Future trends in hepatology: Challenges and opportunities
Authors: Vinod K. Rustgi, Gary L. Davis, Steven K. Herrine, Arthur J. McCullough, Scott L. Friedman, Gregory J. Gores
Journal: Hepatology (2008)

As a professional society, the American Association for the Study of Liver Diseases (AASLD) is an important instrument for coordinating and focusing the professional objectives of hepatology. As a prelude to an AASLD-sponsored strategic planning initiative, a Future Trends Meeting was convened on January 4-5, 2008. The focus was on the burden of liver disease, the current status of AASLD U.S. physician members, external forces shaping the profession, and manpower/training paradigms. Despite enormous advances in the prevention, diagnosis, and therapy of patients with liver diseases, the burden of liver disease in the United States is substantial. There is an unmet public health need for professional expertise in liver diseases, which is not addressed by current training paradigms. New models of care are needed, funding challenges for sustaining hepatologists need to be addressed, and new training paradigms conceived and implemented. The information reviewed and emerging solutions developed to address the above challenges are reviewed herein. As a new AASLD strategic plan emerges to further refine the concepts developed at this meeting, it will be published in a separate document. Despite advances in diagnosis, disease-specific interventions, and hospital care, liver-related mortality has remained relatively stable over the last 30 years while overall mortality in patients with liver disease has declined slightly.1 Much of the overall mortality is due to reduction in deaths due to gallstone disease and gallbladder cancer.1 Overall liver-related mortality rate exclusive of gallbladder disease has remained relatively stable during this time, though chronic liver disease mortality declined from 1979 to 2004 and has remained steady since that time.1 The factors involved in these trends are complex and vary by the cause of liver disease. Hepatitis A virus (HAV) is the most common cause of clinically apparent acute viral hepatitis, accounting for about half of cases.2 However, the estimated incidence of acute HAV infection and its age-adjusted mortality have fallen dramatically during the last decade.1, 2 HAV vaccine is highly efficacious, and its more widespread use would result in further reductions of the infection. Although acute HAV infection can result in considerable short-term morbidity, particularly in adults, it does not result in chronic liver disease and therefore its contribution to healthcare resource utilization has declined significantly. Hepatitis B virus (HBV) is the most common cause of acute hepatitis virus infection and is estimated to account for about a third of clinically apparent cases of acute hepatitis.3 The incidence has declined over the last two decades, probably as a result of widespread vaccine use in high-risk groups and reduction in high-risk behaviors. A variable proportion of acute cases develop chronic infection, and it is estimated that about 1.25 million persons in the United States have chronic hepatitis B.2 This number may be rising as a result of immigration from areas where the infection is endemic. Indeed, the prevalence of chronic HBV infection may be as high as 9%–21% among Asian immigrants.4, 5 Nonetheless, age-adjusted mortality and the number of patients requiring liver transplant for advanced hepatitis B are declining, which are likely attributable to the availability and effectiveness of antiviral drugs.6 On the other hand, data from the National Ambulatory Medical Care Survey (NAMCS), National Hospital Ambulatory Medical Care Survey (NHAMCS), and the National Hospital Discharge Survey (NHDS)7 all indicate that HBV-related disease is accounting for an increasing number of clinic and hospital visits, most likely due to the high prevalence of chronic infection and new treatment options. The discovery of the hepatitis C virus (HCV) in 1989, which enabled screening of blood products, resulted in a marked fall in the incidence of new infection beginning in 1990.1-3 However, a large proportion of acutely infected individuals develop chronic hepatitis, resulting in an estimated 2.7 million to 5 million infected persons in the United States.8, 9 As a consequence of ever-improving antiviral therapies, the number of ambulatory care visits and inpatient admissions have more than doubled since 1990.7 Disease modeling predicted a surge in HCV-related morbidity and mortality over the first two to three decades of this century, which is now being realized, although recent mortality data suggests that the trend may be reaching a plateau.2, 10, 11 Furthermore, the number of liver transplants for complications of chronic hepatitis C has remained relatively stable since 2000.12 Hepatocellular carcinoma (HCC) accounts for 662,000 deaths worldwide per year and is the third leading cause of cancer-related death.12 In the United States, HCC currently accounts for only about 16,000 or 2.9% of cancer deaths.13 However, the age-adjusted incidence has more than doubled in the last 20 years.14 The overwhelming majority of HCC occurs in patients with chronic viral hepatitis13, 15 and the recent increase is driven by the high prevalence of chronic HCV infection.10, 11 The average annual risk of HCC is 3.2% in patients with cirrhosis from HCV.16, 17 The annual risk is also high in patients with chronic HBV infection, ranging from 0.1%–1.0% among patients positive for hepatitis B surface antigen who did not have cirrhosis to 2.2%–3.2% in patients with cirrhosis.17 Loss of detectable HBV or HCV with antiviral therapy decreases the risk of subsequent HCC, but does not eliminate it.18, 19 The Surveillance Epidemiology and End Results database reports that 76%–95% of patients with HCC die as a direct consequence of tumor progression.14 In fact, HCC now accounts for 50%–70% of liver-related mortality.20, 21 The prevalence of obesity has more than doubled in the United States over the last 30 years and is now at least 35%.22 Nonalcoholic fatty liver disease (NAFLD) is commonly associated with obesity and/or accompanying metabolic syndrome. It has been estimated that 10% of children and adolescents and 34% of adults have hepatic steatosis.23, 24 Steatosis or steatohepatitis are present in 65% and 20% of obese individuals, and in 90% and 50% of the morbidly obese (body mass index ≥ 40 kg/m2), respectively. Those with central obesity have a hazard ratio of 2.2 for death due to cirrhosis.25 Overall, patients with NAFLD have reduced long-term survival, with liver disease accounting for about 10% of overall mortality, surpassed only by malignancy and cardiovascular deaths.26, 27 Clearly, it appears that NAFLD will become a more prevalent problem in coming years. The above analysis indicates that the burden of chronic viral liver diseases is substantial and translates into a significant public health problem. Therapies for these diseases have become increasingly complex and require special expertise. The emergence of hepatobiliary neoplasia and NAFLD as public health problems also will require additional medical resources. Although predictions regarding the future are difficult because they can be dramatically altered by disruptive technologies (for example, percutaneous ablation) and therapies, the future demand for hepatology expertise and manpower is likely to grow. The future U.S. physician manpower need is currently an area of controversy.28, 29 AASLD, American Association for the Study of Liver Diseases; ABIM, American Board of Internal Medicine; ACGME, American College of Graduate Medical Education; HAV, hepatitis A virus; HBV, hepatitis B virus; HCC, hepatocellular carcinoma; HCV, hepatitis C virus; NAFLD, nonalcoholic fatty liver disease; NIH, National Institutes of Health; PQRI, Physician Quality Reporting Initiative. Although there were 3,362 dues-paying members in the AASLD in 2007, only 1,630 (46%) of these were U.S.-based physicians. Furthermore, only 52% of this U.S. physician membership considered the AASLD their primary professional societal affiliation based on a member survey. Consistent with this information, only 55% of members indicate that more than 50% of their clinical practice was solely focused on patients with liver disease. A majority of the membership have an academic appointment and participate in a liver transplant program. Although the majority of AASLD members are in academic institutions, only a small minority conduct laboratory-based research (14%), whereas the majority view clinical care as a primary job description. Thus, although the majority of hepatologists are academic and transplant physicians, a large number practice combined gastroenterology and hepatology. Changes in training models (vide infra) must take this dual practice preference into account. The lack of individuals with careers in discovery-based research is of concern for the advancement of the profession. There is an unmet demand for transplant hepatologists. For example, as of September 2007, there were 45 advertised positions for hepatologists. The open positions were widely distributed throughout the United States. These data suggest that almost one-half of all United Network for Organ Sharing (UNOS)-approved liver transplant programs (124 as of April 14, 2008) are recruiting hepatologists. If all 36 American College of Graduate Medical Education (ACGME) training programs in transplant hepatology are successful in recruiting and training transplant hepatologists, these positions could be filled over the next several years. However, not all of the ACGME positions are currently filled, and retention of hepatology faculty is challenged by issues of work-life balance and remuneration. The demand for competent, well-trained hepatologists is likely to continue. To date, hepatologists are gastroenterologists who desire marketplace salaries commensurate with their training. Also, hepatologists are in demand, which further enhances their market value. The practice of hepatology is predominantly cognitive, and examination and management charges are insufficient to cover salaries. Yet, the downstream revenue from a hepatology practice is substantive.30 A wide variety of models for support of hepatologists have been developed to address these complex issues (Table 1). These models intertwine support from hospitals and transplant programs. All of these models have strengths and weaknesses in their implementation, and a universally accepted model does not exist. No direct support for hepatology Direct hospital support Indirect hospital support through a transplant program Direct support from transplant surgical departments Creation of a fiscally independent, multidisciplinary transplant institute or center Cross-subsidization of hepatology by proceduralists within divisions of gastroenterology Given the differentiation of hepatology from gastroenterology and its integration within transplant programs, a compelling rationale can be developed for the creation of independent hepatology divisions within departments of medicine. The strengths of these divisions are their focus on "all things liver" and the optimal integration of basic, translational, and clinical hepatology. The weaknesses are often their small size, which limits flexibility and financial solvency. Currently, there is no national consensus on the advisability of separate hepatology divisions. For those who practice hepatology outside of an academic institution, the majority practice outpatient hepatology with an integrated group practice or gastroenterology practice. From an analysis of a large midwestern gastroenterology group practice, Minnesota Gastroenterology, 10%–15% of all evaluation and management codes were hepatology codes. Care of hepatology patients in this practice was labor intensive (more than six visits per year versus two visits per year for gastroenterology patients). There is a significant financial disincentive to treat hepatology patients in the private practice setting because of the lower reimbursement (compared to endoscopy) and the necessity for chronic disease management. Also, the private practice is not a beneficiary of the hospitalized care of these patients who are usually referred to tertiary care centers for hospitalization. Models for health care delivery will need to incorporate these issues to provide adequate hepatology care for the U.S. population. Nonetheless, the opportunity for large, integrated gastroenterology (GI) practices to help solve the problem of treating liver patients is substantial. The combination of management tools, midlevel providers, creative contracts with third-party payers, and physicians with expertise and training in hepatology can help address these challenges. Quality measures and indices will affect the practice of hepatology in the future. Quality has been defined by the Institute of Medicine as the provision of care in a safe, effective, patient-centered, timely, efficient, and fair manner. Although the federal Health Care Quality Improvement Act was passed in 1986, the clarion call to change was instigated by the death of 39-year-old Boston Globe medical columnist Betsy Lehman from an accidental overdose of chemotherapy. The Institute of Medicine launched its quality initiative in 1996, publishing the seminal papers "To Err is Human," and "Crossing the Quality Chasm" in 1999 and 2001, respectively. With wide public awareness of the avoidable morbidity and mortality of medical errors, the U.S. Department of Health and Human Services redoubled its efforts to reduce such events. As part of the Tax Relief and Health Care Act of 2006, the Physician Quality Reporting Initiative (PQRI) was established by the Centers for Medicare and Medicaid Services. Intending to enhance the value of care provided to Medicare beneficiaries, the PQRI authorizes bonus payments for practitioners who voluntarily report on quality measures. The development of quality measures, which form the backbone of PQRI, is a process which continues to be shaped. Quality measures, as promulgated by PQRI, must be developed, as well as endorsedor adopted by a voluntary consensus standards body, defined as an entity that maintains openness, balance of interest, due process, an appeals process, and consensus. Once developed, measures must be endorsed by the National Quality Forum or adopted by the AQA Alliance (formerly the Ambulatory Care Quality Alliance) prior to inclusion in PQRI. As a member of the American Medical Association Physician Consortium for Performance Improvement, the AASLD (in collaboration with the American Gastroenterology Association [AGA] Institute) was involved in the development of measures related to the management of hepatitis C, which were adopted in the 2008 Medicare quality reporting program along with many other PQRI measures. The AASLD is also committed to the development of Patient Improvement Modules, instruments which are required in American Board of Internal Medicine (ABIM) Maintenance of Certification programs, and which may be helpful in the development of future quality measures suitable for submission to PQRI. As the Centers for Medicare and Medicaid Services changes from a passive payer to active purchaser of services, incentives for higher resource utilization without regard to patient outcomes or quality of care will vanish. As a result, the development, endorsement, and implementation of quality measures will continue to expand, becoming an integral part of health care delivery. Hepatologists and the AASLD must be proactive and participate in this process. Currently, the lack of focus on quality measures represents an unmet and critical professional opportunity in hepatology. Combined with an increasing prevalence of advanced liver disease and HCC due to the epidemics of viral hepatitis and obesity-related liver disease, advances in hepatology care have led to an unmet need for hepatology expertise that is likely to widen in the coming decade. Nonetheless, there are no reliable data defining what percentage of patients with liver disease are currently managed by appropriately trained individuals (either gastroenterologists or hepatologists). A compelling indicator of the unmet need are the dozens of unfilled faculty positions for transplant hepatologists in academic centers throughout the United States (see "Current Demand for Hepatologists" above). Still, more reliable data is urgently needed to assess whether patients with liver disease have adequate access to the most advanced, high-quality care. Nonetheless, it is clear that creative models are needed to address the unmet demand for specialized hepatology care. The formal development of an advanced hepatology training fellowship, a major significant step toward addressing this unmet need, was conceived by the AASLD with the cooperation of the related GI societies and ultimately approved by the Gastroenterology Board of the ABIM. This initiative followed a workforce study commissioned by the AASLD in 1998–1999 that helped establish hepatology as a distinct subdiscipline of gastroenterology. A standardized curriculum was established, certification status was granted by the ABIM, and training programs were approved by the ACGME. The effort was consummated with the first examination in Transplant Hepatology offered in November 2006. Two hundred sixty-one individuals sat for the examination, with 87% achieving a passing score certifying expertise in this discipline. Despite this momentous step toward increasing the training of hepatologists, a number of constraints continue to limit the emergence of an adequate workforce. Principal among these is the length of this advanced training, which requires individuals who are interested in hepatology at the time of their internal medicine residency to first complete a 3-year fellowship in gastroenterology, during which they must apply for separate hepatology training thereafter. Lengthened training of this type is viewed more broadly by the ABIM as a deterrent to U.S. medical school graduates choosing internal medicine and its subspecialities for their careers. Combined with mounting debt of many medical school graduates, the increasing demand for clinical gastroenterologists to meet the need for expanded colon cancer screening, and the increased remuneration for these positions, there is significant attrition in the number of trainees initially attracted to a career in hepatology who ultimately pursue this pathway. Moreover, acceptance into GI fellowship is intensely competitive at present, such that any candidate interested in hepatology who fails to obtain a fellowship slot in gastroenterology is effectively denied the chance to become a hepatologist through the conventional training route. With this background in mind, there is a growing impetus for further refinement in hepatology training to shorten its duration and increase the availability of specialists. If successful, such an effort is likely to improve the quality of care and accelerate further advances in the field. Although a number of potential pathways are possible, including direct entry in a hepatology training program after internal medicine residency, the most appealing option is to utilize the existing framework of a 3-year GI fellowship to offer more accelerated entry into advanced hepatology training within this 3-year period (Table 2). Specifically, candidates interested in a career in hepatology could indicate this interest in applying to designated fellowships that offer 1 year of general gastroenterology followed by 2 years of advanced hepatology training. Additional fellowship slots are envisioned to meet this need rather than redirecting current GI fellowship slots toward this purpose. The hepatology portion of the fellowship would eventually replace the current fourth-year advanced hepatology fellowship and incorporate all its curricular components. A specialized examination would be required to certify this advanced level of hepatology expertise, either as part of a customized GI fellowship examination or as a separate, complementary test akin to the current advanced hepatology examination. This hepatology track within a GI fellowship would yield a number of tangible advantages. It would: (1) shorten the overall training period for hepatology by 1 year; (2) allow hepatology trainees to begin their specialized liver training 2 years earlier than in the current training model; (3) obviate the need for a separate application to hepatology fellowship; (4) provide a grounding in general gastroenterology with proficiency in standard endoscopic procedures (upper endoscopy and colonoscopy) that are part of a typical hepatology/gastroenterology hybrid practice; and (5) offer a component for research, although additional training beyond this period would likely be required for laboratory-based trainees or those seeking advanced degrees in patient-based research (for example, Masters in Public Health or Masters in Clinical Research). This proposal is also consistent with the ABIM's goal of shortening training and accelerating the entry into the most specialized, last phase of clinical training. Moreover, this template for further subspecialty training within the 3-year GI fellowship period could be expanded by the GI Board of ABIM in partnership with related societies (AGA, American College of Gastroenterology, American Society for Gastrointestinal Endoscopy) to establish similar training programs in other subdisciplines, for example inflammatory bowel disease, motility, and advanced endoscopy, among others. This proposal would have no impact on trainees seeking training in general gastroenterology under the current fellowship format, which would continue to offer 30% of the training period in hepatology. Ongoing dialogue will be essential to further refine this proposal and adequately align the interests of key stakeholders including other GI-related societies, the ABIM, the American Board of Medical Specialties, and the ACGME, among others. Additional data are needed to quantify the current unmet need in specialized hepatology care. Nonetheless, there is rising impetus for change in the current hepatology training paradigm, and the AASLD is committed to providing responsive leadership in seeking creative solutions to the benefit of patients with liver disease. Hepatology represents a burgeoning field in academic medicine not only in the United States, but also throughout the world. There has been, and continues to be, robust growth in research, education, and clinical care. This degree of unprecedented historic growth and expansion has served to highlight the intrinsic strengths of hepatology as a broad-based discipline, and simultaneously, has focused attention on mechanisms to fund academic hepatology in medical centers. This perspective will dissect the opportunities for funding and the vehicles for navigating them. Recognizing that a plateau of the National Institutes of Health (NIH) budget ensued after an unparalleled doubling in the budget, it is nonetheless important to emphasize NIH grants as the prominent source of funding for scientists and clinicians engaged in basic, translational, population, and patient-oriented research in hepatology. Given the NIH Roadmap Initiatives and the National Institute of Diabetes and Digestive and Kidney Diseases (NIDDK) Action Plan for Liver Disease Research (http://www2.niddk.nih.gov/AboutNIDDK/ResearchAndPlanning/Liver_Disease/Action_Plan_For_Liver_Disease_Intro.htm), it is equally important to emphasize interdisciplinary research in liver and biliary diseases. Apart from R01 and related Program Project (P01), Center (P30), and consortium (U01) funding for investigators, it is critical to emphasize the identification and nurturing of fellows and junior faculty through NIH training grants, fellowships, and career development grants. Although it is natural to look to the NIH as the predominant source of federal funding, selective opportunities should be pursued through other federal agencies, such as the Veteran's Administration and Center for Diseases Control and Prevention. It will be increasingly important to complement federal funding sources through other vehicles. These relate to alliances with pharmaceutical and biotechnology companies and private philanthropy to support and foster investigator-initiated as well as programmatic efforts. The gastroenterology or hepatology division can play a great role in these endeavors given the wide prevalence and incidence of diseases such as viral hepatitis B and C, nonalcoholic steatohepatitis, fibrosis, cirrhosis, HCC, portal hypertension, and parallel considerations of liver transplantation. The unique roles of transplant hepatology, as a subdiscipline of hepatology, shape a number of complex interactions between hepatology, departments of medicine and surgery, transplantation centers, medical schools, and hospital/health system administration. Transplant hepatology fuels primary and downstream revenue gains, but the transplant hepatologists require subsidy as a platform for fiscal viability from a clinical perspective for either hepatology divisions or hepatology programs within gastroenterology divisions. These complex interactions should be pursued in a manner that is mutually beneficial to all involved parties, and plans need to be durable over time. Transient arrangements, namely those arranged from year to year, tend to be distracting and prevent long-term planning of faculty recruitment and retention. At the same time, hepatologists should also work to increase the fiscal viability of the specialty by broadening the reach of their practice through inclusion of hepatic oncology, imaging, and interventional procedures such as transjugular pressure measurements and transjugular intrahepatic portosystemic shunts. Academic hepatology is vibrant with a bright, energetic future. The explosion of new information from all sectors of research and clinical care and the need to groom future hepatologists through formalized education and training programs conspire to make hepatology attractive as a specialized discipline. Funding for academic hepatology needs to take into account traditional (federal, state, city) and nontraditional (industry, philanthropy) sources for research funding, as well as intrainstitutional collaborations and partnerships for clinical revenue allocation. These two cardinal features furnish a strong platform for hepatology. Long-term strategic planning is necessary to avoid transient solutions and intermittent fluctuations, because the latter result in disruptions in faculty development, recruitment, and retention, which in turn have adverse consequences on trainees. Academic hepatology is poised to play a prominent role in academic medical centers into the next decade. Unfortunately, current and projected NIH funding, by all assessments, will remain static. Furthermore, federal regulation of industry support for academic research is constrained and unlikely to change in the future, again based on various evaluations. These troubling factors pose a serious impediment to critical components of academic medicine, in particular as they relate to the recruitment and retention of junior faculty hepatologists, who are the very essence of the future of hepatology. Thus, there is an urgent and compelling imperative to diversify the sources of funding for research. To that end, fundraising through philanthropy needs to be a top priority. The creation and maintenance of revenue from philanthropy would permit the AASLD to endow research granting mechanisms for fellowships, junior faculty scholar awards, and bridge funding. Creation of a fundraising foundation under the auspices of the AASLD An annual budget for the fundraising foundation Goals for revenue generation Membership donations One can only surmise universal support for this venture so that AASLD can continue to carry out its mission as well as support its membership, particularly those who will constitute its future. The tremendous progress in the science and practice of hepatology in recent decades, fostered by the AASLD, is a great success story. Effective vaccines, antiviral therapies, liver transplantation, and the bounty of emerging diagnostics and therapies reflect important dividends from investment in basic and clinical research, and point toward a golden era in the specialty in the coming years. Yet, many challenges must be overcome to realize this potential. These include: (1) epidemiologic trends that portend a rising incidence in several types of chronic and neoplastic diseases; (2) growing disparities between the need for advanced hepatology care and the availability of adequately trained practitioners to provide it; (3) limited options for supporting the salaries of hepatologists whose practices do not include either transplant hepatology and/or endoscopic procedures, reflecting a lack of sufficient recognition of the highly cognitive, demanding nature of clinical hepatology; (4) a growing focus on defining and implementing quality measures; and (5) constrained extramural funding for basic, translational, and clinical research. Modify current training paradigms to accelerate the entry of motivated trainees into the specialty of hepatology, in order to expand the workforce to meet these growing needs. Support evolving practice paradigms and regulatory changes to more fully recognize the unique skill set and demands of clinical hepatology, which should promote revised metrics for reimbursement. Maintain a leading voice, in partnership with related societies and government agencies, in defining and implementing quality measures that will improve outcomes for patients with liver disease. Continue to seek new sources of research funding to complement the ongoing support from NIH and other federal agencies, in order to realize the research goals outlined in the NIH Action Plan for Liver Disease. These efforts will include new initiatives for independent fundraising by the AASLD from philanthropy and other sources, and partnership with sister organizations to create synergies that will accelerate basic, translational, and clinical research advances. These recommendations will be complemented by a Strategic Planning Initiative in 2009 to clarify priorities and optimize approaches to achieve these goals. The AASLD is committed to tackling these challenges and maximizing the opportunities with creativity and determination.