key: cord-1041350-ddvpc3z6
authors: Graney, Bridget A.; He, Christophe; Marll, Michael; Matson, Scott; Bianchi, Pauline; Cosgrove, Gregory P.; Lee, Joyce S.; Abrencillo, Rodeo; Bascom, Rebecca; Scholand, Mary Beth; Bhatt, Nitin; Case, Amy; Chaudhary, Sachin; Culver, Daniel; Danoff, Sonye; Desai, Alpa; Dilling, Daniel; Glazer, Craig; Gulati, Mridu; Gupta, Nishant; Hamblin, Mark; Hamzeh, Nabeel; Huie, Tristan; Kim, Hyun; King, Christopher; Kreider, Maryl; Lacamera, Peter; Lancaster, Lisa; Luckhardt, Tracy; Mageto, Yolanda; Kottman, Robert Matthew; McCormick, James; Mehrad, Borna; Menon, Prema; Montesi, Sydney; Mooney, Joshua; Moore, Doug; Moua, Teng; Nambiar, Anoop; Oldham, Justin; Patel, Divya; Paul, Tessy; Perez, Rafael; Podolanczuk, Anna; Ramaswamy, Murali; Roe, David; Saad, Mohamed; Sandbo, Nathan; Schaumberg, Thomas; Schmidt, Shelley; Shea, Barry; Shifren, Adrian; Strek, Mary; Thavarajah, Krishna; Todd, Nevins; Veeraraghavan, Srihari; Weight, Stephen; Wolters, Paul; Zibrak, Joseph
title: Essential Components of an Interstitial Lung Disease Clinic: Results from a Delphi Survey and Patient Focus Group Analysis
date: 2020-10-05
journal: Chest
DOI: 10.1016/j.chest.2020.09.256
sha: 93e1a24b9e133aa550e096dca3e699f272c37e96
doc_id: 1041350
cord_uid: ddvpc3z6

Background Management of patients with interstitial lung disease (ILD) requires subspecialized, comprehensive, multidisciplinary care. The Pulmonary Fibrosis Foundation established the Care Center Network (CCN) in 2013 with identified criteria to become a designated CCN site. Despite these criteria, the essential components of an ILD clinic remain unknown. Research Questions How are ILD clinics within the CCN structured? What are the essential components of an ILD clinic according to ILD physician experts, patients, and caregivers? Study Design and Methods This study had 3 components. First, all 68 CCN sites were surveyed to determine the characteristics of their current ILD clinics. Second, an online, three-round modified Delphi survey was conducted between October and December 2019 with 48 ILD experts participating in total. Items for round one were generated using expert interviews. During rounds 1 and 2, experts rated the importance of each item on a 5-point Likert scale. The a priori threshold for consensus was greater than 75% of experts rating an item as important or very important. In round 3, experts graded items that met consensus and ranked items deemed essential for an ILD clinic. Third, ILD patient and caregiver focus groups were conducted and analyzed for content to determine their perspectives of an ideal ILD clinic. Results Forty items across four categories (members, infrastructure, resources and multidisciplinary conference) achieved consensus as essential to an ILD clinic. Patient and caregiver focus groups identified three major themes: comprehensive, patient-centered medical care; expanded access to care; and comprehensive support for living and coping with ILD. Interpretation The essential components of an ILD clinic are well-aligned between physician experts and patients. Future research can use these findings to evaluate the impact of these components on patient outcomes and inform best-practices for ILD clinics throughout the world.

Interstitial lung diseases (ILD) represent a rare and heterogeneous group of over 100 diseases. Among them, idiopathic pulmonary fibrosis (IPF) is the most common and carries significant morbidity and mortality, with a median survival of 41 months (1) . The scope of care for patients with ILD can be challenging and complex, ranging from obtaining accurate diagnoses, initiating disease-modifying treatments, providing supportive care including oxygen therapy, and managing comorbidities, to discussing lung transplantation and providing palliative and end-of-life care.

The multidimensional, complex, and longitudinal needs of this patient population has led to the emergence of specialized, comprehensive ILD clinics in the last two decades. The Pulmonary Fibrosis Foundation (PFF) is a nonprofit organization dedicated to providing support to those living with pulmonary fibrosis. In 2013, the PFF started the Care Center Network (CCN) which now consists of 68 designated medical centers across the United States recognized for having expertise in the diagnosis and treatment of ILD through multidisciplinary care and patient engagement in education, support, and research.

Although the PFF CCN delineates the criterion to qualify and maintain designated site status (2) , little is known about the composition, structure, and function of an "ideal" ILD clinic. Due to a lack of clinical practice guidelines to inform the structure of an ILD clinic, we identified three objectives for this study: first, to assess the current structure of ILD clinics within the PFF CCN; second, to determine the essential components of an ILD clinic using a three-round modified Delphi survey administered to a group of ILD experts, all of whom are Directors of PFF CCNs; and third, to identify the essential components of an ILD clinic from the perspectives of ILD patients and caregivers utilizing a series of focus groups. 

Survey A 60-item, web-based survey using REDCap was sent to all 68 PFF CCN Directors via e-mail to determine baseline characteristics and composition of their ILD clinics.

Items included in the first round of the modified Delphi survey were compiled based on content analysis of transcripts from individual, semi-structured telephone interviews with PFF CCN Directors (Text Supplement 1). Nine directors were selected based on their clinical expertise and background to ensure representation with respect to gender, geography, and size of ILD clinic. All interviews were conducted by C.H., digitally recorded and transcribed verbatim.

All PFF CCN Directors, including those that had participated in the telephone interviews, were invited via e-mail to participate in the modified Delphi survey.

We conducted a three-round Delphi survey utilizing a secure, online REDCap database between October and December 2019. In rounds one and two, the Delphi collaborators ranked items by degree of importance on a five-point Likert scale ("very important", "important", "less important", "not important", and "not sure"). In the third round, participants were instructed to rank items on a five-point Likert scale based on if items were thought to be essential to an ILD clinic ("strongly agree", "agree", "disagree", "strongly disagree", and "not sure").

Results were anonymously analyzed and reported according to the defined methodological criteria for Delphi studies (3). The a priori threshold for an item to be considered important to an ILD clinic in Delphi rounds 1 and 2 was defined as greater than 75% consensus among experts rating an item as "very important" or "important" and the a priori threshold for an item to be considered not important to an ILD clinic was defined as greater than 75% consensus among experts rating an item as "not important" or "less important". The same thresholds were used for the third Delphi round, but in relationship to level of agreement with an item being "essential" for an ILD clinic.

We conducted focus groups with patients with ILD and self-identified caregivers. We chose a qualitative study design using content analysis as our methodologic framework to gain a J o u r n a l P r e -p r o o f comprehensive understanding of the experiences, wants, and needs of patients and caregivers seeking medical care at ILD clinics.

Eligible participants had to currently reside in the United States. Participants were not excluded if they were not currently or had not previously received care at a PFF CCN site. Participants were recruited at the PFF 2019 Summit at an informational table and through a recruitment flyer distributed electronically to the PF Warrior community e-mail distribution list. Informed consent was obtained from all participants at the time of the focus group. Participants were not compensated for their time.

Real-time focus groups were conducted using a secure, web-based meeting interface and facilitated by authors (B.A.G., C.H., M.M.) from November 2019 through January 2020. The focus groups followed a semi-structured, open-ended approach to elicit participants' opinions and experiences of ILD clinics (Text Supplement 2). All focus groups were audio-recorded and transcribed verbatim. Three focus groups were initially planned but new themes emerged from the second and third groups. Therefore, two additional focus groups were conducted, after met regularly to discuss coded data, reconcile differences and achieve consensus. Both coders double coded all focus groups. Coded data were analyzed within and across groups to identify the emergent themes.

A total of 36 of 68 (53%) PFF CCN Directors completed the survey (Table 1 and e- Table 1 ). The median number of new patient visits per year was 250 (interquartile range [IQR] 150-383) and the median number of total patient visits per year was 1000 (IQR 500-1500). 67% of clinics were staffed with 2-5 physicians. Nearly all clinics (92%) had nursing support, with 56% of sites having dedicated ILD nurses. Available ancillary support staff varied across clinics. Every clinic participated in research and clinical trials. All clinics, except for one, had a multidisciplinary conference and held conferences at least once a month.

J o u r n a l P r e -p r o o f 8 of the 9 identified PFF CCN Directors participated in the telephone interviews. Eighty-seven total items were generated for inclusion in the first round of the modified Delphi survey. Items were divided into four categories: members of an ILD team, infrastructure for an ILD clinic, resources for an ILD clinic, and multidisciplinary conference.

Of the 67 PFF CCN Directors invited to participate (J.S.L. as PFF CCN Director at the University of Colorado was not invited to participate), the response rate for the three rounds of modified Delphi was 48 (72%) for the first round, 42 (63%) for the second round and 40 (60%) for the third round ( Figure 1 ). The number of items in each round is summarized in Figure 2 and detailed results of all three rounds can be found in the supplement (e-Tables 2-4). At completion of the third round, 40 unique items achieved consensus as essential for an ILD clinic (Table 2 ).

In the third round, if we change the threshold for essential to 70%, this would have added six items to the list of essential items for an ILD clinic including inclusion of more specific personnel (clinic and research coordinators, access to rheumatologists with expertise in ILD) and a minimum frequency of multidisciplinary conference (e- Table 4 ). In contrast, if the threshold were more stringent, only allowing for those with greater than 80% agreement, seven items would be excluded from the essential list including a minimum number of unique patients seen yearly, specific ancillary services at the same institution, and proximity of a pulmonary rehabilitation center ( Table 2 ).

A total of 21 individuals participated -16 patients and 5 family caregivers. We conducted five focus groups with a range of three to seven participants per group. Among the patient participants, 69% were male and 31% were female. Among the caregiver participants, 20%

were male and 80% were female. Additional demographics were not obtained to maintain participant confidentiality; some participants provided details of their diagnoses voluntarily. We identified three major themes from the focus groups that encompass patients' and caregivers' perspectives of an ideal ILD clinic: comprehensive patient-centered medical care; expanded access to care; and support for living and coping with ILD. See Table 3 for the three major themes, with subthemes and representative quotations.

In all five groups, patients and caregivers expressed the desire for comprehensive, patient-centered, and coordinated care center. One male patient with ILD who had undergone a lung transplant succinctly characterized this type of experience: "To have a facility that was totally all-inclusive would be ideal." Participants expressed the desire for a wide-ranging group of providers and services to be incorporated into an ILD clinic or at minimum, be readily available. These included: physicians and surgeons; various diagnostic capabilities (laboratory, imaging, pulmonary function testing); multidisciplinary teams for diagnosis; access to all available treatment modalities; pulmonary rehabilitation; psychosocial support (e.g. counselors, psychologists, social workers); and palliative care. One female participant with connective tissue disease-related ILD stated: The concept of integrated care was viewed as being particularly important at the time of diagnosis due to the physical toll of travel, numerous appointments and diagnostic testing in addition to the psychological impact of receiving the initial diagnosis of ILD.

Participants expressed that timely and efficient care was equally important, particularly coordination of follow-up specialist appointments on the same day. Assistance working with insurance companies to avoid delays in care and other necessary treatments (diagnostic testing approval, oxygen prescriptions, medications, particularly antifibrotics) was also frequently mentioned.

The ideal ILD clinic described by participants was one that ensured adequate and timely communication, was geographically accessible, and included opportunities to be involved in a range of treatments, specifically pulmonary rehabilitation and clinical trials.

Utilization of online patient portals if available was frequently suggested for ease and timeliness of communication, including results of diagnostic testing, and for questions that were perceived as not needing a physician to personally answer. One suggestion echoed in several groups was to establish a single point of contact within the clinic to improve Geographical constraints and accessibility of ILD centers was a concern for participants. Some stated that it was a "luxury" to be close to specialty centers and expressed concern for patients who could not easily access one. Accessibility and travel time were linked with the importance of coordinating appointments and ensuring comprehensive care due to the challenges of traveling numerous times.

Expanded access to care encompassed access to pulmonary rehabilitation and clinical trials participation. Pulmonary rehabilitation was viewed as a necessary but underutilized treatment option. This was attributed to difficulties with accessibility and travel logistics, and many patients (including some participants) being unaware of its benefits. Receiving care at a center that offered research and clinical trials opportunities was also valued by participants, giving them access to new therapeutics and to "help make discoveries" that would "make things better for other people" in the future.

The most consistently voiced topic across the five focus groups was the need for additional support for patients and families. Patients and caregivers felt that the ideal care experience had to specifically include increased disease-state education, availability and use of counseling and support services, patient support groups and assistance with obtaining, using and living with supplemental oxygen.

The most commonly expressed need within this theme, and the most frequent suggestion from participants as a way to address the broader support needs described above, was the concept of a "patient advocate." This phrase was independently used in three of the five focus groups, with the other two groups using terms such as "ambassador" and "personal coach" to describe a similar concept. Patient advocates were seen as necessary personnel within an ILD clinic to ensure patients' needs were met. The roles of patient advocates were broad. First and foremost, they were envisioned as providing patient support and information, particularly at the time of diagnosis. One participant expressed, "Having an advocate in the clinic who understands the dynamic of getting hit over the head in the appointment with all of the information that they've gotten, just have an advocate be in there to respond to all of the terminology and the questions that the doctor left you with because you didn't have enough time to ask…a translator."

Advocates were described as a bridge to the clinic, a point person with the necessary breadth and depth of disease-state knowledge to provide additional support and education at the time of diagnosis; provide resources such as support groups information and appropriate online references; and to be the primary point-of-contact for any patient or caregiver question or need. Advocates were described as a person who could coordinate appointments and "maneuver through…the system." Suggestions for who could perform these myriad roles included a dedicated ILD clinic nurse, respiratory therapists, social workers, case managers, or patient volunteers.

This study systematically identifies and describes the necessary components of an ILD clinic from the vantage point of two distinct groups of ILD experts -ILD specialist physicians and ILD patients and caregivers.

Through the Delphi process, we identified personnel, infrastructure, and resource needs, including specifics around multidisciplinary conference, that are essential to providing care for patients with ILD. Many of the essential items identified are consistent with the PFF CCN requirements to become a designated site (2) . Our findings support these criteria including personnel, availability and timeliness of new patient appointments, multidisciplinary diagnosis, access to support groups, clinical research opportunities, and specific CT-imaging capabilities.

Additional details that emerged which are not included in the PFF CCN criteria include the level of physician expertise and experience (PFF CCN criteria specify 3 years of post-fellowship experience in PF to be a Center Director but no guidelines for other physicians or providers), additional staff and their roles in the clinic, and the breadth of available ancillary procedures.

The focus groups allowed for patients and caregivers to describe a clinic environment that would best serve their needs. In many ways, the experience of and components of the "ideal ILD clinic" described in the focus groups mirrored the essential items identified through the Delphi process (Figure 3 ). Two areas emphasized in the focus groups that were not identified from the Delphi were improved access to communication and more explicit support services such as availability of psychologists or counselors, and direct education and support for supplemental oxygen. Findings from the focus groups are similar to what has been previously described as the "unmet needs" of ILD patients (6) (7) (8) (9) . Collectively, incorporating results from J o u r n a l P r e -p r o o f both the Delphi and the focus groups may help inform future efforts at establishing bestpractices at the CCN and other ILD specialty clinics.

While there is a great deal of literature to support the "gold standard" of a multidisciplinary approach to diagnosis (10), the resultant improved diagnostic accuracy (11) , and the impact on patient management (12), the results from this study may represent a firststep toward understanding essential components of care delivery to improve outcomes or careexperiences for patients with ILD. This could be modeled after the Cystic Fibrosis Foundation practice of implementing standardized care across centers and utilizing benchmarks to advance best-practices that have been shown to improve patient outcomes (13) .

There are limitations to this study. The Delphi items were developed through interviews with eight site-directors and may not represent the full breadth of items that other directors may have identified as important, though participants were allowed to add items in the first round. As only PFF CCN sites were invited to participate in the Delphi process, the results are inherently influenced by the existing CCN criteria (e.g., requirement for research opportunities, support group and multidisciplinary conference) and therefore may not be generalizable to other clinics that provide care to patients with ILD, including those outside of the United States.

Focus group participants were initially recruited in-person at the PFF 2019 Summit. This is a highly motivated, self-selected group of patients and caregivers that are aware of the PFF and are physically and financially able to travel. Subsequent recruitment was completed through the assistance of the PF Warriors Support Group, which reaches a broad international audience.

Including participants recruited in both manners may have mitigated some of the bias of patients already involved in the PFF.

Further, this data was collected prior to the current SARS-CoV-2 global pandemic. Given that patients with ILD are considered high-risk for severe disease, many ILD clinics have rapidly adopted telehealth services in order to provide ongoing care. In personal communication with the PFF CCN, telehealth access increased from 8% at the time of our original survey to approximately 98% during the month of June 2020. While many providers and patients are still adjusting to providing and receiving care in this format, this modality may be one method to meaningfully address and expand access to patients who are otherwise limited in their access to specialized centers. The shift to telehealth has also required many patients not previously utilizing portals to become familiar with them as a communication and care-delivery avenue, improving timeliness of communication. Leveraging virtual applications in other areas (e.g. education, support groups, pulmonary rehabilitation) may also help address some of the needs identified in this study.

Future work should focus on understanding the process and limitations for the widespread implementation of these essential items across clinics that care for ILD patients, like the PFF CCN. Financial, geographic, and other resource constraints including the number of experienced ILD physicians available may limit the implementation of these findings. Further, work should be done to demonstrate the impact of implementing these measures in the care and outcomes of patients with ILD, as this may help convince payors of the value of properly resourced ILD clinics. This would also allow us as an ILD community to better understand what components may influence long-term outcomes for patients. We should also strive to address the needs of our patients particularly in the form of coordinated care, communication, and patient advocates (e.g. ILD nurses) to provide support, education, and patient-centered care.

ILD patients require subspecialized, comprehensive, multi-disciplinary care. The essential components of an ILD clinic identified in our study are well-aligned between clinical experts and patients with an emphasis on personnel, infrastructure, resources, and a multidisciplinary approach to diagnosis. Future research assessing the impact of these essential components of an ILD clinic on patient outcomes across the PFF CCN would inform bestpractices for the broader ILD community. Patients in whom a surgical lung biopsy is being considered *Maximum time to new patient visit < 1 month or < 3 months for a standard new patient visit were important, but not essential † If threshold for agreement were increased to >80%, these items would have been considered important but not essential for an ILD clinic J o u r n a l P r e -p r o o f collaborators were asked to rank items in degree of importance for ILD clinics on a five-point

Likert scale during each of the three-rounds. During round one, participants were given the opportunity to add any additional items they found important for an ILD clinic that were not already included in the first-round items. In the second round, the amended list of items (including the items generated in round 1) and results of the first round which did not achieve consensus were presented. Participants were asked to rate this amended list on the same fivepoint Likert scale. In the final round, participants ranked consensus items on a five-point Likert scale on whether these items were not only important, but essential for an ILD clinic. 

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