Abstract
Objective:
Clinical guidelines have expanded the indications for nonalcoholic fatty liver disease (NAFLD) screening to type 2 diabetes mellitus and obesity, which are conditions common in populations who receive care in urban safety-net settings. This study aimed to evaluate safety-net primary care and endocrinology clinicians’ knowledge of NAFLD, determine barriers and facilitators to screening, and examine perspectives on the use of electronic health record tools for risk assessment.
Methods:
Sequential explanatory mixed methods using survey and qualitative interviews with primary care, primary care subspecialty, and endocrinology clinicians in an urban safety-net health care system.
Results:
A total of 109 participants completed the survey (36.5% response rate), and 13 participated in interviews. Most respondents underestimated or did not know the prevalence of NAFLD (68%), did not use the recommended noninvasive tests for risk stratification (65%), and few were comfortable with screening for (27%) or managing (17%) NAFLD. Endocrinologists had greater knowledge of risk factors but lower rates of comfort and more often felt that screening was not their responsibility. The qualitative themes included the following: (1) lack of knowledge about screening, (2) concern for underdiagnosing NAFLD, (3) perception of severity impacts beliefs about screening, (4) screening should occur in primary care but is not normative practice, (5) concerns exist about benefit, (6) competing demands with a complex population hinder screening, and (7) a need for easier ways to integrate screening into practice.
Conclusion:
Knowledge gaps may hamper uptake of new guidelines for NAFLD screening in primary care and endocrinology clinics in an urban safety-net health care system. Implementation strategies focused on training and educating clinicians and informed by behavioral economics may increase screening.
Keywords: guideline implementation, noninvasive tests, mixed methods, nonalcoholic fatty liver disease, implementation science
Introduction
Nonalcoholic fatty liver disease (NAFLD) is the most common cause of chronic liver disease in the United States, and its prevalence is increasing globally.1 The prevalence of NAFLD is projected to increase in the next decade with a two- to threefold increase in nonalcoholic steatohepatitis, advanced fibrosis/cirrhosis, and complications such as hepatocellular carcinoma.1-3 Guidelines have expanded the recommendations for screening for NAFLD and advanced fibrosis to patients with obesity, prediabetes, and type 2 diabetes mellitus (T2DM), in addition to those with hepatic steatosis on imaging or elevated liver enzyme levels.4-6 However, NAFLD remains underdiagnosed.7
NAFLD disproportionately affects minoritized groups, particularly individuals of Hispanic ethnicity and those with lower socio-economic status, who are also at highest risk of progression and development of complications.8,9 Urban safety-net hospitals care for higher proportions of minoritized groups and, thus, populations with an increased risk and higher prevalence of NAFLD.10,11 Therefore, primary care and endocrinology clinics within safety-net systems are an important setting in which to identify and implement effective strategies to enhance screening for NAFLD and advanced fibrosis.
Although some data exist regarding clinicians’ knowledge of screening for NAFLD,12 data for safety-net settings are unclear, and barriers to screening in this setting have not yet been examined. This study explored implementation context in anticipation of an initiative to test an electronic health record (EHR) tool to prompt clinicians to screen for NAFLD using noninvasive serum tests (Fibrosis-4 score) and imaging (transient elastography). This study aimed to evaluate and compare knowledge, attitudes, and practices of primary care and endocrinology clinicians around screening; identify barriers and facilitators to screening for NAFLD in primary care and endocrinology clinics; and explore perspectives on the use of EHR tools to assist with risk stratification and screening.
Methods
Study Design and Participants
We conducted a sequential explanatory mixed methods study comprising a survey followed by qualitative interviews with clinicians at an urban academic health system and the largest safety-net hospital in New England. Participants included attending physicians, residents and fellows, and nurse practitioners (NPs) participating in primary care (adult internal medicine [IM] and family medicine [FM]), primary care subspecialists (geriatrics and human immunodeficiency virus [HIV]), and endocrinologists. The Boston University Medical Center Institutional Review Board determined this study exempt. Consent was obtained before the survey and interviews.
Data Collection
The 25-question survey (Supplementary Material) was developed following a knowledge, attitudes, and practices survey model.13 Questions assessed the knowledge of the prevalence of NAFLD, risk factors, evaluation modalities, typical practice, and barriers to screening. Five-point Likert scale questions assessed comfort with screening for and management of NAFLD, beliefs about consequences of NAFLD, and effectiveness of treatment. The survey was reviewed by a hepatologist (M.T.L.) before distribution. The survey was sent via email with 2 completion reminders and administered in REDCap14 between January and March 2022. An invitation to participate in a semistructured interview was included generating a convenience sample of participants for interviews.
Individual, semistructured interviews were conducted using a guide (Supplementary Material) that was developed by the authors. Topics explored comfort with NAFLD screening and management, beliefs about responsibility for screening, and attitudes toward EHR-based reminders. The guide was reviewed before use by an expert in qualitative methods (M.-L.D.) and a hepatologist (M.T.L.). Interviews were conducted by 2 authors (K.L.F., K.A.) during April 2022. Interviews were audio-recorded and conducted via telephone or Zoom, professionally transcribed, corrected for accuracy, and anonymized before analysis. Participants received a $25 debit card for participation.
Data Analysis
Surveys were analyzed using descriptive statistics. Categorical variables were summarized as relative percentages. The Х2 and Fisher exact tests were used to assess differences between primary care providers (PCPs) and subspecialists and between endocrinologists and subspecialists who provide primary care (geriatrics and infectious disease/HIV). Survey data were analyzed using SAS OnDemand for Academics. Statistical significance was assessed at alpha = 0.05.
Deductive qualitative coding of interviews was guided by the theoretical domains framework (TDF)15 and technology acceptance model (TAM)16 using thematic analysis.17 The TDF integrates 33 theories to identify influences on health professionals’ behavior regarding the use of evidence-based practices. Constructs of perceived usefulness and perceived ease of use from the TAM were included because acceptance of the EHR tools to promote screening was of interest.
Two team members (K.L.F., K.A.) with training in the qualitative methods generated an initial codebook using constructs from the TDF and TAM as a priori codes. Before coding, the team reviewed and discussed the constructs and coding definitions. Two transcripts were then independently coded. The team then met to review coding and revise the codebook. This process was continued with 2 additional transcripts after which consensus was reached and the codebook finalized. All transcripts were then independently coded and analyzed using qualitative data analysis software (Nvivo Release 1.6.1; QSR International Pty Ltd). The team then met to discuss findings, generate final themes, and identify representative quotes.
Results
The survey was sent to 299 clinicians from the following: (1) primary care (n = 244), (2) endocrinology (n = 23), (3) geriatrics (n = 23), and (4) HIV (n = 30). In total, 109 participants completed the survey, with a response rate of 36.5% (range, 35.7% [PCPs] to 60.8% [endocrinology]). No partial survey responses were documented. Demographic data are presented in Table 1. All 13 respondents who indicated interest on the survey agreed to participate in interviews—9 from primary care and 2 each from geriatrics and endocrinology. Of these, there were 4 attending physicians, 4 NPs, 3 residents, and 2 fellows; 8 were women, and 11 identified as White, 1 as Hispanic, and 1 as Asian.
Table 1.
Characteristics of the Survey Respondents
| Characteristic | Survey respondents (n = 109) |
|---|---|
| Professional role | |
| Nurse practitioner | 14 (12.8) |
| Attending physician | 65 (59.6) |
| Resident | 26 (23.8) |
| Fellow | 4 (3.7) |
| Specialty | |
| Primary care | 80 (73.4) |
| Endocrinology | 14 (12.8) |
| Geriatrics | 10 (9.2) |
| Infectious disease | 5 (4.6) |
| Time in practice (y) | |
| ≤5 | 47 (43.1) |
| 6-10 | 27 (24.8) |
| 11-20 | 18 (16.5) |
| >20 | 17 (15.6) |
| Practice volume (patients/wk) | |
| <25 | 48 (44) |
| 25-50 | 40 (36.7) |
| 51-75 | 21 (19.3) |
| >75 | 0 |
| Age (y) | |
| <30 | 13 (12) |
| 30-39 | 53 (49.1) |
| 40-49 | 20 (18.5) |
| 50-59 | 13 (12) |
| 60-69 | 6 (5.6) |
| ≥70 | 3 (2.8) |
| Gender identity | |
| Man | 31 (28.7) |
| Woman | 73 (67.6) |
| Nonbinary/nonconforming | 2 (1.9) |
| Prefer not to answer | 2 (1.9) |
| Race/ethnicity | |
| Asian or Pacific Islander | 19 (17.4) |
| Black or African American | 5 (4.6) |
| Native American or Alaskan Native | 1 (0.9) |
| White | 77 (70.6) |
| Hispanic | 6 (5.6) |
| Other | 3 (2.8) |
| Prefer not to answer | 6 (5.5) |
Data are presented as numbers (percentages).
Knowledge About NAFLD Diagnosis and Treatment
Survey Data
Table 2 contains data on the knowledge of NAFLD and comfort with screening. Less than one-third identified the prevalence of NAFLD in the United States as approximately 30%, although a higher proportion of endocrinologists than other specialists answered correctly (57% vs 33%, P = .05). When asked to select risk factors for NAFLD, most (>89%) correctly selected obesity, overweight, and T2DM. A higher proportion of subspecialists (including 93% of endocrinologists) than PCPs identified polycystic ovary syndrome, whereas a higher proportion of PCPs recognized alcohol use disorder as a risk factor.
Table 2.
Knowledge and Comfort With Nonalcoholic Fatty Liver Disease Screening and Management
| Variable | Overall (n = 109) | Primary care (n = 80) | Subspecialists (n = 29) | P value |
|---|---|---|---|---|
| Prevalence of NAFLD | .25 | |||
| <5% | 3 (2.8) | 3 (3.8) | 0 | |
| 15% | 58 (53.2) | 44 (55) | 14 (48.3) | |
| 30% | 34 (31.2) | 21 (26.2) | 13 (44.8) | |
| I don’t know | 14 (12.8) | 12 (15) | 2 (6.9) | |
| Risk factors for NAFLD | ||||
| Overweight | 97 (89) | 71 (88.8) | 26 (89.7) | 1 |
| Obesity | 109 (100) | 80 (100) | 29 (100) | |
| Type 2 diabetes mellitus | 107 (98.2) | 78 (97.5) | 29 (100) | 1 |
| Obstructive sleep apnea | 43 (39.5) | 31 (38.8) | 12 (41.4) | .8 |
| Alcohol use disorder | 66 (60.6) | 54 (67.5) | 12 (41.4) | .01 |
| Polycystic ovary syndrome | 60 (55.1) | 38 (47.5) | 22 (75.9) | .008 |
| I don’t know | 0 | 0 | 0 | |
| Screening modalities | ||||
| Liver function tests | 95 (87.2) | 72 (90) | 23 (79.3) | .14 |
| Abdominal ultrasound | 87 (79.8) | 72 (90) | 15 (51.7) | <.001 |
| Transient elastography | 51 (46.8) | 44 (55) | 7 (24.1) | .004 |
| CT scan | 52 (47.7) | 9 (11.3) | 4 (13.8) | .74 |
| Fibrosis prediction score (FIB-4 or NAFLD fibrosis score) | 37 (33.9) | 44 (55) | 8 (27.6) | .01 |
| Referral to gastroenterology | 37 (33.9) | 28 (35) | 9 (31) | .7 |
| I don’t evaluate patients for NAFLD | 10 (9.2) | 4 (5) | 6 (20.7) | .02 |
| Other | 0 | 0 | 0 | |
| I feel comfortable screening for NAFLD | .02 | |||
| Strongly disagree | 5 (4.6) | 2 (2.5) | 3 (10.3) | |
| Disagree | 37 (33.9) | 23 (28.8) | 14 (48.3) | |
| Neutral | 37 (33.9) | 27 (33.7) | 10 (34.5) | |
| Agree | 25 (22.9) | 23 (28.8) | 2 (6.9) | |
| Strongly agree | 5 (4.6) | 5 (6.2) | 0 | |
| I feel comfortable managing NAFLD | .13 | |||
| Strongly disagree | 7 (6.4) | 4 (5) | 3 (10.3) | |
| Disagree | 50 (45.9) | 33 (41.3) | 17 (58.6) | |
| Neutral | 33 (30.3) | 26 (32.5) | 7 (24.1) | |
| Agree | 19 (17.4) | 17 (21.3) | 2 (6.9) | |
| Strongly agree | 0 | 0 | 0 | |
| I am familiar with the guidelines on evaluating patients for NAFLD | .07 | |||
| Strongly disagree | 14 (13) | 9 (11.4) | 5 (17.2) | |
| Disagree | 60 (55.6) | 43 (54.4) | 17 (58.6) | |
| Neutral | 21 (19.4 | 14 (17.7) | 7 (24.1) | |
| Agree | 13 (12) | 13 (16.5) | 0 | |
| Strongly agree | 0 | 0 | 0 |
Abbreviations: CT = computed tomography; FIB-4 = Fibrosis-4; NAFLD= nonalcoholic fatty liver disease.
Data are presented as numbers (percentages). The chi-square tests were used to compare primary care clinicians with subspecialists, except for cell with counts of <5 for which the Fisher exact test was used.
Regarding evaluating patients for NAFLD, most clinicians indicated using liver function tests and abdominal ultrasound. One-third used noninvasive fibrosis prediction scores, with more frequent use in primary care than in specialty care. A higher proportion of PCPs indicated using imaging modalities including abdominal ultrasound and transient elastography. One-third of the respondents referred patients to gastroenterology for evaluation of NAFLD, and approximately 10% did not evaluate patients for NAFLD at all. Several respondents did not feel comfortable with screening for (n = 42, 39%) or managing (n = 57, 52%) NAFLD, and most were not familiar with practice guidelines (n = 74, 69%). A higher proportion of subspecialists than PCPs disagreed or strongly disagreed with the statement “I feel comfortable with screening for NAFLD” (58.6% vs 31.3%, P = .02); however, no differences in response by provider specialty were noted.
Qualitative Interviews
Analysis of the qualitative data generated 2 themes related to knowledge about NAFLD: (1) lack of knowledge about when and how to screen, influenced by clinical experience, and (2) concern about underdiagnosing NAFLD.
The lack of knowledge about, and minimal direct clinical experience with, NAFLD contributed to widespread discomfort in diagnosis and management:
“I have to admit, my baseline knowledge of NAFLD is not very good…how to screen for it, and then additionally, how to make the appropriate diagnosis.”
Geriatrics physician
Comfort screening for NAFLD and associated fibrosis was impacted by previous training and experience in the management of other chronic liver diseases:
“I do a fair amount of Hep C management, so I would imagine it’s similar in the sense of getting a CMP and INR and then evaluating for the amount of fibrosis or cirrhosis”
FM physician #2
Clinicians without this experience felt unfamiliar with methods for risk stratification and screening and articulated the desire for resources to support screening and management:
“I’d like to have more education around it…but also, I think it’d be nice…it would be appropriate in our clinic to have tools available and the guidelines we can follow.”
Endocrinology NP
Given the high prevalence of NAFLD risk factors among their patients, clinicians expressed concern that limited knowledge and comfort with screening guidelines and modalities resulted in underrecognition of NAFLD:
“I think it’s more common than I know, because I don’t do ultra-sounds or have imaging of liver often, but there’s so, so much obesity, that I think that there’s probably a fair amount of it.”
IM NP #1
Attitudes and Beliefs About NAFLD, Screening, and Management
Survey Data
Table 3 contains data on attitudes and beliefs related to NAFLD. Most respondents (>75%) agreed or strongly agreed that NAFLD is a leading cause of liver disease, an important health problem for patients, and a condition with serious health consequences if left untreated. A significantly higher proportion of PCPs than subspecialists strongly agreed that untreated NAFLD has serious health consequences. Only approximately one-third (36%) of respondents, and 50% of endocrinologists, agreed with the statement that effective treatments for NAFLD exist. Over half of respondents felt that they did not have adequate resources to manage NAFLD, and approximately one quarter felt that all patients with suspected NAFLD should be referred to gastroenterology.
Table 3.
Attitudes and Beliefs About Nonalcoholic Fatty Liver Disease
| Variable | Overall (n = 109) | Primary care (n = 80) | Subspecialists (n = 29) | P value |
|---|---|---|---|---|
| NAFLD is a leading cause of liver disease | .77 | |||
| Strongly disagreea | 0 | 0 | 0 | |
| Disagree | 2 (1.87) | 2 (2.5) | 0 | |
| Neutral | 14 (13.1) | 11 (13.9) | 3 (10.7) | |
| Agree | 55 (51.4) | 38 (48.1) | 17 (60.7) | |
| Strongly agree | 36 (33.6) | 28 (35.4) | 8 (28.6) | |
| Untreated NAFLD has serious health consequences | .01 | |||
| Strongly disagree | 0 | 0 | 0 | |
| Disagree | 2 (1.8) | 1 (1.3) | 1 (3.5) | |
| Neutral | 24 (22) | 19 (23.7) | 5 (17.2) | |
| Agree | 56 (51.4) | 35 (43.8) | 21 (72.4) | |
| Strongly agree | 27 (24.8) | 25 (31.2) | 2 (6.9) | |
| I believe that NAFLD is an important health problem for patientsa | .85 | |||
| Strongly disagree | 0 | 0 | 0 | |
| Disagree | 3 (2.8) | 2 (2.5) | 1 (3.5) | |
| Neutral | 15 (13.9) | 10 (12.5) | 5 (17.9) | |
| Agree | 61 (56.5) | 46 (57.5) | 15 (53.6) | |
| Strongly agree | 29 (26.8) | 22 (27.5) | 7 (25) | |
| My patients see NAFLD as a health prioritya | .22 | |||
| Strongly disagree | 31 (28.7) | 23 (28.8) | 8 (28.6) | |
| Disagree | 55 (50.9) | 37 (46.3) | 18 (64.3) | |
| Neutral | 11 (10.2) | 9 (11.3) | 2 (7.1) | |
| Agree | 10 (9.3) | 10 (12.5) | 0 | |
| Strongly agree | 1 (0.9) | 1 (1.3) | 0 | |
| I am optimistic that we can improve outcomes for people with NAFLD | .02 | |||
| Strongly disagree | 1 (0.9) | 0 | 1 (3.5) | |
| Disagree | 17 (15.6) | 16 (20) | 1 (3.5) | |
| Neutral | 33 (30.3) | 20 (25) | 13 (44.8) | |
| Agree | 48 (44) | 35 (43.8) | 13 (44.8) | |
| Strongly agree | 10 (9.2) | 9 (11.2) | 1 (3.5) | |
| I believe that effective treatments for NAFLD exist | .14 | |||
| Strongly disagree | 2 (1.9) | 2 (2.6) | 0 | |
| Disagree | 18 (16.8) | 16 (20.5) | 2 (6.9) | |
| Neutral | 48 (44.9) | 35 (44.9) | 13 (44.8) | |
| Agree | 35 (32.7) | 21 (26.9) | 14 (48.3) | |
| Strongly agree | 4 (3.7) | 4 (5.1) | 0 | |
| I believe that all patients suspected of having NAFLD should be referred to gastroenterologya | .4 | |||
| Strongly disagree | 6 (5.6) | 4 (5) | 2 (7.1) | |
| Disagree | 45 (41.7) | 36 (45) | 9 (32.1) | |
| Neutral | 32 (29.6) | 22 (27.5) | 10 (35.7) | |
| Agree | 20 (18.5) | 13 (16.2) | 7 (35) | |
| Strongly agree | 5 (4.6) | 5 (5.3) | 0 | |
| I have the resources I need to manage patients with NAFLD | .65 | |||
| Strongly disagree | 10 (9.2) | 8 (10) | 2 (6.9) | |
| Disagree | 50 (45.9) | 33 (41.3) | 17 (58.6) | |
| Neutral | 34 (31.2) | 27 (33.7) | 7 (24.1) | |
| Agree | 14 (12.8) | 11 (13.7) | 3 (10.3) | |
| Strongly agree | 1 (0.9) | 1 (1.3) | 0 |
Abbreviations: NAFLD = nonalcoholic fatty liver disease.
Data are presented as numbers (percentages). The X2 tests were used to compare groups, and the Fisher exact tests were used in the event of cell counts of <5.
Twenty-eight of 29 subspecialists responded.
Qualitative Interviews
Three themes related to attitudes and beliefs about screening were identified: (1) perception of NAFLD severity impacts beliefs about need for screening; (2) primary care is the appropriate venue for screening, but it is not normative practice; and (3) concerns exist about the benefit of screening.
In contrast to the survey results demonstrating that most respondents felt NAFLD was a leading cause of liver disease with serious health consequences, several interview participants expressed doubt that NAFLD was responsible for complications:
“It’s not a big deal. Except if a person is [an] alcoholic, that’s when it’s a bigger problem…. With alcoholic patients, you have to do more stuff, find out whether they have complications.”
IM NP #2
Participants articulated cases in which there had been doubt that NAFLD alone, without other contributors such as heavy alcohol use, had led to severe complications and implying a belief that NAFLD was less common and severe than other causes of liver disease:
“I have seen some patients who have cirrhosis that’s thought to be due to like NAFLD or NASH, but less commonly than from alcohol. Sometimes it’s often noted to be like maybe contributing to cirrhosis, but not too often like just from NAFLD”
IM PGY-3 #1
Participants from both primary care and subspecialties felt that screening for NAFLD should be performed within primary care. In part, this belief was related to the capabilities and function of PCPs:
“…primary care is the gateway oftentimes to the healthcare system for lots of patients… we are very much equipped and…ought to be responsible for screening for this diagnosis in patients.”
FM physician #2
The rationale for screening in primary care was also related to concerns about resource constraints:
“Specialists are a limited resource…. I think, if there’s ways for us to be able to more easily filter through who should actually go to a gastro specialist then that’s great.”
Geriatrics fellow
Endocrinology clinicians voiced a preference to not be responsible for screening but felt responsible for management of certain comorbid cardiometabolic conditions if they were seeing patients for longitudinal diabetes management and primary care involvement was limited:
“…it’s probably better for primary care to do it. But there’s a lot of patients with diabetes, they come to see us so often that they don’t see the primary care that often…. Especially in all those diabetes peripherals, sometimes we end up managing blood pressure and stuff like that. I think, I try not to, I’d rather someone else did, but if no one else is doing it, sometimes we do.”
Endocrinology NP
Despite believing that they should be responsible for screening, PCPs indicated that it was not yet standard of care in primary care:
“I’ve never ordered [a fibroscan], preceptors have never suggested me to order it…. I think that’s maybe one thing where if somebody feels that they want to get a Fibroscan, then I can see my preceptor saying ‘Oh, if you’re going to get a fibroscan just refer them to GI.’”
IM PGY-3 #1
Interviewees articulated 2 key areas of hesitation related to benefit that impacted motivation to integrate NAFLD screening into practice. First, some questioned whether evidence existed for NAFLD screening:
“I think I would like to know more about if it’s been studied, and if it’s been found to have like positive effects on reducing progression to cirrhosis?”
IM PGY-3 #1
Second, others doubted whether diagnosing NAFLD would change their clinical management given a perceived lack of treatment options beyond recommendations for lifestyle changes:
“That’s another thing, like what do you do once we find NAFLD, just like more of the same? Like, it’s important to eat healthy and get exercise. So…how much is this going to change management?”
IM physician #1
Barriers and Facilitators to Screening for NAFLD
Survey Data
The most frequent barriers to screening for NAFLD identified (Fig.) were competing and more pressing issues (75%) and lack of confidence in NAFLD management (63%) and screening (61.5%). Several respondents (59%) also felt that there was not enough time to address NAFLD. Compared with PCPs, endocrinologists (1% vs 17%, P = .005) felt that identifying NAFLD was outside their responsibility.
Fig.
Barriers to screening for nonalcoholic fatty liver disease. The percent of respondents reporting barrier to screening is shown by specialty. The solid black represents primary care, the dashed line represents primary care subspecialties including geriatrics and infectious disease (ID)/human immunodeficiency virus (HIV) primary care. *Statistically significant at P < .05.
Qualitative Interviews
We identified 2 themes related to barriers and facilitators to screening for NAFLD: (1) competing demands with a complex patient population and (2) a need for easier ways to integrate screening into practice.
Participants expressed that there were too many active, competing demands during clinical encounters that require more urgent attention than screening for NAFLD:
“So, it tends to be like duly noted, but I’m trying to put out active fires.”
FM physician #1
The difficulty prioritizing screening for NAFLD was exacerbated by limited time during clinic visits, particularly with a complex patient population:
“Our visits are 20 minutes, people often have four plus complaints, especially for an interpreter…it’s not always a lot of time to be looking at making sure that we’re up to date on everything…I think it’s a limiting factor often.”
FM physician #2
Additionally, a perception of screening for NAFLD as requiring additional discussion and explanation to patients compounded the difficulty of integrating screening into routine care.
Although concerns about benefits of screening existed, several clinicians felt that they would be more likely to incorporate NAFLD screening into practice if tools to offset time and cognitive burden existed. These included ways to identify patients who may benefit from screening for fibrosis and reminders to screen within the EHR:
“Anything that just reduces this mental load for PCPs is going to really increase the uptake. And often there’s questions about like which ultrasound do I order? What labs do I order? And if it’s already there, and as long as it’s not like you can’t override it, that is going to really increase it.”
FM physician #1
However, participants had clear preferences about the format of screening reminders. EHR best practice advisories (BPAs) that required multiple steps to navigate were perceived negatively. Instead, clinicians preferred alternative reminders including the use of the Epic Health Maintenance activity, which can be used to identify patients with specific conditions or risk factors for routine care activities:
“Maybe it would come up on their healthcare management list. I do check that. The pop-ups are really annoying…but I do check the healthcare management list all the time, and if it’s on there, then I would definitely do it…[BPAs] I can’t get rid of them, it takes me so long. And a lot of times, I find that they have been done, but there’s still the pop-up or…it’s not something that I’m doing that day…and it takes me so long to make it go away.”
IM NP #1
Alternatively, some preferred to create their own systems to remind them of necessary activities including the use of smart phrases and templated notes.
Discussion
In this mixed-methods study of PCPs, primary care subspecialists, and endocrinologists at an urban safety-net hospital, we identified multiple barriers to screening, including low knowledge regarding screening modalities and practice guidelines, perceived lack of disease-focused treatment options, competing priorities during visits, and beliefs about responsibility for screening. Although participants felt that NAFLD screening should occur in primary care, barriers prevent clinicians from screening and generate fear of underdiagnosing NAFLD.
Our survey findings are consistent with a previous U.S. study of PCPs and subspecialists that showed low knowledge of risk factors for NAFLD outside of T2DM and overweight/obesity.12 The barriers we identified to screening for NAFLD within a U.S. urban safety-net hospital are similar to those identified in previous studies conducted outside the US.18,19 The findings overall suggest that knowledge gaps need to be targeted to effect behavior change and increase screening for NAFLD.
Although few previous studies outside the United States have included endocrinologists and diabetologists,18,20 unique to our study was the finding that endocrinologists had low confidence in their ability to screen for and manage NAFLD and felt that this was beyond the scope of their professional responsibilities. This is juxtaposed with our finding of higher rates of knowledge about risk factors among endocrinologists and a clinical practice enriched with individuals at high risk of NAFLD. It is also directly in contrast with the clinical practice guidelines from diabetes- and endocrinology-specific organizations, including the American Diabetes Association Standards of Care21 and American Association of Clinical Endocrinology guidelines on the diagnosis and management of NAFLD,4 which recommend screening for NAFLD and the use of noninvasive risk stratification.
Until 2022, the clinical practice guidelines from U.S. professional societies, including the American Diabetes Association21 and American Association for the Study of Liver Diseases,22 had not recommended NAFLD screening for high-risk groups without abnormal liver function test results or imaging demonstrating hepatic steatosis. This was in contrast to the international practice guidelines.23 Before completion of qualitative interviews for this study, the American Association of Clinical Endocrinology in conjunction with the American Association for the Study of Liver Diseases published new guidelines for the diagnosis and management of NAFLD in primary care and endocrinology4 broadening screening recommendations. Considering new evidence and these recently published guidelines, our study adds to the literature by identifying current barriers to NAFLD screening, allowing for the identification of implementation strategies that may be more effective at improving uptake of NAFLD screening in clinical settings with populations at increased risk.
Based on the results of our study, implementation strategies24 that may prove effective for increasing screening rates for NAFLD include strategies focused on training and educating stakeholders. However, our interviews suggest that knowledge about screening is necessary but insufficient unless clinicians are educated about treatment options. Our findings revealed the perception that there may be limited benefit to screening given a belief that no available treatments apart from modification of risk factors, such as encouraging weight loss, exist. Thus, several clinicians appeared to be unaware of both established and emerging evidence for benefit of several drug classes25-27 in NAFLD. Additionally, our qualitative findings regarding screening prioritization and screening as nonnormative practice suggest that present and status quo biases influence decisions to screen for NAFLD and strategies from behavioral economics aimed to overcome these biases including changes to choice architecture are helpful.28 To that end, our interviews explored EHR features that could support NAFLD screening. Clinicians welcomed reminders to screen given competing priorities. However, BPAs were not preferred, and instead, clinicians preferred nonintrusive or self-developed reminders. Although the clinicians who we interviewed did not routinely screen for NAFLD, many obtained liver function test results at least annually, indicating that integrating a risk calculator into the EHR using the Fibrosis-4 score may not require much change in clinical practice because clinicians are already obtaining the laboratory test results required for this calculation.
This study has several strengths and weaknesses. To our knowledge, this is the first study to evaluate clinicians’ knowledge, attitudes, practices, and barriers to screening for NAFLD in an urban safety-net health care setting in the United States, an important practice setting given the disproportionate burden of NAFLD and metabolic risk factors for NAFLD in Black and Hispanic communities. In addition, the sequential explanatory design allowed for greater depth of understanding of the barriers to uptake of screening for NAFLD in primary care and endocrinology than would have been possible through a survey alone. The limitations of this study include the single-center nature and survey completion response rate of 36.5%, although this is similar to the response rate in other studies. Possible reasons for the low survey response rate among primary care clinicians include the uncompensated nature of the survey, low interest in NAFLD and screening for NAFLD, and potential beliefs about an additional condition that would require screening and management. A convenience sample participated in semistructured interviews; these participants may be more interested in NAFLD than the overall population surveyed. Although we were unable to confirm that we had achieved thematic saturation given the smaller number of participants in our convenience sample, our qualitative and quantitative findings were consistent, suggesting validity of the themes we observed. Our results are likely transferrable to other urban safety-net health care systems but may not be generalizable to broader settings.
Conclusions
Our study identified knowledge gaps and beliefs about professional responsibility as barriers to screening for NAFLD in primary care and endocrinology. Implementation strategies focused on education and modifying social norms may help increase screening. Should health systems use EHR-based strategies as a method to increase screening for NAFLD, attention to clinician preferences should be considered in the design and implementation.
Disclosure
M.T.L. is a full-time employee of Novo Nordisk but at the time of study completion was not employed by this company. A.M. has received research grants from Gilead Sciences and NASHNET (paid to Boston Medical Center) and has served on an advisory board for Gilead Sciences. The other authors have no conflicts of interest to disclose.
Supplementary Material
Highlights.
Screening for NAFLD is not considered normative practice in safety-net primary care
The reported use of noninvasive tests for fibrosis risk stratification is uncommon
Screening and management knowledge gaps may hinder uptake of recent guidelines
Clinical Relevance.
Clinical guidelines have expanded the indications for nonalcoholic fatty liver disease (NAFLD) screening. This mixed-methods study revealed that knowledge gaps related to NAFLD screening and management may limit guideline uptake by primary care and endocrinology. Strategies to train, educate, and support clinicians in NAFLD screening and management may increase screening behavior.
Acknowledgment
This study was supported by Gilead Sciences (protocol number IN-US-989-5880 (M.T.L. and A.M.). Gilead Sciences did not have a role in the study design, analysis, interpretation of the data, and drafting of the manuscript. Effort on this study and manuscript were also made possible for K.L.F. and K.A. by the Boston University Clinical & Translational Science Institute (award number 1UL1TR001430).
Abbreviations:
- BPA
best practice advisory
- EHR
electronic health record
- FM
family medicine
- HIV
human immunodeficiency virus
- IM
internal medicine
- NAFLD
nonalcoholic fatty liver disease
- NP
nurse practitioner
- PCP
primary care provider
- TAM
technology acceptance model
- TDF
theoretical domains framework
- T2DM
type 2 diabetes mellitus
References
- 1.Younossi ZM, Koenig AB, Abdelatif D, Fazel Y, Henry L, Wymer M. Global epidemiology of nonalcoholic fatty liver disease-meta-analytic assessment of prevalence, incidence, and outcomes. Hepatology. 2016;64(1):73–84. 10.1002/hep.28431 [DOI] [PubMed] [Google Scholar]
- 2.Wong RJ, Aguilar M, Cheung R, et al. Nonalcoholic steatohepatitis is the second leading etiology of liver disease among adults awaiting liver transplantation in the United States. Gastroenterology. 2015;148(3):547–555. 10.1053/j.gastro.2014.11.039 [DOI] [PubMed] [Google Scholar]
- 3.Petrelli F, Manara M, Colombo S, et al. Hepatocellular carcinoma in patients with nonalcoholic fatty liver disease: a systematic review and meta-analysis: HCC and Steatosis or Steatohepatitis. Neoplasia. 2022;30:100809. 10.1016/j.neo.2022.100809 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Cusi K, Isaacs S, Barb D, et al. American Association of Clinical Endocrinology clinical practice guideline for the diagnosis and management of nonalcoholic fatty liver disease in primary care and endocrinology clinical settings: cosponsored by the American Association for the Study of Liver Diseases (AASLD). Endocr Pract. 2022;28(5):528–562. 10.1016/j.eprac.2022.03.010 [DOI] [PubMed] [Google Scholar]
- 5.Rinella ME, Neuschwander-Tetri BA, Siddiqui MS, et al. AASLD practice guidance on the clinical assessment and management of nonalcoholic fatty liver disease. Hepatology. 2023;77(5):1797–1835. 10.1097/HEP.0000000000000323 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6.European Association for the Study of the Liver (EASL), European Association for the Study of Diabetes (EASD), European Association for the Study of Obesity (EASO). EASL-EASD-EASO clinical practice guidelines for the management of non-alcoholic fatty liver disease. J Hepatol. 2016;64(6):1388–1402. 10.1016/j.jhep.2015.11.004 [DOI] [PubMed] [Google Scholar]
- 7.Alexander M, Loomis AK, Fairburn-Beech J, et al. Real-world data reveal a diagnostic gap in non-alcoholic fatty liver disease. BMC Med. 2018;16(1):130. 10.1186/s12916-018-1103-x [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Talens M, Tumas N, Lazarus JV, Benach J, Pericâs JM. What do we know about inequalities in NAFLD distribution and outcomes? A scoping review. J Clin Med. 2021;10(21):5019. 10.3390/jcm10215019 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.Weston SR, Leyden W, Murphy R, et al. Racial and ethnic distribution of nonalcoholic fatty liver in persons with newly diagnosed chronic liver disease. Hepatology. 2005;41(2):372–379. 10.1002/hep.20554 [DOI] [PubMed] [Google Scholar]
- 10.Balasubramanian BA, Garcia MP, Corley DA, et al. Racial/ethnic differences in obesity and comorbidities between safety-net- and non safety-net integrated health systems. Med (Baltim). 2017;96(11):e6326. 10.1097/MD.0000000000006326 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.Huynh MP, Bradshaw PT, Tana MM, Rachocki C, Somsouk M. Obesity and metabolic outcomes in a safety-net health system. Biodemography Soc Biol. 2020;65(3):257–267. 10.1080/19485565.2020.1765732 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Saeed N, Glass LM, Habbal H, et al. Primary care and referring physician perspectives on non-alcoholic fatty liver disease management: a nationwide survey. Therap Adv Gastroenterol. 2021;14:17562848211042200. 10.1177/17562848211042200 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.World Health Organization. Advocacy, communication and social mobilization for TB control: a guide to developing knowledge, attitude and practice surveys. World Health Organization; 2008. [Google Scholar]
- 14.Harris PA, Taylor R, Thielke R, Payne J, Gonzalez N, Conde JG. Research electronic data capture (REDCap)-—da metadata-driven methodology and workflow process for providing translational research informatics support. J Biomed Inform. 2009;42(2):377–381. 10.1016/j.jbi.2008.08.010 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Cane J, O’Connor D, Michie S. Validation of the theoretical domains framework for use in behaviour change and implementation research. Implement Sci. 2012;7:37. 10.1186/1748-5908-7-37 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16.Venkatesh V, Morris MG, Davis GB, Davis FD. User acceptance of information technology: toward a unified view. MIS Q. 2003;27(3):425–478. 10.2307/30036540 [DOI] [Google Scholar]
- 17.Braun V, Clarke V. Using thematic analysis in psychology. Qual Res Psychol. 2006;3(2):77–101. 10.1191/1478088706qp063oa [DOI] [Google Scholar]
- 18.Gracen L, Hayward KL, Aikebuse M, et al. An exploration of barriers and facilitators to implementing a nonalcoholic fatty liver disease pathway for people with type 2 diabetes in primary care. Diabet Med. 2022;39(6):e14799. 10.1111/dme.14799 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19.Vali Y, Eijk R, Hicks T, et al. Clinicians’ perspectives on barriers and facilitators for the adoption of non-invasive liver tests for NAFLD: a mixed-method study. J Clin Med. 2022;11(10):2707. 10.3390/jcm11102707 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20.Hallsworth K, Dombrowski SU, McPherson S, Anstee QM, Avery L. Using the theoretical domains framework to identify barriers and enabling factors to implementation of guidance for the diagnosis and management of nonalcoholic fatty liver disease: a qualitative study. Transl Behav Med. 2021;10(4):1016–1030. 10.1093/tbm/ibz080 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21.American Diabetes Association Professional Practice Committee. 4. Comprehensive medical evaluation and assessment of comorbidities: standards of medical care in diabetes-2022. Diabetes Care. 2022;45(Suppl 1):S46–S59. 10.2337/dc22-S004 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22.Chalasani N, Younossi Z, Lavine JE, et al. The diagnosis and management of nonalcoholic fatty liver disease: practice guidance from the American Association for the Study of Liver Diseases. Hepatology. 2018;67(1):328–357. 10.1002/hep.29367 [DOI] [PubMed] [Google Scholar]
- 23.Schattenberg JM, Anstee QM, Caussy C, Bugianesi E, Popovic B. Differences between current clinical guidelines for screening, diagnosis and management of nonalcoholic fatty liver disease and real-world practice: a targeted literature review. Expert Rev Gastroenterol Hepatol. 2021;15(11):1253–1266. 10.1080/17474124.2021.1974295 [DOI] [PubMed] [Google Scholar]
- 24.Waltz TJ, Powell BJ, Matthieu MM, et al. Use of concept mapping to characterize relationships among implementation strategies and assess their feasibility and importance: results from the Expert Recommendations for Implementing Change (ERIC) study. Implement Sci. 2015;10(1):109. 10.1186/s13012-015-0295-0 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25.Vadarlis A, Antza C, Bakaloudi DR, et al. Systematic review with meta-analysis: the effect of vitamin E supplementation in adult patients with non-alcoholic fatty liver disease. J Gastroenterol Hepatol. 2021;36(2):311–319. 10.1111/jgh.15221 [DOI] [PubMed] [Google Scholar]
- 26.Lian J, Fu J. Pioglitazone for NAFLD patients with prediabetes or type 2 diabetes mellitus: a meta-analysis. Front Endocrinol (Lausanne). 2021;12:615409. 10.3389/fendo.2021.615409 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 27.Wong C, Lee MH, Yaow CYL, et al. Glucagon-like peptide-1 receptor agonists for non-alcoholic fatty liver disease in type 2 diabetes: a meta-analysis. Front Endocrinol (Lausanne). 2021;12:609110. 10.3389/fendo.2021.609110 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 28.Reed KL, Harvey EM, Everly CJ. The intersection of behavioral economics and the general medicine literature. Am J Med. 2021;134(11):1350–1356.e2. 10.1016/j.amjmed.2021.06.041 [DOI] [PubMed] [Google Scholar]
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