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Effects of COVID-19 pandemic on the management of pulmonary hypertension

Published:November 25, 2022DOI:https://doi.org/10.1016/j.rmed.2022.107061

      Abstract

      The coronavirus of 2019 (COVID-19) disrupted delivery of healthcare. Patients with pulmonary hypertension (PH), especially pulmonary arterial hypertension (PAH), require significant resources for both diagnosis and management and are at high risk for decompensation due to disruption in their care. A survey consisting of 47 questions related to the care of patients with PH was designed by the American College of Chest Physicians 2020–2021 Pulmonary Vascular Disease (PVD) NetWork Steering Committee and sent to all members of the PVD NetWork, as well as the multiple other professional networks for PH. Participation was voluntary and anonymous. Responses were collected from November 2020 through February 2021. Ninety-five providers responded to this survey. The majority (93%) believe that care of PH patients has been affected by the pandemic. Sixty-seven percent observed decreased referrals for PH evaluation. Prior to the pandemic, only 15% used telemedicine for management of PH patients compared to 84% during the pandemic. Telemedicine was used most for follow up of selected low-risk patients (49%). While 22% respondents were completely willing to prescribe new PAH therapy via telemedicine, 11% respondents were completely unwilling. Comfort levels differed based on type of medication being prescribed. Over 90% of providers experienced disruptions in obtaining testing and 31% experienced disruptions in renewal or approval of medications. Overall, providers perceived that the COVID-19 pandemic caused significant disruption of care for PH patients. Telemedicine utilization increased but was used mostly in low-risk patients. Some providers had a decreased level of comfort prescribing PAH therapy via telemedicine encounters.

      Keywords

      Abbreviations

      6MWD
      6-min walk distance
      ACCP
      American College of Chest Physicians
      ATS
      American Thoracic Society
      BNP
      B-type natriuretic peptide
      COVID-19
      coronavirus disease of 2019
      Echo
      transthoracic echocardiogram
      FPHR
      French Pulmonary Hypertension Registry
      ISHLT
      International Society for Heart and Lung Transplantation
      NT-proBNP
      N-terminal prohormone B-type natriuretic peptide
      PAH
      pulmonary arterial hypertension
      PFTs
      pulmonary function tests
      PH
      pulmonary hypertension
      PHA
      Pulmonary Hypertension Association
      PHCR
      Pulmonary Hypertension Clinicians and Researchers
      PHPN
      Pulmonary Hypertension Professional Network
      PRO
      patient-reported outcome
      PVD
      pulmonary vascular disease
      PVRI
      Pulmonary Vascular Research Institute
      RAP
      right atrial pressure
      RHC
      right heart catheterization
      RIGHT-NET
      RIGHT Heart International NETwork
      V/Q
      ventilation/perfusion
      WHO
      World Health Organization

      1Introduction

      The coronavirus disease of 2019 (COVID-19) has caused significant disruption in non-COVID related medical care since its debut. A significant decrease in healthcare utilization occurred in March of 2020, when the World Health Organization (WHO) first announced pandemic status, with dramatic drops in office visits in the following weeks [
      • Patel S.Y.
      • Mehrotra A.
      • Huskamp H.A.
      • et al.
      Trends in outpatient care delivery and telemedicine during the COVID-19 pandemic in the US.
      ,
      • Whaley C.M.
      • Pera M.F.
      • Cantor J.
      • et al.
      Changes in health services use among commercially insured US populations during the COVID-19 pandemic.
      ]. Estimates of missed or delayed care ranged from 20% to over 40% of adults in the United States [
      • Ni B.
      • Gettler E.
      • Stern R.
      • et al.
      Disruption of medical care among individuals in the southeastern United States during the COVID-19 pandemic.
      ,
      • Findling M.G.
      • Blendon R.J.
      • Benson J.M.
      Delayed care with harmful health consequences—reported experiences from national surveys during coronavirus disease 2019.
      ]. In one study, basic laboratory testing during the early pandemic decreased by 81–90% and new medication therapy prescriptions for even common drugs decreased by 52–60% [
      • Wright A.
      • Salazar A.
      • Mirica M.
      • et al.
      The invisible epidemic: neglected chronic disease management during COVID-19.
      ]. There is an increased likelihood of healthcare delays among women and patients who had greater perceived risk from COVID-19 infection [
      • Ni B.
      • Gettler E.
      • Stern R.
      • et al.
      Disruption of medical care among individuals in the southeastern United States during the COVID-19 pandemic.
      ].
      Patients with pulmonary hypertension (PH) are a particularly high-risk group for disruption of care due to their extensive care needs and highly specialized care teams. Current guidelines for pulmonary arterial hypertension (PAH) in particular recommend updated risk assessment with tools such as the REVEAL 2.0 calculator at every clinical encounter [
      • Galiè N.
      • Channick R.N.
      • Frantz R.P.
      • et al.
      Risk stratification and medical therapy of pulmonary arterial hypertension.
      ,
      • Humbert M.
      • Kovacs G.
      • Hoeper M.M.
      • et al.
      ESC/ERS Guidelines for the diagnosis and treatment of pulmonary hypertension: developed by the task force for the diagnosis and treatment of pulmonary hypertension of the European Society of Cardiology (ESC) and the European Respiratory Society (ERS).
      ]. These calculators include laboratory and echocardiographic values and pulmonary diagnostic assessments which require frequent healthcare contact. PAH therapies include medications with potent hemodynamic effects that need careful and frequent monitoring for titration. Delays in diagnosis and referral to PH centers is well documented and has been further compounded by the pandemic [
      • Deaño R.C.
      • Glassner-Kolmin C.
      • Rubenfire M.
      • et al.
      Referral of patients with pulmonary hypertension diagnoses to tertiary pulmonary hypertension centers: the multicenter RePHerral study.
      ,
      • Yogeswaran A.
      • Gall H.
      • Tello K.
      • et al.
      Impact of SARS-CoV-2 pandemic on pulmonary hypertension out-patient clinics in Germany: a multi-centre study.
      ].
      PH patients are considered a high risk group for increased morbidity and mortality from COVID-19 [
      • Ryan J.J.
      • Melendres-Groves L.
      • Zamanian R.T.
      • et al.
      ,
      • Belge C.
      • Quarck R.
      • Godinas L.
      • et al.
      COVID-19 in pulmonary arterial hypertension and chronic thromboembolic pulmonary hypertension: a reference centre survey.
      ]. Ryan et al. published general recommendations for the management of PH during the COVID-19 pandemic, which include suggestions to limit testing in select patients to decrease exposure to risks from healthcare encounters [
      • Ryan J.J.
      • Melendres-Groves L.
      • Zamanian R.T.
      • et al.
      ]. Similar recommendations were made for patients with left heart failure [
      • DeFilippis E.M.
      • Reza N.
      • Donald E.
      • et al.
      Considerations for heart failure care during the COVID-19 pandemic.
      ], the most common cause of PH, as well as the use of cardiac imaging in general [
      • Skulstad H.
      • Cosyns B.
      • Popescu B.A.
      • et al.
      COVID-19 pandemic and cardiac imaging: EACVI recommendations on precautions, indications, prioritization, and protection for patients and healthcare personnel.
      ]. In line with general healthcare trends [
      • Patel S.Y.
      • Mehrotra A.
      • Huskamp H.A.
      • et al.
      Trends in outpatient care delivery and telemedicine during the COVID-19 pandemic in the US.
      ,
      • Bossone E.
      • Mauro C.
      • Maiellaro A.
      • et al.
      Cardiac teleconsulting in the time of COVID-19 global pandemic: the “Antonio Cardarelli” Hospital project.
      ,
      • Salzano A.
      • D'Assante R.
      • Stagnaro F.M.
      • et al.
      Heart failure management during the COVID-19 outbreak in Italy: a telemedicine experience from a heart failure university tertiary referral centre.
      ], use of telehealth services among PH patients has increased [
      • Hinojosa W.
      • Cristo‐Ropero M.J.
      • Cruz‐Utrilla A.
      • et al.
      The Impact of Covid 19 Pandemic on Pulmonary Hypertension. What Have We Learned? Pulm Circ.
      ]. A recent review discusses how risk assessment for PH patients can be adapted to increasing usage of telehealth during the COVID-19 pandemic [
      • Wesley Milks M.
      • Sahay S.
      • Benza R.L.
      • et al.
      Risk assessment in patients with pulmonary arterial hypertension in the era of COVID 19 pandemic and the telehealth revolution: state of the art review.
      ]. It is unclear if this initiative was sufficient in counterbalancing the decrease in access to in-person care.
      While a portion of the pandemic disruption is from decreased patient-initiated contact with healthcare [
      • Kopeć G.
      • Tyrka A.
      • Jonas K.
      • et al.
      The coronavirus disease 2019 pandemic prevents patients with pulmonary hypertension from seeking medical help.
      ], it has not been well-described in what other ways the care of patients with PH has been disrupted. There are scant data on how PH providers changed practice patterns in response to the challenges posed by the COVID-19 pandemic. This survey was designed to evaluate how respondents perceived care of PH patients changed during the pandemic.

      2Methods

      The survey was designed and reviewed by the American College of Chest Physicians (ACCP) 2020–2021 Pulmonary Vascular Disease (PVD) NetWork Steering Committee. In total, the survey consisted of 47 questions regarding the care of PH patients during the COVID-19 pandemic.
      The survey was then sent to providers involved in the management of PH via multiple routes, including the ACCP PVD NetWork, the American Thoracic Society (ATS) DocMatter Community, Pulmonary Hypertension Clinicians and Researchers (PHCR), Pulmonary Hypertension Professional Network (PHPN), International Society for Heart and Lung Transplantation (ISHLT), Pulmonary Vascular Research Institute (PVRI), and the RIGHT Heart International NETwork (RIGHT-NET). No patient specific information was obtained. This survey did not require IRB submission or approval. No external funding was used for completion of this project. Responses were collected from November 2020 through February 2021. There were a total of 95 respondents to the survey. Respondents were allowed to abstain from any question and therefore not all questions were answered by all respondents. The number of responses to each question ranged from 53 to 94, with one question garnering only 23 responses due to being contingent on the prior question. Percentages were calculated using the number of responses per question as the denominator (Supplement 1).

      3Results

      3.1Demographics

      There were a total of 95 respondents to the survey. Of these, 44 (47%) were female and 72 (83%) were physicians. The primary specialty of respondents was pulmonary (63%), followed by cardiology (32%). Most respondents were from the United States (87%). Respondents were primarily from academic hospitals (77%) and in urban settings (78%). The majority of respondents (65%) had been in practice for 11 years or more, and 67% of respondents had an outpatient PH practice with over 100 patients. Over a third (37%) of respondents practiced at a Pulmonary Hypertension Association (PHA) Comprehensive Care Center with another 11% practicing at a PHA Regional Clinical Program. These demographics are summarized in Table 1.
      Table 1Respondent demographics.
      n%
      Total95100.0
      Female4446.8
      Physician720.8
      Nurse Practitioner1517.2
      Specialty89
      Cardiology3032.4
      Pulmonary5963.4
      Other44.3
      Country89
      United States8187.1
      Other
      Region of Country78
      Northeast2125.9
      Southeast1417.3
      Midwest2530.9
      Southwest1822.2
      Northwest33.7
      Practice Setting87
      Academic Hospital7076.9
      Community Hospital1819.8
      VA or Military11.1
      Other22.2
      Community Setting87
      Urban7178.0
      Suburban1516.5
      Rural55.5
      Provider Years in Practice87
      In training55.5
      <5 years1112.1
      5–10 years1617.6
      11–20 years2426.4
      >20 years3538.5
      Outpatient Practice Patient Volume82
      <50 patients1618.6
      50-100 patients1214.0
      101-250 patients2124.4
      >250 patients3743.0
      Practice Accreditation82
      PHA CCC3237.2
      PHA RCP910.6
      VA: Veteran's Health Administration; PHA: Pulmonary Hypertension Association; CCC: Comprehensive Care Center; RCP: Regional Care Program.

      3.2Decreasing risk of COVID-19 transmission

      Seventy-nine (93%) respondents believe the way they provided care for patients with PH has been affected by the COVID-19 pandemic. Most providers observed a reduction in in-person office visits, with 39 (46%) respondents estimating less than 50% of their patients are being seen in-person, and another 26 (31%) respondents estimating less than 75% of their patients are being seen in person. Of the patients being seen in-person, 69 (82%) respondents screened patients for COVID-19 prior to the visit, with the most common screening measures being symptom questionnaires and temperature assessments, used by 66 (100%) and 47 (71%) respondents respectively (Fig. 1). Patients who screen positive were primarily transitioned to telehealth visits by 36 (55%) respondents and sent to a centralized testing site for further testing and triaging by 23 (35%) respondents.
      Fig. 1
      Fig. 1Provider Screening Effects on Usage of Telehealth
      Percentages provided indicate the proportion of respondents who performed each option. For providers still seeing patients in clinic, the majority utilized some form of screening for patients who were higher risk of transmitting COVID in the clinic. Screening measures varied, although all used some form of symptoms questions. If a patient screening positive, measures taken also varied, with more than half of respondents transitioning the patients to telemedicine appointments.
      Within outpatient clinics, the primary measures used to decrease risk of COVID-19 transmission to patients were masking of both patients and staff (99%), physical distancing between patients (88%), sanitizing rooms between patient visits (83%), physical distancing between patients and providers (72%), and only allowing patients into the clinic at time of visit to limit time in a common waiting area (62%). Primary measures to decrease risk of transmission between staff members were encouraging self-quarantine in the event of exposure or symptom onset (90%), daily symptom screening prior to start of clinic (80%), daily temperature checks (59%), testing staff with recent exposures (58%), and testing staff if daily screening is positive (56%). These preventative measures are summarized in Table 2.
      Table 2Common precautions taken with patients or staff members to reduce transmission of COVID.
      Requirements for Patients
      Typen%
      Patient wears mask8099
      Distancing between patients7188
      Sanitizing exam rooms between visits6783
      Distancing between patient and provider5872
      Restricted access to waiting room5062
      Distancing with plexiglass between patients and staff4454
      Requirements for Staff
      Typen%
      Staff wears mask8099
      Encourage self-quarantine if exposed or symptomatic7390
      Daily verbal symptom screening6580
      Daily temperature checks4859
      Testing staff if recent exposure4758
      Testing staff if screening positive4556

      3.3Usage of telemedicine

      Prior to the COVID-19 pandemic, only 12 (15%) respondents used telemedicine for patients with PH (Table 3). This shifted dramatically to 69 (84%) respondents using telemedicine during the pandemic with varying rates of use. For 27 (33%) respondents, less than 25% of their patients with PH were seen via telemedicine, whereas 17 (21%) respondents saw over 50% of their patients with PH via telemedicine. Many providers had a period of time during which they saw patients with PH only via telemedicine, primarily in March and April of 2020 with 24 (29%) respondents only using telemedicine during that time. Utilization of telemedicine services has varied since early in the pandemic, with 30 (37%) respondents reporting increased use and 43 (53%) respondents reporting decreased use. Despite this, 24 (30%) respondents still reported seeing over 50% of patients with PH via telemedicine. The most popular platforms for performing telemedicine visits were Zoom (43%), electronic medical record based video clients (40%), telephone (35%), or Doximity (28%).
      Table 3Change in telemedicine use throughout the pandemic.
      Prior to the current CoVID-19 pandemic, did you provide care for PH patients in your practice using telemedicine? (n=82)
       Yes1214.6%
       No7085.4%
      For providers using telemedicine, what percentage of patients are seen via telemedicine? (n=75)
       < 25%2733.0%
       25–50%2530.5%
       50–75%1113.4%
       > 75%67.3%
       Not using67.3%
      How has the current percentage of PH patients seen with telemedicine changed since early in the pandemic? (n=81)
       Increased to > 50%1721.0%
       Increased but <50%1316.0%
       No change89.9%
       Decreased to < 50%364.4%
       Decreased but >50%78.6%
      Respondents varied in patient selection for telemedicine visits. For patients who specifically requested telemedicine services, 63 (77%) respondents provided them. Telemedicine was used most commonly for select low risk follow up patients (49%), followed by intermediate risk follow-up patients (38%). A quarter of providers (26%) used telemedicine for all follow-up encounters, and a small portion (15%) used telemedicine for all new patient visits.
      Respondents also varied in comfort level with managing patients with PH using telemedicine (Fig. 2). While 16 (22%) respondents were completely willing to prescribe new PAH therapy via telemedicine, 8 (11%) respondents were completely unwilling to do so. The rest had varying levels of comfort with 20 (27%) being somewhat willing, 18 (25%) being somewhat unwilling, and 11 (15%) being neutral regarding prescribing new PAH therapy via telemedicine. Comfort levels differed based on type of medication being prescribed. While 18 (25%) respondents were completely willing to initiate oral PAH therapy via telemedicine, only 11 (15%) respondents were completely willing to initiate inhaled prostacyclin and 8 (11%) respondents were completely willing to initiate parenteral therapy. Likewise, only 5 (7%) respondents were completely unwilling to initiate oral PAH therapy via telemedicine, compared to 12 (16%) for inhaled prostacyclin and 35 (48%) for parenteral therapy.
      Fig. 2
      Fig. 2Provider Willingness and Comfort Level in Managing PAH via Telemedicine
      Respondents were asked how willing or comfortable they were in initiating pulmonary arterial hypertension (PAH) specific therapy after evaluating a patient through telemedicine. Answers varied based on the type of therapy.

      3.4Disruption of care

      Over 90% of respondents reported difficulties obtaining routine tests for diagnosis and monitoring of patients with PH during the pandemic. This appears primarily related to difficulties with limited test availability followed by patient choice. Respondents were asked to rank 8 tests in order of which were most impacted by the COVID-19 pandemic with 1 being the most impacted and 8 being the least. The most significantly impacted test was pulmonary function tests (PFT), followed by ventilation/perfusion (V/Q) scans, right heart catheterizations (RHC), 6-min walk distance (6MWD), and transthoracic echocardiograms (ECHO), in order. While most respondents still performed 6MWD, the portion of patients being evaluated decreased, with 33 (48%) respondents assessing less than 50% of their patients with a 6MWD. Most 6MWD tests were conducted in clinic, with masks. In replacement of 6MWD, 63 (93%) respondents used questions to assess functional status, whereas 7 (10%) respondents requested a 6MWD to be completed at home.
      Certain tests, such as PFTs, generate aerosols, and have thereby undergone changes in how they are conducted. While most respondents were still able to obtain PFTs, 9 (13%) respondents were not. Others obtained them only after negative pre-procedural testing for COVID-19 (60%), with providers wearing N95 masks and other personal protective equipment (54%), using expiration filters on PFT machines (37%), or in rooms with negative pressure or HEPA filters (21%). RHCs were unavailable only to 3 (4%) respondents and required similar precautions as PFTs with pre-procedural testing (83%), patients wearing surgical masks (58%), and providers wearing N95 masks (38%).
      Most respondents (69%) did not experience disruptions to renewal or approval of medications for patients with PH. For those that did, disruptions were primarily due to logistical delays related to the pandemic (74%), limited patient assessment due to decreased clinic visits (70%), and inability to obtain required testing for medication approval or renewal (57%). For patients on teratogenic medications, 28 (38%) respondents allowed substitution with home pregnancy tests to continue renewing medication prescriptions, whereas 22 (30%) respondents required mandatory laboratory testing as usual. Others (32%) encouraged laboratory testing but allowed occasional missed tests.
      Referral rates generally decreased, although 5 (7%) respondents had increased referral volume and 19 (26%) had no change. Otherwise, 25 (34%) respondents had a decrease in referral volume of up to 25% and 17 (23%) experienced a decrease up to 50%. Similar trends were seen in follow-up visit volume, with 5 (7%) respondents reporting increased volume, 16 (22%) reporting no change, 23 (31%) reporting a decrease up to 25%, and 24 (32%) reporting a decrease up to 50%. Respondents did not report large changes in how COVID-19 affected the time they had in clinic to see patients, with 13 (18%) reporting increased time, 30 (41%) reporting no change, and 19 (26%) reporting a decrease of less than 25%.

      3.5Effect on research

      For 60 (81%) of respondents, the COVID-19 pandemic affected research activities for patients with PH in their clinic. Of those affected, 31 (53%) respondents reported a pause on all new research activities and 30 (51%) reporting inability to obtain tests as required per research protocols. Conversion of research patient encounters to telemedicine visits occurred for 15 (25%) respondents.

      3.6COVID-19 infections

      Over 80% of respondents reported having patients with PH infected with COVID-19. Respondents reported an average of 8 patients in their practice testing positive for COVID-19, 4 requiring outpatient symptomatic management, 3 requiring inpatient admission, and 1 requiring intensive care. There was an average of 1 death from COVID-19 per respondent.

      4Discussion

      Provider and institutional response to the COVID-19 pandemic in regards to the care of patients with PH was notably varied. This survey is the first to evaluate both how PH providers perceive the care for patients with PH has been disrupted and how they perceive practice patterns have adapted to the challenges of this pandemic.
      Following national trends, PH providers perceived significant disruption to the care of patients with PH, primarily in obtaining diagnostic tests. The two most impacted tests were PFTs and V/Q scans, likely related to the risk of aerosolizing COVID-19. RHCs were still available to almost all respondents, although we did not ask about delays in obtaining RHCs specifically. The addition of pre-procedural COVID-19 testing to reduce transmission risk, recommended as best clinical practice during the pandemic, also unfortunately adds an extra step to the process for patients [
      • Qaiser K.N.
      • Lane J.E.
      • Tonelli A.R.
      ]. Usage of N95 masks was mixed, likely reflecting the at-times conflicting recommendations as to their necessity from national organizations. The decrease in referral rates is particularly concerning, as patients with PH already suffer from late referrals, which negatively affects prognosis [
      • Deaño R.C.
      • Glassner-Kolmin C.
      • Rubenfire M.
      • et al.
      Referral of patients with pulmonary hypertension diagnoses to tertiary pulmonary hypertension centers: the multicenter RePHerral study.
      ,
      • Badagliacca R.
      • Pezzuto B.
      • Poscia R.
      • et al.
      Prognostic factors in severe pulmonary hypertension patients who need parenteral prostanoid therapy: the impact of late referral.
      ].
      Of note, most respondents did not experience disruptions related to medication renewal or approval. Similarly, while there have been disruptions in the available healthcare workforce, only a portion of respondents reported a decrease in their clinic availability. This implies that disruptions to care were largely based around diagnostic testing and is reflected in the pandemic's effects on research activities, where 51% of respondents reported an inability to obtain tests required by research protocols. Ultimately, this highlights a need for the development of improved remote monitoring of patients with PH. Telemedicine has already and will likely continue to play a large role in filling this need.
      As expected, there was a dramatic increase in rates of telemedicine use from 15% to 84%, although rates of usage and how telemedicine visits were utilized varied significantly. Most interestingly, a number of respondents were comfortable initiating PAH therapies via telemedicine. Variation in willingness to do so likely has a multifactorial basis, including availability of access to other kinds of healthcare services, such as laboratory or echocardiographic testing, and the provider-patient relationship. The variation highlights the question of what parameters are necessary for the initiation of PAH therapies. CHEST guidelines for PAH therapy are based primarily on WHO functional classes, with clinical goals primarily being improvement of functional class or 6MWD [
      • Klinger J.R.
      • Elliott C.G.
      • Levine D.J.
      • et al.
      Therapy for pulmonary arterial hypertension in adults: update of the CHEST guideline and expert panel report.
      ]. European Respiratory Society guidelines are based on risk categories, which can be calculated using a variety of risk assessment tools, with WHO functional class generally being a consideration [
      • Galiè N.
      • Channick R.N.
      • Frantz R.P.
      • et al.
      Risk stratification and medical therapy of pulmonary arterial hypertension.
      ,
      • Humbert M.
      • Kovacs G.
      • Hoeper M.M.
      • et al.
      ESC/ERS Guidelines for the diagnosis and treatment of pulmonary hypertension: developed by the task force for the diagnosis and treatment of pulmonary hypertension of the European Society of Cardiology (ESC) and the European Respiratory Society (ERS).
      ].
      The simplest risk assessment tool was developed from the French Pulmonary Hypertension Registry (FPHR) with only 4 variables, utilizing WHO functional class, 6MWD, right atrial pressure (RAP), and cardiac index [
      • Boucly A.
      • Weatherald J.
      • Savale L.
      • et al.
      Risk assessment, prognosis and guideline implementation in pulmonary arterial hypertension.
      ]. Within the same study, Boucly et al. demonstrate that RAP and cardiac index could be replaced with B-type natriuretic peptide (BNP) or N-terminal prohormone BNP (NT-proBNP) measurements, creating a 3-variable version with only WHO functional class, 6MWD, and BNP/NT-proBNP. Likewise, REVEAL Lite 2 truncates the 13-variable REVEAL 2.0 into just 6 variables: WHO functional class, systolic blood pressure, heart rate, 6MWD, BNP/NT-proBNP, and renal insufficiency [
      • Benza R.L.
      • Kanwar M.K.
      • Raina A.
      • et al.
      Development and validation of an abridged version of the REVEAL 2.0 risk score calculator, REVEAL lite 2, for use in patients with pulmonary arterial hypertension.
      ]. This is important as per our survey, serum bloodwork was the least impacted of all the different types of testing used to monitor and evaluate patients with PH. Risk assessment tools that rely on more easily obtainable measurements will likely be preferable in the foreseeable future.
      In Italy, a scoring system for heart failure patients was implemented in a small cohort as they transitioned to telemedicine, relying on home measurements of vital signs and patient reports of medication adherence and symptomatology for the titration of medical therapy [
      • Orso F.
      • Migliorini M.
      • Herbst A.
      • et al.
      Protocol for telehealth evaluation and follow-up of patients with chronic heart failure during the COVID-19 pandemic.
      ]. Although most PAH therapies have more potent hemodynamic effects as compared to the components of goal-directed medical therapy for heart failure, development of a structured telemedicine system may be a way to increase provider comfort and willingness to initiate at least oral PAH therapy, thereby improving patient access to care. Caution should be used when relying on physician gestalt, as a prior study by Sahay et al. has showcased its unreliability [
      • Sahay S.
      • Tonelli A.R.
      • Selej M.
      • et al.
      Risk assessment in patients with functional class II pulmonary arterial hypertension: comparison of physician gestalt with ESC/ERS and the REVEAL 2.0 risk score.
      ]. Instead, multiple patient-reported outcome (PRO) questionnaires have already been developed for use in PAH patients, including CAMPHOR, PAH-SYMPACT, and emphasis-10, although they are not currently utilized in PAH guidelines [
      • McKenna S.P.
      • Doughty N.
      • Meads D.M.
      • et al.
      The Cambridge Pulmonary Hypertension Outcome Review (CAMPHOR): a measure of health-related quality of life and quality of life for patients with pulmonary hypertension.
      ,
      • Yorke J.
      • Corris P.
      • Gaine S.
      • et al.
      EmPHasis-10: development of a health-related quality of life measure in pulmonary hypertension.
      ,
      • McCollister D.
      • Shaffer S.
      • Badesch D.B.
      • et al.
      Development of the Pulmonary Arterial Hypertension-Symptoms and Impact (PAH-SYMPACT®) questionnaire: a new patient-reported outcome instrument for PAH.
      ]. Implantable devices like CardioMEMS will also likely have significant effects on remote management of PAH, but it is unclear how widespread their implementation would be or if they will be utilized in lower-risk patients [
      • Benza R.L.
      • Doyle M.
      • Lasorda D.
      • et al.
      Monitoring pulmonary arterial hypertension using an implantable hemodynamic sensor.
      ]. The utility of other biometric wearable devices has yet to be ascertained. In the meantime, encouraging use of home blood pressure cuffs or pulse oximeters, PRO questionnaires, and risk assessment tools that rely on easily obtainable variables may improve management of many patients with PAH via telemedicine.
      This study has several limitations. This is anonymous survey and thus likely has selection bias. Although several providers from non-US countries responded, the vast majority of respondents were based in the US. The practice patterns shown here are thus largely representative of US providers. Although there were a total of 95 respondents, not all respondents answered every question, decreasing the utility of certain questions. We asked questions about referral volume and infection rates, but it is unclear if respondents answered based off known numbers or gestalt estimates.
      It will be some time before the full effects of the COVID-19 pandemic can be reviewed. In the meantime, our survey has highlighted some key areas in which COVID-19 has already impacted the care of patients with PH, as well as areas of needed improvement. Disruptions in care were primarily related to obtaining diagnostic testing, with aerosolizing and invasive testing being the most heavily impacted. Overall, this showcases the need to improve remote monitoring and clinical assessment of patients with PH with validated metrics that rely on easily obtainable data. Adapting to the challenges that COVID-19 has presented will ultimately simplify the care of patients with PH by necessity, thereby increasing accessibility and hopefully improving patient outcomes.

      Author participation

      Conception and design of this study and creation, revision, and final approval of this manuscript: All authors.
      Analysis and interpretation: C.Z., S.S., J.E.
      Data acquisition: S.S., J.E.
      Drafting the manuscript for important intellectual content: All authors.

      Declaration of competing interest

      None of the authors have conflicts of interest to disclose on the topic of this pulmonary hypertension survey.

      Appendix A. Supplementary data

      The following is the Supplementary data to this article:

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