Auteurs:
Angela M. Stover, Debbie Liang, Dana Mueller, Rachel Kurtzman, Christiana Ikemeh, Courtney Canter, Sonali Acharya, Jill Brese, Kaitlyn Buhlinger, Kevin Chen, Evan W. Colmenares, Aimee Faso, Benyam Muluneh, Bianka Patel, Jeffrey S. Reichard, Rushabh M. Shah, Michael Tilkens, John Valgus, Lorinda A. Coombs, Jennifer Elston Lafata, Jennifer L. Lund, Emily M. Ray, Gita Mody, Mary-Haston Vest
Portions of this work were presented at the Cancer and Aging Research Group (CARG) annual conference in February 2023, the International Society for Quality of Life research (ISOQOL) in October 2023, and the Hematology/Oncology Pharmacy Association (HOPA) conference in April 2024. The views and opinions expressed in this article are those of the authors and do not reflect the views of sponsors.
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Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Plain English Summary
Why is this study needed?
Health systems typically monitor side effects of chemotherapy taken by mouth via nurses and physicians. However, pharmacists who provide direct patient care also have the skills and medical training to monitor side effects, and need symptom questionnaires that are relevant to the essential care they provide.
What is the key problem/issue/question this manuscript addresses?
Implementing side effect monitoring in clinics is challenging due to barriers at the patient, physician, and system-levels. The main challenges are that side effect monitoring needs to be part of usual workflow for pharmacists and not burdensome, and some patients do not have access to (or comfort with) the internet.
What is the main point of your study?
By engaging pharmacists and patients, we were able to design a side effect monitoring system in the electronic health record that addressed known barriers and meets their needs.
What are your main results and what do they mean?
Pharmacists and patients were consistent in prioritizing side effects to ask all patients (nausea, diarrhea, constipation, appetite, pain, mouth/throat sores, fatigue, neuropathy, dyspnea, rash). Patients advocated asking whether they can do their usual activities, while pharmacists added medication adherence and focused on the need for form simplicity.
Introduction
Patient reported outcome measures (PROMs) are a proven way to enhance side effect detection during cancer treatment [1‐3], but multi-level barriers make effective implementation challenging [4‐8]. Increasingly, PROMs are used in oncology care by nurses and physicians [9‐11], but additional care team members have been overlooked. Pharmacists who provide direct patient care are well positioned to lead clinic-based PROM initiatives because they complete a rigorous 4 year pharmacy school training, with options to pursue specialized residencies, fellowships, board certification, and prescribing privileges [12, 13]. Most academic health centers have integrated clinic-based pharmacists on oncology teams who collaboratively manage patients receiving oral oncolytics (chemotherapy medication taken by mouth) that must be dispensed through accredited specialty pharmacies [13]. This presents opportunities for pharmacist-led PROM implementation.
The IRB at the University of North Carolina at Chapel Hill approved the study. Patients gave verbal informed consent for telephone interviews (IRB# 22-0745) and the remainder of activities were exempt from oversight (IRB# 22-1466).
Study setting
UNC Health and its affiliates are the largest public healthcare system in North Carolina. UNC Health's pharmacist-led oral oncolytic management program has been established since 2014 as an integrated, closed-loop care model for managing oncology patients across the medication use process, including prescribing, verifying, dispensing, administering, and patient monitoring [26]. At UNC's main campus, the program includes 19 board-certified clinical and specialty pharmacists treating a variety of cancer types. Specialty pharmacy services include prior authorization and copayment assistance support, clinical assessments and monitoring, free home delivery of medications, and 24/7 on-call support for clinical concerns or questions. Clinic-based pharmacists on oncology teams provide direct patient care and oversee the prescribing and monitoring of oral oncolytics.
Patients and pharmacists from three oncology clinics (breast, thoracic, and hematological cancers) were eligible for study participation. In the thoracic clinic, patients with sarcoma were also eligible. Adults prescribed oral oncolytics have a high symptom burden with > 60% experiencing moderate to severe side effects [28, 29]. They also risk disease progression and mortality if medication adherence is poor [30‐32].
For patients, inclusion criteria were adults (aged 18 +) receiving oral oncolytics at a participating clinic who had at least one in-person or telephone encounter with a clinical or specialty pharmacist in the past 12 months. We excluded patients who could not participate in an English language interview and those not receiving pharmacist care for their cancer between October 2021 and September 2022. Eligible patients were identified by querying an EHR data warehouse. Purposive sampling was used to achieve a minimum of 50% of patients aged ≥ 65 and 20% of Black patients for each clinic to reflect the catchment area demographics. Thoracic and hematology patients included a minimum of 50% women (the breast clinic had mostly women).
The study coordinator contacted patients via telephone to determine interest and obtain verbal agreement to participate. Three trained interviewers conducted telephone interviews using a semi-structured interview guide. Interviews lasted a mean of 22.5 min (range of 9 to 42 min), and participants were given a $40 gift card. Interviews were audio-recorded and transcribed prior to analyses. Interviews with patients occurred before the Delphi panel with pharmacists.
For the Delphi panel, a total of 19 pharmacists who provide direct patient oncology care were eligible and sent email invitations to participate via the pharmacy leadership team. The exclusion criterion was not providing care in a participating clinic between October 2021 and September 2022.
KTA knowledge creation steps
Figure 1 shows our conceptual model with our research methods mapped to the KTA knowledge creation steps [24]. Future work will address the action cycle.
Fig. 1
Knowledge to action framework mapped to our methods. Based on Graham and colleagues’ knowledge to action framework [24].
The sample size was determined by a systematic review suggesting saturation of interview themes occurs at 9–12 interviews when the objective is narrowly defined and groups are relatively homogenous [33]. Patients may have differing side effect profiles based on their cancer type and oral oncolytic family, and thus we chose 12 patients per clinic to start. If necessary, we had planned additional interviews if thematic saturation was not reached when reviewed at 12 interviews.
Key side effects to prioritize were then compared across pharmacists and patients. Side effects were selected if pharmacists and at least two patient groups (by clinic) endorsed the side effect as important. An exception is medication adherence because patient interviews were conducted before the Delphi panel, and thus patients could not be asked about it directly.
Selecting PROM items
The research team matched the side effects selected to individual items on PROMs with desired characteristics (developed with patient and clinician input, calibrated with modern psychometric methods, and validity and reliability evidence in multiple cancer types) [40‐42].
Pharmacists’ recommendations were summarized, and potential changes were reviewed with the health system’s pharmacy leadership and EHR analysts. Subsequent rounds were planned if major revisions were requested.
Results
Phase 1: Knowledge Inquiry
Interviews with patients
We interviewed 36 adults receiving oral oncolytics (12 breast, 12 thoracic, 12 hematology oncology). Demographic characteristics are in Table 1. Our target percentages were met or exceeded. Patients with thoracic and hematologic malignancies were 50% women, and patients with breast cancer were 83% women. Across the 3 clinics, patients identifying as Black ranged from 25% (thoracic) to 42% (hematology), and those aged 65 + ranged from 50% (hematology) to 75% (thoracic). At 12 interviews in each clinic, thematic saturation was reviewed and met.
Table 1
Patient demographic characteristics for interviews (Phase 1)
Characteristic
Breast (n=12)
n (%)
Thoracic (n=12)
n (%)
Hematology (n=12)
n (%)
Women
10 (83)
6 (50)
6 (50)
Men
2 (17)
6 (50)
6 (50)
Non-Hispanic White
4 (33)
8 (75)
6 (50)
Non-Hispanic Black
4 (33)
3 (25)
5 (42)
Non-Hispanic other race
4 (33)
1 (8)
1 (8)
Age 65 and older
7 (58)
8 (75)
6 (50)
Completed interview by video call
5 (42)
7 (58)
2 (17)
Completed interview by phone
7 (58)
5 (42)
10 (83)
Table 2 shows the themes and supporting quotes from the patient interviews. Almost all patients reported that they wanted their pharmacist to ask them about side effects on a regular basis instead of the burden falling to them to mention a side effect. One patient said, “I would like for them to ask that. What's wrong? What side effects are you having pertaining to your medicine and stuff? If they didn't ask, you would never know. I think they should ask.” Another said, “Unless I report a side effect, nobody asks me about it.” Patients also emphasized that an important marker of health for them is whether they can continue to do their usual activities, such as working or taking care of children, and thus they recommended asking all patients about it.
Mouth sores: “I would say.. the mouth sores… I think they should ask other people if they’re having the same”
Flushing, appetite, bloating, fatigue: “Then the comfortability of the flushing and sweating, and then the appetite and bloating and feeling tired because those are all the things I’ve been feeling”
Dyspnea: “If I were a patient and didn’t know what I know, I would want somebody to tell me, “If you have trouble breathing, you need to seek help”
Diarrhea: “I would say hot flashes and loose stool diarrhea”
Nausea, vomiting, diarrhea, losing weight: “I’m continuing to have nausea and diarrhea. I’ve lost 30 pounds, so I can’t make myself take this stuff [medication]. I got so neurotic about it. When it came time to take it, I would throw it up. This is really neurotic… What we decided to do was I’d take two days off a week, and I did that for a while”
Mucositis: “Yeah. The mucositis is number one. Boy, it’s a bad actor. [Laughter] I would want to know that that was a potential side effect”
Neuropathy: "Okay, …is this severe, or making sure—especially with the neuropathy in your hands and feet, that's very important … because you don't want to get to the point that if you don't sit here and tell 'em in time that it get to the point where it'll be just untreated. Because the neuropathy is very serious, and you don't want it to sit here and actually get to the point where it can't be treated. That's real big; the neuropathy”
Nausea, indigestion: “I guess, you might say, like nausea, aches, or whatever, indigestion…”
Fatigue: “I would want them to ask people what the fatigue and maybe being uncomfortable like your joint pains. I wish they would ask more detail about that… like I said, I'm retired, so there's not like a scale from 1 to 10 if my joints are hurting or if it's 1 to 10 if my fatigue is there. Maybe if there was more of a sliding scale type of thing where people can respond in that way. Maybe they can get a better, I don't know, a better thought on how this is affecting people, I guess”
Nausea, bowel movements, sleep: “Well, if they have nausea, if they have with the bowel movements, if there’s any change. If they have nausea, if they have stomach pains, if they have—how are they sleeping”
Weight gain: “Weight gain”
Diarrhea: “The diarrhea. That fluttering in the stomach”
Diarrhea, rash, loss of appetite: “Well, the three main ones I was concerned about was diarrhea, rash, and loss of appetite…”
Prioritize mental health symptoms
“Ask patients about their initial mental state. I also had headaches, confusion and forgetting things and wasn’t sure if it was because of my medication or my cancer”
“I think that the mental health aspect is probably an important thing just to check in on”
“Cause I tell you, it affected my mental state. My ability to do anything was no. It wasn't gonna happen 'cause in my head I was on a ledge. I was on a ledge one time and I almost didn't get off. You know, come down. It was really, really hard for me”
“Hey, I’m feeling kind of down because of this drug side effect or because now I know I have cancer”
“Oh, my advantages, he encouraged me just keep doing what I'm doing. I like the things they say. They keep my morale up, keep me from going to depression. I don't want to fall back into that mode”
Prioritize whether patients can do their usual activities
“Then, the joint pain, it’s definitely affecting [my activities] me going up and down the stairs in my house. It’s not to the point where I can say, “Oh, I need crutches” or “Oh, I need a cane.” It’s tolerable for the moment. It’s just uncomfortable”
“The doctor was concerned because it [diarrhea] was something that like changin' my lifestyle. Whether I had to take something else to fight it”
“Yeah, they should discuss if they’re havin’, like you just said, which side effect interferes with their daily routine the most and what they wanna—if there’s anything they can do with it”
“My stomach issues do interfere with some of my activities. I sometimes I have a sense of urgency to go to the bathroom, and then sometimes it happens repeatedly and then that’s when I'll take some medicine to stop it”
“For speaking specifically of [drug name], the fatigue was enough that doing some of the simple physical activities of just working in the yard or some of those types of things—it’s been significant enough that—before, I could go out there and work for hours. Now it would be you work for 5 or 10 min; you gotta sit down and rest. A lot more frequency of resting time and just gettin’ worn out a lot quicker. That’s changed things. It’s such that maybe things that we would’ve done before—more physical like a—I don’t know—don’t go to a concert or something”
“How their daily routine has changed”
“I wasn't able to work any during my [oral] chemo. It was just too much going on. I had to get my body back, to be in my strength and everything”
“I initially started out with the full dose, then six, and immediately had terrible nausea and vomiting, awful fatigue, and amazing diarrhea, and thought, if this is my life, it's not worth fighting for. [Laughter] under normal circumstances, I vomit about once every ten years. It's just not somethin' that I'm used to. When I was troubled with that [nausea and vomiting], it was really disruptive. I could compensate for the diarrhea. I could wear the adult diapers and never be more than ten paces from a toilet. I got one of those waterproof things for under my seat, so I didn't have to wash the whole mattress pad and all that. I could compensate for that, but the nausea's just put me down”
“Diarrhea, I was taking the medicine in the morning time, but I was trying to teach school, and it was causing diarrhea. I didn't ever know when it was going to hit, so I started taking the medicine at night and that worked out better, 'cause if it reacted on me then, then it'd be through the night, and I wouldn't have to worry about trying to get out of class and all that”
“Like I said, this has been a tough year because the weight loss is what caused the problems. Slowly but surely, I stopped driving a car because I didn’t trust myself. I’m allowed to, but I just felt that I might hurt myself or other people on the road. I’m working on getting myself back upstairs to my own bedroom ‘cause I’ve been sleeping in the downstairs guestroom, and it’s not set up properly. It's one thing for a guest. It’s another thing to live in it. I’m working with physical therapy on that, to get up and down the stairs safely. I went through a period of time where I was falling a lot”
“Well, at this point in my life I really don’t have any responsibilities, and I don’t have many activities, but yes, it has. I don’t have the strength and the stamina to do a lot”
“It is hard. That’s the one a the hardest things that I really struggle with is the fatigue. Some days, I don’t even leave the house’cause I’m just tired”
Recommendations for how to ask patients how they are feeling and functioning
"How are you coming along with your new meds? What can I do to better assist you?"
“It's just having them ask you general questions. Are you having any difficulties with anything or problems with anything. I think having a pharmacist there, that can say, "Oh, this is something that's common or something that this medication can cause. Why don't you try or do this or let me research this and get back to you." I think that's what's important”
“That right there, I would like for them to ask that. What's wrong? What side-effects are you having pertaining to your medicine and stuff? You know what I mean? If they didn't ask, you would never know. I think they should ask”
“She…this is what she—this is our whole meeting—went down every one the graph with me, every lab with me, and told me what they look at. She was really, really nice. Very detailed. This is what I needed to know from my pharmacist..”
“Unless I report a side-effect, nobody asks me about it”
“Now, I did see some things that were errors that I was gonna let her know. I was reading over her report, and it said that I said that I didn't—that she [patient] denies missing any doses. I never told anybody that. That's a lie. I mean, that's a—she misheard me. I have missed doses. Remember, I—and the doctor—every doctor knows this, that I don't take my medicine correctly. I don't want that on here because that's not fair and that's not right”
Advantages of meeting with a pharmacist
“I guess the only thing I would say is it’s very helpful when you start a new medication to have somebody go over with you what’s a possible side effect could be”
“I guess warning people what to look out for, and I know that’s largely the oncologist’s job. That’s always been really helpful to me to have somebody [pharmacist] tell me before I start taking it what things I should be concerned about”
“I really don't know 'cause the advantage is that she helped me take the medicine and tell you how to take it and make sure you're taking it the right way, eating the proper food and stuff. I didn't see no disadvantage”
“Well, after having talked to the oncologist and telling him some things I was feeling, and then she [pharmacist] called me, that's the advantage. I think she seems to have a little bit—this is just me speculating—she seems to have more insight into what might really be a side effect. Yeah, you might have a headache, but could it be related to sinuses? Is it constant? Does it feel like this, or does it feel like that? You might be forgetful about somethings, but we all are. Are you losing your balance? Things like that, she just seems to have a little bit more, I don't know, experience or information or whatever with what might be going on”
“That they may be able to pass that information on to the oncologist, and if required to make some changes in dosage or, I don’t know, whatever is needed”
“I think it's very important in the beginning [to talk with a pharmacist. For many of us who have had cancer previous to this, we have expectations when we go in. Those expectations include knowing that things are gonna crop up that we don't expect or don't think, oh, well, that's not gonna bother me very much, and it does. It can be scary for some people. I'm a lucky person”
“My pharmacist explains things clearer when—'cause she asks me questions that my doctor doesn't sometimes, and she also, when I talk to her, if I tell her something, my pharmacist always goes back and talks with my doctor. With other pharmacy and she's told me about some of my symptoms, and then she comes back with answers for me. I feel very comfortable talking with [name]”
“I feel like he's [pharmacist]—can make those decisions without having to go back and forth with Dr. [oncologist name] and anybody else. I kind of like that part of it. I guess a negative aspect is there are sometimes where we’ve had conversations or decisions where I’m kind of questioning goin’ “Hmm. Is this the same thing [oncologist name] would say? Are you guys on the same page?” That kind of thing. I definitely see good parts and bad parts”
“I think that’s a good advantage. Because especially for me since I’m not too close to UNC, to get a phone call and be able to discuss the side effects and what I could be doin’ for them, it’s very helpful”
Delphi panel
Nineteen invitations were sent for each round and n = 11/19 (58%), n = 13/19 (68%), and n = 19/19 (100%) pharmacists participated, respectively, in rounds 1, 2, and 3. In round 1, most (11/16) of the original side effect domains were endorsed by at least 75% of pharmacists (Online Appendix A). The domains with 25–74% endorsement were sexual health (45%), breast tenderness or swelling (45%), genitourinary (64%), visual/perceptual (64%), and attention/memory (73%). No domains had fewer than 25% endorsement, and thus none were excluded in this round. Pharmacists requested adding items assessing medication adherence to future rounds.
In round 2, 53 specific side effects, 1 item on usual activities, and medication adherence items were listed. Of the 53 side effects, 34/53 (64%) were endorsed by at least 75% of pharmacists (Online Appendix B). Decreased sweating, hiccups, and stretch marks had fewer than 25% endorsement and were excluded. The new items on ability to do usual activities and medication adherence were endorsed at 100% and retained.
Table 3 shows that patients and pharmacists agreed on most side effects to prioritize, including gastrointestinal (nausea, diarrhea, constipation, appetite, mouth/throat sores), pain, fatigue, neuropathy, dyspnea, rash, anxiety, and depression. The domains for usual activities and medication adherence were also retained.
Table 3
Combined results for delphi and patient interviews
*Reasons for exclusion: Side effects may be unrelated to oral oncolytics, not required for state payer reporting, and pharmacists reported they did not have training in independent management of these medications
**Patients were not asked directly about medication adherence during interviews
Selecting PROM items
The research team matched the retained side effects, usual activities, and medication adherence to individual items on PROMs. PRO-CTCAE [44, 45] is an item bank of 124 items representing 78 symptomatic toxicities that met our PROM criteria of being developed with patient and clinician input, calibrated with modern psychometric methods, and has validity and reliability evidence in cancer [40, 44, 45]. To meet patients’ recommendation about assessing whether they can do their usual activities, we added an item from the National Institutes of Health’s PROMIS (PRO Measurement Information System) global health scale [46]. We also added Wilson’s medication adherence items [47].
The second round of usability testing was done via a conference call with all participating pharmacists. The changes requested from the prior round were perceived by the pharmacists to be satisfactory and fit with their workflow. One more change was requested to add a radio button for “not applicable to drug” beside the severity options. This was judged by the pharmacists to be a minor change, and the usability testing concluded.
At the pharmacist level, we addressed the barrier of a PROM increasing workload [22, 23] in several ways. We added a verbal PROM to calls already being made by specialty pharmacists for education and medication refill outreach. Clinical pharmacy practitioners with prescribing privileges then managed severe side effects reported by patients, which matched the previous workflow if a patient spontaneously mentioned a side effect when the specialty pharmacist called them. Adding 12 side effects, activity, and medication adherence questions was perceived by specialty pharmacists to fit with their typical telehealth workflow reasonably. To address the time-consuming process of documenting patient information, a clinical note-writing shortcut was created that captured patient responses within an aesthetic table customizable to each pharmacist's progress note template and was perceived to be efficient.
Second, interviews with patients occurred before the Delphi panel, and thus, we could not add medication adherence to the patient interviews. However, some patients did mention it spontaneously as a question their pharmacist typically asks them.
Despite these limitations, the strengths of this study included attention to equity, key partner engagement, and diverse patient participants (including those who do not have access/comfort with the internet), which may improve program acceptability and sustainability. Calvert and colleagues [50] provide recommendations for ensuring PROM systems are equitable and inclusive so more groups benefit from healthcare innovations. For example, some recommendations are to allow for resource allocation for different individuals to reach the same outcomes and to address when health data are not representative of the diversity in a patient population [50]. Their paper is available as part of an excellent compilation of PROM implementation best practices called “Patient-Reported Outcomes Tools: Engaging Users and Stakeholders” (PROTEUS-Practice) [8].
Conclusion
With iterative input from pharmacists and diverse patients, we developed a PROM monitoring system in the EHR that supports specialty pharmacists, during routine patient outreach calls, verbally collecting and monitoring a key set of symptoms that are important to both patients and pharmacists. By using an implementation science framework and presenting screenshots of our work, our findings are useful to other healthcare systems and researchers looking for a PROM solution for usual care integrated in the EHR, with a reasonable pharmacist/clinician workload, and no requirement for patients to have internet access/comfort.
AMS: unrelated funding in the past two years from Sivan Innovation, UroGen Pharma Ltd., and the American Society of Clinical Oncology (all awarded to institution). Dr. Stover received a honorarium for serving on the steering committee for PROTEUS. LAC: serves on the Board of Directors for APSHO. GM: Unrelated research funding from Sivan Innovation. KC: Unrelated consulting fees or speaking honoraria in the last 24 months from: Pfizer, Blueprint Medicines, G1 Therapeutics. JLL: In the last 24 months, Dr. Lund’s spouse was employed by GSK and owned stock in the company. Dr. Lund is also a member of one of the sponsors funding this work, the Cancer and Aging Research Group (CARG). MHV and DL: unrelated Pfizer funding. EMR: unrelated research funding from Pfizer, OptumHealth, and the American Society of Clinical Oncology (awarded to institution). RS: consultant for the American Society of Health-System Pharmacists on an unrelated project. JEL: unrelated funding from Genentech (awarded to institution). DM, RK, CI, CC, SA, JB, KB, EWC, AF, BM, BP, JSR: none.ma Ltd., and the American Society of Clinical Oncology (all awarded to institution). Dr. Stover received a honorarium for serving on the steering committee for PROTEUS. LAC: serves on the Board of Directors for APSHO. GM: Unrelated research funding from Sivan Innovation. KC: Unrelated consulting fees or speaking honoraria in the last 24 months from: Pfizer, Blueprint Medicines, G1 Therapeutics. JLL: In the last 24 months, Dr. Lund’s spouse was employed by GSK and owned stock in the company. Dr. Lund is also a member of one of the sponsors funding this work, the Cancer and Aging Research Group (CARG). MHV and DL: unrelated Pfizer funding. EMR: unrelated research funding from Pfizer, OptumHealth, and the American Society of Clinical Oncology (awarded to institution). RS: consultant for the American Society of Health-System Pharmacists on an unrelated project. JEL: unrelated funding from Genentech (awarded to institution). DM, RK, CI, CC, SA, JB, KB, EWC, AF, BM, BP, JSR: none.
Consent to Participate
Patients gave verbal informed consent for telephone interviews (IRB# 22-0745) and the remainder of activities were exempt from oversight (IRB# 22-1466).
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Angela M. Stover Debbie Liang Dana Mueller Rachel Kurtzman Christiana Ikemeh Courtney Canter Sonali Acharya Jill Brese Kaitlyn Buhlinger Kevin Chen Evan W. Colmenares Aimee Faso Benyam Muluneh Bianka Patel Jeffrey S. Reichard Rushabh M. Shah Michael Tilkens John Valgus Lorinda A. Coombs Jennifer Elston Lafata Jennifer L. Lund Emily M. Ray Gita Mody Mary-Haston Vest
