Conceptualization and Implementation of an interdisciplinary clinic for children with drug-resistant epilepsy during the COVID-19 pandemic

Abstract

Objective

To describe the rapid conceptualization and implementation of an interdisciplinary epilepsy clinic for children with drug-resistant epilepsy (DRE) at Arkansas Children’s Hospital (ACH) during the COVID 19 pandemic.

Methods

Focusing on care design and care coordination for children with DRE, multiple stakeholder groups decided to implement a clinic after the systematic rating of constructs present in a theoretical meta-analytic framework. Based on the projected success, the new interdisciplinary clinic (composed of an epileptologist, a neurosurgeon, and a neuropsychologist and coordinated by a full-time nurse) was established. Clinic operations were further refined through discussions with patients, families, and care providers. We collected data retrospectively (August 2020 to June 2021) to determine referral patterns, clinic scheduling metrics, patient characteristics, clinical recommendations, and epilepsy quality metrics.

Results

Of the 32 Consolidated Framework for Implementation Research constructs assessed, 24 were positively rated to predict a high probability of successful implementation of the clinic. For approximately 100 patient visits, appearance and usage rates were >75%, yielding a clinic utilization rate of approximately 60%. Among 76 unique patients (average age of 12 years, 60% focal epilepsy), 39 patients (51.3%) were deemed eligible for epilepsy surgery evaluation. The majority of the patients (53.9%) were advised for additional diagnostic testing, and 31.6% of patients were scheduled for vagus nerve stimulation. More patients (33%) had changes in their existing anti-seizure medication (ASM) regimen rather than an addition of a new ASM (7.9%). Standardized epilepsy quality measures showed >80% to 90% adherence in 3 (reproductive counseling, depression and anxiety screening, documentation of seizure frequency) out of 4 metrics.

Significance

This is the first study to show that an interdisciplinary clinic can be a valuable attribute of care models in high-need children with DRE by enabling comprehensive one-stop service for diagnostic evaluation, surgical consideration, and brief assessment of psychiatric comorbidities without compromising consensus-based best practices.

Introduction

Epilepsy is the costliest and most common chronic neurological condition in children. [1] Although most children with epilepsy have self-limiting and easy-to-control seizures, approximately one third of patients develop drug-resistant epilepsy(DRE). [2] These children with DRE have a high risk of mortality, poor intellectual growth, and development of psychiatric comorbidities. [2]

The Institute of Medicine (US) Committee on the Public Health Dimensions of Epilepsies recommended improving access to a more advanced level of care for patients with DRE, emphasizing the coordination of epilepsy-specific services. [3] Integrated specialist services can significantly help many children with DRE by optimizing medical therapy, adopting dietary therapy, or using neuromodulation and epilepsy surgery. [4] Despite the accumulation of solid evidence of the use of epilepsy surgery and other nonmedical treatment approaches for DRE, these are underutilized due to the need for an expert interdisciplinary team dedicating to conduct all necessary evaluations [detailed history, physical examination, recording of ictal events with simultaneous electroencephalography( EEG) and video monitoring, neuropsychological evaluation, advanced anatomic and functional neuroimaging]. [5,6] This complex workup usually requires multiple outpatient and inpatient visits, all of which became significantly restricted during the novel coronavirus disease 2019 (COVID-19) pandemic. A global survey reported that >90% of pediatric neurology services had been affected by restricted outpatient care, decreased access to EEG, limited use of dietary therapy, restricted admission in epilepsy monitoring units, and canceled or limited epilepsy surgery. [7] Although most health care systems worldwide face unique challenges in providing basic epilepsy care with the increasing adoption of telehealth during this time, existing literature does not shed light on how to integrate highly specialized quality epilepsy care, especially when interdisciplinary evaluation and workup was not feasible in a virtual care environment. [8,9,10]

Arkansas Children’s Hospital (affiliated with the University of Arkansas for Medical Sciences [UAMS] and serves as a teaching hospital with the College of Medicine Department of Pediatrics) is the only pediatric healthcare system in Arkansas. Its comprehensive epilepsy program is the state’s only pediatric Level 4 program. As a Level 4 program, ACH is committed to offering complete evaluation and treatment options for epilepsy, including epilepsy surgery. However, providing coordinated and streamlined care for children with DRE has been difficult during the COVID-19 pandemic. These children require multiple clinic visits by various specialists, additional diagnostic tests, and inpatient admission for optimum treatment.

Although a multidisciplinary care model can allow mitigation of stress associated with attending multiple hospital or clinic visits by coordinating management across various disciplines, there is limited knowledge on how to systematically evaluate a local context to decide the appropriateness of clinical service and effectively assess clinic performance to optimize patient access and operational efficiency. There is also a paucity of data regarding various clinical recommendations provided during interdisciplinary complex epilepsy clinics and the quality of epilepsy care using standardized metrics. This paper describes how ACH designed and adapted an integrated complex epilepsy clinic based on a systematic meta-analytic framework analysis during the COVID pandemic and maintained operational efficiency without compromising the quality of epilepsy care.

Methods

Organizational planning and strategy

Since 2017, ACH has successfully used many organizational strategies to expand its epilepsy surgery service. The main challenges for the service expansion were identifying all children with DRE, streamlining workup for these patients, and improving care coordination among disciplines to provide high-quality patient-centered care. In 2020, a neurologist received an Implementation Science/Clinical and Translational Science Awards (CTSA) grant to evaluate the epilepsy treatment gap at the ACH. He met with neuroscience leaders to brainstorm solutions for improving epilepsy care and subsequently conducted several group meetings and one-to-one semi-structured interviews with 11 individual stakeholders, focusing on care design and care coordination for children with DRE. A meta-analytic theoretical framework, the Consolidated Framework for Implementation Research (CFIR), was applied for coding the transcribed interview data against 32 constructs of the 5 major domains: characteristics of the clinic (e.g., evidence, strength, quality, complexity), the outer setting (e.g., patient needs and resources), the inner setting (e.g., compatibility of the clinic with the existing epilepsy services, leadership engagement), characteristics of individuals(e.g., stakeholders’ attitudes toward the clinic establishment), and the process of implementing the program (e.g., quality and extent of planning, engagement of key stakeholders). [11] A systematic rating process was applied to determine the implementation success of the clinic.[12]

Based on the projected success, a new interdisciplinary clinic (named Complex Epilepsy Clinic or CEC) moderated by a full-time epilepsy nurse coordinator was proposed to evaluate children with DRE to address the unique needs of the population (Figure 1). Barriers and facilitators of the clinic were comprehensively evaluated (Table 1). Finally, the decision was made to move forward with the establishment of the CEC for various reasons: the need for an integrated team to optimally manage children with DRE, demand for efficient means of delivering patient care (‘one-stop approach’), improvement in care coordination and patient satisfaction, continuing education resources for referring physicians, enhancement in collaborative teaching, promotion of research-based disease-specific patient registry, and an upgrade in the expedited treatment approach using nonmedical therapy (including appropriate presurgical diagnostic evaluation via the Epilepsy Surgery pathway for selected patients).

Figure 1.

Operation of the interdisciplinary clinic (CEC). Neurologists and epileptologists refer children with drug-resistant epilepsy. Potential surgical candidates enter the epilepsy surgery pathway for presentation in the epilepsy surgery case conference, and the recommendations (consensus opinion of proceeding to intracranial monitoring, direct surgery, or other nonsurgical therapies) from the meeting are discussed with patients and families in the clinic. Nonsurgical patients are treated with optimization of medical treatment, completion of the diagnostic workup, and other options (dietary therapy and neuromodulation).

Table 1.

Key factors as Barriers and Facilitators

Factors	Barriers	Facilitators
The interdisciplinary clinic	Schedule clash among various specialists The relative efficacy of the interdisciplinary clinic for the management of epilepsy is unknown The cost-effectiveness of the intervention is unknown Time lag to understand the effectiveness of the clinic	Initial EEG data, seizure semiology, brain MRI can be discussed among key clinicians responsible for the particular patient to develop tailored recommendations about further testing to complement the evaluation. Faster evaluation of the patient in this weekly clinic without waiting for the epilepsy surgical conference, which occurs once every four weeks, and pediatric cases are discussed with adult cases Potentially allow fewer studies and resources due to the tailored approach to the diagnostic workup and thus may decrease healthcare expenses Joint discussion and decision making with patients and families More convenient knowledge sharing among various specialists More effortless longitudinal follow-up of these children with drug-resistant epilepsy
External influence over the organization	Reimbursement challenges for the multispecialty clinic	Several other comprehensive epilepsy centers have already established similar clinics. Sharing experience, brainstorming ideas, and networking opportunities with other similar clinics to successful implementation and expansion of the clinic Formation of a disease-specific database that can facilitate intramural research and foster multicenter research collaboration, for example, participation in the Pediatric Epilepsy Research Collaboration efforts Implementation grant awarded to a neurologist for planning and maintenance of the clinic. Patient preference and wish to get to see all the relevant providers in a single visit
Organization characteristics	Lack of standardized workflow in the clinic Lack of availability of a dedicated research coordinator and robust technological support	The regular clinic of the assigned epileptologist was blocked for that day to facilitate dedicated time for the clinic Neuroscience leadership /organizational commitment Establishment of a REDCap data registry to collect clinical information of these patients to facilitate longitudinal follow-up and assess clinical outcomes Consensus about the added value of multidisciplinary care
Practice staff and clinicians	The busy workload of specialists, particularly the availability of the neurosurgeon Initial skepticism about the feasibility of the clinic among both epileptologists and general neurologists Concern about the autonomy of the neurologists referring patients for further evaluation	A full-time nurse navigator to coordinate the visit and other diagnostic tests Availability of opinion leader Availability of administrative personnel for scheduling

CEC startup

We centralized the clinic’s location in the Neuroscience Center to streamline patient visits and improve communication among providers. Rather than separate discussions with various specialists, patients were allowed to discuss treatment options with all relevant specialists available in the clinic room. The interdisciplinary team included an epileptologist (weekly rotation among 5 board-certified physicians), a neurosurgeon, a neuropsychologist, and the nurse care coordinator. Epileptologists were involved to ensure completeness of previous diagnostic evaluation, optimization of medical therapy, and exploration of other appropriate nonpharmacological options. The neurosurgeon was engaged to play a collaborative role in guiding the multidisciplinary conversation about epilepsy surgery and neuromodulation. The neuropsychologist was involved in the rapid assessment of these children’s cognitive challenges and psychiatric issues. A dietician, rehabilitation specialist, and social worker contributed on a part-time basis. The team holds a weekly half-day clinic and consults four patients per session.

Patient identification and workflow

Because of the rapid roll-out of the program, 2 strategies were used for patient identification of children with DRE following the definition of the International League Against Epilepsy(ILAE). [13] Neurologists and epileptologists were able to refer patients directly to the clinic by contacting the care coordinator. It was determined that one epileptologist would temporarily take primary responsibility for the potential surgical patients referred by neurologists to complete the remaining diagnostic workup, present the patient’s information to the epilepsy surgery conference, facilitate surgical planning with the neurosurgeon, and provide immediate follow-up after surgery. However, the patient would eventually return to the original neurology providers, who would maintain autonomy during the shared decision-making process. [14] To further promote the referral process, the coordinator also used a self-service cohort query tool (Epic Slicer-dicer) to identify all patients with DRE who are scheduled for clinic. [15] She sent weekly reminders to the providers with a list containing potentially eligible patients to allow providers to offer CEC appointments to the willing families during the regular clinic visit. We educated providers about ideal referral candidates, focusing on recognized etiologies and syndromes associated with DRE, such as tumors, mesial temporal sclerosis, cortical dysplasia, hypothalamic hamartoma, and hemispheric syndromes. [16] We also expressly indicated that cases typically perceived as difficult candidates for surgery (e.g., very young age, developmental disabilities, psychiatric issues, lesion overlapping the eloquent cortex, multifocal epilepsy) would not be a contraindication to referral to this clinic. We encouraged earlier referral for younger patients. Additionally, we considered some patients eligible for the clinic even if they were not formally diagnosed with DRE but had an epilepsy syndrome strongly associated with DRE and were potentially surgically remediable. Some DRE patients were not included in the clinic if they were already receiving coordinated care in another multispecialty clinic, such as tuberous sclerosis, neurogenetics, and neuro-oncology clinics. The CEC medical director met weekly with the care coordinator to discuss new referrals for assessing eligibility and urgency in scheduling patients. The care coordinator scheduled patients for clinic visits, coordinated diagnostic tests, entered patient data in a Research Electronic Data Capture (REDCap) database, communicated with the surgical case conference coordinator to present appropriate patients in the conference, talked directly with patients and families assigned to the clinic during office hours, and handled all electronic messages received from these families.

The clinic started operating in August 2020. The cohort of all patients attending the clinic (with at least one visit) was identified from August 2020 to June 2021. We collected data retrospectively from the electronic medical record and the REDCap registry to determine referral patterns, clinic scheduling metrics, patient characteristics, treatment recommendations, and epilepsy quality metrics.

Clinical recommendations and quality of epilepsy care data during the first clinic visit were manually abstracted from the individual charts. Clinical recommendations included noninvasive diagnostic recommendations (e.g., video EEG, neuroimaging, advanced source imaging specific for presurgical evaluation), invasive diagnostic tests (e.g., intracranial monitoring), optimization of medical treatment by either dose change of ASM or addition of a new ASM, recommendations for epilepsy surgery, and recommendations for vagus nerve stimulation (VNS) and dietary therapy. Quality of epilepsy care was evaluated by 4 metrics from the American Academy of Neurology (AAN) 2017 Epilepsy Quality Measurement Set: 1. counseling for women of childbearing potential with epilepsy (percentage of all patients of childbearing potential, 12–44 years old, diagnosed with epilepsy and counseled regarding epilepsy treatment and its effects on contraception and pregnancy in at least 2 of the 3 counseling topics, which include the need for folic acid supplementation, the drug interactions with contraception medication, and potential antiseizure medications effect[s] on fetal/child development and/or pregnancy); 2. depression and anxiety screening for patients >12 years old with epilepsy (percentage of patients with a diagnosis of epilepsy who were screened for depression and anxiety; no specific screening tool was required, but most frequently depression was screened by the Patient Health Questionnaire 2 [PHQ2] and 9 [PHQ-9], and anxiety was screened by the Generalized Anxiety Disorder 2 [GAD-2] and 7 [GAD-7]; 3. patient visits with current seizure frequency documented for each seizure type; 4. patients >4 years old with age-appropriate condition-specific quality of life assessed (no specific screening tool was required, but most frequently, Pediatric Epilepsy Learning Healthcare System Quality of Life Questions [PELHS-QOL-2] was used). [17] Descriptive statistics were used to summarize the patient population, frequency of various recommendations, and quality of epilepsy care data. [18]

To further optimize clinic functioning, 6 providers and 26 caregivers were interviewed following a semistructured format regarding satisfaction with the services, including the overall quality of the clinic. The caregivers also provided feedback regarding the amount of information given in the clinic, the attitude of the clinic staff, time spent during visits, recommendations for clinic use to other patients, and comfort in contacting clinic staff after the clinic visit. The feedback was used to enhance the effectiveness of the clinical program.

Our project received approval from our ethical standards committee on human experimentation (UAMS Institutional Review Board associated with the Arkansas Children’s Hospital) for any experiments using human subjects.

Results

Systematic rating of constructs using CFIR framework

Of 32 CFIR constructs assessed, 24 constructs were positively rated (+1 or +2) to predict a high degree of implementation success of the interdisciplinary clinic (Table 2). Only 7 constructs did not have adequate data or could not be applied in our context. We identified four constructs (cost, cosmopolitanism, compatibility, and external change agents) with the potential to affect the implementation plan negatively. As many stakeholders were concerned about the costs and compatibility of the clinic with the existing workflows, we employed several strategies-template modification, close monitoring of scheduling metrics, and employment of a dedicated clinic coordinator- to overcome these concerns during the pre-implementation period. We also actively networked with other organizations and healthcare professionals from other institutes to understand the on-the-ground challenges to run similar clinics and further refined our implementation plan.

Table 2.

Systematic ratings of Consolidated Framework for Implementation Research Constructs

INTERVENTION: Organization and Implementation of an interdisciplinary clinic for children with drug-resistant epilepsy
Construct		Short Description	Ratings*
I. INTERVENTION CHARACTERISTICS
A	Intervention Source	Perception of key stakeholders about whether the intervention is externally or internally developed.	+1
B	Evidence Strength & Quality	Stakeholders’ perceptions of the quality and validity of evidence supporting the belief that the intervention will have desired outcomes.	+1
C	Relative Advantage	Stakeholders’ perception of the advantage of implementing the intervention vs an alternative solution.	+2
D	Adaptability	The degree to which an intervention can be adapted, tailored, refined, or reinvented to meet local needs.	+1
E	Trialability	The ability to test the intervention on a small scale in the organization, and to be able to reverse course (undo implementation) if warranted.	0
F	Complexity	Perceived difficulty of implementation, reflected by duration, scope, radicalness, disruptiveness, centrality, and intricacy and number of steps required to implement.	0
G	Design Quality & Packaging	Perceived excellence in how the intervention is bundled, presented, and assembled.	+1
H	Cost	Costs of the intervention and costs associated with implementing the intervention, including investment, supply, and opportunity costs.	−1
II. OUTER SETTING
A	Patient Needs & Resources	The extent to which patient needs, and the barriers and facilitators to meet those needs, are accurately known and prioritized by the organization.	+2
B	Cosmopolitanism	The degree to which an organization is networked with other external organizations.	−1
C	Peer Pressure	Mimetic or competitive pressure to implement an intervention; typically because most or other key peer or competing organizations have already implemented or are in a bid for a competitive edge.	+2
D	External Policy & Incentives	A broad construct that includes external strategies to spread interventions, including policy and regulations (governmental or other central entity), external mandates, recommendations and guidelines, pay-for-performance, collaboratives, and public or benchmark reporting.	+1
III. INNER SETTING
A	Structural Characteristics	The social architecture, age, maturity, and size of an organization.	+2
B	Networks & Communications	The nature and quality of webs of social networks and the nature and quality of formal and informal communications within an organization.	0
C	Culture	Norms, values, and basic assumptions of a given organization.	+2
D	Implementation Climate	The absorptive capacity for change, shared receptivity of involved individuals to an intervention, and the extent to which use of that intervention will be rewarded, supported, and expected within their organization.	+1
1	Tension for Change	The degree to which stakeholders perceive the current situation as intolerable or needing change.	+2
2	Compatibility	The degree of tangible fit between meaning and values attached to the intervention by involved individuals, how those align with individuals’ own norms, values, and perceived risks and needs, and how the intervention fits with existing workflows and systems.	−1
3	Relative Priority	Individuals’ shared perception of the importance of the implementation within the organization.	+1
4	Organizational Incentives & Rewards	Extrinsic incentives such as goal-sharing awards, performance reviews, promotions, and raises in salary, and less tangible incentives such as increased stature or respect.	+1
5	Goals & Feedback	The degree to which goals are clearly communicated, acted upon, and fed back to staff and alignment of that feedback with goals.	NA
6	Learning Climate	A climate in which: a) leaders express their own fallibility and need for team members’ assistance and input; b) team members feel that they are essential, valued, and knowledgeable partners in the change process; c) individuals feel psychologically safe to try new methods; and d) there is sufficient time and space for reflective thinking and evaluation.	NA
E	Readiness for Implementation	Tangible and immediate indicators of organizational commitment to its decision to implement an intervention.	+2
1	Leadership Engagement	Commitment, involvement, and accountability of leaders and managers with the implementation.	+2
2	Available Resources	The level of resources dedicated for implementation and on-going operations, including money, training, education, physical space, and time.	0
3	Access to Knowledge & Information	Ease of access to digestible information and knowledge about the intervention and how to incorporate it into work tasks.	+1
IV. CHARACTERISTICS OF INDIVIDUALS
A	Knowledge & Beliefs about the Intervention	Individuals’ attitudes toward and value placed on the intervention and familiarity with facts, truths, and principles related to the intervention.	+1
B	Self-efficacy	Individual belief in their own capabilities to execute courses of action to achieve implementation goals.	+1
C	Individual Stage of Change	Characterization of the phase an individual is in, as he or she progresses toward skilled, enthusiastic, and sustained use of the intervention.	NA
D	Individual Identification with Organization	A broad construct related to how individuals perceive the organization, and their relationship and degree of commitment with that organization.	NA
E	Other Personal Attributes	A broad construct to include other personal traits such as tolerance of ambiguity, intellectual ability, motivation, values, competence, capacity, and learning style.	NA
V. PROCESS
A	Planning	The degree to which a scheme or method of behavior and tasks for implementing an intervention are developed in advance, and the quality of those schemes or methods.	+1
B	Engaging	Attracting and involving appropriate individuals in the implementation and use of the intervention through a combined strategy of social marketing, education, role modeling, training, and other similar activities.	+2
1	Opinion Leaders	Individuals in an organization who have formal or informal influence on the attitudes and beliefs of their colleagues with respect to implementing the intervention.	+2
2	Formally Appointed Internal Implementation Leaders	Individuals from within the organization who have been formally appointed with responsibility for implementing an intervention as coordinator, project manager, team leader, or other similar role.	+2
3	Champions	“Individuals who dedicate themselves to supporting, marketing, and ‘driving through’ an [implementation]”, overcoming indifference or resistance that the intervention may provoke in an organization.	+2
4	External Change Agents	Individuals who are affiliated with an outside entity who formally influence or facilitate intervention decisions in a desirable direction.	−1
C	Executing	Carrying out or accomplishing the implementation according to plan.	NA
D	Reflecting & Evaluating	Quantitative and qualitative feedback about the progress and quality of implementation accompanied with regular personal and team debriefing about progress and experience.	NA

^*Criteria used to assign ratings: +2, the majority of interviewees provides explicit examples of how the construct affects the implementation in a positive way; +1, the majority of interviewees provides general statement about how the construct affects the implementation in a positive way; 0, the construct has positive and negative influences balancing each other out; −1, the majority of interviewees provides general statement about how the construct affects the implementation in a negative way; −2; the majority of interviewees provides explicit examples of how the construct affects the implementation in a negative way; NA, not applicable for the intervention or not enough or missing data for appropriate rating

In summary, the systematic rating process confirmed that stakeholders saw the benefits of establishing this new clinic.

Operational efficiency of the clinic

The clinic scheduling metrics were assessed for the operational efficiency of the clinic (Figure 2). Parameters included, clinic slots eligible to have patients scheduled (total 164 slots available during the study period), slots occupied by appointments (127 scheduled), and slots for which patients attended the associated visit (100 appeared with 76 new visits; 10 no-shows, 17 cancellations). The appearance rate (appeared/scheduled) was calculated as 78.7%, the usage rate (scheduled/available) as 77.4%, and the utilization rate (appeared/available = usage rate*appearance rate) as 61%.

Figure 2.

Monthly Scheduling Metrics of the Clinic

Demographics

Our population demographics (N=76) showed an average age of 12 years (±5) when presented to the clinic (Table 3). As expected, more than two-thirds of these patients were referred by neurologists. Due to the primary focus on epilepsy surgery, the most common seizure type was intractable focal epilepsy (60%). Still, due to expedited evaluation for other nonmedical therapies, patients with generalized (27.6%) or mixed seizures (9.2%) were also seen in the clinic. The most common etiologies of epilepsy were either structural (34.2%) or genetic (32.9%) in nature.

Table 3.

Demographics of referred unique patients (N=76)

Patients
Mean age (SD)	12 (±5) years
Sex	n (%)
Male	42 (55)
Female	34 (45)
Race	n (%)
Caucasian	56 (73.7)
African American	8 (10.5)
Hispanic	5 (6.6)
Asian	1 (1.3)
Others	6 (7.9)
Seizure type	n (%)
Focal	46 (60.5)
Generalized	21 (27.6)
Both focal and generalized	7 (9.2)
Unspecified	2 (2.6)
Seizure etiology	n (%)
Structural	26 (34.2)
Genetic	25 (32.9)
Structural and genetic	6 (7.9)
Infectious	1 (1.3)
Unknown	17 (22.4)
Immune-mediated	1 (1.3)
Referred by	n (%)
Neurologist	54 (71)
Epileptologist	22 (29)

Clinical recommendations

We reviewed the individual chart of the first CEC visit to screen recommendations (Table 4). A total of 39 patients (51.3%) were deemed eligible for epilepsy surgery evaluation. But most patients did not have enough previous diagnostic workup to proceed to direct intracranial monitoring or epilepsy surgery. Therefore, only 12 (15.8%) patients were recommended for intracranial monitoring (stereo-EEG or subdural grid and strip methods), and an additional 4(5.3%) patients were scheduled for epilepsy surgery. The majority of the patients (41; 53.9%) were advised for further diagnostic testing, and 13(17%) patients benefited from diagnostic bundling (scheduling multiple diagnostic tests in a single session). Although only 5(6.6%) patients were recommended for dietary therapy, 24 (31.6%) patients were scheduled for VNS. Regarding optimization of medical treatment, more patients (25; 33%) had a change in their existing ASM regimen rather than an addition of a new ASM (6; 7.9%).

Table 4.

Recommendations from the first clinic visit

Clinical recommendations	n (%)
Noninvasive diagnostic recommendation	41 (53.9)
Dose change of existing ASM	25 (32.9)
Addition of a new ASM	6 (7.9)
Invasive diagnostic recommendation*	12 (15.8)
Epilepsy surgery	4 (5.3)
Recommendation for specific dietary therapy	5 (6.6)
Recommendation for neuromodulation	24 (31.6)
Diagnostic bundling (≥3 tests scheduled together)	13 (17.1)
Epilepsy surgical pathway	39 (51.3)

^*Intracranial monitoring (stereo-EEG or subdural grid and strip methods)

Abbreviation: ASM, anti-seizure medication

Quality epilepsy care

Four metrics for assessment of quality epilepsy care showed excellence in documenting seizure type (100% adherence) and reproductive counseling for women of childbearing potential (only 1 out of 19 patients did not meet the criterion for counseling recommendation as her clinic note had documentation of folic acid supplementation but without any mention of potential drug-drug interaction and impact of ASM on the fetus and/or pregnancy) (Table 5). Adherence to anxiety and depression screening was good, but many patients were excluded from the screening due to known active diagnoses of anxiety and/or depression. Finally, the quality of life assessment was only modest, with close to 40% of the charts not having specific screening documentation.

Table 5.

Epilepsy Quality metrics

Quality measurement	Eligible population	Exclusions	Given population to which measure applies	In the subset of patients, the clinical action or service has been provided	%
Seizure Frequencya	76	5	71	71	100
Depression and Anxiety Screeningb	41	20	21	17	81
Quality of Life Assessmentc	71	5	66	39	59
Counseling for Women of Childbearing Potentiald	19	0	19	18	94.7

^aOf 76 eligible patients, 5 patients were excluded because a caregiver was unavailable for a patient who is noncommunicative or has an intellectual disability.

^bOf 41 eligible patients that were ≥ 12 years old, 20 were excluded due to patient denial or inability to complete an assessment or if the patient has a diagnosis of depression or anxiety on the active problem list.

^cOf 71 eligible patients that were ≥ 4 years old, 5 were excluded due to patient inability to complete quality of life assessment, and no proxy was available.

^dA total of 19 females were in the cohort of ≥ 12 years old.

Discussion

This article details the conceptualization and processes that contributed to the rapid organization and implementation of an interdisciplinary clinic for children with DRE. To our knowledge, this is the first study that used a meta-analytic framework (based on Implementation Science theories) to project the successful implementation of a coordinated interdisciplinary epilepsy clinic. The limited use of implementation theories to guide clinical services may be related to the unfamiliarity of the Implementation Science in neuroscience research. However, the typical use of the rapid cycle improvement (Plan-Do-Study-Act model) process can be challenging in situations where prior systematic context analysis for the first implementation process is necessary. [19,20] We utilized a systematic rating process to project high-degree implementation success before carrying out the change process. Using a systematic framework is also beneficial for generating generalizable knowledge for future applicability in diverse real-world contexts, bringing a higher degree of methodological rigor in the clinical investigation compared to traditional quality improvement efforts, and strengthening external validity over time as other centers may use the same framework to estimate probabilities of success or failure of a particular clinical service. [12]

After establishing the clinic, schedule-based analysis was used to provide a framework to assess changes in the clinic operations. For approximately 100 patient visits, appearance and usage rates were >75%, yielding a utilization rate of approximately 60%. Other international and US studies showed similar no-show and cancellation rates in pediatric neurology clinics before the COVID pandemic to suggest a robust clinic efficiency in the middle of this challenging time. [21,22] As previous studies suggested, long distances from the clinic (patients from all over the state traveled to this clinic) and insurance status (Medicaid population) may be responsible for some scheduling inefficiency. [23] A long delay of the appointment time was perhaps not related as most patients were scheduled within 4 weeks of the referral. Though not directly assessed, periodic extreme weather, sickness in patients or caregivers (COVID and other infections), fear of COVID exposure in the clinic, lack of transportation, and transient improvement in seizure control were perhaps associated with some cancellations. Tracking cancellation lag time and trying to schedule another patient in the slot may further improve scheduling efficiency. The patients were reminded about the upcoming visits, from 7 days to 24 hours before the visit, using text messages, phone calls, and email to decrease no-shows related to forgetfulness. We also plan to have the coordinator call families 72 hours before the appointment as some patients did not have the optimum benefit from the clinic because their seizures were already better controlled between the referral and the actual visit in the CEC or they had a recent change in the medical therapy before the CEC visit that required longer follow-up to assess response rather than another change of treatment plan during the clinic visit.

The clinic’s establishment was motivated by the desire to expand epilepsy services amid the COVID pandemic. Although the clinic was primarily developed to streamline diagnostic workup to move patients faster toward epilepsy surgery, overtime, the model was adapted to serve patients more comprehensively by medical therapy optimization, completion of the diagnostic tests, the use of alternative nonmedical medical therapies (diet and neuromodulation), and the attention paid to behavioral and cognitive challenges associated with DRE. We had only 4 patients with lesional epilepsy who could proceed directly to surgery based on concordant video EEG and MRI data. As noted in recent studies, the complexity of epilepsy surgery has dramatically increased with a further need for intracranial monitoring and/or advanced noninvasive source imaging before surgery. [24–27] Within a brief period, the clinic facilitated a robust uptake of presurgical evaluation (10–20/year previously to 40/year), intracranial diagnostic procedures (0–5/year to 12/year, and the implantation of neuromodulation devices (10–12/year to 24/year). Other patients with multifocal or generalized epilepsy and children with epileptic encephalopathies benefited from genetic testing (a more defined pathway for genetic testing in the clinic can further improve the workflow), medical therapy, neuromodulation, dietary therapy, and palliative surgery. [16, 28–31] Interestingly, we observed significantly more patients receiving a recommendation for VNS compared to dietary therapy. It is unclear if regular access of a neurosurgeon in the clinic caused a bias recommendation toward VNS. It is also possible that providers refer more patients suitable for VNS to this clinic due to the presence of a neurosurgeon in the clinic. We did not capture information regarding previous or existing dietary therapy, which may have excluded some patients for repeat recommendations about dietary treatment.

Multidisciplinary care is more effective than traditional clinic visits in many disciplines in medicine, including neurology. [32–36] The literature to support interdisciplinary care for many chronic neurological disorders showed its effect on increased adherence to clinical care guidelines, efficient resource utilization, reduced hospital admissions and emergency room visits, improved quality of life, and decreased mortality. [37, 38] For example, a multidisciplinary intervention for Parkinson’s disease showed improved quality of life and disease-specific rating scores than standard general neurology care. [39] While the need for an interdisciplinary clinic in children with epilepsy makes intuitive sense, there is a paucity of data in the literature with only some data available related to multidisciplinary transitional clinics for adolescents and patients with psychogenic nonepileptic events. [38,39] In the only previous study of a multidisciplinary clinic of children with DRE, Williams et al described the establishment of the epilepsy clinic with various specialists (pediatric neurologist, nurse practitioners, psychologist, psychology examiner, social worker, educational specialist), assessed the referral patterns, and analyzed the factors predictive of parental satisfaction attending the clinic. [42] However, this study did not specifically evaluate the clinical recommendations of the clinic visit and did not determine the quality of the epilepsy care. Multidisciplinary discussions are common for intractable patients (especially in the presurgical evaluation), but usually happen in the absence of and with no direct input from the patients during the meeting. [43] The distinct benefit of the interdisciplinary clinic is that epileptologists, neurosurgeons, and neuropsychologists can discuss and review the surgical option with patients and families, in person and from multiple viewpoints, to develop a practical treatment decision in one visit. Epileptologists can give input regarding potential epileptogenic zone, completeness of diagnostic workup, and the probability of seizure freedom. Neurosurgeons can elaborate on the technical limitations and risks of the proposed procedure, and neuropsychologists can discuss the impact of surgery on the behavioral and memory comorbidities. We noted that several patient profiles benefited most from the clinic: 1. children with focal intractable epilepsy with no previous advanced source imaging (e.g., 14 patients scheduled for magnetoencephalography); 2. potential neuromodulation candidates but needing comprehensive review by a multidisciplinary team for evaluation of epilepsy surgery (24 patients scheduled to receive VNS); 3. patients needing bundling of diagnostic tests; and 4. patients needing neuropsychiatric evaluation (other than determining patients who would need detailed assessment, the presence of neuropsychologist was helpful for practical tips for children with learning disorders, autism, and attention deficit hyperactive disorder, and neuropsychologists had more information about the patients directly from the other physicians, which may lead to better neuropsychiatric assessment). In general, both healthcare professionals and families expressed that the interdisciplinary clinic was a highly effective method of evaluating children with DRE, and the combined expertise of the team was estimated to be superior to individual specialists working alone. [44]

We noted >80% to 90% adherence to the 3 out of 4 AAN standardized epilepsy quality measures (updated 2017 version), which were created to improve the delivery of care for patients with epilepsy. [18] This finding was consistent with previous studies (primarily based on the first set of epilepsy measures published in 2009) showing 83% to 94% adherence for providers with high volume exposure to epilepsy patients or additional fellowship training in epilepsy. [45] The adherence rate was much better than that noted in other studies (including our unpublished data from our general neurology clinics, recorded in previous years during divisional audits and quality improvement efforts) involving a broad group of neurologists. [46] However, we had only modest documentation of screening information about health-related quality of life. Although physicians consistently documented various components of a patient’s life affected by seizures or ASM, specific quality of life scores or screening methods were frequently omitted in the clinic notes. Further quality improvement initiatives (provider education, reminders for documentation, standardized template, structured support tool in the electronic medical record, and electronic data capture with near-time data analysis) to address this gap may allow patients, families, and physicians to identify areas of concern related to poor quality of life, improve clinical practice, and track trends longitudinally to determine the impact of a new treatment. [45,47–50]

Besides the benefit of interdisciplinary clinics described above, these clinics for intractable epilepsy are ideally disposed to serve as a gateway to clinical research. We created a comprehensive REDCap registry to track clinical outcomes, evaluate adherence to clinical standards, maintain quality care, and follow these patients longitudinally. The availability of a disease-specific registry allowed us to participate in multicenter Pediatric Epilepsy Research Center’s collaborative research projects. Additionally, patients and families seeking multidisciplinary care are very motivated to learn about and participate in the research. Finally, the research staff may follow a relatively smaller pool of patients to recruit for the relevant clinical studies (as most epilepsy trials involve patients with DRE).

Despite the rapid implementation of this clinic, many challenges remain, including the unbillable service of the nurse coordinator, who played an essential role in the smooth functioning of the clinic and provided interdependent interaction within and across disciplines. Although not directly assessed, a single-person contact for the clinic allowed easier coordination of tests, consistent tracking of patients, and prompt case presentation for the surgical conference. However, interdisciplinary clinics are expensive to establish and run. Institutional profit may not be higher than the traditional one patient-one doctor model without a significant increase in the downstream revenue. A formal definition and assessment of the quality and value of multidisciplinary care for DRE are increasingly needed, which can justify using a dedicated care coordinator for the clinic. Alternatively, this position may be funded by philanthropic support in the future. Although the clinic reduced the significant travel burden for the families, many patients still had to travel long distances (as CEC was the only such specialized clinic in the state) to come to our clinic. Further improvement in care value is possible by using telehealth without losing the quality of care. [51] However, most families showed hesitancy to substitute in-person visits for telehealth, and many families live in rural areas without the high-speed internet access needed at home to participate in telehealth visits. Improvement in the mobile health technology and establishment of the networked programs (remote health clinics with high-speed internet connections) and point-to-point connections (linking several primary care clinics to our organization, allowing patients to be evaluated from their pediatrician’s office) in the future may be helpful in that regard. A further concern would be reimbursement for multidisciplinary video visits. Further expansion of the clinic may also need to optimize community support, involve advocacy groups, and engage families via social media.

The research has several limitations. The clinic cohort has been relatively small so far, and some patient characteristics were not systematically investigated in the study, including seizure frequency, complete ASM regimen, and the impact of clinic recommendations. We acknowledge that we lack longitudinal follow-up data in the current pilot phase to fully understand the clinic’s impact. However, the study has not been primarily designed to evaluate the effectiveness of the interdisciplinary clinic or study healthcare utilization and cost-benefit analysis. Instead, the study focused on the successful implementation of a practice model. Regardless, we will follow these patients long-term to determine clinical outcomes and cost-effectiveness of surgery in eligible patients. Moreover, in this cohort, we also did not have a control group for comparison purposes. In the future, children assigned to the interdisciplinary clinic and children receiving regular care can be compared objectively to assess differential outcomes. However, the lack of previous studies related to interdisciplinary epilepsy care may cause problems reaching consensus about definite metrics to track related to patient-centered outcome data to prove the impact of a multidisciplinary clinic.[52] However, we successfully followed several pertinent quality metrics in this cohort to show high-quality care. An additional limitation of the study is that the structure and personnel of the CEC were based on the availability of needed experts. The implementation process is based on a single center and may not be generalizable outside the population. To counteract that, we demonstrated a systematic rating system that other centers could use before implementing a new clinical service; consistent use of this systematic framework may generate robust evidence supporting a particular establishment when rapid improvement cycles are difficult to implement.

In summary, our study suggests that it is feasible to implement an interdisciplinary complex epilepsy clinic at an academic medical center with rapid uptake of comprehensive evaluation and treatment. Throughout the continually evolving pandemic, our clinic provided consistent care for children with DRE with robust utilization. We believe the framework shared here could be adapted for practical implementation in other institutions to provide individualized, specialized, and comprehensive care in children with DRE. With limited previous evidence that interdisciplinary clinics have an impact on the quality of epilepsy care, our study showed care coordination integrated into the care delivery system could be a valuable attribute of care models in high needs children with DRE by enabling comprehensive one-stop service for diagnostic evaluation, surgical consideration, and brief assessment of psychiatric comorbidities and cognition without compromising evidence-based and consensus-based best practices.

Constructs with illustrative statements that strongly and positively influenced the implementation.

Relative advantage:

‘That intractable clinic; that’s going to help a lot. Before, I wouldn’t be quite sure how to send them to somebody other than asking my nurse. Just try to figure out what to do before. So it was a little bit complicated. Now, we have this clinic and I can refer to the clinic coordinator; I think that’s going to make things a lot better’. (Neurologist)

Patient Needs & Resources:

‘It is a huge advantage for the patients to get to see so many specialists in one visit and informed about the plan’ (Neuroscience scheduler)

‘Does Arkansas have something to offer us? And they start looking go, Oh my God. Yeah, they have this clinic. We should go at least check them out. And those people, when they have good experiences and then they go back to their homes, they then sing your praises and sing the institution’s praises to everybody they know, and you start getting more patients from that area’(Neuroscience leader)

Peer Pressure:

‘Most large centers have multidisciplinary programs that they want to bring in people from everywhere... Come here and get, you know, high-end specialty diagnostic assessment and treatment’ (Epileptologist)

‘I think it’s a very reachable goal... it would put us into the top tier of some of the busiest places in the country’. (Neuroscience administrator)

‘We’ll do like a collaborative conference together’(Epileptologist)

Structural Characteristics:

‘Neuroscience council and physician-nurse dyad is vital to organize this[clinic]’(Neurosurgeon)

Culture:

‘We collaborate with neurosurgery with so many projects’ (Nurse coordinator)

Tension for Change:

‘I’m interested in quality. I want us to get the clinic right. And as we continue to grow and see more and more patients, several things are going to transpire. One is as a team; we’re going to synergize better. We will communicate with each other better’. [Neuroscience leader]

Not just the epileptologists, not just the surgeon, not just the nursing staff, all of us will sync with each other better and better over time, our volumes will increase. So experiences, individual provider’s experiences will also go up. And as you see more, you will be more confident about doing more. [Epileptologist]

‘“Good fences. Make good neighbors” So I’m happy to be friendly with you [other programs]. I’m happy to collaborate with you. I’m happy to have conferences with you, but I’m not interested referring all patients to you. I prevent that by providing a competitive service. So it’s not, it’s not by trashing you, it’s not by trying to tear down what you’re doing. It’s by trying to build up a comprehensive service and let the people decide where they want to go’. [Neuroscience leader]

• We conceptualized and implemented an interdisciplinary epilepsy clinic after systematically rating constructs present in a theoretical meta-analytic framework (Consolidated Framework for Implementation Research).

• Throughout the pandemic, robust clinic efficiency was maintained with appearance and usage rates of >75%, yielding a clinic utilization rate of approximately 60%.

• Among 76 unique patients (average age of 12 years, 60% focal epilepsy), 39 patients (51.3%) were deemed eligible for epilepsy surgery evaluation.

• Standardized epilepsy quality measures showed >80% to 90% adherence in 3 (reproductive counseling, depression and anxiety screening, documentation of seizure frequency) out of 4 metrics.