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Cite this article: Quiros-Roldan E, Pezzoli MC, Berlendis M, Raffetti E, Ferraresi A, et al. (2017) Chronic Obstructive Pulmonary Disease Screening Program in a HIV Outpatient Clinic of Northern Italy. Clin Res HIV/AIDS 4(2): 1039.

*Corresponding authorAlice Ferraresi, Department of Infectious and Tropical Diseases, University of Brescia and Spedali Civili General Hospital, P.le Spedali Civili number 1, 25123, Brescia, Italy, Tel: 39-0303995677; Fax: 39-0303396084; Email:

Submitted: 09 May 2017

Accepted: 20 July 2017

Published: 21 July 2017

Copyright© 2017 Ferraresi et al.

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Keywords•Chronic•Adherence•Spirometry•Screening

Research Article

Chronic Obstructive Pulmonary Disease Screening Program in a HIV Outpatient Clinic of Northern ItalyEugenia Quiros-Roldan1, Maria Chiara Pezzoli1, Marialma Berlendis2, Elena Raffetti2, Alice Ferraresi1*, Paola Rodari1, Francesco Castelli1 and the COPD in HIV Study Group1 1Department of Infectious and Tropical Diseases, University of Brescia and Spedali Civili General Hospital, Italy2Department of Medical and Surgical Specialties, University of Brescia, Italy

Abstract

Chronic Obstructive Pulmonary Disease (COPD) is under diagnosed in HIV-infected people and screening guidelines are lacking. This study aims to determinate the feasibility of a screening program and the prevalence of COPD under diagnosis in a HIV-positive cohort. We screened all outpatients attending their routine visit for HIV monitoring at the Clinic of Spedali Civili General Hospital, Brescia, from February 2015 to January 2016. The screening program consisted in: a) a questionnaire, b) a pre-bronchodilator peak flow measured with portable spirometer c) a post-bronchodilator peak flow measured with spirometer performed during a Pneumologist visit, for people who were positive for dot b. We invited 1463 subjects but only 89.6% of them completed the program. Two-hundred-eighy-two had a positive questionnarie and 65 patients showed respiratory impairment at portable spirometer. Diagnostic spirometry evidenced COPD in 22 patients (1.7% of all patients), among them 2 patients (9.1%) had severe grade COPD (GOLD stage 3, according to the Global Initiative for Chronic Obstructive Lung Disease). Only 89.6% of patients completed the program. Patients with, compared to patients without exacerbations, showed lower CD4 count at screening (534/mm3 vs 781/mm3 for patients with GOLD 1 and 495/mm3 vs 781/mm3 for patients with GOLD 2). The positive predictive value (the probability that a patient with abnormal test results had truly a COPD), was 33.8% for COPD screening questionnaire and the portable spirometer applied in series. Screening programs seems to be problematic as part of routine practice in HIV-infected patients: one in ten patients did not completed the program. Moreover, we found a prevalence of COPD under diagnosed of 1.7%.

ABBREVIATIONSCOPD: Chronic Obstructive Pulmonary Disease; Pre-BD

spirometry: Pre-Bronchodilator spirometry; Post-BD spirometry: Post-Bronchodilator spirometry; FVC: Forced Vital Capacity; FEV1: Forced Expiratory Volume in the first second; GOLD: Global Initiative for Chronic Obstructive Lung Disease; cART: Combination Antiretroviral Therapy; PPV: Positive Predictive Value; SD: Standard Deviation

INTRODUCTIONChronic Obstructive Pulmonary Disease (COPD) is a

considerable cause of morbidity and mortality in general population, with a substantial heterogeneity in COPD prevalence rates and high levels of under diagnosis around the world [1-3]. The high smoking rates in developing countries combined with an aging population account for the actual burden of the disease. However, the prevalence of COPD is under estimate, since it is not clinically apparent until it is moderately advanced. The main

factors associated with COPD under diagnosis are younger age, lower severity of airway obstruction and fewer respiratory symptoms [4].

HIV-infected patients have a high prevalence of COPD [1-3] partly due to the increased age and the frequent and continued smoking of tobacco in this population. In addition, HIV itself is an independent risk factor for COPD [5-7]. Notwithstanding these risk factors, screening guidelines for COPD in HIV-infected patients, as well as treatment management, are lacking [8] and data on under diagnosis of COPD in HIV are limited [9,10].

Acknowledgement of the problem in this population is becoming important for implementation of strategies for an early diagnosis, which can modify the prognosis. Primary care screening involves risk assessment via a formal prescreening questionnaire and, if positive, implementation of diagnostic spirometry testing [11].

The present study aims to determinate the feasibility of a

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COPD screening program in HIV-positive patients attending an Italian Center for HIV cure and, subsequently, to determine the prevalence of COPD under diagnosed in this setting.

MATERIALS AND METHODS

Study design and population

The present study was perform at the HIV outpatient Clinic of Spedali Civili General Hospital, Brescia (Italy), which provides care to around 3800 HIV-positive subjects. We invited all HIV-positive subjects that attended their routine visit for HIV monitoring to participate to the COPD screening program from February 2015 to January 2016. All patients with acute or known chronic respiratory illness were excluded.

This study was conducted in accordance with the guidelines of the 1964 Helsinki Declaration and its later amendments and the principles of Good Clinical Practice. The present study was approve by the Ethical Committee of Brescia province. Written informed consent was obtain for all enrolled subjects.

TESTING PROCEDUREThe COPD screening program was structure in three steps: a)

COPD questionnaire, b) fast spirometry with portable spirometer to identify patients in need of further diagnostic evaluation and c) post-bronchodilator peak flow measured with spirometer (post-BD spirometry).

Briefly, a COPD questionnaire was administrate during the HIV clinical visit. Patients with risk of COPD at questionnaire were invite to perform a fast spirometry with portable spirometer. Finally, patients with mild or severe airway obstruction measured with portable spirometer were invite to perform a Pneumologist visit and a post-BD spirometry.

a) COPD questionnaire

We used the five questions COPD screener tool published for the general population [12], which includes the following items: i) aged 40 years or older, ii) former (patients who have smoked more than 5 packs in the entire lifetime but now declare that they don’t smoke) or current smoker, iii) chronic cough with phlegm production, iv) shortness of breath and v) limited exercise. The questionnaire was administer by a HIV-specialist using a face-to-face interview during the routine HIV clinical appointment. All subjects, who answered positively to at least three questions were consider meeting satisfactory spirometry criteria and were invite for measuring airway obstruction by fast spirometry (forced vital capacity maneuver measured by portable spirometer) in the same day.

b) Pre-broncodilatator spirometry with portable spirometer (fast- spirometry)

Lung function measurements were performed according to the manufacturer’s recommendations using portable spirometer (Spirometer QM-SP100, Quirumed®, Health & Care) at the HIV clinic. Patients underwent three forced vital capacity (FVC) maneuvers and the mean reported as result. Efforts that were incomplete or in which the patient coughed were exclude.

Forced expiratory volume in the first second (FEV1) was also

measure. All measurements were perform for all patients by the same person of the sanitary staff at the HIV Clinic. Patients with FEV1 less than or equal to 80% predicted were considered have probable COPD and invited to consult at the Pneumology unit, including diagnostic spirometry test and recording the number of exacerbations of respiratory symptoms episodes during the last year. An exacerbation was defined as an acute event characterized by worsening of respiratory symptoms that was beyond normal day-to-day variations and leaded to medication.

c) Diagnostic spirometry testing

Spirometry was perform by trained technicians at the Pneumology Unit using Vmax® Encore PFT system (CareFusion, CA, USA). It was perform on participants before and 15 minutes after the administration of 400 mcg of salbutamol by a pressurized metered dose inhaler (pMDI) with a space chamber.

According to the Global Initiative for Chronic Obstructive Lung Disease (GOLD) guidelines [13] and based on lung function values obtained by spirometry examination, airway obstruction was define as FEV1 to FVC ratio less than 0.7. Mild airway obstruction (GOLD 1) was define as a FEV1 greater than 80% predicted among those with airway obstruction. Moderate airway obstruction (GOLD 2) was define as a FEV1 among 50% and 80% predicted and severe (GOLD 3) when FEV1 was less than 50% predicted.

STATISTICAL ANALYSISAll statistical tests were two-sided, assumed a level of

significance of 0.05, and were performed using Stata 12 software (Stata Statistics/Data Analysis 12.0 - Stata Corporation, College Station, TX, USA).

RESULTSFrom February 2015 to January 2016 a total of 1463 HIV

positive subjects were invited to the COPD screening program; among them, 1435 subjects agreed to participate (98.1% participation rate) (Figure 1). Among participants, 76.3% was represent by males, with an average age of 46.2 ± 10.3 years. Current and former smoker were 47.0% and 21.1%, respectively. Almost all patients (98.1%) were on combination antiretroviral therapy (cART).

The Figure 1 shows the flowchart of the screening program.

COPD screening program steps

COPD screening questionnaire: Among 1435 patients that completed the questionnaire, 282 (19.6%) subjects had at least 3 out of 5 positive responses to COPD screening tool with the consequent clinical indication to spirometry. As regard to the 5 items, 1148 subjects (80.1%) were aged 40 years or older, 981 (68.4%) were former or current smokers, 220 (15.3%) reported chronic cough with phlegm production, 196 (13.7%) shortness of breath and 132 (9.2%) limited exercise.

Subjects with at least 3 out of 5 positive responses to COPD screening tool, compared to those without, had a lower proportion of immigrants (8.5% vs 17.1%) and higher proportion of intravenous drug users (44.5% vs 20.5%) (Table 1).

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Figure 1 Flowchart of the COPD screening program.

Pre-BD spirometry with portable spirometer (fast spirometry): Among subjects with indication for spirometry, 190 performed it (67.4% adherence rate). 65 patients (34.2%) showed respiratory impairment defined as FEV1 < 80%. Impairment was moderate in 60 patients (FEV1% predicted 60-79%) and severe in 5 patients (FEV1% predicted 40-59%). These subjects were refer to the Pneumology Unit to confirm the diagnosis. Among patients with a provisory diagnosis of COPD according to the fast spirometry that refused diagnostic spirometry, 4 had FEV1% predicted of 40-59% and 28 had a FEV1% predicted of 60-79%.

Among subjects with, compared to those without positive fast spirometry had a higher proportion of males (86.2% vs 70.4%) and former and current smokers (98.5% vs 96.0%) (Table 1).

Diagnostic spirometry: Among subjects referred to the Pneumology Unit, only 33 (50.8% adherence rate) joined the program. Diagnostic spirometry evidenced COPD in 22 (66.6%) patients: 12 (54.5%) patients had mild grade of airway obstruction (GOLD stage 1), 8 (36.3%) had moderate grade of airway obstruction (GOLD stage 2) and 2 (9.1%) had severe

grade (GOLD stage 3). None Gold stage 3 patients reported exacerbations during the last year but 5/12 Gold stage 1 and 2/8 GOLD stage 2 patients reported at least one exacerbation in the last year. No differences were find as regards to demographic and clinical characteristics undergoing or refusing the screening program (Table 2).

Interestingly, patients with, compared to patients without exacerbations, showed lower CD4 count at screening (534/mm3 vs 781/mm3 for patients with GOLD 1 and 495/mm3 vs 781/mm3 for patients with GOLD 2).

Positive predictive value of the screening program

The positive predictive value (PPV), i.e. the probability that a patient with abnormal test results had COPD, was 33.8% (95% CI: 22.6%-46.6%) for COPD screening questionnaire and pre-BD spirometry with portable spirometer applied in series.

DISCUSSION AND CONCLUSIONHere, we describe that in spite of a high participation

rate to the COPD screening program (98.1%) in our cohort

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Table 1: Demographic and clinical characteristics according to results of the three steps of the screening program.Negative Positive p-value

COPD screening questionnaire (n = 1435) 1153 282Male n (%) 852 (73.9) 218 (77.3) 0.238Migrant n (%) 197 (17.1) 24 (8.5) <0.001Intravenous drug user n (%) 227 (20.5) 121 (44.5) <0.001CD4 cell count, cell/mm3, mean (SD) 735.3 (322.8) 729.9 (347.8) 0.827Pre-BD spirometry (n = 190) 125 65Male n (%) 88 (70.4) 56 (86.2) 0.016Age, years ≥ 40 n (%) 114 (91.2) 62 (95.4) 0.295Migrant n (%) 10 (8.0) 5 (7.7) 0.941Intravenous drug use n (%) 33 (52.4) 46 (39.0) 0.083CD4 cell count, cell/mm3, mean (SD) 731.9 (367.8) 732.4 (348.2) 0.994Tobacco smoking Never smokers n (%) 5 (4.0) 1 (1.5) 0.049 Former smokers n (%) 90 (72.0) 57 (87.7) Current smokers n (%) 30 (24.0) 7 (10.8)Post-BD spirometry (n=33) 11 22Male n (%) 11 (100.0) 17 (77.3) 0.111Age, years ≥40 n (%) 10 (90.9) 22 (100.0) 0.333Migrant n (%) 0 (0) 1 (4.5) 1.000Intravenous drug use n (%) 7 (77.8) 10 (45.5) 0.132CD4 cell count, cell/mm3, mean (SD) 689.4 (295.7) 649.0 (276.0) 0.720Tobacco smoking Never smokers n (%) 0 (0) 0 (0) 0.542 Former smokers n (%) 11 (100.0) 20 (90.9) Current smokers n (%) 0 (0) 2 (9.1)Abbreviations: COPD: Chronic Obstructive Pulmonary Disease; SD: Standard Deviation; Pre-BD spirometry: Pre-Bronchodilator spirometry; Post-BD spirometry: Post-Bronchodilator spirometry

Table 2: Demographic and clinical characteristics related to screening program participation and adherence.COPD screening questionnaire, number of patients Not completed Completed p-values

Male n (%) 22 (78.6) 1070 (74.6) 0.629Age, years ≥40 n (%) 24 (85.7) 1148 (80.1) 0.457Migrant n (%) 4 (14.3) 221 (15.4) 0.869Intravenous drug use n (%) 6 (23.1) 348 (25.3) 0.798CD4 cell count, cell/mm3, mean (SD) 649.1 (416.6) 734.2 (328.1) 0.265Tobacco smoking Never smokers n (%) 8 (57.1) 454 (31.6) 0.104 Former smokers n (%) 5 (35.7) 676 (47.1)

Current smokers n (%) 1 (7.1) 305 (21.3)

Patients with pre-BD spirometry indication Not performed Performed p-valuesMale n (%) 74 (80.4) 166 (76.1) 0.409Age, years ≥40 n (%) 87 (94.6) 200 (91.7) 0.386Migrant n (%) 9 (9.8) 19 (8.7) 0.765Intravenous drug use n (%) 42 (46.2) 85 (41.1) 0.413CD4 cell count, cell/mm3, mean (SD) 724.4 (314.7) 723.5 (366.1) 0.986Tobacco smoking Never smokers n (%) 4 (4.3) 14 (6.9) 0.701 Former smokers n (%) 70 (76.1) 152 (74.5) Current smokers n (%) 18 (19.6) 38 (18.6)Patients with post-BD spirometry indication Not performed Performed p-valuesMale n (%) 28 (87.5) 30 (85.7) 0.830Age, years ≥40 n (%) 30 (93.8) 34 (97.1) 0.502Migrant n (%) 4 (12.5) 1 (2.9) 0.134Intravenous drug use n (%) 16 (50.0) 18 (54.6) 0.714

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of HIV-infected patients, only 89.6% completed the program. Interestingly, one of every five HIV-positive patients screened by COPD questionnaire had indications for spirometry, but adherence to pre-BD spirometry and diagnostic spirometry were only 67.4% and 50.8% respectively. 1.7% (22/1311) of patients that completed the screening program met the criteria for GOLD stage I or higher, but COPD had not been previously ascertained.

Early detection and correct diagnosis of COPD are extremely important. In fact, COPD is a chronic, slowly progressive disorder characterized by airflow obstruction, but it is also a preventable and treatable disease. COPD is linked with multiple comorbidities that include diabetes, cardiovascular disease, bone mineral density loss, kidney disease, cancer and cognitive decline and it seems that common pathways may be involved in the pathogenesis of COPD and those comorbidities [14,15]. Treated HIV infection is also associated with excess risk for all above cited comorbidities, which are also recognized as complications of ageing [16,17]. In our study, almost all patients invited to participate COPD screening program accepted to take part to it but, after that, a proportion failed to complete the program: 32.6% of patients with clinical criteria (positive questionnaire) and 49% of patients with probable COPD (FEV1 measured by portable spirometer < 80%) did not continued to the following screening step. Recently, other authors [9,10-18] found high drop-out rates to the COPD screening programs performed in USA and Canada in people with HIV infection. A recent study in general population describes that more than half (57.1%) of subjects with COPD who underwent pre-bronchodilatator spirometry refused to undergo post-BD spirometry [19]. We did not find demographic or epidemiological factors associated with the screening program success and they suggest a lack of COPD risk perception among HIV-infected people in spite of the high proportion of smokers. These data show that barriers during COPD screening program exist, contributing to the high rates of under diagnosed (ie ignorance of the risk, fear of being force to quit smoking, lack of time, deferred).

Patients on stable cART could have a wrong perception of health and, when severe symptoms are absent, they are focus only on CD4 number and HIV viral load leading to decline COPD screening offered. In fact, 98% of the patients included in the study were on stable cART and with optimal viro-immunological results and the engaging in the improvement of their own care by COPD screening was not appreciate enough. COPD was unrecognized in 22 screened patients (1.7%) even though in patients with FEV1 < 80% (10/22 patients) measured with a portable spirometer or patients who reported acute exacerbations during the previous year (7/22). These findings parallel those from others authors confirming the high rate of underdiagnosed COPD and other obstructive lung disease both in general population and in HIV-infected individuals [9,10,18-20].

Office spirometry (portable spirometer) and formal laboratory based spirometry have demonstrate an acceptable correlation between patients with [21] and without [22,23] obstructive lung disease in general population. Very few data are available about the portable spirometer performance in HIV positive population. Shirley et al. [9], showed that questionnaire and abnormal peak flow (pre-BD spirometry with portable spirometer) together yielded very poor in predicting COPD in HIV-infected patients (sensitivity of 20%, specificity of 93%, positive predictive value of 14.3% and negative predictive value of 95%). In our study the PPV of COPD questionnaire plus pre-BD spirometry with portable spirometer was 33.8%. These test performed more poorly in our study compared to previously studies of the general population [11,23], so that the most appropriate screening tools in this population remains unclear. Age, education and socioeconomic status, as well as co-morbidities, could be confounding factors and alter the performance of screening.

Finally, we confirm previous data noting that patients with more advanced immunosuppression endorsed worst respiratory symptoms [5,24].

The strength of this study is the large sample size that includes all patients followed in our HIV clinic, without restrictive exclusion (except previous or current respiratory diseases) or inclusion criteria. Our study has also some limitations. First, we could not record the reasons that could be associated with non-completion of the screening cascade. Second, lung function tests were perform only in patients with a previous positive step in the screening program. Therefore, it was impossible to study the performance of the screening program in people with HIV infection.

Obstructive lung diseases remain under diagnosed in HIV-infected people and COPD screening programs seem be problematic as part of routine practice in these patients. Further studies are necessaries to address HIV-infected patients motivations to adhere and complete COPD screening flow. Possible future strategies to improve patient acceptance include clear explanation of COPD and diagnostic procedures involved and educating them on the importance of completing the screening program.

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Quiros-Roldan E, Pezzoli MC, Berlendis M, Raffetti E, Ferraresi A, et al. (2017) Chronic Obstructive Pulmonary Disease Screening Program in a HIV Outpatient Clinic of Northern Italy. Clin Res HIV/AIDS 4(2): 1039.

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