Lessons learned from the diversity of thyroid nodule practice

There are so many different approaches to the same diseases in thyroid fine-needle aspiration (FNA) cytology among us (Table 1), and these have been highlighted in a recent commentary by Hirokawa et al.1 The diversity in medical practice is not due to economic conditions alone, and the best example that we have recently witnessed is the coronavirus disease 2019 (COVID-19) pandemic. The COVID-19 pandemic has revealed several differences between Asian and Western countries in medical practice and health care management. Asian countries such as China, Japan, South Korea, Taiwan, Thailand, and Vietnam demonstrated relatively low mortality rates in comparison with Western countries. This disparity can be attributed to diverse public health strategies, including the rapid implementation of widespread testing, contact tracing, strict quarantine measures, and effective public communication. In some instances, Asian countries were able to allocate resources more efficiently, and this led to better outcomes in terms of mortality rates. This highlights the importance of resource management in navigating health care crises. By March 29, 2023, the World Health Organization’s COVID-19 dashboard had recorded 6,887,000 deaths among 761,402,282 patients (the cumulative total) and an average mortality rate of 0.905%.2 In response to the COVID-19 pandemic, various strategies were adopted among countries. In high-income countries with a high Global Health Security Index (GHSI),3 mortality rates were not consistently low. High-income and high-GHSI countries in North America had mortality rates (1.123 in Canada and 1.188 in the United States) that were above the international average (0.905) and not well controlled. On the other hand, the mortality rates of some Asian countries were relatively low (0.111 in South Korea, 0.122 in China, 0.221 in Japan, 0.375 in Vietnam, and 0.718 in Thailand2 as well as 0.183 in Taiwan).4 The diversity in mortality rates was due to various factors, including antivirus measures and health care resources such as medical budgets and health insurance systems. Asian countries have low GHSIs (65.4 in South Korea, 45.7 in China, 60.5 in Japan, 42.9 in Vietnam, and 68.2 in Thailand) in comparison with the United States (75.9) and Canada (69.8). Thus, economic conditions alone are not the only important factor, and other factors contribute to cost-efficiently achieving the best clinical practice. The COVID-19 pandemic highlighted differences in health care resource allocation between Asian and Western countries. Asian countries may prioritize cost-effective solutions to achieve the best clinical practice, whereas Western countries may have greater access to advanced diagnostic tools and techniques. Therefore, it is reasonable to expect differences in medical practice between Asian and Western countries in the field of thyroid cytopathology. These differences may arise from various factors, including health care resource allocation, cultural perspectives, accessibility to advanced diagnostic techniques, and the emphasis on cost-effectiveness in health care. Cultural factors and patient preferences may also contribute to differences in medical practice between Asian and Western countries. For example, patients in Asian countries may be more accepting of watchful waiting or active surveillance as a management approach for thyroid nodules, whereas patients in Western countries may prefer more aggressive diagnostic and treatment options. One of us experienced a challenging situation when acting as a reviewer for a prominent thyroid journal. He positively reviewed a study that examined the use of repeat FNA in the assessment of indeterminate thyroid nodules. However, another reviewer had expressed confusion regarding the necessity of using repeat FNA in regions where gene panel tests are not readily available for patient triage before surgery. This second reviewer had taken issue with the author’s remark that “repeat FNA is more cost-effective in areas that do not have molecular testing” and claimed that this constituted an unacceptable justification for “bad science.” We believe that this researcher had a narrow perspective and was unable to appreciate alternative approaches to his or her own preferred method. Moreover, this reviewer did not seem to appreciate the importance of cost efficiency in health care, which is critical for most patients and society. The reviewer might have had a conflict of interest related to gene panel testing, which could have motivated him or her to dismiss alternative methods despite evidence showing that resection rates and malignancy risks in Western practices with molecular tests are equivalent to those in Asian practices without molecular tests.5 However, another possibility is that this reviewer might have been motivated by a fear of medical malpractice lawsuits stemming from missed diagnoses of cancer and thus preferred molecular testing as a means of avoiding such legal action. Embracing the existing diversity in thyroid nodule practice is crucial, and efforts should be made to promote mutual understanding among healthcare professionals. Previous publications by our group on diversity in thyroid nodule practice support this perspective.1, 5-14 Drawing from lessons learned from such diversity, we propose that opportunities exist for establishing a better reporting system, thyroid tumor classification, and clinical guidelines for thyroid nodules based on scientific evidence.15 Several variations, including the indication for FNA cytology, the handling of cystic fluid–only samples, the impact of noninvasive follicular thyroid neoplasm with papillary-like nuclear features (NIFTP), molecular testing for indeterminate thyroid nodules, and active surveillance for low-risk papillary thyroid microcarcinoma, are thoroughly examined in a recent commentary by Hirokawa et al.1 and an editorial by Nishino.16 Here, we focus on the malpractice climate and the low threshold for RAS-like nuclear features (RAS-like dysplasia). The relationship between the malpractice climate and a low diagnostic threshold for malignancy is complex and multifaceted. On the one hand, a high-risk malpractice climate may encourage physicians to adopt a more cautious approach to diagnosis and lead to a lower threshold for considering malignancy as a possible diagnosis, which may result in the earlier detection and treatment of cancer and potentially improve patient outcomes. However, a low diagnostic threshold for malignancy may also have negative consequences. It may lead to overdiagnosis and overtreatment as well as unnecessary costs for patients and society. Moreover, a low diagnostic threshold may lead to defensive medical practices, where physicians order more tests and procedures than are strictly necessary to protect themselves from litigation. This can contribute to the overuse of health care resources and may not necessarily result in improved patient outcomes. Although a high-risk malpractice climate may encourage physicians to be more cautious in their diagnostic practices, it is important to strike a balance between responsible risk management and appropriate diagnostic thresholds. Clinicians should consider the potential benefits and risks of diagnostic tests and treatments and make decisions on the basis of the best available evidence and the individual needs of each patient. The fear of medical malpractice lawsuits can have a significant impact on pathology diagnosis. Pathologists are responsible for making accurate diagnoses of tissue samples, which are often critical for guiding patient care and treatment decisions. However, there is always the risk of diagnostic error, which can have serious consequences for patients and may lead to medical malpractice lawsuits. To avoid the risk of being sued, pathologists may feel pressured to be overly cautious and make conservative diagnoses, which can result in overdiagnosis and overtreatment. Conversely, pathologists may also feel pressured to be overly confident in their diagnoses, and this can lead to underdiagnosis and missed opportunities for proper treatment. This pressure can lead to defensive medicine practices, where pathologists may order additional tests or seek second opinions to protect themselves from litigation. Moreover, the fear of medical malpractice lawsuits may also lead to overreliance on molecular testing and other advanced diagnostic techniques, which can be more expensive and may not always be necessary or appropriate for all patients. This can result in higher health care costs and may contribute to the overuse of health care resources. Therefore, it is important to balance responsible diagnostic practices and appropriate risk management in the face of potential litigation. Mehrzad et al.18 in the United States reviewed 851 patients who underwent surgery between January 1, 2004, and December 31, 2013. The incidence of follicular variant of papillary thyroid carcinoma (FV-PTC) increased approximately 4-fold, whereas the incidence of follicular adenoma (FA) decreased in a reverse fashion; this resulted in a more than 10-fold increase in the FV-PTC/FA ratio. They suggested that some tumors previously diagnosed as FA are increasingly being classified as FV-PTC (particularly noninvasive FV-PTC). Furthermore, some tumors currently classified as FV-PTC may be overdiagnosed as cancer and treated more aggressively than needed if the increased incidence of FV-PTC reflects a lowered threshold for the diagnosis of FV-PTC. Widder et al.19 in Canada reported that when two pathologists re-reviewed their 185 histological samples (the original diagnoses were benign [n = 118], FV-PTC [n = 56], and follicular thyroid carcinoma [FTC; n = 11]), 46 patients (25%) had a change in diagnosis on re-review. Thirty-five of the 46 cases were reclassified from a benign diagnosis to a re-reviewed malignant diagnosis, with five reclassified as minimally invasive FTC, four reclassified as occult PTC, and 26 (74%) reclassified as FV-PTC. None of the 26 reclassified FV-PTCs had evidence of recurrence or persistent disease after a mean follow-up period of 105 months. They concluded that there had been no clinical ramifications for the patients with a changed diagnosis. We believe that the majority of these FV-PTCs could have been biologically benign NIFTPs or well-differentiated tumors of uncertain malignant potential. Cipriani et al.20 in the United States reviewed 66 cases of FTC diagnosed between 1965 and 2007 and evaluated their long-term survival and recurrences. Their histological review changed the diagnoses in 24 cases (36%) to PTC, in 18 cases (27%) to FA, and in 5 cases (8%) to poorly differentiated carcinomas. Only 19 (29%) maintained their original FTC diagnosis. There were no cancer-specific deaths in the FA or PTC groups. We believe that the majority of their PTCs reclassified from FTCs were encapsulated FV-PTCs or biologically benign well-differentiated tumors of uncertain malignant potential, as there were no cancer-specific deaths in this group. Delicate nuclear changes (nuclear enlargement, nuclear membrane irregularity, and chromatin clearing as defined by Nikiforov et al.21) can be found in RAS-like tumors, which are FAs (nuclear score [NS]: 0–1), NIFTPs (NS: 2–3), FV-PTCs (NS: 2–3), FTCs (NS: 0–1), high-grade well-differentiated carcinomas (NS: 0–3), and poorly differentiated carcinomas (NS: 0–1). They are called PTC-type nuclear features in Western pathology practices, in the third edition of the World Health Organization classification of thyroid tumors,22 and in the Bethesda System for Reporting Thyroid Cytopathology.23 They were diagnostic for PTC-type malignancies even though they were subtle in noninvasive and encapsulated follicular-pattern thyroid nodules.21-23 In recent years, the diagnostic threshold for RAS-like PTC nuclear features has been lowered in North American pathology practices,17 and this has been attributed to the malpractice climate.24-26 The tendency to overdiagnose FV-PTC in the United States was thoroughly discussed by Renshaw and Gould.26 The lower threshold for RAS-like dysplasia in North America has resulted in large differences between Eastern and Western thyroid pathology communities and an increased incidence of NIFTP and FV-PTC in North America.8, 9, 13, 14 By gaining a better understanding of the diverse medical practices across countries, pathologists can enhance their cultural competency and improve their ability to diagnose and manage thyroid nodules in patients from different backgrounds. We plan to publish the third edition of a unique thyroid FNA textbook this year.15 Unlike other existing textbooks on thyroid FNA cytology that focus on a single country, our textbook incorporates critical opinions and perspectives from various countries to provide valuable insights into alternative approaches to thyroid FNA cytology. It focuses on providing alternative approaches and insights from multiple countries to facilitate better communication and understanding among health care providers with different backgrounds. This could ultimately lead to improved patient care outcomes and better overall health care delivery. We hope that publishing a textbook that embraces diversity and promotes critical thinking in thyroid FNA cytology will benefit pathologists who perform this procedure. The authors thank all the members of the Asian Working Group on Thyroid Pathology/Cytology for their generous support and collaborations on thyroid disease studies. The authors declare no conflicts of interest. Kennichi Kakudo, MD, PhD, is a consultant pathologist at Izumi City General Hospital (Izumi, Japan) and is the director of the Cancer Genome Center and Thyroid Disease Center. He is an emeritus professor at Wakayama University Medical School. His scientific contributions have been published in more than 300 peer-reviewed papers covering borderline thyroid tumors, intrathyroidal thymic carcinoma, C-cell carcinoma, prognostic risk classification of thyroid carcinoma using the Ki67 labeling index, and immunoglobulin G4 thyroiditis. He is an author of the fourth and fifth editions of the World Health Organization classification of thyroid tumors as well as clinical guidelines by the Japanese Thyroid Association, including its reporting system for thyroid fine-needle aspiration cytology. His is a founding member and the first president of the Asian Thyroid Pathology/Cytology Working Group. Zhiyan Liu, MD, PhD, is the director of the Department of Pathology of Shanghai Sixth People’s Hospital (affiliated with the Shanghai Jiao Tong University School of Medicine). She received her PhD from Wakayama Medical College in 2011, and she was a visiting scholar at the University of Michigan in 2018. She performs general surgical pathology, thyroid fine-needle aspiration cytology, and predominantly endocrine pathology. Her research work focuses on the initiation and progression of endocrine tumors (especially thyroid tumors). Chan Kwon Jung, MD, PhD, is a professor of pathology at Seoul St. Mary’s Hospital (Catholic University of Korea). His research encompasses both basic and clinical investigations across a diverse range of topics, including the thyroid, lungs, gastrointestinal tract, bones, and soft tissues. His main fields of expertise are thyroid pathology/cytopathology, molecular pathology, and digital pathology. Dr Jung served as a coauthor on the fifth edition of the World Health Organization classification of thyroid tumors and has published more than 300 peer-reviewed articles. He is currently editor-in-chief for the Journal of Pathology and Translational Medicine and an associate editor for Endocrine Pathology and serves on the editorial boards of Thyroid, Cancers, and the Journal of Korean Medical Science. Dr Jung is actively involved in collaborative projects with the Working Group of Asian Thyroid Cytology. Chiung-Ru Lai, MD, has been the president of the Taiwan Society of Clinical Cytology (2015–2021) and the Taiwan Society of Pathology (2017–2023) and the chairperson of the Taiwan Gynecology Pathology Study Group (2015–2019), and she has been responsible for the national quality assurance program for cytopathology and for the cervical cancer screening policy in Taiwan for more than 20 years. She is the regional editor of Acta Cytologica and also serves as an editorial board member of Diagnostic Cytopathology. She is one of the members of the National Cancer Policy Committee and the advisory board for national regulations for laboratory-developed tests.

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