Cardiovascular Pathology 53 (2021) 107340 Contents lists available at ScienceDirect Cardiovascular Pathology journal homepage: www.elsevier.com/locate/carpath The illness and death of King George VI of England: the pathologists’ reassessment ✩,✩✩ Rolf F. Barth, MD 1,a,∗, L. Maximillian Buja, MD 2,a 1 Department of Pathology, The Ohio State University, Columbus, Ohio 43210, USA Department of Pathology and Laboratory Medicine, McGovern Medical School, The University of Texas Health and Science Center at Houston, Houston, Texas 77030, USA 2 a r t i c l e i n f o Article history: Received 11 March 2021 Revised 28 April 2021 Accepted 30 April 2021 Keywords: illness and death of King George VI coronary thrombosis vs lung cancer pulmonary embolus vs hemothorax a b s t r a c t The illness and death of King George VI has received renewed attention based on the events portrayed in the Netflix blockbuster series, The Crown. The King, a heavy smoker, underwent a left total pneumonectomy in September 1951 for what euphemistically was called "structural abnormalities" of his left lung, but what in reality was a carcinoma. His physicians withheld this diagnosis from him, the public, and the medical profession. The continuation of hemoptysis following surgery suggested that his cancer had spread to his right lung. Although he made a slow and uneventful recovery from his surgery, King George VI died suddenly and unexpectedly in his sleep on February 6, 1952, at the age of 56. Since the King had a history of peripheral vascular disease, it was assumed that the cause of death was a "coronary thrombosis." In this report, we explore the cardiovascular and oncologic findings relating to his illness and death and consider an alternative explanation for his demise, namely, that he may have died of complications from a carcinoma that had originated in his left lung and spread to his right lung, as evidenced by continued hemoptysis. We suggest that this possibly could have led to his sudden death due to either a pulmonary embolus or a massive intra-thoracic hemorrhage rather than a "coronary thrombosis." © 2021 Published by Elsevier Inc. 1. Introduction The first season of the Netflix blockbuster series, The Crown, begins with a dramatic portrayal in Episode 1 of the illness and, in Episode 2, the subsequent death of King George VI leading to the coronation of his daughter, Elizabeth, as Queen of the United Kingdom [1,2]. Albert Frederick Arthur George Windsor (called “Bertie” within the royal family) reluctantly ruled England as George VI for almost 16 years. This followed the abdication of his brother, Edward VIII in 1936 in order to marry the twice divorced American, Wallis Simpson. Edward subsequently lived the rest of his life in exile as the Duke of Windsor, and King George VI reigned until his death on February 6, 1952 at the age of 56. The official statement of King George VI’s death was as follows: "The King was found dead in bed at Sandringham House in Norfolk, on the morning of February 6. He had died from a coronary thrombosis – a blocking of blood flow to the heart – as a result of a blood clot in an artery – in his sleep. . . . The tea was never drunk: a blood clot had stilled George VI’s valiant heart as he slept [3]." But was this really the cause of death of King George VI? Since there was at that time a social stigma associated with the diagnosis of cancer, there was strong reason not to reveal that he had undergone a total left pneumonectomy for lung cancer in September of the previous year. His medical history is complex and not well documented and raises questions as to the nature of the acute event leading to his death that we will address in the following report. 2. Clinical history ✩ This research received no specific grant support from funding agencies in the public, commercial, or not-for-profit sectors. ✩✩ The authors declare that there is no conflict of interest. ∗ The corresponding author is: Rolf F. Barth, MD. The Ohio State University, Department of Pathology, 4132 Graves Hall, 333 W. 10th Avenue, Columbus, Ohio 43210 USA. Tel.: (614) 292-2177; fax: (614) 292-5844. E-mail address: rolf.barth@osumc.edu (R.F. Barth). a Both authors have contributed equally to the writing of this report. https://doi.org/10.1016/j.carpath.2021.107340 1054-8807/© 2021 Published by Elsevier Inc. George VI was a moderate drinker, but a heavy smoker, having begun as a teenager. Although it is impossible to determine precisely how heavy his cigarette smoking was, biographical descriptions [4,5] suggest that it is reasonable to estimate that his 40-year history of smoking possibly 2 packs of cigarettes per day would be equivalent conservatively to 80 pack-years. This would be an R.F. Barth and L.M. Buja Cardiovascular Pathology 53 (2021) 107340 extraordinarily high number for someone who was only 56 years old at the time of his death. Furthermore, there was a strong family history of heavy cigarette smoking [4,5]. His father, George V, also was a heavy cigarette smoker and developed chronic obstructive pulmonary disease that required intermittent oxygen and ultimately led to his death at age 71. His mother, also a smoker, died at age 86 with a suspected lung tumor. His brother, the former Edward VIII, also was a heavy smoker, developed laryngeal cancer, received cobalt radiotherapy, and ultimately succumbed to it at age 77 in 1972. Finally, his daughter, Princess Margaret, also had a heavy smoking history and underwent left partial pneumonectomy in January 1985 at the age of 55 for an unspecified lesion, possibly a malignancy. George VI’s medical history included an appendectomy at age 19 and a duodenal ulcer at 22, for which at that time he most likely would have had a gastrojejunostomy [6]. In 1948, at the age of 54, he gave up public appearances because of pain in his right leg and foot. His doctors conclulded that the King suffered from thromboangitis obliterans (Buerger’s disease) and that “all his arteries were hardened beyond his years” [7]. "Hardening of the arteries" is a lay term for arteriosclerosis, which is generally used interchangeably with atherosclerosis. Because of the increasing severity of his symptoms, amputation was considered; however, fortunately a less drastic procedure was carried out. The King underwent a right lumbar sympathectomy on March 12, 1949 in a specially outfitted operating room in Buckingham Palace [4,5]. Unrelated to his physical health, he was noted to be shy and had a severe stutter that he eventually overcame later in life [4,5]. In the summer of 1951, at age 56, George VI began to complain of a severe cough with blood-tinged sputum (hemoptysis), and generalized weakness extending over a 4-month period [4,5]. He then developed a respiratory illness that began with fever, chills, and a mild cough. An X-ray taken at that time revealed an area of consolidation in his left lung, which euphemistically was called "catarrhal inflammation." This was diagnosed as pneumonia, and he was treated with a 1-week course of penicillin and bed rest. However, his pulmonary symptoms persisted; and approximately 2 months after their onset, he had a chest X-ray that showed radiological signs in his left lung that were interpreted by Dr. Peter Kerley, a Westminster Hospital radiologist, to be characteristic of lung cancer [8]. However, it is noteworthy that the word, cancer, never was used in any bulletin before or after surgery [6]. Shortly thereafter, the King’s surgeon, Clement Price Thomas, who was one of the leading lung cancer surgeons in Britain at that time, was consulted. A bronchoscopy was performed by his son Brian Thomas, and a biopsy firmly established the diagnosis of lung cancer. On September 23, 1951, one week after the bronchoscopy, Thomas, assisted by two Surgical Residents, Charles Drew and Peter Jones, performed a left total pneumonectomy. Because the King did not want to be hospitalized, the operation was performed at Buckingham Palace in the Buhl room, which had been outfitted to resemble Thomas’s operating theater in the Westminster Hospital [9]. This event was depicted in Season 1, Episode 1, of The Crown. Although there appears to be no published operative report in the medical literature, a detailed description of the anesthetic used was written much later by an anesthesiologist, I. D. Conacher, who was not a participant in the operation. This also included some information relating to the pneumonectomy [8] that was performed for "structural abnormalities" involving his left lung. The left recurrent laryngeal nerve was "sacrificed" during the surgery, and the King’s speech consequently was husky, slow, and muted during his Christmas speech on December 25, 1951 [6]. Although it was not specifically stated, most doctors assumed that the euphemistic "structural changes", first announced on September 18, 1952, were in fact lung cancer. Parenthetically, it should be noted that Thomas, who was a heavy cigarette smoker himself, developed lung cancer Fig. 1. Two photographs of King George VI (A and B) taken sometime during 1951 or January 1952. (A was obtained from Pinterest and there was no identified source of B, but both of them were freely available on the Internet). Based on his appearance, Professor Harold Ellis stated “Every doctor and nurse in the country realized he (George VI) had a malignant disease, he looked terrible [6]. in 1964 at age 70. He was successfully operated on by Mr. Charles Drew, one of his assistants for the King’s pneumonectomy in 1964, and died in 1973 at the age of 79 [6]. Despite a slow but uneventful recovery, the King slowly returned to his usual state of health and resumed his normal activities. However, a particularly ominous sign was the continued hemoptysis, as depicted in The Crown (Season 1, Episode 2) [2] by a bedside box of blood-tinged tissues, suggesting that his cancer had spread to his right lung. On February 5, 1952, he went to Sandringham House in Norfolk to shoot hares and rabbits, and he was purportedly in "great form" [4]. However, as shown in Fig. 1, although the official photograph showed him looking well, the "last" official photograph suggested quite the contrary. This was in keeping with the palace’s efforts not to reveal how sick the King really was. Later in the evening, he retired to his bedroom, and he purportedly was last seen alive at midnight by some gardeners who saw him at a window [4]. At 7:30 on the morning of February 6, his valet, James MacDonald, entered the bedroom with a cup of tea and found the King dead in his bed. Dr James Ansell, "Surgeon Apothecary" to the royal household at Sandringham was summoned, and he officially pronounced the King’s death, attributing it to a "coronary thrombosis" [7]. However, considering how closely a guarded secret the King’s diagnosis of lung cancer was, it was very likely that Ansell was unaware of this. Although no official announcement was made as to the cause of the King’s death, medical circles concluded that it was a "coronary thrombosis." Therefore, it subsequently was reported in the popular press that a blood clot had caused his heart to stop. During a lecture on operations that made history, Professor Harold Ellis, CBE, FRCS, provided a personal perspective on the illnesses and death of King George VI [6], although he himself was not involved in the operation or subsequent care. Ellis stated that, when photographs emerged of an ailing George VI in 1951, “Every doctor and nurse in the country realized he had malignant disease, he looked terrible.” (as shown in Fig. 1) Ellis also said, “I think George VI should be on every cigarette packet, because he had severe vascular disease in his legs – 99% due to smoking. He had carcinoma of the lung – 99% due to smoking. [And] he died of coronary thrombosis – 90% due to smoking" [10]. Professor Ellis’s confident and quotable summary of King George VI’s medical history not withstanding [6], we think his unequivocal statement as to the cause of death should be reexamined from an evidence-based perspective. The diagnosis of 2 R.F. Barth and L.M. Buja Cardiovascular Pathology 53 (2021) 107340 lung cancer was suppressed because of a strong motivation by the royal family and the government to avoid instability among the British public [5], as well as the stigma associated with a diagnosis of cancer at the time. Based on the chest X-rays, the King most likely had a squamous cell carcinoma of the lung, which is strongly associated with a history of heavy cigarette smoking [11]. Since, lung cancer can result in death by numerous and complex ways, we discuss herein alternatives to the diagnosis of "coronary thrombosis" as an explanation for King George’s demise. We also discuss the evolution of perceptions of the medical establishment and the lay public regarding coronary artery disease, coronary thrombosis, and lung cancer. Sudden death is generally defined as a natural, unexpected fatal event occurring within 6 hours of onset of a pathophysiological derangement; the episode may or may not elicit symptoms from the victim and may or may not be witnessed. Cardiovascular sudden death is by far the most frequent type (over 90%), followed by deaths induced by cerebral causes or respiratory causes. Cardiovascular causes of sudden death are numerous and include obstructive coronary atherosclerosis which is the most frequent and often is associated with plaque disruption and thrombosis, followed by cardiomyopathies, and a variety of other conditions. Most cases have arrhythmic cardiac arrest as the pathophysiological mechanism (over 90% of cases) and a minority are due to mechanical cardiac arrest caused by conditions such as aortic rupture and pulmonary thromboembolism [24,25]. Did King George VI have a sudden arrhythmic death due to a coronary thrombosis in the setting of clinically silent coronary atherosclerosis? This question brings up the issue of the speculative and often inaccurate statements regarding the cause of death and information entered on death certificates in the absence of an autopsy. In 1971, Walford published a study of the accuracy of death certification in 142 patients who died suddenly and were designated as dying of coronary thrombosis [23]. Eleven physicians were asked to make an estimate of how accurate they thought each death certificate was. They were asked to assign each patient to one of three groups: Group 1, 100% accurate; Group 2, probably fairly accurate; and Group 3, a “toss-up,” no good evidence one way or another. The physicians assigned their cases as follows: Group 1 - 60 cases (42%), Group 2 -40 cases (28%) and Group 3 -42 cases (30%). Of the 60 Group 1 cases, 46 were proven by autopsy or documented history of previous angina pectoris or coronary thrombosis. The 40 Group 2 cases had significant past histories of angina pectoris, coronary thrombosis or other cardiovascular conditions. The certification of death due to coronary thrombosis in the 42 Group 3 cases was by definition little more than guesswork. We posit that King George VI was in the Group 3 category of certification of death due to coronary thrombosis by guesswork, perhaps based on the history of significant peripheral vascular disease, but not conclusively shown to be of atherosclerotic etiology. Walford points out that, given the prevalence of coronary artery disease, the guesswork is bound to be right in many cases [23]. In fact, we could find no record of a formal medical certification of King George VI’s cause of death other than the statement attributed to Dr. James Ansell, Surgeon Apothecary to the royal household that the King had died of a "coronary thrombosis." Speculation by medical specialists in press reports apparently led to general acceptance of coronary thrombosis as the cause of the King’s death (UPI website 2/6/52). Nevertheless, Walford correctly states that without postmortem confirmation, a considerable although unquantifiable error is introduced in death certification records [23]. 4. King George VI’s cardiovascular disease At issue are the extent, severity, and nature of King George VI’s vascular disease. As previously described, he was a heavy smoker. In 1949, 2 years before developing lung cancer, he developed another smoking-related malady, namely, arterial insufficiency of his right lower extremity, as manifested by claudication [12]. To alleviate these symptoms, a lumbar sympathectomy was performed [6]. This procedure frequently was used at the time to improve arterial circulation to the lower limbs [13]. Peripheral vascular disease of the lower extremities is most often due to arteriosclerosis. However, it also can result from a variety of nonatherosclerotic conditions [14] and is frequently complicated by thrombosis of the iliofemoral arteries [15,16]. Major risk factors are cigarette smoking and diabetes mellitus. In the case of George VI, he had been diagnosed with Buerger’s disease in 1949 [17]. This is a non-necrotizing vasculitis with luminal inflammatory thrombosis involving medium and small arteries, veins and nerves [14,18]. Pathogenesis likely involves an immune-mediated reaction to components of cigarette smoke [17]. It typically presents in young men in their 40s or younger who are heavy smokers, but onset can also occur in older individuals. Buerger’s disease usually begins with lower extremity ischemia due to involvement of the distal small arteries and veins [17]. As the disease progresses, it may involve more proximal arteries, including the iliac artery [18]; but, coronary artery involvement is rare [17]. Statements made by King George’s physicians have led us to believe that he suffered from both Buerger’s disease and arteriosclerosis [6]. He undoubtedly had an increased risk for coronary artery disease based on his history of heavy smoking. Yet, if the King did have coronary artery disease, he was clinically asymptomatic, since, to the best of our knowledge, angina pectoris never was reported as a symptom that he had experienced [4]. Whether the King had more than minimal coronary atherosclerosis is a key issue, since thrombosis of a major coronary artery, which was declared to be his immediate cause of death, only occurs as a complication of coronary atherosclerosis involving arteries with atherosclerotic plaques. There is a long and convoluted history of evolving interpretations of the relationships among coronary atherosclerosis, coronary thrombosis, acute myocardial infarction and sudden death [19-22]. Up until the first part of the twentieth century, sudden coronary occlusion always was considered to produce sudden cardiac arrest. There also was confusion between myocarditis and myocardial infarction. Coronary thrombosis was considered a secondary event following decreased blood flow to the inflamed, necrotic myocardial region [23]. In 1912, a breakthrough came when James Herrick proposed that coronary thrombosis did not always cause sudden death but could cause death of heart muscle in patients with an acute myocardial infarction [19]. Subsequently, coronary thrombosis became established as a major cause of both sudden cardiac death and acute myocardial infarction. 5. King George VI’s lung cancer King George VI, a heavy cigarette smoker with a possible 80pack year history of cigarette smoking, developed a mass in his left lung that was identified by X-ray and chest tomography as cancer and which was easily reached by bronchoscopy and then biopsied. These features point to a centrally located bronchial tumor, most likely a squamous cell carcinoma [11,26]. His slow recovery and sudden death 4.5 months after his pneumonectomy raises the possibility that, although complete resection of the primary tumor was achieved, it already had spread to the right lung. Briefly summarized, Clement Price Thomas, the King’s surgeon, was one of the leading British chest surgeons specializing in cancer of the lung [27]. Between 1935 and 1958, he performed a to3 R.F. Barth and L.M. Buja Cardiovascular Pathology 53 (2021) 107340 tal of 826 operations for lung cancer, of which only 163 were resectable. The early death rate, defined as death in the hospital following surgery, was 21%; and the five-year survival rate for patients with resectable tumors, which would have included those who had lobectomies or pneumonectomies, was 11.6%. As stated by Thomas, the criterion for a standard lobectomy was that the tumor should be confined to the excised lobe. The very fact that a pneumonectomy was performed on the King would clearly indicate that the tumor had spread to other lobes of his left lung. We can only speculate that George VI’s tumor also had spread to his right lung, as suggested by the continuation of hemoptysis, as depicted in The Crown (Season, 1, Episode 2) [2]. Death from lung cancer can result from many complications, including: pneumonia secondary to bronchial obstruction; fatal hemorrhage from invasion and disruption of blood vessels; a hypercoagulable state leading to fatal pulmonary thromboembolism; pulmonary and/or hepatic failure due to large tumor burden; and severe cachexia due to extensive metastatic disease [28]. Nichols et al. characterized the immediate and contributing causes of death for 100 patients with lung cancer [28]. The immediate cause of death was attributed to major tumor burden in 30 decedents, infection in 20, complications of metastatic disease in 18, pulmonary hemorrhage in 12, pulmonary embolism in 12, and diffuse alveolar damage in 7 decedents. The most likely causes of sudden death are either a large pulmonary thromboembolism leading to cardiogenic shock or erosion into a major blood vessel with massive bleeding into the chest cavity leading to hypovolemic shock. We suggest that either of these two causes could explain George VI’s sudden death. Although the King was shown lying peacefully dead in his bed in The Crown, there is no hard evidence to support that this indeed was the case. It is possible that the King might have had a paraneoplastic syndrome, which could have resulted in a hypercoagulopathy that could have led to a massive pulmonary thrombus, resulting in sudden death [29,30]. Alternatively, presuming that his cancer had spread to his right lung, it is possible that it could have eroded the wall of a major vessel and produced a massive hemorrhage into his right hemithorax, a contained space that could have hidden any external evidence of bleeding. The only possible way that blood could have escaped from the chest cavity would be if the tumor simultaneously had eroded the wall of both a major blood vessel and an adjacent bronchus. Only an autopsy would have provided a definitive answer confirming or refuting these alternative hypotheses [31]. Following the prevailing custom at the time [32,33], King George VI’s physicians chose to withhold the diagnosis of lung cancer from the King and the general public, opting instead to say that his operation was necessary to remove certain "structural abnormalities" involving his left lung. Undoubtedly the fear of an adverse reaction and the possible stigma among the populace if such a diagnosis was rendered for the head of state of Great Britain weighed heavily on the approach used by the King’s physicians. Also, this lack of candor was the norm at the time. In the 1950s, the general attitude among physicians in Western countries did not favor fully discussing with patients either the diagnosis or prognosis associated with their cancer [32,33]. The attitude among the public regarding wanting to know was not particularly different up until later. The change in attitude in the West in the 1970s was due to multiple factors. Major epidemiological studies, such as the one led by the British Doctors Study, were performed and reported in the medical literature. These definitively established the causal role of cigarette smoking as a major risk factor for a number of diseases, including lung cancer, chronic obstructive pulmonary disease, and cardiovascular disease [33,34]. This was a period of social upheaval when movements for human rights were in the fore. Patients be- gan to demand that they be fully informed about their diagnosis, prognosis, and treatment options. In parallel with this development, physicians recognized the need for greater communication as an effective means of increasing patients’ understanding of their disease and compliance with their physician’s recommendations [34]. This new attitude of openness among physicians was documented in a 1987 international survey of physicians’ attitudes and practice in regard to revealing the diagnosis of cancer [33]. Needless to say the outcome of King George VI’s illness and cause of death may well have been different had he been diagnosed in the 2020s. 6. Conclusions Our interest in medical history is based on our belief that knowledge of major events and people that influenced the evolution of medical science and practice enriches and enhances the contemporary practice of medicine. This extends to the role of the autopsy in medicine[31,35]. Another interest is the elucidation of new information and insights into the deaths of historically noteworthy individuals [36,37]. It is in this vein that we have reexplored the death of King George VI, and we would like to suggest that he may have died as a result of a fatal complication of his lung cancer rather than the speculative diagnosis of a "coronary thrombosis." The final take home message is that if an autopsy had been performed, we would have had a definitive answer to this question! Acknowledgments We could like to thank Mr. Pankaj Chandak, Transplant Surgery (Adult and Pediatric), Guys and Great Ormond Street Hospitals, London, England; Dr. Nahush Mokadam, Division of Cardiac Surgery, and Dr. Sergey Brodsky, Department of Pathology, The Ohio State University, Columbus, Ohio; and Dr. Christofer Barth, Director, Cardiac Surgery Intensive Care Unit, St. Luke’s Hospital/Aurora Health Care, Milwaukee, Wisconsin for their insightful comments relating to the sudden death of King George VI. Finally, we would like to thank Mr. Shawn Scully for his assistance in retrieving unretouched photographs of the King and Mr. David Carpenter for assistance with the preparation of this manuscript and for his remarkable good looks, genial attitude, and natty fashion sense. References [1] Daldry S. Wolferton Splash (Episode 1). The Crown. BBC; 2016. [2] Daldry S. Hyde Park Corner (Episode 2). The Crown. BBC; 2016. 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