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Diagnostic delay in lung cancer in Morocco: A 4-year retrospective study

Open AccessPublished:June 28, 2022DOI:https://doi.org/10.1016/j.cegh.2022.101105

      Abstract

      Background

      Lung cancer is a major cause of morbidity and mortality worldwide. The diagnosis of lung cancer is complex and can be easily missed or delayed. The aim of this study is to describe the delay in diagnosis and evaluate the factors associated with diagnosis delay.

      Methods

      All patients diagnosed with primary lung cancer at Moulay Youssef University hospital in Rabat from January 2014 to December 2017 were investigated retrospectively. Data relating to patient characteristics, tumor characteristics, and all dates of visits and investigations were collected. Multivariate linear regression analysis was used to identify risk factors linked to delayed diagnosis.

      Results

      A total of 81 patients were included (81,5% were men). Around 85.2% of patients presented lung-related symptoms. Cough and dyspnea were the most common symptoms. The median time of the patient presentation was 75 days (interquartile interval (IQI) = 30–150 days), patient referral time was 08 days (IQI = 02–14 days), diagnosis time was 21 days (IQI = 14–22 days). In multivariate analysis, a higher age (p = 0.044) and weight loss (p = 0.038) were associated with an increased presentation patient time. Asthma (p = 0.004) and chronic obstructive pulmonary disease (COPD) (p = 0.040) were significantly associated with delayed referral time. Diagnosis time was longer in patients with non-suspected Chest-X ray (p = 0.045) and earlier in patients diagnosed with computed tomography-guided biopsy (p = 0.030).

      Conclusion

      Intervals of diagnosis were significantly delayed and highly affected by patients and diagnostic times. Thus, the results emphasize the extreme need to develop efficient strategies to improve lung cancer diagnosis intervals.

      Keywords

      1. Introduction

      Lung cancer is a serious problem of public health worldwide.
      • Ferlay J.
      • Soerjomataram I.
      • Dikshit R.
      • et al.
      Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012: globocan 2012.
      Over the past century, lung carcinoma has grown from a rare disease to the leading cancer and the most common cause of cancer death in the world,
      • De Groot P.M.
      • Wu C.C.
      • Carter B.W.
      • Munden R.F.
      The epidemiology of lung cancer.
      registering 2.2 million new cases and 1.8 million death by 2020.
      • Sung H.
      • Ferlay J.
      • Siegel R.L.
      • et al.
      Global cancer Statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries.
      In Morocco, lung cancer is the deadliest cancer for both sexes.
      • Abdelaziz A.B.
      • Melki S.
      • Nouira S.
      • et al.
      Cancers in the central maghreb: epidemiology from 1990 to 2017 and trends in 2040.
      This disease will continue to rank first in the list of cancers in Morocco, in 2040, with a rate of mortality of 16/100 000.
      • Abdelaziz A.B.
      • Melki S.
      • Nouira S.
      • et al.
      Cancers in the central maghreb: epidemiology from 1990 to 2017 and trends in 2040.
      Lung cancer is often diagnosed in symptomatic patients.
      • Leiro-Fernández V.
      • Botana-rial M.
      • Tilve-Gomez A.
      • Represas-Represas C.
      • Pallarés- Sanmartin A.
      • Fernandez-Villar A.
      Predicting delays in lung cancer diagnosis and staging: delays in LC diagnosis and staging.
      The core symptoms of lung cancer include cough, dyspnea, chest pain, fatigue, hemoptysis, and weight loss.
      • Ellis P.M.
      • Vandermeer R.
      Delays in the diagnosis of lung cancer.
      Those symptoms are very common in general practice, it would be difficult to distinguish them from the symptoms of other respiratory diseases.
      • Ellis P.M.
      • Vandermeer R.
      Delays in the diagnosis of lung cancer.
      Such overlap of symptoms could cause delays in diagnosis of lung cancer,
      • Bjerager M.
      • Palshof T.
      • Dahl R.
      • Vedsted P.
      • Olesen F.
      Delay in diagnosis of lung cancer in general practice.
      which may alter the tumor stage and, in that way, patients lose their chance for surgery. In addition, cancer patients face many psychological, socioeconomic, and familial obstacles to receive the required diagnosis and treatment.
      • Massimo A.
      • Claudia B.
      • Cinzia D.G.
      • Fabio F.
      • Luigi C.
      Distance as a barrier to cancer diagnosis and treatment: review of the literature.
      Shortening the delay times might increase the number of early-stage cancer, and consequently, improve survival. In the literature, several studies have focused on the study of diagnosis delays of patients with lung cancer.
      • Leiro-Fernández V.
      • Botana-rial M.
      • Tilve-Gomez A.
      • Represas-Represas C.
      • Pallarés- Sanmartin A.
      • Fernandez-Villar A.
      Predicting delays in lung cancer diagnosis and staging: delays in LC diagnosis and staging.
      • Ellis P.M.
      • Vandermeer R.
      Delays in the diagnosis of lung cancer.
      • Bjerager M.
      • Palshof T.
      • Dahl R.
      • Vedsted P.
      • Olesen F.
      Delay in diagnosis of lung cancer in general practice.
      • Massimo A.
      • Claudia B.
      • Cinzia D.G.
      • Fabio F.
      • Luigi C.
      Distance as a barrier to cancer diagnosis and treatment: review of the literature.
      Some countries have implemented guidelines for the optimal timing of diagnosis and treatment of lung cancer.
      • Malalasekera A.
      • Nahm S.
      • Blinman P.L.
      • et al.
      Times to diagnosis and treatment of lung cancer in new south wales, Australia: a multicenter, medicare data linkage study.
      The British Thoracic Society (BTS) has made various recommendations concerning the diagnosis and treatment delays for patients with lung cancer.
      • Thoracic Society British
      BTS recommendations to respiratory physicians for organizing the care of patients with lung cancer. The lung cancer working party of the British thoracic society standards of care committee.
      The American College of Chest Physicians evidence-based clinical practice guidelines suggest that efforts should be made to deliver timely care,
      • Ost D.E.
      • Jim Yeung S.-C.
      • Tanoue L.T.
      • Gould M.K.
      Clinical and organizational factors in the initial evaluation of patients with lung cancer.
      without presenting specific guidelines on the timeliness of lung cancer.
      • Maiga A.W.
      • Deppen S.A.
      • Pinkerman R.
      • et al.
      Timeliness of care and lung cancer tumor-stage progression: How long can we wait?.
      American guidelines recommend timeframes of 10 days for specialist review.
      • Malalasekera A.
      • Nahm S.
      • Blinman P.L.
      • et al.
      Times to diagnosis and treatment of lung cancer in new south wales, Australia: a multicenter, medicare data linkage study.
      Standards from Australia recommend 14 days maximum delay between first general practitioner (GP) referral and first lung cancer specialist appointment, and between diagnosis to treatment.
      • Stirling R.G.
      • Evans S.M.
      • McLaughlin P.
      • et al.
      The victorian lung cancer registry pilot: improving the quality of lung cancer care through the use of a disease quality registry.
      A systematic review including 49 studies concluded that times to diagnosis and treatment of lung cancer often exceeded recommendations.
      • Olsson J.K.
      • Schultz E.M.
      • Gould M.K.
      Timeliness of care in patients with lung cancer: a systematic review.
      In Morocco, little is known about delays in the diagnosis of primary lung cancer. This study aimed to explore the presentation of symptoms in Moroccan patients with primary lung cancer. Description of times from the onset of symptoms to diagnosis was also performed. An assessment of causes related to delayed diagnosis was also explored.

      2. Material and methods

      This study was conducted at Moulay Youssef hospital affiliated with the Ibn Sina University Hospital center in Rabat. It is the largest hospital specializing in respiratory disease in Morocco.
      Access to this hospital is only possible by referral from primary care or directly through the emergency department.
      After lung cancer diagnosis, patients are transferred according to the stage of the disease to the thoracic surgery department of the Ibn Sina hospital if the disease is operable, otherwise to the national oncology institute.
      We adopted a retrospective study of all patients with primary lung cancer diagnosed between January 2014 and December 2017. Patients with other pathology, those with metastatic lung cancer from other organs, and those with non-found or incomplete records were excluded from the study.
      The following data were extracted from the patients' file: sex, age, social security status, address, smoking habits, symptoms, comorbidities, pathology method, tumor histology, tumor stage, date of first symptoms, date of first general practitioner (GP) visit, date of first pulmonary-disease specialist visit, date of diagnosis.
      We adapted operational definitions to extract data about time intervals from first clinical presentation until diagnosis for lung cancer.
      • Olesen F.
      • Hansen R.P.
      • Vedsted P.
      Delay in diagnosis: the experience in Denmark.
      ,
      • Weller D.
      • Vedsted P.
      • Rubin G.
      • et al.
      The Aarhus statement: improving design and reporting of studies on early cancer diagnosis.
      Fig. 1 describes these time intervals.
      Fig. 1
      Fig. 1Components of the times from the first symptoms to diagnosis
      Patient presentation time (a) is the time from the onset of symptoms until the first visit to a general practitioner. Referral time (b) is the time between the first GP visit and the first specialist visit. Diagnosis time (c) is the time between the first specialist visit and the date of diagnosis. Total time (d) is the time from the onset of the first symptom and the date of diagnosis.
      Patient presentation time was defined as the time from the onset of symptoms until the first visit to a general practitioner (GP). If patient presentation interval exceeded 30 days, it was considered indicative of a patient's delay.
      • Koyi H.
      • Hillerdal G.
      • Brandén E.
      Patient's and doctors' delays in the diagnosis of chest tumors.
      ,
      • Yurdakul A.S.
      • Kocatürk C.
      • Bayiz H.
      • et al.
      Patient and physician delay in the diagnosis and treatment of non-small cell lung cancer in Turkey.
      Referral time was defined as the time between the first GP visit and the first specialist visit. Diagnosis time was defined as the time between the first specialist visit and the date of diagnosis.
      Based on the British Thoracic Society (BTS) recommendations, a referral time longer than two weeks and diagnosis time that exceeding two weeks are considered to be late.
      • Massimo A.
      • Claudia B.
      • Cinzia D.G.
      • Fabio F.
      • Luigi C.
      Distance as a barrier to cancer diagnosis and treatment: review of the literature.
      Considering these recommendations, a time between the first visit to a general practitioner (GP) and the date of diagnosis over four weeks was taken as a criterion for doctor delay. A time from the onset of the first symptom and the date of diagnosis that exceeds 58 days (4 weeks +30 days) was considered as a criterion for the total delay.
      Continuous variables were presented as median and interquartile interval. Categorical variables were presented as frequencies and percentages. The normality of all quantitative variables was verified. The main possible factors of delay were analyzed by uni- and multivariate linear regression analysis using a selection of factors associated (p ≤ 0.30) with delay in univariate analysis. However, the factors sex, smoking, and distance to the nearest cancer center were forced into the model. A p-value of less than 0.05 was considered significant. All data were analyzed using Jamovi version 2.0.0.

      3. Results

      From 286 patients hospitalized during the study period, 102 patients were diagnosed with primary lung cancer and 184 with other thoracic malignancy or non-malignant conditions. Among patients diagnosed with primary lung cancer, 21 patients were excluded because of missing data. In total, 81 patients with primary lung cancer were included in this study, consisting of 66 (81.50%) men and 15 (18.50%) women. The mean age at diagnosis was 58.34 ± 10.01 years (range, 33–85 years). Characteristics of the study population are listed in Table 1. Patients came mainly (81.50%) from primary care, and were referred to the hospital because of a suspect X-ray in 65.15% of cases, hemoptysis, chest pain, and cough in 13.63%, 10.60%, and 9.10% of cases, respectively.
      Table 1Main characteristics of patients in Moulay Youssef hospital in Rabat.
      CharacteristicN%
      Sex
       Male6681.48
       Female1518.52
      Age, years
       Adult (≤60 year)5365.43
       Elderly (>60 years)2834.57
      Health insurance
       Yes7693.83
       No56.17
      Traveling distance to nearest cancer center (Km
      Km: Kilometer.
      )
       ≤ 305466.67
       >302733.33
      Smoking habits
       Smokers6276.54
       Nonsmokers1923.46
      Respiratory symptoms at presentation
       Yes6985.18
       No1214.82
      Other pulmonary diseases
       COPD
      COPD: Chronic Obstructive Pulmonary Disease.
      2834.57
       Tuberculosis2429.60
       Asthma1012.34
       Pneumonia089.88
      Diagnostic method
       Bronchoscopy5669.14
       CT-guided biopsy
      CT-guided biopsy: Computed Tomography guided biopsy.
      1214.81
       Pleural biopsy1012.35
       Lymph node biopsy033.70
      Tumor histology
       Adenocarcinoma5162.96
       Squamous cell1417.29
       Small cell cancer0911.11
       Others078.64
      Disease stage
       II78.6
       IIIA1316.0
       IIIB1214.8
       IV4960.50
      a Km: Kilometer.
      b COPD: Chronic Obstructive Pulmonary Disease.
      c CT-guided biopsy: Computed Tomography guided biopsy.
      More than two-thirds (76.54%) of the participants were smokers. The mean pack-years of smoking was 38.2 ± 18.42 pack-years. The patients were presented at the hospital with many different symptoms. The majority (85.18%) of them reported respiratory symptoms before the diagnosis. Cough was the most common symptom, followed by dyspnea, chest pain, and hemoptysis, with 74.1%, 61.73%, 51.85%, and 50.61%, respectively. Eight of these patients had also symptoms related to brain metastases. Only 13.58% of patients had atypical symptoms such as lack of appetite, fever, or fatigue. One patient was asymptomatic and was diagnosed by chance. A pulmonary lesion was found on a routine chest X-ray. Table 2 shows the presentation of symptoms of the study population.
      Table 2Presentation of symptoms of patients in Moulay Youssef hospital in Rabat.
      SymptomNo. Cases%
      Cough6074.10
      Dyspnea5061.73
      Weight loss4251.85
      chest pain4150.61
      Lack of appetite2530.86
      Fever2125.92
      Hemoptysis2125.92
      Condensation syndrome1720.98
      Fatigue1113.58
      Cerebral symptoms89.87
      Musculoskeletal pain67.41
      Visible lymph node on the neck56.17
      Dysphonia44.94
      Anorexia33.70
      Vena cava superior syndrome33.70
      No symptoms (incidental finding)11.23
      The median patient presentation time was 75 days (IQI = 30–150 days). This time was ranged from 7 days to a maximum of 365 days. Only 14.81% of patients visited the doctors within one month from the onset of symptoms. On univariate analysis, there were no significant differences in time taken to consult between symptomatic and asymptomatic patients or between smokers and never smokers. Also, sex, age, cough, hemoptysis, and history of previous no malignancies lung disease were not significantly associated with earlier consulting in GPs. After adjusting with other variables (Table 3), there is a significant difference in patient presentation time between patients aged 60 years or less and those aged more than 60 years (p = 0.044). Also, a significant difference was noted in patients presenting a weight loss (p = 0.038).
      Table 3Univariate/multivariate linear regression analyses of factors associated with patient presentation, patient referral, and diagnosis times.
      VariablesUnivariate analysis

      β (95% CI)
      P-valueMultivariate analysis

      β (95% CI)
      P-value
      Patient presentation time (n = 66)
      Sex
      Forced factors into the model.
       Men-women−10.1 (−76.4 to 56.2)0.762
      Age (years)
       ≤ 60 - > 60−33 (−83.6 to 17.5)0.197−56.8 (−112.02 to −1.57)0.044
      Smoking
      Forced factors into the model.
       Yes- no4.98 (−56.1 to 66.0)0.871−22.92 (−122.56 to 76.71)0.637
      Adenocarcinoma
       Yes- no−29.2 (−83.6 to 25.3)0.289
      Chest pain
       Yes- no32.4 (−18.2 to 82.9)0.206
      Weight loss
       Yes- no42.7 (−7.93 to 93.4)0.09753.8 (3.00–104.52)0.038
      Patient referral time (n = 66)
      Respiratory disease
       Yes- no8.38 (−4.03 to 20.8)0.182
      Tuberculosis
       Yes- no9.33 (−5.00 to 23.7)0.198
      COPD
       Yes- no9.60 (−3.24 to 22.4)0.14018.74 (0.280–37.19)0.040
      Asthma
       Yes- no24.0 (5.87–42.1)0.01028.67 (9.441–47.90)0.004
      Distance
      Forced factors into the model.
       ≤ 30 km- > 30 km1.64 (−11.56 to 14.8)0.805−4.47 (−18.144 to 9.21)0.516
      Diagnosis time (n = 81)
      Sex
       Men-women3.87 (−3.72 to 11.4)0.3132.21 (−5.839 to 10.251)
      Age
       ≤60 years- > 60 years−3.64 (−9.53 to 2.24)0.222−3.90 (−10.716 to 2.918)
      Non-suspected chest X-ray
       Yes- no7.48 (0.765–14.2)0.0307.01 (0.158–13.855)0.045
      COPD
       Yes- no5.91 (−0.181 to 12.0)0.0574.64 (−2.018 to 11.293)
      CT-guided biopsy
       Yes- no7.48 (0.765–14.2)0.030−9.97 (−18.93 to −1.000)0.030
      Distance
      Forced factors into the model.
       ≤ 30 km- > 30 km4.54 (−1.67 to 10.7)0.1505.58 (−1.231 to 12.38)0.107
      a Forced factors into the model.
      From the first contact with the general practitioner (GP) until the first visit to the specialist, the median time was 08 days (IQI = 02–14 days). Over two-thirds (74.24%) of participants were referred within two weeks. GPs wrote a referral on the same day of the visit for twenty-nine patients. On univariate analysis, neither distance to the nearest cancer center, asthma nor COPD was associated with patient referral time. After adjusting with other factors (Table 3), both asthma (p = 0.004) and COPD (p = 0.040) were significantly associated with longer referral time.
      The median time between the first visit to a specialist and diagnosis was 21 days (IQI = 14–22 days). Only 27.16% of cases had the diagnosis within two weeks. When exploring factors of diagnostic delay (Table 3), were increased in patients with non-suspected chest-X ray (p = 0.04) and earlier in patients diagnosed with CT-guided biopsy (p = 0.003).
      The median doctor time was 33.5 days (IQI = 20–43 days). Over half of cases (54.55%) had a delayed doctor time. The median total time from the first symptom to the final diagnosis (the sum of all times) was 123 days (IQI = 63–202 days). Over three quarters (81.82%) of patients had a delayed total time. The total time was not affected by any of the studied factors.

      4. Discussion

      To our knowledge, this study is the first in Morocco to calculate delays using a validated model about time intervals from the onset of the first symptom until diagnosis and assess factors of these delays.
      Almost the majority of our patients were symptomatic at the first presentation, cough was the most common symptom. Several studies found that cough is frequent in patients with lung cancer.
      • Bjerager M.
      • Palshof T.
      • Dahl R.
      • Vedsted P.
      • Olesen F.
      Delay in diagnosis of lung cancer in general practice.
      ,
      • Bourkadi D.
      • Sahraoui K.
      • Zaoui A.
      • Bouchareb A.
      • Bouzidi E.E.
      • Bennani M.A.
      Délais de prise en charge du cancer bronchopulmonaire primitif, expérience du service de pneumologie B, CHU d'Oran.
      Also, cough in patients with lung cancer is more severe than patients with chronic obstructive pulmonary disease (COPD) and asthma.
      • Harle A.S.M.
      • Blackhall F.H.
      • Molassiotis A.
      • et al.
      Cough in patients with lung cancer.
      Based on our results as well as the results of other studies around the world, the patient interval in our series was very delayed. The majority of published studies find a shorter time except for a cross-sectional study in the UK that found a median of 99 days.
      • Smith S.M.
      • Campbell N.C.
      • MacLeod U.
      • et al.
      Factors contributing to the time taken to consult with symptoms of lung cancer: a cross-sectional study.
      In Turkey and Tunisia, the mean patient delay was, respectively, 49.9 days and 82.9 days.
      • Yurdakul A.S.
      • Kocatürk C.
      • Bayiz H.
      • et al.
      Patient and physician delay in the diagnosis and treatment of non-small cell lung cancer in Turkey.
      ,
      • Bourkadi D.
      • Sahraoui K.
      • Zaoui A.
      • Bouchareb A.
      • Bouzidi E.E.
      • Bennani M.A.
      Délais de prise en charge du cancer bronchopulmonaire primitif, expérience du service de pneumologie B, CHU d'Oran.
      In Sweden, Finland, Malaysia, Denmark, and Netherlands, the median was respectively 11 days, 14 days, 60 days, 33 days, and 22 days.
      • Bjerager M.
      • Palshof T.
      • Dahl R.
      • Vedsted P.
      • Olesen F.
      Delay in diagnosis of lung cancer in general practice.
      ,
      • Koyi H.
      • Hillerdal G.
      • Brandén E.
      Patient's and doctors' delays in the diagnosis of chest tumors.
      ,
      • Salomaa E.-R.
      • Sällinen S.
      • Hiekkanen H.
      • Liippo K.
      Delays in the diagnosis and treatment of lung cancer.
      • Loh L.-C.
      • Chan L.-Y.
      • Govindaraju S.
      • et al.
      Time delay and its effect on survival in MALAYSIAN patients with NON-small cell lung carcinoma.
      • Brocken P.
      • Kiers B.
      • Looijen-Salamon M.
      • et al.
      Timeliness of lung cancer diagnosis and treatment in a rapid outpatient diagnostic program with combined 18FDG-PET and contrast enhanced CT scanning.
      We found no significant differences in the time taken to consult between patients with respiratory symptoms and those without respiratory symptoms. Various reasons may be suggested to explain this. The main is that patients did not interpret these symptoms, and therefore did not react in a timely way. A cross-sectional study found that patients were unaware of the symptoms related to lung cancer and did not consider them as an indication of this disease.
      • Smith S.M.
      • Campbell N.C.
      • MacLeod U.
      • et al.
      Factors contributing to the time taken to consult with symptoms of lung cancer: a cross-sectional study.
      In our study, factors associated with time to consult was weight loss and elderly age. A French team found no difference regarding the patient presentation time between elderly and younger patients with lung cancer.
      • Giroux Leprieur E.
      • et al.
      Delay between the initial symptoms, the diagnosis and the onset of specific treatment in elderly patients with lung cancer.
      On the other hand, the referral time in our study appears acceptable. 74.24% of patients were referred within the standards of international recommendations. For only 10.6% of patients, the time was longer than one week. A Dutch study found a median of 7 days, and a Turkish study an average of 61.6 days.
      • Yurdakul A.S.
      • Kocatürk C.
      • Bayiz H.
      • et al.
      Patient and physician delay in the diagnosis and treatment of non-small cell lung cancer in Turkey.
      ,
      • Brocken P.
      • Kiers B.
      • Looijen-Salamon M.
      • et al.
      Timeliness of lung cancer diagnosis and treatment in a rapid outpatient diagnostic program with combined 18FDG-PET and contrast enhanced CT scanning.
      Our results showed that previous lung diseases, in particular asthma and COPD, were associated with a delayed referral time. Many studies showed that comorbidities are major contributors to delay.
      • Bjerager M.
      • Palshof T.
      • Dahl R.
      • Vedsted P.
      • Olesen F.
      Delay in diagnosis of lung cancer in general practice.
      ,
      • Malalasekera A.
      • Nahm S.
      • Blinman P.L.
      • et al.
      Times to diagnosis and treatment of lung cancer in new south wales, Australia: a multicenter, medicare data linkage study.
      ,
      • Yurdakul A.S.
      • Kocatürk C.
      • Bayiz H.
      • et al.
      Patient and physician delay in the diagnosis and treatment of non-small cell lung cancer in Turkey.
      Regarding the diagnosis delay, only 27.16% of the cases were consistent with the British Thoracic Society (BTS) recommendations.
      • Thoracic Society British
      BTS recommendations to respiratory physicians for organizing the care of patients with lung cancer. The lung cancer working party of the British thoracic society standards of care committee.
      Our median of 21- day was longer than 9 days, and 10 days reported respectively from Sweden and France.
      • Koyi H.
      • Hillerdal G.
      • Brandén E.
      Patient's and doctors' delays in the diagnosis of chest tumors.
      ,
      • Virally J.
      • Choudat L.
      • Chebbo M.
      • et al.
      Épidémiologie et délais de prise en charge de 355 patients atteints de cancer bronchique.
      Studies performed in Turkey and the USA found an average time between the visit to a pulmonary disease specialist and diagnosis of 20.4 days and 43 days, respectively.
      • Yurdakul A.S.
      • Kocatürk C.
      • Bayiz H.
      • et al.
      Patient and physician delay in the diagnosis and treatment of non-small cell lung cancer in Turkey.
      ,
      • Rao S.S.
      • Saha S.
      Timeliness of lung cancer diagnosis and treatment: a single- center experience.
      Non-suspicious chest X-ray was associated with delayed diagnosis time in our series. This association has been found previously in other studies.
      • Bjerager M.
      • Palshof T.
      • Dahl R.
      • Vedsted P.
      • Olesen F.
      Delay in diagnosis of lung cancer in general practice.
      ,
      • Turkington P.M.
      • Kennan N.
      • Greenstone M.A.
      Misinterpretation of the chest x ray as a factor in the delayed diagnosis of lung cancer.
      Conversely, when comparing the method of diagnosis, diagnosis time was earlier in patients diagnosed with CT-guided biopsy, which may result in waiting times required at the hospital for each diagnostic method.
      Distance to the cancer center was not associated with longer delays in our study. A review of the literature found that distance is an important factor influencing access to timely and appropriate diagnosis of cancer.
      • Massimo A.
      • Claudia B.
      • Cinzia D.G.
      • Fabio F.
      • Luigi C.
      Distance as a barrier to cancer diagnosis and treatment: review of the literature.
      It appears from our results, that patients take a long time to consult a doctor, undergo investigations, and then have a diagnosis. The majority of our patients were in a late stage of the disease. Results from a previous study showed that patients diagnosed in earlier stages had better clinical outcomes.
      • van Rens M.T.
      • de la Rivière A.B.
      • Elbers H.R.
      • van Den Bosch J.M.
      Prognostic assessment of 2,361 patients who underwent pulmonary resection for non-small cell lung cancer, stage I, II, and IIIA.
      Also, delays might be stressful for both patients and families.
      • Moody A.
      • Muers M.
      • Forman D.
      Delays in managing lung cancer.
      Some studies seem very promising to shortness delays. The time to treat Program of Canada has reduced the delay from 128 to 20 days for the entire management process and consequently has generated growing satisfaction in patients and professionals.
      • Lo D.S.
      • Zeldin R.A.
      • Skrastins R.
      • et al.
      Time to treat: a system redesign focusing on decreasing the time from suspicion of lung cancer to diagnosis.
      In the USA, an experience using nurse navigation improve the time between the suspicion of cancer until treatment from 136 days to 55 days.
      • Hunnibell L.S.
      • Rose M.G.
      • Connery D.M.
      • et al.
      Using nurse navigation to improve timeliness of lung cancer care at a veterans hospital.
      A recent study has shown that Rapid lung cancer diagnosis units have reduced delays and positively impacted the quality of care.
      • Ezer N.
      • Navasakulpong A.
      • Schwartzman K.
      • Ofiara L.
      • Gonzalez A.V.
      Impact of rapid investigation clinic on timeliness of lung cancer diagnosis and treatment.
      The major strengths of our study are its originality and the reliable collection of data from several sources: patient charts, reports from general practitioners and specialists, and reference files. In addition, we have used valid models for the presentation of the different intervals. Nevertheless, the retrospective nature of the study constitutes an important limitation, as it did not provide information such as the educational and socioeconomic level, that has a significant impact on the delays of lung cancer diagnosis.

      5. Conclusion

      This study showed an important aspect of lung cancer healthcare. Intervals of diagnosis were significantly delayed and highly affected by patients and diagnosis times. Thus, the results emphasize the extreme need to develop efficient strategies to improve lung cancer diagnosis intervals, based on general public awareness, particularly in high-risk groups, of the importance of certain key symptoms related to lung cancer, and the shortening waiting times for investigations.

      Author contributions

      Ouassima Erefai: Conceptualization, methodology, investigation, data curation, formal analysis, writing-original draft preparation, writing-review an editing. Abdelmajid Soulaymani: Conceptualization, investigation, writing-review and editing. Abdelrhani Mokhtari: Conceptualization, investigation, writing-review and editing. Majdouline Obtel: Conceptualization, investigation, formal analysis, writing-review an editing. Hinde Hami: Conceptualization, methodology, investigation, formal analysis, writing-original draft preparation, writing-review an editing.

      Sources of funding

      This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

      Declaration of competing interest

      The authors have no conflicts of interest to declare for this study.

      References

        • Ferlay J.
        • Soerjomataram I.
        • Dikshit R.
        • et al.
        Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012: globocan 2012.
        Int J Cancer. 2015; 136: E359-E386
        • De Groot P.M.
        • Wu C.C.
        • Carter B.W.
        • Munden R.F.
        The epidemiology of lung cancer.
        Transl Lung Cancer Res. 2018; 7: 220-233
        • Sung H.
        • Ferlay J.
        • Siegel R.L.
        • et al.
        Global cancer Statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries.
        CA A Cancer J Clin. 2021; (0): 1-41
        • Abdelaziz A.B.
        • Melki S.
        • Nouira S.
        • et al.
        Cancers in the central maghreb: epidemiology from 1990 to 2017 and trends in 2040.
        Tunis Med. 2019; 97: 739-770
        • Leiro-Fernández V.
        • Botana-rial M.
        • Tilve-Gomez A.
        • Represas-Represas C.
        • Pallarés- Sanmartin A.
        • Fernandez-Villar A.
        Predicting delays in lung cancer diagnosis and staging: delays in LC diagnosis and staging.
        Thorac Cancer. 2019; 10: 296-303
        • Ellis P.M.
        • Vandermeer R.
        Delays in the diagnosis of lung cancer.
        J Thorac Dis. 2011; 3: 183-188
        • Bjerager M.
        • Palshof T.
        • Dahl R.
        • Vedsted P.
        • Olesen F.
        Delay in diagnosis of lung cancer in general practice.
        Br J Gen Pract. 2006; 6
        • Massimo A.
        • Claudia B.
        • Cinzia D.G.
        • Fabio F.
        • Luigi C.
        Distance as a barrier to cancer diagnosis and treatment: review of the literature.
        Oncol. 2015; : 1378-1385
        • Malalasekera A.
        • Nahm S.
        • Blinman P.L.
        • et al.
        Times to diagnosis and treatment of lung cancer in new south wales, Australia: a multicenter, medicare data linkage study.
        J Oncol Pract. 2018; 14 (e621–e630)
        • Thoracic Society British
        BTS recommendations to respiratory physicians for organizing the care of patients with lung cancer. The lung cancer working party of the British thoracic society standards of care committee.
        Thorax. 1998; 53: S1-S8
        • Ost D.E.
        • Jim Yeung S.-C.
        • Tanoue L.T.
        • Gould M.K.
        Clinical and organizational factors in the initial evaluation of patients with lung cancer.
        Chest. 2013; 143: e121S-e141S
        • Maiga A.W.
        • Deppen S.A.
        • Pinkerman R.
        • et al.
        Timeliness of care and lung cancer tumor-stage progression: How long can we wait?.
        Ann Thorac Surg. 2017; 104: 1791-1797
        • Stirling R.G.
        • Evans S.M.
        • McLaughlin P.
        • et al.
        The victorian lung cancer registry pilot: improving the quality of lung cancer care through the use of a disease quality registry.
        Lung. 2014; 192: 749-758
        • Olsson J.K.
        • Schultz E.M.
        • Gould M.K.
        Timeliness of care in patients with lung cancer: a systematic review.
        Thorax. 2009; 64: 749-756
        • Olesen F.
        • Hansen R.P.
        • Vedsted P.
        Delay in diagnosis: the experience in Denmark.
        Br J Cancer. 2009; 101 (S5–S8)
        • Weller D.
        • Vedsted P.
        • Rubin G.
        • et al.
        The Aarhus statement: improving design and reporting of studies on early cancer diagnosis.
        Br J Cancer. 2012; 106: 1262-1267
        • Koyi H.
        • Hillerdal G.
        • Brandén E.
        Patient's and doctors' delays in the diagnosis of chest tumors.
        Lung Cancer. 2002; 35: 53-57
        • Yurdakul A.S.
        • Kocatürk C.
        • Bayiz H.
        • et al.
        Patient and physician delay in the diagnosis and treatment of non-small cell lung cancer in Turkey.
        Cancer Epidemiol. 2015; 39: 216-221
        • Bourkadi D.
        • Sahraoui K.
        • Zaoui A.
        • Bouchareb A.
        • Bouzidi E.E.
        • Bennani M.A.
        Délais de prise en charge du cancer bronchopulmonaire primitif, expérience du service de pneumologie B, CHU d'Oran.
        Rev Mal Respir. 2018; 35: A221
        • Harle A.S.M.
        • Blackhall F.H.
        • Molassiotis A.
        • et al.
        Cough in patients with lung cancer.
        Chest. 2019; 155: 103-113
        • Smith S.M.
        • Campbell N.C.
        • MacLeod U.
        • et al.
        Factors contributing to the time taken to consult with symptoms of lung cancer: a cross-sectional study.
        Lung Cancer. 2009; 9
        • Salomaa E.-R.
        • Sällinen S.
        • Hiekkanen H.
        • Liippo K.
        Delays in the diagnosis and treatment of lung cancer.
        Chest. 2005; 128: 2282-2288
        • Loh L.-C.
        • Chan L.-Y.
        • Govindaraju S.
        • et al.
        Time delay and its effect on survival in MALAYSIAN patients with NON-small cell lung carcinoma.
        Malays J Med Sci. 2006; 6
        • Brocken P.
        • Kiers B.
        • Looijen-Salamon M.
        • et al.
        Timeliness of lung cancer diagnosis and treatment in a rapid outpatient diagnostic program with combined 18FDG-PET and contrast enhanced CT scanning.
        Lung Cancer. 2012; 75: 336-341
        • Giroux Leprieur E.
        • et al.
        Delay between the initial symptoms, the diagnosis and the onset of specific treatment in elderly patients with lung cancer.
        Clin Lung Cancer. 2012; 13: 363-368
        • Virally J.
        • Choudat L.
        • Chebbo M.
        • et al.
        Épidémiologie et délais de prise en charge de 355 patients atteints de cancer bronchique.
        Rev Mal Respir. 2006; 23: 43-48
        • Rao S.S.
        • Saha S.
        Timeliness of lung cancer diagnosis and treatment: a single- center experience.
        Asian Cardiovasc Thorac Ann. 2019; 27: 670-676
        • Turkington P.M.
        • Kennan N.
        • Greenstone M.A.
        Misinterpretation of the chest x ray as a factor in the delayed diagnosis of lung cancer.
        Postgrad Med. 2002; 78: 158-160
        • van Rens M.T.
        • de la Rivière A.B.
        • Elbers H.R.
        • van Den Bosch J.M.
        Prognostic assessment of 2,361 patients who underwent pulmonary resection for non-small cell lung cancer, stage I, II, and IIIA.
        Chest. 2000; 117: 374-379
        • Moody A.
        • Muers M.
        • Forman D.
        Delays in managing lung cancer.
        Thorax. 2004; : 591-593
        • Lo D.S.
        • Zeldin R.A.
        • Skrastins R.
        • et al.
        Time to treat: a system redesign focusing on decreasing the time from suspicion of lung cancer to diagnosis.
        J Thorac Oncol. 2007; 2: 1001-1006
        • Hunnibell L.S.
        • Rose M.G.
        • Connery D.M.
        • et al.
        Using nurse navigation to improve timeliness of lung cancer care at a veterans hospital.
        Clin J Oncol Nurs. 2012; 16: 29-36
        • Ezer N.
        • Navasakulpong A.
        • Schwartzman K.
        • Ofiara L.
        • Gonzalez A.V.
        Impact of rapid investigation clinic on timeliness of lung cancer diagnosis and treatment.
        BMC Pulm Med. 2017; 17: 178