterns were associated with post-bronchodilator airway obstruction, a hallmark of COPD, in dairy farmers exposed to organic dusts. All subjects were identified by screening programs and patients with airflow obstruction were matched with subjects with normal spirometry. Six groups were compared, defined by their exposures (non-smoking dairy farmers, smokers ≥ 10 pack-years with no occupational exposure, and smoking dairy farmers) and the presence or absence of post-bronchodilator airflow obstruction, resulting in 321 study subjects. The Alternative Healthy Eating Index (AHEI) score was calculated based on an adapted food frequency questionnaire. Mean total AHEI scores were similar in all groups. Comparison between smokers with post-bronchodilator airway obstruction and subjects with post-bronchodilator airway obstruction related to occupational exposure found minimal differences in dietary patterns: dairy farmers had lower scores for the ratio of white to red meat and higher scores for cereal fiber consumption. As in previous studies, smokers with post-bronchodilator airway obstruction exhibited higher lipid intakes and lower carbohydrate intakes than their counterparts with normal spirometry. No evidence of any meaningful difference in dietary patterns was found between subjects with post-bronchodilator airway obstruction detected by screening and healthy controls, either in dairy farmers or in smokers with no occupational exposure.
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http://dx.doi.org/10.1080/15412555.2019.1631775DOI Listing
April 2019

Is atopy a risk indicator of chronic obstructive pulmonary disease in dairy farmers?

Respir Res 2019 Jun 17;20(1):124. Epub 2019 Jun 17.

Service de Pneumologie, Oncologie thoracique et Allergologie respiratoire, 3 Boulevard Fleming, 25000, Besancon, France.

Allergic mechanisms related to environmental and occupational exposure have been suggested to contribute to the development of chronic obstructive pulmonary disease (COPD).

Objectives: To investigate the relationships between atopy markers, persistent airflow limitation (PAL) and occupational exposure in dairy farmers.

Methods: Clinical and biological (total IgE and 21 allergen specific IgE) markers of atopy were assessed in 101 dairy farmers with PAL (DF-PAL), 85 non-farmers with PAL (NF-PAL) (both groups were prospectively included from a screening program performed between 2011 and 2015), and matched controls, i.e. 98 farmers without PAL (DF-controls) and 89 non-farming subjects without PAL (NF-controls). Occupational exposure in farmers was estimated using a validated questionnaire.

Results: Prevalence of allergy history was significantly higher in DF-PAL and in NF-PAL than in controls. Polysensitization, and sensitization to seasonal and food allergens were more frequent in DF-PAL than in DF-controls, respectively: 13.8% vs 1% (adjusted odds ratio (aOR): 17.5 (2.2-134), 11.9% vs 3.1% (aOR: 4.4 (1.2-7.2) and 16.8% vs 4.1% (aOR: 5.2 (1.7-7.2)). The prevalence of atopy markers was similar between NF-PAL patients and NF-controls.

Conclusions: PAL in farmers is associated with a high rate of markers of atopy, supporting atopy as a risk indicator. Clinical trial registered with ClinicalTrials.gov (NCT02540408).
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http://dx.doi.org/10.1186/s12931-019-1082-2DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6580567PMC
June 2019

Does air pollution really impact the onset of spontaneous pneumothorax? A French case-crossover study.

Environ Int 2019 06 3;127:317-323. Epub 2019 Apr 3.

Emergency Department, CHU de Besançon, 3 boulevard Alexandre Fleming, 25030 Besançon, France; Laboratory Chrono-environnement, UMR 6249 Centre National de la Recherche Scientifique, 16 route de Gray, 25000 Besançon, France; Université Bourgogne Franche-Comté, 32 avenue de l'Observatoire, 25000 Besançon, France.

Rationale: A link is established between air pollution and respiratory diseases. Very few studies evaluated this link with primary spontaneous pneumothorax (PSP). Contrasted results, low statistical power and methodological limits of these studies brought us to evaluate in a more thorough way this link.

Objectives: (1) to estimate the relation between PSP and air pollutants namely nitrogen dioxide (NO, ozone (O and particulate matter with a diameter ≤ 10 μm (PM); (2) to investigate a time lag effect between these pollutants and occurrence of PSP.

Methods: This study has a case-crossover design. Subjects aged ≥18 years admitted from 1st June 2009 to 31st May 2013, in 14 Emergency Departments centers on the French territory. Were excluded: patients with traumatic, secondary, recurrent or history of previous pneumothorax. NO, O and PM data were collected hourly in monitoring stations. Three exposure assessments were retained: quantitative values, fast increase concentration of air pollutants and peak of pollution. These assessments were calculated for the entire exposure period and for each of the four days of all case and control periods.

Results: 948 subjects included. Whatever the pollutant considered, no differences were observed between case and control periods, regardless of whether the quantitative values of air pollutants exposure (p > 0.09), fast increase concentration (p > 0.46) and peak of pollution (p > 0.20).

Conclusions: We failed to show a relation between PSP and short-term air pollution exposure to low levels of NO and PM. An association between O exposure and PSP cannot be ruled out. An impact at higher exposure level, and/or a potentiating effect of different meteorological factors remain to be demonstrated.
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http://dx.doi.org/10.1016/j.envint.2019.01.056DOI Listing
June 2019

Association between antibiotic treatment during pregnancy and infancy and the development of allergic diseases.

Pediatr Allergy Immunol 2019 06 5;30(4):423-433. Epub 2019 Mar 5.

Christine Kühne-Center for Allergy Research and Education, Davos, Switzerland.

Background: Allergies are a serious public health issue, and prevalences are rising worldwide. The role of antibiotics in the development of allergies has repeatedly been discussed, as results remain inconsistent. The aim of this study was to investigate the association between pre- and post-natal antibiotic exposure and subsequent development of allergies (atopic dermatitis, food allergy, asthma, atopic sensitization and allergic rhinitis).

Methods: A total of 1080 children who participated in a European birth cohort study (PASTURE) were included in this analysis. Data on antibiotic exposure during pregnancy and/or first year of life and allergic diseases were collected by questionnaires from pregnancy up to 6 years of age and analysed by performing logistic regressions. To take into account reverse causation, we included models, where children with diagnosis or symptoms of the respective disease in the first year of life were excluded.

Results: Antibiotic exposure in utero was significantly and positively associated with atopic dermatitis and food allergy. The strongest effect was on diseases with onset within the first year of life (for atopic dermatitis: aOR 1.66, 95% CI 1.11-2.48 and for food allergy: aOR 3.01, 95% CI 1.22-7.47). Antibiotics in the first year of life were positively associated with atopic dermatitis up to 4 years (aOR 2.73, 95% CI 1.66-4.49) and also suggested a dose-response relationship. A tendency was observed with asthma between 3 and 6 years (aOR 1.65, 95% CI 0.95-2.86).

Conclusions: Our findings show positive associations between exposure to antibiotics and allergies, mainly atopic dermatitis and food allergy within the first year of life, after prenatal exposure, and atopic dermatitis and asthma after post-natal exposure to antibiotics in children born in rural settings.
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http://dx.doi.org/10.1111/pai.13039DOI Listing
June 2019

Clinical and microbiological characteristics of cystic fibrosis adults never colonized by Pseudomonas aeruginosa: Analysis of the French CF registry.

PLoS One 2019 8;14(1):e0210201. Epub 2019 Jan 8.

UMR/CNRS 6249 Chrono-Environnement, University of Franche-Comté, Besançon, France.

Pseudomonas aeruginosa is the main cause of chronic airway infection in cystic fibrosis (CF). However, for unclear reasons some patients are never colonized by P. aeruginosa. The objectives of this study were to better define the clinical, genetic, and microbiological characteristics of such a subpopulation and to identify predictive factors of non-colonization with P. aeruginosa. The French CF patient registry 2013-2014 was used to identify CF patients aged ≥ 20 years. The clinical outcomes, CF Transmembrane conductance Regulator (CFTR) genotypes, and microbiological data of patients reported positive at least once for P. aeruginosa ("Pyo" group, n = 1,827) were compared to those of patients with no history of P. aeruginosa isolation ("Never" group, n = 303). Predictive factors of non-colonization by P. aeruginosa were identified by multivariate logistic regression model with backward selection. Absence of aspergillosis (odds ratio (OR) [95% CI] = 1.64 [1.01-2.66]), absence of diabetes (2.25 [1.21-4.18]), pancreatic sufficiency (1.81 [1.30-2.52]), forced expiratory volume 1 (FEV1) ≥ 80% (3.03 [2.28-4.03]), older age at CF diagnosis (1.03 [1.02-1.04]), and absence of F508del/F508del genotype (2.17 [1.48-3.19]) were predictive clinical factors associated with absence of infection ("Never" group). Microbiologically, this same group was associated with more frequent detection of Haemophilus influenzae and lower rates of Stenotrophomonas maltophilia, Achromobacter xylosoxidans and Aspergillus spp. (all p<0.01) in sputum. This study strongly suggests that the absence of pulmonary colonization by P. aeruginosa in a minority of CF adults (14.2%) is associated with a milder form of the disease. Recent progress in the development of drugs to correct CFTR deficiency thus may be decisive in the control of P. aeruginosa lung infection.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0210201PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6324790PMC
September 2019

COPD, airflow limitation and chronic bronchitis in farmers: a systematic review and meta-analysis.

Occup Environ Med 2019 01 27;76(1):58-68. Epub 2018 Nov 27.

Service Hospitalier Universitaire Pneumologie Physiologie, Pôle Thorax et Vaisseaux, Grenoble, France.

Introduction: The current definition of chronic obstructive pulmonary disease (COPD) associates persistent airflow limitation and chronic respiratory symptoms. Agricultural work has been associated with an increased risk of developing COPD, but the prevalence and definition of the disease vary greatly between studies. This meta-analysis aimed to assess the association between agricultural work and COPD using the most widely used definitions of the disease.

Methods: Inclusion criteria were: (1) design: cross-sectional or longitudinal, (2) groups: at least one group of farmers and a control group of non-farmers, (3) outcome: prevalence or unadjusted OR of COPD, airflow limitation and/or chronic bronchitis, (4) study subjects: groups of exposed subjects comprising ≥30 individuals and with a mean age ≥40 years and (5) language: English and French language, full-length, original publications in peer-reviewed journals.

Results: In total, 22 manuscripts were included in the meta-analysis. Eight studies assessed only the prevalence of airflow limitation, nine assessed only the prevalence of chronic bronchitis and four assessed the prevalence of both these parameters. Only one assessed the prevalence of COPD according to its current definition, and this study also provided the prevalence of airflow limitation. Ten studies showed a positive association between farming exposure and airflow limitation or chronic bronchitis, and 12 showed no association (OR (95% CI)=1.77 (1.50 to 2.08), p<0.001). Cattle, swine, poultry and crop farming were associated with either airflow limitation or chronic bronchitis.

Conclusion: Although some features of COPD are associated with some agricultural work, well-designed studies with appropriate diagnostic criteria should be conducted to draw strong conclusions about the relationship between COPD and farming.
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http://dx.doi.org/10.1136/oemed-2018-105310DOI Listing
January 2019

Microbial exposure to dairy farmers' dwellings and COPD occurrence.

Int J Environ Health Res 2019 Aug 21;29(4):387-399. Epub 2018 Nov 21.

a UMR/CNRS 6249 Chrono-Environnement, UFR Sciences médicales et pharmaceutiques , University of Bourgogne Franche-Comté , Besançon , France.

Dairy farming is a risk factor for chronic obstructive pulmonary disease (COPD). The aim was to determine predictive markers either in blood samples or in dwelling dust samples by comparing COPD and healthy controls with or without farming activity. Dust was collected and analyzed by real-time quantitative PCR. ELISA and DELFIA® were performed to assay the level of specific IgG and IgE of 10 targeted microorganisms. The dwelling exposure of farmers was higher than in the non-farmers (Especially and ). The IgG response against and was more often higher in the farmers than the non-farmers. However, exposure and sensitization to the microorganisms tested cannot explain the occurrence of COPD in the dairy farmers' population. COPD development is probably caused by multiple factors associated with exposure over a period of several years.
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http://dx.doi.org/10.1080/09603123.2018.1545900DOI Listing
August 2019

High levels of butyrate and propionate in early life are associated with protection against atopy.

Allergy 2019 04 25;74(4):799-809. Epub 2018 Nov 25.

Christine Kühne-Center for Allergy Research and Education (CK-CARE), Davos, Switzerland.

Background: Dietary changes are suggested to play a role in the increasing prevalence of allergic diseases and asthma. Short-chain fatty acids (SCFAs) are metabolites present in certain foods and are produced by microbes in the gut following fermentation of fibers. SCFAs have been shown to have anti-inflammatory properties in animal models. Our objective was to investigate the potential role of SCFAs in the prevention of allergy and asthma.

Methods: We analyzed SCFA levels by high-performance liquid chromatography (HPLC) in fecal samples from 301 one-year-old children from a birth cohort and examined their association with early life exposures, especially diet, and allergy and asthma later in life. Data on exposures and allergic diseases were collected by questionnaires. In addition, we treated mice with SCFAs to examine their effect on allergic airway inflammation.

Results: Significant associations between the levels of SCFAs and the infant's diet were identified. Children with the highest levels of butyrate and propionate (≥95th percentile) in feces at the age of one year had significantly less atopic sensitization and were less likely to have asthma between 3 and 6 years. Children with the highest levels of butyrate were also less likely to have a reported diagnosis of food allergy or allergic rhinitis. Oral administration of SCFAs to mice significantly reduced the severity of allergic airway inflammation.

Conclusion: Our results suggest that strategies to increase SCFA levels could be a new dietary preventive option for allergic diseases in children.
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http://dx.doi.org/10.1111/all.13660DOI Listing
April 2019

The protective effect of cheese consumption at 18 months on allergic diseases in the first 6 years.

Allergy 2019 04 19;74(4):788-798. Epub 2018 Nov 19.

University Hospital of Besançon, Respiratory Disease, UMR6249 ChronoEnvironnement, CNRS and Université Bourgogne Franche-Comté, Besançon, France.

Background: The effect of exposure to microorganisms on allergic diseases has been well studied. The protective effect of early food diversity against allergic diseases was previously shown in the PASTURE cohort study. The consumption of cheese, a food potentially rich in microbial diversity, deserves further examination. We aimed to evaluate whether cheese consumption is associated with allergic diseases.

Methods: In the PASTURE study (birth cohort in 5 European countries), data on feeding practices, environmental factors, and allergic diseases were collected by questionnaires from birth to 6 years (N = 931). Cheese consumption at 18 months of age was quantified in terms of frequency and diversity (ie, number of consumed types among 6 types: hard pressed, semipressed, soft, blue, fresh cheese, and cheese from the farm). Multiple logistic regressions were performed to evaluate the effect of cheese consumption on atopic dermatitis (AD), food allergy (FA), allergic rhinitis, asthma, and atopic sensitization at 6 years after adjustment for confounders of atopy.

Results: Cheese consumption (vs. nonconsumption) had a significant protective effect on AD (OR = 0.51 [0.29-0.90], P = 0.02) and FA (OR = 0.32, [0.15-0.71], P = 0.004), but no effect on atopic sensitization, allergic rhinitis, and asthma at 6 years. This effect on AD and FA may be related to the diversity of consumed cheeses (OR = 0.64 [0.48-0.85] per cheese type, P = 0.002; OR = 0.55 [0.33-0.92], P = 0.02, respectively).

Conclusion: Although reverse causality cannot totally be ruled out, cheese diversity at 18 months had a protective effect against AD and FA at 6 years in addition to the protective effect of diversity of other foods.
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http://dx.doi.org/10.1111/all.13650DOI Listing
April 2019

Fungal contamination of wind instruments: Immunological and clinical consequences for musicians.

Sci Total Environ 2019 Jan 25;646:727-734. Epub 2018 Jul 25.

Service de Pneumologie, Centre Hospitalier Universitaire de Besançon, Besançon, France; UMR-CNRS 6249 Chrono-environnement, Université de Franche-Comté, Besançon, France.

Introduction: Playing a wind instrument is an increasingly reported cause of hypersensitivity pneumonitis. However, current knowledge about contamination of wind instruments by fungi and specific fungal sensitization is scarce. Therefore, we aimed: (i) to assess the current prevalence and type of fungal contamination of wind instruments, (ii) to identify potential risk factors associated with instrument contamination, and (iii) to evaluate the prevalence of sensitization to these fungi among musicians.

Material And Methods: Musicians from music schools in eastern France and who played a wind instrument were prospectively recruited (NCT01487850). The mouthpiece and the reed of their instrument were sampled to quantify the magnitude and type of fungi. Each subject had a physical examination, a mycological analysis of saliva and a blood sample in search of serum precipitins against the most frequent fungi isolated from instruments. The results were compared with those of 40 healthy non-exposed controls.

Results: Forty musicians playing a wind instrument (bassoon, clarinet, oboe, saxophone) were included. (i) 95% of wind instruments were colonized by fungi, mainly with Phoma spp., Penicillium spp. and Rhodotorula mucilaginosa; (ii) absence of systematic drying of the instrument was a main contributing factor; (iii) serum precipitins were significantly more present in the musicians' sera than in control sera and were consistent with the fungi present in their instrument.

Conclusion: This study reveals a constant and specific fungal contamination among wind reed instruments with a significant sensitization among musicians, pleading in favour of regular instrument cleaning. Physicians should be aware of this possible source of antigenic exposure.
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http://dx.doi.org/10.1016/j.scitotenv.2018.07.284DOI Listing
January 2019

Current and emerging techniques for the diagnosis of hypersensitivity pneumonitis.

Expert Rev Respir Med 2018 06 11;12(6):493-507. Epub 2018 May 11.

a Service de Pneumologie , CHU de Besançon , Besançon , France.

Introduction: Hypersensitivity pneumonitis (HP) is the result of an immunologically induced inflammation of the lung parenchyma in response to inhalation exposure to a large variety of antigens in genetically susceptible individuals. HP shares clinical and radiological features with other acute and chronic interstitial lung diseases and is sometimes difficult to diagnose if exposure to an antigenic agent is not detected. Several classifications and diagnostic criteria have been proposed but are not currently recommended by guidelines from any scientific society. However, advances have been made over the past ten years in improving the diagnosis of HP. Areas covered: This article will provide a summary of the different classification and diagnostic criteria proposed in acute and chronic forms of HP. In addition, we review current diagnostic procedures including antigen detection, high resolution computed tomography, histopathology and provide an overview of emerging techniques. Expert commentary: Important changes are occurring in the field of HP and knowledge of the disease will likely progress enormously in the coming 5 to 10 years as many techniques continue to be developed, including genomic signature and diagnostic biomarkers.
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http://dx.doi.org/10.1080/17476348.2018.1473036DOI Listing
June 2018

Anxiety and depression among dairy farmers: the impact of COPD.

Int J Chron Obstruct Pulmon Dis 2018 19;13:1-9. Epub 2017 Dec 19.

Department of Respiratory Diseases, University Hospital, Besançon, France.

Background: Chronic obstructive pulmonary disease (COPD) and farming are two conditions that have been associated with an increased risk of anxiety and depression. Dairy farming is an independent risk factor for COPD.

Objective: To test the hypotheses that the prevalence of anxiety and/or depression is higher in dairy farmers with COPD than in farmers without COPD, and higher in dairy farmers with COPD than in non-farmers with COPD.

Methods: Anxiety and depression were evaluated using the Hospital Anxiety and Depression Scale in 100 dairy farmers with COPD (DF-COPD), 98 dairy farmers without COPD (DF-controls), 85 non-farming patients with COPD (NF-COPD) and 89 non-farming subjects without COPD (NF-controls), all identified by screening in the Franche-Comté region of France. Anxiety and depression were considered present when the Hospital Anxiety and Depression Scale score was ≥8. COPD was defined by a post-bronchodilator forced expiratory volume in 1 second/forced vital capacity ratio <0.7.

Results: The crude prevalence of anxiety did not differ between the four groups, ranging from 36% in NF-controls to 47% in NF-COPD (=0.15 between groups). Similarly, the prevalence of depression did not differ significantly between the four groups (=0.16 between groups). In dairy farmers (n=198), the only factors associated with anxiety were quality of life and current smoking. Depression in dairy farmers was associated with airflow limitation (lower forced expiratory volume in 1 second and COPD grade 2 or more) as well as with some COPD-related features (dyspnea severity, current smoking, and poorer quality of life). In non-farmers, both anxiety and depression were associated with airflow limitation and COPD-related features.

Conclusion: In our population, the prevalence of anxiety and/or depression was similar in dairy farmers with and without COPD and in non-farmers with COPD. Nevertheless, the degree of airway obstruction and some COPD-related features were associated with depression among dairy farmers, whereas these factors were not associated with anxiety.
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http://dx.doi.org/10.2147/COPD.S143883DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5741076PMC
September 2018

[COPD: think about occupational exposures!]

Rev Prat 2018 Jan;68(1):74-78

Service de pneumologie, hôpital Jean-Minjoz, université de Franche-Comté, CHRU, Besançon, France.

Copd: think about occupational exposures! Unfortunately, the occupational exposures of COPD are still poorly taught and poorly researched, although they account for 15 to 20% of all COPD. The clinician must know them well and therefore systematically seek them for any newly diagnosed case. A thorough and rigorous professional interview allows to trace the entire professional career, even when the patient smokes. The main exposures in industrial and agricultural sectors are described. Recognition of COPD in occupational diseases is only possible in France since a few years, in a restrictive way. The prevention of occupational COPD (reduction or elimination of environmental pollution in the workplace) is likely to reduce the incidence of COPD in exposed workers. A regular monitoring to detect early COPD (spirometry) is needed.
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January 2018

Usefulness of à la carte antigens for bird fancier's lung serodiagnosis: total dropping extract and/or dropping's microflora antigens.

J Med Microbiol 2017 Oct 13;66(10):1467-1470. Epub 2017 Sep 13.

UMR 6249 Chrono-Environment, University of Bourgogne-Franche-Comté, Besançon, France.

Bird fancier's lung (BFL) is a pulmonary disease caused by inhalation of avian proteins. The involvement of the microorganisms of droppings has been assumed in the past and this idea still persists today. Our study aimed to compare by immunoprecipitation assay the detection of antibodies against both droppings and microorganisms in the sera of patients (n=15) and asymptomatic exposed controls (n=18). We found that 14/15 BFL patients had negative serological results for isolated microorganisms of the droppings, only one positive against Enterobacter sakasakii. Serological arguments were in accordance with diagnosis in 87 % of cases by testing à la carte antigens from each bird dropping versus 20 % using the standard antigenic panel. Otherwise, the microorganisms antigens issued from dropping flora were negative in 93 % of cases. Consequently, it's preferable to use the total extract from the patient's bird droppings to establish the serodiagnosis of the disease.
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http://dx.doi.org/10.1099/jmm.0.000586DOI Listing
October 2017
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