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Risk Factors for Diagnostic Delay in Idiopathic Pulmonary Fibrosis Nils Hoyer1* , Thomas Skovhus Prior2, Elisabeth Bendstrup2, Torgny Wilcke1 and Saher Burhan Shaker1

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Risk Factors for Diagnostic Delay in Idiopathic Pulmonary Fibrosis Nils Hoyer1* , Thomas Skovhus Prior2, Elisabeth Bendstrup2, Torgny Wilcke1 and Saher Burhan Shaker1 Hoyer et al. Respiratory Research (2019) 20:103 https://doi.org/10.1186/s12931-019-1076-0 RESEARCH Open Access Risk factors for diagnostic delay in idiopathic pulmonary fibrosis Nils Hoyer1* , Thomas Skovhus Prior2, Elisabeth Bendstrup2, Torgny Wilcke1 and Saher Burhan Shaker1 Abstract Background: Surveys and retrospective studies of patients with idiopathic pulmonary fibrosis (IPF) have shown a significant diagnostic delay. However, the causes and risk factors for this delay are not known. Methods: Dates at six time points before the IPF diagnosis (onset of symptoms, first contact to a general practitioner, first hospital contact, referral to an interstitial lung disease (ILD) centre, first visit at an ILD centre, and final diagnosis) were recorded in a multicentre cohort of 204 incident IPF patients. Based on these dates, the delay was divided into specific patient-related and healthcare-related delays. Demographic and clinical data were used to determine risk factors for a prolonged delay, using multivariate negative binomial regression analysis. Results: The median diagnostic delay was 2.1 years (IQR: 0.9–5.0), mainly attributable to the patients, general practitioners and community hospitals. Male sex was a risk factor for patient delay (IRR: 3.84, 95% CI: 1.17–11.36, p = 0.006) and old age was a risk factor for healthcare delay (IRR: 1.03, 95% CI: 1.01–1.06, p = 0.004). The total delay was prolonged in previous users of inhalation therapy (IRR: 1.99, 95% CI: 1.40–2.88, p < 0.0001) but not in patients with airway obstruction. Misdiagnosis of respiratory symptoms was reported by 41% of all patients. Conclusion: Despite increased awareness of IPF, the diagnostic delay is still 2.1 years. Male sex, older age and treatment attempts for alternative diagnoses are risk factors for a delayed diagnosis of IPF. Efforts to reduce the diagnostic delay should focus on these risk factors. Trial registration: This study was registered at http://clinicaltrials.gov (NCT02772549) on May 10, 2016. Keywords: IPF, Diagnosis, Delay, Cohort, Observational Background prognosis [5]. Current medical treatment of IPF can slow Idiopathic Pulmonary Fibrosis (IPF) is a debilitating down the progression of the disease but does not seem chronic lung disease. Despite recent advances in antifi- to reverse any fibrotic changes that already have oc- brotic therapy, the prognosis is poor with a median sur- curred [9–11]. Timely diagnosis is therefore important vival of 2–5 years [1, 2]. The diagnosis of IPF can be in order to initiate early treatment, prevent lung tissue challenging, and due to its rarity, few physicians gain from developing fibrosis, delay disease progression and enough expertise to become familiar with the disease. In prolong survival [4, 8]. addition, the diagnosis often requires a multidisciplinary The cause of the diagnostic delay is not well known team, which is not available in all centres [3, 4]. Surveys but is probably multifactorial. Surveys suggest that mis- and retrospective studies have shown a significant diag- interpretation of respiratory symptoms could be a con- nostic delay from the onset of symptoms until the final tributing factor [6, 12]. The first symptoms of IPF are diagnosis is made [5–8]. This results in a delayed start of often cough and shortness of breath, which are often at- effective antifibrotic treatment and lung transplant tributed to old age, smoking or more common cardio- evaluation, and can affect the disease course and vascular or respiratory diseases by either the patient or healthcare professionals as it is the case in patients with chronic obstructive pulmonary disease (COPD) [13]. * Correspondence: [email protected] 1Department of Respiratory Medicine, Herlev and Gentofte Hospital, The distribution of the diagnostic delay between Kildegårdsvej 28, 2900 Hellerup, Denmark patient-related and healthcare-related causes is still Full list of author information is available at the end of the article © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Hoyer et al. Respiratory Research (2019) 20:103 Page 2 of 9 largely unknown. Moreover, we are not aware of any severity were collected from the patients’ electronic re- studies detailing the risk factors for a delayed diagnosis. cords: comprehensive pulmonary function tests with spir- A thorough understanding of these risk factors is essen- ometry and diffusing capacity for carbon monoxide tial for any attempts to reduce the diagnostic delay. (DLCO), six-minute walk test (6MWT) and high reso- To answer these questions, we used a well character- lution computed tomography (HRCT) scan. ized multicentre cohort of incident IPF patients to inves- The diagnostic delay was calculated based on six tigate the diagnostic delay and determine specific risk pre-defined time points on the patients’ path towards an factors for a delayed diagnosis. IPF diagnosis (Fig. 1). The first two time points (dates of symptom onset and first contact with a general practi- Materials and methods tioner) were part of the survey which was completed by Patient cohort each patient shortly after their diagnosis. All remaining The Pulmonary Fibrosis Biomarker (PFBIO) cohort pro- time points were collected from the patients’ electronic re- spectively recruits incident patients with IPF from two cords. The specific delays were calculated from these time large interstitial lung disease (ILD) centres in Denmark points and are illustrated in Fig. 1. If a time point was not serving a population of 4.2 million. The main purpose of relevant in a patient’s path towards an IPF diagnosis (i.e. if the cohort is to follow a broad population of patients the first contact with a physician was at a community hos- with IPF and create a biorepository for biomarker re- pital or if a patient was referred directly to an ILD centre search. Antifibrotic therapy is centralized in Denmark by the general practitioner), the jumped delay was ex- and referral to one of the three specialized ILD centres cluded for that patient in the statistical analysis. is necessary for patients to be eligible for treatment. Re- cruitment for the PFBIO cohort started in 2016 and is Statistical analysis still ongoing at one of the participating centres (Gentofte Descriptive data are presented as frequency tables, mean Hospital) for future studies. At the time of analysis, the (SD) or median (interquartile range, IQR) as appropriate cohort had included 204 patients. All participants had for the data. Univariate analyses of baseline characteris- received a diagnosis of IPF according to the 2011 ATS/ tics were performed with a t-test or chi-squared test as ERS/JRS/ALAT guidelines at an ILD centre, based on a appropriate for the data. multidisciplinary team approach [3, 14]. Patients were None of the specific delays were normally distributed recruited on the same day as they received the diagnosis and are presented as medians with IQR. We used multi- or up to a maximum of two months later but prior to variate negative binomial regression models to deter- initiating antifibrotic treatment. All patients with IPF mine specific risk factors for patient delay, healthcare were eligible for participation unless they were unable to delay and total delay respectively, as the delays were provide written informed consent. A flowchart of the re- counts of days and did not fit a Poisson distribution. cruitment process is presented in the Additional files 1. Covariates were tested for normality before inclusion into any statistical analysis. Missing data were handled by Data collection listwise deletion using complete cases without any imput- Patients completed a detailed survey at the time of diag- ation of data. nosis which was followed up by an interview if needed for clarification (see Additional file 1). The survey included Ethics, consent and permissions questions about the onset of symptoms, initial healthcare All participants were included after written informed con- contact, smoking history, alternative diagnoses for respira- sent, and none had chosen to withdraw from the study at tory symptoms, and previous therapies. The patients’ the time of analysis. The study has been approved by the quality of life was assessed by the St. George’sRespiratory Capital Region regional ethics committee (H-16001790) Questionnaire (SGRQ) with higher scores indicating and the Danish Data Protection Agency (HGH-2016-017). worse quality of life [15]. Several measures of disease The study was also registered at http://clinicaltrials.gov Fig. 1 Diagnostic delay from patients’ awareness of symptoms until an IPF diagnosis is made. The total delay is divided into patient delay and healthcare delay (GP delay, hospital delay, waiting delay and specialized delay combined) Hoyer et al. Respiratory Research (2019) 20:103 Page 3 of 9 (NCT02772549). We conducted the study according to on the diagnostic HRCT, which however did not reach stat- the principles of the Declaration of Helsinki and adhered istical significance (Table 2). Although rarely performed, to the STROBE guidelines. transbronchial cryobiopsies were more common in patients with a short delay (Table 2). We were unable to calculate Results total delay for 14 patients, due to imprecise data about their The baseline characteristics of the 204 participants in the onset of symptoms. Baseline data for this group is pre- PFBIO cohort are listed in Table 1. Patients were stratified sented in the Additional file 1. according to length of total diagnostic delay above or below 2 years.
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