Idiopathic pulmonary fibrosis in Saudi Arabia: Demographic, clinical, and survival data from two tertiary care hospitals
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1 Original Article Idiopathic pulmonary fibrosis in Saudi Arabia: Demographic, clinical, and survival data from two tertiary care hospitals Nahid Sherbini, Maun N Feteih 1, Siraj O Wali 2, Omer S Alamoudi 2, Salem M Al-Faifi 1, Imran Khalid 3 King Fahad Hospital, Madinah, 1 King Faisal Specialist Hospital and Research Center, 2 King Abdulaziz University Hospital, 3 John D Dingell VA Medical Center, Detroit, MI, USA and King Faisal Specialist Hospital and Research Center, Jeddah, Kingdom of Saudi Arabia Address for correspondence: Dr. Imran Khalid, Staff Physician John D Dingell VA Medical Center, Department of Medicine, 4646 John R, Detroit, MI, 48201, USA. and Consultant Intensivist KFSHRC-Jeddah, Kingdom of Saudi Arabia. dr.imrankhalid@ yahoo.com Submission: Accepted: Access this article online Quick Response Code: Website: DOI: / Abstract: BACKGROUND: Idiopathic pulmonary fibrosis (IPF) is rare and can be challenging to diagnose. Limited data is available from the Middle Eastern region, especially Saudi Arabia. METHODS: This was a retrospective study that looked at all the patients diagnosed with IPF between 2007 and 2012 at two tertiary care hospitals in Saudi Arabia. We collected the demographical, clinical, laboratory and radiological data from the patients medical records. Medications administered and 1 year survival was also assessed. RESULTS: Between 2007and 2012, 134 IPF patients were identified. Their baseline characteristics (Mean ± SD) included: age 64 ± 13 years, body mass index 29 ± 8 kg/m 2, FEV 1 56 ± 15 percent of predicted, FVC 53 ± 13 percent of predicted, FEV 1 /FVC 0.81 ± 0.09, total lung capacity 75 ± 13 percent of predicted, diffusing capacity of the lung for carbon monoxide 57 ± 15 percent of predicted, on home oxygen at presentation 71 (53%), mean ejection fraction 0.50 ± 0.07, mean pulmonary artery systolic pressure (via echocardiogram) mmhg, presentation mean S po2 92 ± 7%, presentation 6-min walk distance 338 ± 64 m and lowest S po2 during 6-min walk test 88 ± 5%. Patients were predominantly female (56%), and 42% of patients had diabetes and were active smokers. The IPF patients frequency of hospital admission (n = 99) was 2.4 ± 1.7 per year and duration of hospital stay (n = 99) was 17.4 ± 23.8 days. Overall 1 year survival in all IPF patients was good, 93% (124) patients remained alive after 1 year. CONCLUSIONS: In Saudi Arabia, IPF patients tended to be slightly older and the disease progression was somewhat slower than reported IPF cohorts in other populations. They had frequent hospital admissions and a long hospital length of stay. The influence of genetics and co-morbid diseases on the incidence and outcome of IPF should be explored further. Key words: Characteristics, idiopathic pulmonary fibrosis, survival, Saudi Arabia Interstitial lung diseases (ILDs) are defined as diffuse parenchymal pathologies that begin in the lung interstitium. [1] The American Thoracic Society (ATS)/European Respiratory Society (ERS) International Multidisciplinary Consensus Classification of the Idiopathic Interstitial Pneumonias gives a clear approach to idiopathic interstitial pneumonias. [1] Idiopathic pulmonary fibrosis (IPF) is a major subtype, defined as a specific form of chronic, progressive, fibrosing interstitial pneumonia of unknown cause, occurring primarily in older adults, limited to the lungs, and is associated with the histopathologic and/or radiologic pattern of usual interstitial pneumonia. [2] IPF is rare and usually idiopathic, and has a poor predictable clinical course with a high mortality rate. It is also challenging to diagnose, requiring extensive workup. Clinical and demographic data on IPF are limited yet show substantial differences in different world regions. [3] Worldwide, the prevalence estimates for IPF range from 6 to 32 per 100,000. One review found that the males with IPF were more likely to be in their 60s. [4] A study from Saudi Arabia included 330 patients with ILD, out of which 23% had IPF. [5] The age of presentation is typically years, and symptom onset is typically 2-4 years prior to presentation. [6] Nalysnyk et al., [7] estimated that in the United Kingdom there are approximately 15,000 IPF patients, with approximately 5000 new IPF patients being diagnosed each year, while Navaratnum et al., [8] believe the incidence is on the rise. Raghu et al., [9] estimated that in the United States, there are 132, ,000 IPF patients with an annual incidence of 50,000. The usual presenting symptoms are dry cough and moderate to severe dyspnea on exertion. However, comprehensive data is lacking from Saudi Arabia and the Middle East. [5] 168 Annals of Thoracic Medicine - Vol 9, Issue 3, July-September 2014
2 In the absence of a diagnostic biopsy, typical clinical findings (described below) would suggest the diagnosis of IPF. [10] The differential diagnoses include other idiopathic interstitial pneumonias, connective tissue diseases (systemic sclerosis, polymyositis, and rheumatoid arthritis), chronic hypersensitivity pneumonitis, and environmental and/or occupational exposures. High-resolution computed tomography (HRCT) is essential in diagnosing IPF and has become more widely available. The 2011 ATS guidelines for diagnosing IPF require HRCT for patients in whom surgical lung biopsy is contraindicated. HRCT features add prognostic information to the histologic diagnosis of usual interstitial pneumonia. A significantly increased mortality rate was observed in patients who displayed both HRCT and histologic criteria (i.e., radiographic honeycombing). [11] Following the diagnosis of IPF in the United States, the median survival period was found to be 2-5 years. [2,12] However, Esam et al. found the median survival period to be 7.6 years in Saudi Arabia, contrasting years in other studies. [13] Associated comorbidities such as gastroesophageal reflux disease (GERD) and ischemic heart disease confound the progression of IPF. [14] Maintained lung physiology correlated to improved survival in some studies. [15] Anti-inflammatory, anti-fibrotic, and immunosuppressive therapies are often used to treat IPF, though have not been proven to improve neither survival nor quality of life. [16] We retrospectively studied data from IPF patients in Saudi Arabia, in particular the frequency, characteristics, and cofactors of IPF in Saudi Arabia, in order to compare our findings to other regions. Data in this regard are very limited, and the only few available studies about ILD only report a small cohort of patients with IPF. Therefore, IPF patients were the main focus of this study. Methods This retrospective study was approved by the institutional review boards of study institutions, which deemed informed consent unnecessary because the study was retrospective and no patient-identifying data would be disclosed. Patient data from King Faisal Specialist Hospital and Research Center-Jeddah and King Abdulaziz University Hospital- Jeddah during the period 2007 to 2012 were used. All patients presenting to the out-patient pulmonary clinics and in-patient services were screened, out of which, patients with diagnosis codes for interstitial lung disease, idiopathic lung fibrosis, lung fibrosis, and diffuse parenchymal lung disease, were included. Additional IPF cases were identified from the radiology department database by selecting those with computed tomography-requiring diagnoses. IPF symptoms, along with laboratorial, radiologic, and pathological signs, as well as pulmonary function tests, were also considered. The diagnosis of IPF was established when the patient met the following criteria, according to the ATS/ ERS recommendations: [10] Exclusion of other known causes of ILD by complete history, mainly other symptoms that could suggest autoimmune disease, drugs, or occupational or exposure history Pulmonary function test results showed restrictive and/or gas-transfer defects Unexplained dyspnea on exertion Illness duration 3 months Bilateral basal inspiratory crackles Typical HRCT findings: Predominantly basal/sub-pleural coarse reticular or linear opacities, honeycombing, and traction bronchiectasis, but no ground-glass opacities Negative laboratory serology for autoimmune diseases Data on demographics, physical examination findings, laboratory, chest X-rays, HRCTs, electrocardiograms, echocardiograms, pulmonary function test results, pathological and bronchoalveolar lavage findings, functional illness severity assessments, and comorbidities was collected. Furthermore, data was collected on drugs administered and disease course (including hospital admissions, and outcomes). Exclusion criteria included a previously established diagnosis of a connective-tissue disease, occupational and/or environmental exposure to a substance that could potentially cause ILD, and a history of ingesting drugs and other agents that are known to cause pulmonary fibrosis. Statistical analysis Missing values were assumed to represent the worst-case scenario. One-way analysis of variance and the Monte Carlo test were suitably applied to analyze the overall variables. Qualitative and categorical variables were compared using the Kruskal-Wallis test and the chi-square test. Quantitative continuous variables were analyzed with the chi-square test. All analyses were carried out on an intention-to-treat basis. Results There were 176 patients with interstitial lung diseases, of whom 134 were diagnosed with IPF. The patients were predominantly female and were overweight with average body mass index 29 ± 8 kg/m 2. More than half were already on home oxygen at presentation [Table 1]. Patients signs and symptoms at presentation are illustrated in detail in Table 2. They had moderate reduction in FEV1 and FVC, showed restrictive pattern on spirometry and had moderate reduction Table 1: Patients baseline demographics Parameter No (%) Mean ± SD Range Male 59 (44) NA NA Female 75 (56) NA NA Age (years) 134 (100) 64± Age at presentation 134 (100) 56± (years) Body mass index (kg/m 2 ) 134 (100) 29± Weight (kg) 134 (100) 72.6± Height (cm) 134 (100) 157± Smoker 48 (36) NA NA History of tuberculosis 17 (13) NA NA Home oxygen 71 (53) NA NA Annals of Thoracic Medicine - Vol 9, Issue 3, July-September
3 in the diffusing capacity of the lung for carbon monoxide. They also had mild pulmonary hypertension via echocardiography [Table 3]. The findings on Computed Tomographic scans and treatments received are outlined in Table 4. The IPF patients frequency of hospital admission (n = 99) was 2.4 ± 1.7 per year, and hospital stay (n = 99) was 17.4 ± 23.8 days. Overall 1 year survival in all IPF patients was good, 93% (124) patients remained alive after 1 year [Table 5]. Discussion This is the largest reported IPF cohort pertaining to Saudi Arabia to date. The mean age of presentation in our study of 64 ± 13 years is similar to other studies. [6] Similarly, our study population s mean BMI (29 ± 8 kg/m 2 ) was in line with prior reports which show that a higher BMI is associated with a better prognosis. [17] Only 32 percent of our cohort had finger clubbing. Diabetes, common in our patients, is suspected to increase the risk of IPF. [18,19] Ischemic heart disease and GERD were also more common in our cohort than in the general population, as has been found in other studies. [20,21] Use of GERD medications is an independent predictor of longer survival in patients with IPF. That finding supports the hypothesis that GERD and chronic micro-aspiration increase the risk of IPF. [22-24] Twelve percent of our IPF patients had pulmonary hypertension, the presence of which is another predictor of survival. [25] Fiftythree percent of our IPF patients were on home oxygen at presentation, which probably indicates delayed diagnosis and referral to our hospital. [26] Baseline pulmonary function test results can predict the risk of hospitalization. Martinez et al. reported that patients with a median percent-of-predicted FVC of 62% were more likely to be hospitalized (42% vs. 26%) and the similar trend was found in our cohort. Further study is also needed on the relationships between hospitalization risk and pulmonary-function-test and 6-min-walk-test results in IPF patients. [27-29] This study showed that 88/134 (66%) of IPF patients had slowly progressive IPF. [12] This may have contributed to the relatively long mean survival. There was a similitude of findings between Esam et al., [13] and this study in terms of comparable survival rates among patients from different regions of Saudi Arabia. More studies are needed on the subject of IPF among different ethnicities among the Saudi population. [30] There were two limitations in our study. First, as this was a retrospective study, it was not possible to collect data that might have been valuable, such as thorough occupational and environmental exposures, baseline FVC, total lung capacity, and DLCO. Second, there was a chance of selection bias due to the fact that tertiary care centers were used and, also, because of the free availability of HRCT thus facilitating earlier detection of IPF as compared to some of the other regions. Table 2: Co-morbidities, signs and symptoms in patients at initial presentation Parameter Number (Percentage) Smoker 48 (36) Cough 115 (86) Modified Medical Research Council (MMRC) Dyspnea Scale 0 3 (2) I 31 (23) II 21 (16) III 24 (18) IV 55 (41) Wheeze 17 (12) Clubbing 44 (32) Arthralgia 7 (5) Fever 14 (10) Diabetes mellitus 56 (42) Hypertension 52 (39) Chronic kidney disease 9 (7) Gastroesophageal reflux disease 31 (23) Dyslipidemia 15 (11) Pulmonary hypertension 16 (12) Bilateral crackles on auscultation 129 (96) Table 3: Respiratory and cardiac testing at baseline Parameter No. (%) Mean ± SD Range FEV 1 (% of predicted) 134 (100) 56± FVC (% of predicted) 134 (100) 53± FEV 1 /FVC 134 (100) 0.81± Total lung capacity 134 (100) 75± (% of predicted) Diffusing capacity of the 134 (100) 57± lung for carbon monoxide (% of predicted) Ejection fraction, via 134 (100) 0.50± echocardiography Pulmonary artery 134 (100) 40± systolic pressure, via echocardiography (mm Hg) Heart rate (beats/min) 134 (100) 90± Mean SpO 2 (%) 134 (100) 92± min walk distance (m) 134 (100) 338± Lowest SpO 2 during 134 (100) 88± min walk test (%) 6-min-walk-test minutes 134 (100) 5.6± walked Arrhythmias 21 (16) NA NA Conclusions IPF patients in Saudi Arabia are most often elderly, obese, and female. Thirty-six percent of our cohort was smokers, and other types of air pollution (e.g., wood smoke and engine exhaust) might be risk factors for IPF. Compared to cohorts in other studies, our patients had similar symptoms but were a little older at presentation, and disease progression appeared to be slower. Genetic factors probably play a role in IPF risk and progression. Geographic variability of IPF prevalence may be influenced by differences in mortality, possibly as 170 Annals of Thoracic Medicine - Vol 9, Issue 3, July-September 2014
4 Table 4: Laboratory and radiographic findings along with therapies used Parameter Number (percentage) Positive autoimmune test results 6 (5) Bronchoalveolar lavage fluid obtained 11 (8) High-resolution CT of upper lobe 53 (40) Reticular pattern 62 (46) Nodular pattern 71 (53) Honeycombing pattern 67 (50) High-resolution CT of lower lobe 96 (72) Medications received Prednisolone 113 (84) Azathioprine 92 (69) Colchicine 27 (20) N-acetylcysteine 15 (11) Omeprazole 90 (67) Table 5: Hospital admission data along with survival Parameter No. (%) Mean ± SD Range Hospital Admission Admitted to hospital 99 (74) NA NA between Hospital stay (days) 99 (74) 17.4± Frequency of hospital 99 (74) 2.4± admission (per year) FVC of Hospitalized 58% of Patients predicted Overall Survival Overall Survival time in 134 NA NA all patients <1 month 5 (4) NA NA 1-11 months 4 (3) NA NA 1-2 years 24 (18) NA NA >2 years 101 (75) NA NA a result of the influence of comorbidities such as diabetes, GERD, pulmonary hypertension, and ischemic heart disease. Therefore, epidemiologic estimates from other studies cannot be directly compared without accounting for this heterogeneity. Future studies should be prospective and collect more detailed information. Our results are clinically relevant because they may improve early diagnosis. Given the current absence of medical therapies to improve survival, this enhanced understanding of the natural history of IPF strongly encourages more frequent patient reevaluation, research on new approaches to recognizing and managing IPF, and early referral for lung transplantation. Acknowledgments We thank Raed Al-Tayeb for collecting data. References 1. King TE. Clinical advances in the diagnosis and therapy of the interstitial lung diseases. Am J Respir Crit Care Med 2005;172: Raghu G, Collard HR, Egan JJ, Martinez FJ, Behr J, Brown KK, et al. An official ATS/ERS/JRS/ALAT statement: Idiopathic pulmonary fibrosis: Evidence-based guidelines for diagnosis and management. Am J Respir Crit Care Med 2011;183: Coultas DB, Zumwalt RE, Black WC,Sobonya RE. The epidemiology of interstitial lung diseases. Am J Respir Crit Care Med 1994;150: Meltzer EB, Noble PW. Idiopathic pulmonary fibrosis. J Rare Dis 2008;3:8. 5. Alhamad EH. Interstitial lung diseases in Saudi Arabia: A singlecenter study. Ann Thorac Med 2013;8: Olson AL, Swigris JJ, Lezotte DC, Norris JM, Wilson CG, Brown KK. Mortality from pulmonary fibrosis increased in the United States from Am J Respir Crit Care Med 2007;176: Nalysnyk L, Cid-Ruzafa J, Rotella P, Esser D. Incidence and prevalence of idiopathic pulmonary fibrosis: Review of the literature. Eur Respir Rev 2012;21: Navaratnum V, Fleming KM, West J, Smith CJ, Jenkins RG, Fogarty A, et al. The rising incidence of idiopathic pulmonary fibrosis in the UK. Thorax 2011;66: Raghu G, Weycker D, Edelsberg J, Bradford WZ, Oster G. Incidence and prevalence of idiopathic pulmonary fibrosis. Am J Respir Crit Care Med 2006;174: American Thoracic Society. Idiopathic pulmonary fibrosis: Diagnosis and treatment. International consensus statement. American Thoracic Society (ATS), and the European Respiratory Society (ERS). Am J Respir Crit Care Med 2000;161: Gay SE, Kazerooni EA, Toews GB, Lynch JP 3 rd, Gross BH, Cascade PN, et al. Idiopathic pulmonary fibrosis: Predicting response to therapy and survival. Am J RespirCrit Care Med 1998;157: Ley B, Collard H, King TE Jr. Clinical Course and prediction of Survival in Idiopathic pulmonary Fibrosis. Am J Respir Crit Care Med 2011;183: Alhamad EH, Masood M, Shaik SA, Arafah M. Clinical and functional outcomes in Middle Eastern patients with idiopathic pulmonary fibrosis. ClinRespir J2008; 2: Patti MG, Tedesco P, Golden J, Hays S, Hoopes C, Meneghetti A, et al. Idiopathic pulmonary fibrosis: How often is it really idiopathic? J GastrointestSurg 2005;9: Zappala CJ, Latsi PI, Nicholson AG, Colby TV, Cramer D, Renzoni EA, et al. Marginal decline in forced vital capacity is associated with a poor outcome in idiopathic pulmonary fibrosis. EurRespir J 2010;35: Raghu G, Brown KK, Bradford WZ, Starko K, Noble PW, Schwartz DA, et al. Idiopathic Pulmonary Fibrosis Study Group. A placebo-controlled trial of interferon gamma-1b in patients with idiopathic pulmonary fibrosis. N Engl J Med 2004;350: Alakhras M, Decker PA, Nadrous HF, Collazo-Clavell M, Ryu JH. Body mass index and mortality in patients with idiopathic pulmonary fibrosis. Chest 2007;131: Gribbin J, Hubbard R, Smith C. Role of diabetes mellitus and gastro-oesophageal reflux in the aetiology of idiopathic pulmonary fibrosis. Respir Med 2009;103: Enomoto T, Usuki J, Azuma A, Nakagawa T, Kudoh S. Diabetes mellitus may increase risk for idiopathic pulmonary fibrosis. Chest 2003;123: Ponnuswamy A, Manikandan R, Sabetpour A, Keeping IM, Finnerty JP. Association between ischaemic heart disease and interstitial lung disease: Acase-control study. 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5 23. Raghu G, Freudenberger TD, Yang S, Curtis JR, Spada C, Hayes J, et al. High prevalence of abnormal acid gastro-oesophageal reflux in idiopathic pulmonary fibrosis. Eur Respir J 2006;27: Lee JS, Ryu JH, Elicker BM,Lydell CP, Jones KD, Wolters PJ, et al. Gastroesophageal reflux therapy is associated with longer survival in patients with idiopathic pulmonary fibrosis. Am J Respir Crit Care Med 2011;184: Nathan SD, Noble PW, Tuder RM. Idiopathic pulmonary fibrosis and pulmonary hypertension: Connecting the dots. Am J Respir Crit Care Med 2007;175: Martinez FJ, Safrin S, Weycker D, Starko KM, Bradford WZ, King TE Jr, et al. The clinical course of patients with idiopathic pulmonary fibrosis. Ann Intern Med 2005;142: Jegal Y, Kim DS, Shim TS, Lim CM, Do Lee S, Koh Y, et al. Physiology is a stronger predictor of survival than pathology in fibrotic interstitial pneumonia. Am J Respir Crit Care Med 2005;171: Flaherty KR, Andrei AC, Murray S, Fraley C, Colby TV, Travis WD, et al. Idiopathic pulmonary fibrosis: Prognostic value of changes in physiology and six-minute-walk test. Am J Respir Crit Care Med 2006;174: Swigris JJ, Wamboldt FS, Behr J, du Bois RM, King TE, Raghu G, et al. The 6 minute walk in idiopathic pulmonary fibrosis: Longitudinal changes and minimum important difference. Thorax 2010;65: Wells AU, Richards TJ, Martinez FJ. Baseline values and short serial change: A road map for a poor early outcome in idiopathic pulmonary fibrosis. Am J Respir Crit Care Med 2011;184: How to cite this article: Sherbini N, Feteih MN, Wali SO, Alamoudi OS, Al-Faifi SM, Khalid I. Idiopathic pulmonary fibrosis in Saudi Arabia: Demographic, clinical, and survival data from two tertiary care hospitals. Ann Thorac Med 2014;9: Source of Support: Nil, Conflict of Interest: None declared. 172 Annals of Thoracic Medicine - Vol 9, Issue 3, July-September 2014
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