Role of Pirfenidone in Idiopathic Pulmonary Fibrosis - A Longitudinal Cohort Study
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1 36 Journal of The Association of Physicians of India Vol. 64 May 2016 Original Article Role of Pirfenidone in Idiopathic Pulmonary Fibrosis - A Longitudinal Cohort Study KP Suraj 1, Neethu K Kumar 2, E Jyothi 3, Kiran Vishnu Narayan 4, G Biju 5 Abstract Background: But so far there is no proven pharmacological treatment for Idiopathic pulmonary fibrosis (IPF). As trials investigating different agents with different mechanisms of actions are going on, encouraging results have led to the licensing of the first IPF-specific drug, Pirfenidone. Objective: To assess the proportion of IPF among interstitial lung disease patients and to assess their treatment response to Pirfenidone Material and Methods: All consecutive patients attending the outpatient department from 1 st January 2012 to 30 th June 2012 with a proven diagnosis of Interstitial lung Disease (ILD) were included in this longitudinal cohort study. Out of the total ILDs, patients with IPF were identified. The disease, its natural course, available treatment options and the risks and benefits of drugs were discussed with each IPF patient along with their family members. After obtaining their consent, we started 23 patients on a combination of Pirfenidone, N-acetyl cysteine (NAC) and proton pump inhibitors (PPI). Patients were followed up for 52 weeks. Pirfenidone was discontinued in one patient due to an adverse effect 1 month after onset of treatment. Anova test using SPSS software and independent T test was used to analyse the data. Results: During the study period 69 patients with ILD attended our OPD which included 24 IPF patients representing 34.8% and 23 of these patients received treatment with Pirfenidone, NAC and PPI. One patient discontinued Pirfenidone due to adverse effects. After 12 months, 8 patients had worsening of FVC 10%, the FVC of 7 patients remained stable, 8 patients could not repeat the tests and none of them had improvement. There was less than 15% decline in DL CO for 9 patients, 7 patients could not repeat the test and none improved. 8 patients had stable dyspnoea on exertion and 11 had worsening. Three patients died. Combining all the above parameters, only 4 patients had stable disease with the rest having no improvement. Conclusions: The present study does not show any significant beneficial effect for Pirfenidone. Only four patients remained stable which cannot be attributed to the effect of any particular management strategy. Introduction I diopathic pulmonary fibrosis (IPF) is a progressive, and often fatal, inflammatory, fibroproliferative lung disease. Editorial Viewpoint Pirfenidone was the first drug approved for the treatment of idiopathic pulmonary fibrosis (IPF). This study shows that Pirfenidone may be effective in early stage of disease but may not be useful in advanced disease. During the past decade important progress has been made regarding the pathogenesis of IPF, which is the most devastating form of idiopathic interstitial pneumonia. 1 Although substantial progress has been made in the understanding of the clinical management of IPF in the past decade, the 2011 guidelines declared that no proven pharmacological treatment exists for IPF. Only two treatment modalities were recommended with strong support, long-term oxygen supplementation (LTOT) in patients manifesting clinically significant resting hypoxemia and lung transplantation in appropriate individuals. 2 As the trials investigating different agents with different mechanisms of actions are going on, encouraging results have led to the licensing of the first IPF-specific drug, Pirfenidone. But it was recommended only for those IPF patients with forced vital capacity (FVC) between 50% and 1 Professor, 2 Junior Resident, 3 Associate Professor, 4 Assistant Professor, Department of Pulmonary Medicine, 5 Assistant Professor, Department of Community Medicine, Institute of Chest Diseases, Government Medical College, Kozhikode, Kerala Received: ; Accepted:
2 Journal of The Association of Physicians of India Vol. 64 May %. 3 So the road to successful treatment is still long. The present study was done with an objective to know the proportion of Idiopathic Pulmonary Fibrosis among Interstitial Lung Diseases attending the Out-Patient Department (OPD) of a tertiary care centre and to assess the treatment response in patients with IPF. Objective To assess the proportion of IPF among interstitial lung disease patients and to assess their treatment response to Pirfenidone Material and Methods Setting: Institute of Chest Diseases, Government Medical College, Kozhikode Design: A longitudinal cohort study. Period: 1 st Jan th June 2012 Protocol Inclusion Criteria All consecutive patients with proven ILD (diagnosed by a combination of clinical features, chest X ray, pulmonary function tests and HRCT thorax) attending the OPD of the Institute of Chest Diseases, Government Medical College, Kozhikode Exclusion Criteria Patients with cardiac disease not secondary to lung disease, chronic liver disease, chronic renal disease, malignancy and immunosuppression were excluded from the study. Study Procedure The study was initiated after getting ethical clearance from the institutional ethics committee. During the enrolment period from January 2012 to June 2012, there were 69 patients with proven ILD. After a detailed clinical history and physical examination, patients were subjected to investigations like ECG, spirometry, diffusion study (DLco) and 6 minute walk test (6MWT). Specific investigations like rheumatoid arthritis factor, antinuclear antibody (ANA) profile, serum calcium, 24-hour urinary calcium and serum angiotensin converting enzyme level were also done in selected cases. Transbronchial lung biopsy and bronchoalveolar lavage were done in necessary cases. The diagnosis was based on the 2011 ATS/ ERS/ JRS/ALAT statement on IPF. After clinical consensus and the above investigations, 24 out of 69 patients were diagnosed to have IPF. The disease, its natural course, available treatment options and the risks and benefits of drugs were discussed with each patient along with their family members. After obtaining informed consent, 23 patients were started on Pirfenidone along with N-acetyl cysteine (NAC) and proton pump inhibitor (PPI). Pirfenidone was started in the dose of 200 mg thrice daily and increased up to 600 mg thrice daily. N-acetyl cysteine was given in the dose of 600 mg thrice daily. All patients were given PPI, Pantoprazole 40 mg once daily. All patients who were started on Pirfenidone were advised to wear long sleeved clothes, sun protective measures like umbrella, hat and sunscreen body lotions. One patient with end-stage disease was treated only with NAC, PPI and LTOT as consent was not obtained. All the 24 patients were also given psychosocial counselling, exercise training and advice regarding nutritional modulation. Pirfenidone was discontinued in one patient as he developed skin rash with pigmentation and pancytopenia 1 month after onset of treatment and was excluded from the study. Twenty-two patients were followed up for a period of 12 months with quarterly spirometry, 6MWT and half yearly DLco. HRCT of thorax was done at the end of 12 months in selected cases for assessing treatment response. The response was assessed based on the change in percentage of FVC and DLco and change in the grade of dyspnea. A fall in value of FVC 10%, DLco 15% and worsening of dyspnoea score were considered as surrogate markers of disease progression. Improvement was defined as an improvement in dyspnea score along with improvement in DLco. Statistical analysis was done by SPSS software version 16, by analysis of variance (anova test). For comparing two subgroups independent t test was used. A p value less than.05 was considered as significant. Results During the study period 69 patients with ILD attended our OPD which included 24 IPF patients representing 34.8 percent. Diagnosis of all the 69 patients is given in the pie chart (Figure 1). Majority of patients with IPF were living in rural area (n = 22), only two patients were living in urban area. The major presenting complaints were progressive dyspnea on exertion and dry cough.the patient characteristics are given in Table 1 which includes their baseline lung function at the time of presentation. Coexisting illness in IPF patients are given in Table 2. Twelve patients (50%) had history suggestive of gastroesophageal reflux disorder (GERD). Pirfenidone was started for 23 patients along with NAC and PPI and among these 7 patients were on home oxygen therapy. Pirfenidone was not started for one patient because of the advanced stage of the disease and reluctance in giving consent (Figure 2). Follow up at 52 Weeks Eight patients had worsening of FVC, with more than 10% decline. FVC of 7 patients remained stable, and none of them improved. Nine patients were not able to repeat spirometry because of breathlessness. So they were also considered as clinically deteriorated. After 12 months, the decline in DLco in 9 patients was less than 15%. Seven patients who were not able to repeat the
3 38 Journal of The Association of Physicians of India Vol. 64 May 2016 Sarcoidosis 10.1% (n=7) Silicosis 2.9% (n=2) Chemical pneumonitis 2.89% (n=2) n= n % Treatment received HP 10.1% (n=7) IPF 34.8% (n=24) n % Other CTD-ILD 7.2% (n=5) Systemic sclerosis 18.8% (n=13) NSIP 13% (n=9) n % n % Pirf+NAC+PPI Pirf+NAC+PPI+LTOT NAC+PPI+LTOT Discontinued Fig. 1: Diagnosis of all patients (n=69) (CTD-ILD-Connective Tissue Disease related ILD, HP-Hypersensitivity Pneumonitis, NSIP-Non-specific Interstitial Pneumonitis, IPF-Idiopathic Pulmonary Fibrosis) DLco were also considered as clinically deteriorated. None of them showed improvement in DLco. HRCT was repeated in 10 patients in whom at least one Table 1: Characteristics of IPF patients at baseline Patient characteristics No. of pts (%) (n=24) Age >50 years 23 (95.8) Males 11 (46) Symptom duration < 12 months 10 (41.7) months 1 (4.2) months 8 (33.3) months 5 (20.8) Dyspnoea (mmrc scale) 2 13 (54.1) 3 10 (41.7) 4 1 (4.2) Spirometry (FVC) (Restriction) Severe (<45% pred) 7 (29.2) Moderate (45-60%) 11 (45.8) Mild (60-80%) 6 (25) Mean FVC 53.16% DLco # Severe (<40%) 10 (41.7) Moderate (40-60%) 6 (25) Mild (>60%) 0 (0) Mean DLco 38.23% 6MWT (desaturation) # < 6 % 4 (16.7) 6-12% 13 (54.2) >12 % 5 (20.8) 6MWT distance mean m (# DLco and 6MWT could not be performed in 8 patients (33.3%) and 2 patients (8.3%) respectively because of dyspnoea and inability to do the test) parameter was stable. But in all the cases there was progression in the extent of honeycombing and volume loss. Three patients expired during the study, one due to an acute coronary event and two due to acute exacerbation of IPF. The treatment outcome as per various investigations is given in Table 3 and dyspnoea score is given in Table 4. On analysing all the parameters only 4 patients were stable, none improved, 15 patients deteriorated and 3 expired (Table 5). Reduction in FVC and DLCO after 12 months follow up was statistically significant with p value of 0.01 for FVC (mean %, SD 9.02) and for DLCO (mean -6.19%, SD 4.66). The mean Table 2: Co-existing illness in IPF pts Co-morbidities Number (n=24) Diabetes 3 (12.5%) Hypertension 3 (12.5%) Diabetes + Hypertension 3 (12.5%) GERD 12 (50%) (GERD: Gastroesophageal reflux disease) Table 3: Treatment outcome according to investigations (n=22) FVC DLCO 6MWT Improved Stable Worsened Not done Expired Fig. 2: Details of treatment received reduction in distance walked during 6MWT was m (SD 50.22, p 0.023).Among the 22 patients, there were 10 patients with symptoms less than 1 year duration, who were started on Pirfenidone along with NAC and PPI. On analysing their follow up reports, the fall in FVC was statistically significant (p 0.003), but reduction in DLCO was not statistically significant (p 0.088). The quality of life remained stable for these patients based on the mmrc grade of dyspnoea. Eventhough there was a reduction in the rate of decline of DLco in this group, whether this can be attributed to Pirfenidone alone cannot be definitely commented on because of the small sample size. There was no decline in rate of change in FVC in this group as compared to other studies on Pirfenidone. The change in FVC, DLco and 6MWTD after 12 months for different groups are given in Table 6. Considering individual parameters many patients were Table 4: Dyspnea after 12 months Dyspnea status Number (%) (n=22) Improved 0 (0) Stable 8 (36.4) Worsened 11 (50) Expired 3 (13.6) Table 5: Treatment outcome Outcome Number (%) (n=22) Improved 0 (0) Stable 4 (18.2) Worsened 15 (68.2) Expired 3 (13.6)
4 Journal of The Association of Physicians of India Vol. 64 May Table 6: Change in lung function parameters after 1 year of treatment 0 Treatment Response among groups % change in FVC All patients ± 9.02 p year symptoms >1year symptoms ± 9.84 p ± 6.77 p All values mean ± SD, Values in meter % change in DLco ± 4.66 p ± 4.21 p ± 2.16 p stable (FVC-7, DLco-9, 6MWT-4, status of dyspnea-8). Analysing the results, there were 4 patients, whose decline in FVC was <10%, reduction in DLCO <15% and remaining stable in subjective feeling of dyspnoea on exertion. A subgroup analysis was done comparing patients with 1 year symptoms and those with >1 year symptoms. Statistical analysis using independent t test was done comparing three parameters and results are as follows (Table 7). Eventhough there is a numerical difference in all the three parameters between the two groups, statistical significance was present only for DLco. The present study does not show any significant beneficial effect for Pirfenidone. Only four patients remained stable clinically which cannot be attributed to the effect of any particular management strategy. Four patients developed dyspepsia and nausea which was managed by symptomatic measures. The drug was well tolerated, without any significant side effects except in one patient, in our study. This patient developed severe adverse drug reaction in the form of skin rash with pigmentation and pancytopenia 1 month after onset of treatment. So Pirfenidone was discontinued and he was excluded from study. Change in 6 MWTD ± p ± p ± p Discussion Table 7: Lung function parameters of patients with 1 year symptoms Mean ± SD Mean change P value 1 year symptoms > 1 year symptoms Parameters Mean ± SD Mean change after treatment a after treatment b FVC % of predicted ± % 50.71± %.267 DLco% of predicted 40.75± % 35.94± %.047 6MWD ± m 155± m.278 Compares values of a versus b Decline <1 year >1 year Although substantial progress has been made in the understanding of pathogenesis and management of IPF, there is no proven pharmacological treatment for the disorder except Pirfenidone and probably the new TKI Nintedanib 4,5 with promising results in various studies which appears to reduce the risk of disease progression and to provide a beneficial effect. There are no large-scale studies of the incidence or prevalence of IPF in India on which to base formal estimates. The incidence of IPF was estimated at 10.7 cases per 100,000 per year for men and 7.4 cases per 100,000 per year for women in a population-based study from New Mexico with a male predominance. 6 Prevalence estimates for IPF have varied from 2 to 29 cases per 100,000 in the general population constituting at least 30% of total ILDs. The proportion of IPF among ILD patients in our hospital is 35 percent. In the present study IPF is more among females in contrast to the available literature. But this study is based on ILD patients attending the OPD of a referral hospital and not population based. It is unknown whether the FVC DICO 6MWD Fig. 3: Comparison of treatment response of patients with symptoms 1 year and >1 year incidence and prevalence of IPF are influenced by geographic, ethnic, cultural, or racial factors. This data cannot be extrapolated to general population as our institute is a tertiary care referral centre. The second objective of the study was to assess the clinical response of IPF patients to the current recommended treatment modalities. The study failed to show any clinical improvement in IPF patients on Pirfenidone, NAC and PPI combination with or without LTOT. On statistical analysis the mean decline in FVC of these patients after 12 months was 12.66% (SD 9.02, p 0.01), the mean decline in DLCO was 6.19% (SD 4.66, p 0.002) and mean change in distance walked during 6MWT was m (SD 50.22, p 0.023) reduction. Among the total 22 patients only 10 patients were newly diagnosed with duration of symptoms less than one year. So a subgroup analysis of these patients was also done even though statistical analysis is not significant in this small sample size. A subgroup analysis was done comparing patients with 1 year symptoms and those with >1 year symptoms. On analysing the change in FVC, DLCO and 6MWT there was a mean decline in FVC of 10.70% (p 0.003), mean decline in DLCO of 4.34% (p 0.088), mean decline in distance walked during 6MWT of 21 m (p 0.189) in case of patients with 1 year symptoms compared to a mean decline in FVC of 16.60% (p 0.005), mean decline in DLCO
5 40 Journal of The Association of Physicians of India Vol. 64 May 2016 of 10.50% (p 0.014), mean decline in distance walked during 6MWT of 50 m (p 0.076) for those who had symptoms >1 year (Figure 3). So there was a statistically significant reduction in FVC in both groups, but the reduction was much less in newly diagnosed group. There was statistically significant reduction in DLco for those who had symptoms >1 year, but in case of fresh patients decline in DLCO was not statistically significant. In case of 6MWT the reduction was not statistically significant in both groups. Comparing these two sets, the p values were for FVC, for DLco and for 6MWTD. Even though there was a favourable response in all the parameters in newly diagnosed patients with less than one year symptoms, statistical significance was demonstrable only in DLco (p value-0.047). Patients belonging to the group with symptoms >1 year, were most likely having advanced lung disease with end stage fibrosis as evidenced by the diminished lung function and exercise capacity. So considering the progressive nature of the disease it seems logical that Pirfenidone or any other intervention had little effect on the outcome once the disease had progressed to end stage. The alternate group being naive IPF patients had reasonably good lung function and exercise capacity at baseline. So the slow decline in lung function can be ascribed to either slow progression of the disease or to the effect of Pirfenidone. Even though there was significant difference between the two groups in all the three parameters, statistical significance was there only in the case of DLco (p value-0.047). A larger study enrolling new patients will be useful in reaching a conclusion. In a study conducted by Toru Arai et al it was found that in IPF patients with mild disease there were indications of a good response to Pirfenidone. 7 In a study conducted by Iwasawa T et al 8 on CT analysis of the effect of Pirfenidone in patients with idiopathic pulmonary fibrosis, a significantly larger proportion of Pirfenidonetreated patients showed stable respiratory status than the control. The change in fibrous lesions were also significantly smaller in the Pirfenidone group than in the control group in both visual score (p=0.006) and computer analysis (p<0.001). The CAPACITY programme with two concurrent phase 3 clinical trials (studies 004 and 006) also investigated the role of Pirfenidone in patients with mild to moderate IPF and these trials also showed some beneficial effect of Pirfenidone in patients with IPF. 9 The present study does not show any significant beneficial effect for Pirfenidone. This may be due to the advanced stage of the disease at which the drug was started. However subset analyses of newly diagnosed cases with less than one year symptoms show a favourable response with a statistical significant change in diffusion capacity. Only four patients remained stable clinically which cannot be attributed to the effect of any particular management strategy. The clinical course of the disease is highly variable and the rate of progression of the disease is individualised. The course of the disease cannot be modified quantitatively by currently available drugs. The drug was well tolerated, without any significant side effects except in one patient, in our study. So these drugs can be given along with pulmonary rehabilitation, but the long term effects cannot be commented based on this study as the patients were followed up for only 12 months. Limitations There are many, the most important, being the small sample size. Only 22 patients were included in follow up because of the short period for recruitment of patients which resulted in a small sample size. The follow up was done for only 52 weeks, for which we cannot comment on the long term benefits and demerits of the drugs used. Most of the patients were having advanced disease so that the effect of Pirfenidone is debatable. Most of the previous trials of Pirfenidone were done using a higher dose (2403 mg) and NICE guidelines also recommend a dose of 2403 mg (3x267mg capsules 3 times daily). 3,10,11 But the strength of tablets available in India is different from that in Europe. Conclusion The present study does not show any significant beneficial effect for Pirfenidone in IPF. However subset analyses of newly diagnosed cases with less than one year symptoms show a favourable response with a statistical significant change in diffusion capacity. Only four patients remained stable which cannot be attributed to the effect of any particular management strategy. Larger trials enrolling patients with early stage disease is required to find out the effect of Pirfenidone. So better awareness of the disease and early referral may be encouraged, and patients may be enrolled in specific therapy trials at an earlier stage of the disease, when significant fibrosis has not occurred. References 1. Antoniou KM, Margaritopoulos GA, Siafakas NM. Pharmacological treatment of idiopathic pulmonary fibrosis: from the past to the future. Eur Respir Rev 2013; 22: Raghu G, Collard HR, Egan JJ et al. An Official ATS/ERS/JRS/ALAT Statement: Idiopathic Pulmonary Fibrosis: Evidencebased Guidelines for Diagnosis and Management. Am J Respir Crit Care Med 2011; 183: Pirfenidone for treating idiopathic pulmonary fibrosis. NICE technology appraisal guidance.nice.org.uk/ta April Richeldi L, dubois RM, Raghu G et al. Efficacy and Safety of Nintedanib in Idiopathic Pulmonary Fibrosis. N Engl J Med 2014; 370:
6 Journal of The Association of Physicians of India Vol. 64 May King TE Jr, Bradford WZ, Castro-Bernardini S, et al. A Phase 3 Trial of Pirfenidone in Patients with Idiopathic Pulmonary Fibrosis. N Engl J Med 2014; 370: Coultas DB, Zumwalt RE, Black WC, et al. The epidemiology of interstitial lung diseases. Am J Respir Crit Care Med 1994; 150: Toru Arai, Yashikazu Inoue, Yumiko Sasaki et al. Predictors of the clinical effects of Pirfenidone on idiopathic pulmonary fibrosis. Respiratory Investigation 2014; 52: Iwasawa T, Ogura T, Sakai F et al. CT analysis of the effect of pirfenidone in patients with idiopathic pulmonary fibrosis. Eur J Radiol 2014; 83: Noble PW, Albera C, Bradford WZ, et al. Pirfenidone in patients with idiopathic pulmonary fibrosis (CAPACITY): two randomised trials. Lancet 2011; 377: Vincent Cottin: Changing the idiopathic pulmonary fibrosis treatment approach and improving patient outcomes. Eur Respir Rev 2012; 21: Michael Kreuter: Pirfenidone: an update on clinical trial data and insights from everyday practice. Eur Respir Rev 2014; 23:
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