To Err is Human: Can American Medicine Learn from Past Mistakes?

To Err is Human: Can American Medicine  Learn from Past Mistakes?

 

Jeffrey B Ritterman, MD

Perm J 2017;21:16-181 [Full Citation]

https://doi.org/10.7812/TPP/16-181
E-pub: 06/14/2017

ABSTRACT

The history of medicine includes many errors. Some persisted for decades and caused great harm. Several are highlighted in this article, including the mythical thymic diseases: thymic asthma and status thymicolymphaticus. Some medical mistakes, such as the diet-heart hypothesis of Ancel Keys, continue to cause harm. To avoid future errors and their associated harm, I suggest a cultural shift encouraging professional humility and greater questioning of medical dogma. Medical education focused on teaching students this history may help with this cultural shift.

INTRODUCTION

During my medical training, we were taught that stress and lifestyle factors caused gastritis and peptic ulcer disease. We accepted without question the idea that bacteria could not live in the highly acidic environment of the stomach. Patients with severe ulcer disease would be offered surgery. We now know, thanks to the pioneering work of Marshall and Warren,1 that peptic ulcer is caused by a bacterium, Helicobacter pylori.

Warren discovered the curved bacteria in the stomachs of patients with peptic ulcer disease and gastritis in 1979.2 But it wasn’t until his research partner, Marshall, deliberately infected himself with the bacterium and gastritis developed that their findings were taken seriously.

Marshall’s ability to take a fresh look at these gastric bacteria as etiologic agents, rather than to uncritically accept the stress theory of ulcer disease, was in part because of his lack of experience. Having started his study of gastroenterology in 1981, Marshall had an easier time than more seasoned researchers in overcoming a “set of well entrenched beliefs that conflicted with the new ideas.”3

It took a generation for Marshall and Warren’s pioneering work to be recognized and acknowledged. They first published their findings on H pylori in 1984. More than a decade later, in 1995, only 5% of American physicians were prescribing antibiotics for treatment of peptic ulcer disease.3 In 2005, Marshall and Warren received the Nobel Prize in Medicine for their discovery, 26 years after Warren discovered H pylori.2

This problem of mistaken ideas persisting despite scientific evidence to the contrary has been present since the onset of the scientific method. In 1633, Galileo was sentenced to house arrest for the crime of proclaiming that the sun, not the earth, was the center of our planetary system.4

Three hundred years later, Nobel prize-winning physicist Max Planck5 stated: “A new scientific truth does not triumph by convincing its opponents and making them see the light, but rather because its opponents eventually die, and a new generation grows up that is familiar with it.”

Or more succinctly: “Science advances one funeral at a time.”6

This problem is of particular concern in medical science, where outmoded ideas translate into excess morbidity and mortality. How can medicine learn from its mistakes and make these timely corrections? Perhaps a few additional examples will help make clear the importance of doing so.

A Cautionary Tale: Sudden Infant Death Syndrome and the “Enlarged” Thymus Gland

In the first half of the 19th century, physicians were becoming alarmed by sudden infant death syndrome (SIDS). Healthy infants would be put to bed and found dead in the morning. In 1830, pathologists noted that SIDS-affected infants had enlarged thymus glands compared with “normal” autopsy specimens.7 It seemed logical to conclude that these “enlarged” glands were in some way responsible for the deaths.

In 1830, Kopp introduced the term thymic asthma, suggesting that the “enlarged” thymus occluded the trachea.8 The existence of this fictitious disease became widely and quickly accepted, and persisted for at least a century. The thymic syndrome underwent an additional modification by the Austrian physician, Paltauf, who added the term status thymicolymphaticus to the medical lexicon in 1889.8 Paltauf believed that a systemic disorder leading to vascular collapse caused the sudden deaths. The enlarged thymus, it was believed, caused this unexplained vascular collapse, often precipitated by minor stress.

Descriptions and case reports of these thymus “diseases” appeared in medical articles and textbooks.9,10 There was even a list of physical characteristics that accompanied these syndromes, including changes in incisor teeth, heart size, and skin color. The 1924 edition of Management of the Sick Infant claimed that the clinical picture of thymic asthma was “so characteristic that once seen, it is unlikely to be mistaken.”8

If an enlarged thymus was leading to sudden infant death, removal of the thymus might be of preventive value. Radiology had advanced to the point at which physicians began making the diagnosis of thymic enlargement from x-ray films. After radiographic diagnosis, thymectomy was initially recommended, but the mortality rate was unacceptably high. Thymus irradiation became the treatment of choice.8

The first “successful” use of irradiation to shrink the thymus was reported by Friedländer in 1907.11 Thousands of children eventually received radiation to prevent status thymicolymphaticus. Some physicians advocated prophylactic irradiation for all neonates.8

There was only one slight problem. It turned out to be deadly.7

The cadavers used by anatomists to determine the “normal” thymus size were from the poor, most having died of highly stressful chronic illnesses such as tuberculosis, infectious diarrhea, and malnutrition. What was not appreciated at the time was that chronic stress shrinks the thymus gland. The “normal” thymus glands of the poor were abnormally small. Here is where the fatal mistake occurred: because the autopsied thymus glands of the poor were regarded as normal in size, the SIDS-affected infants were erroneously believed to have thymic enlargement.7,8

The thyroid gland, which is highly sensitive to irradiation, sits close to the thymus. The increased risk of thyroid malignancy in the patients who had undergone thymic irradiation was first recognized in 1949.12 The patients subjected to thymic radiation “therapy” also experienced higher rates of breast cancer.13-15

The regular practice of thymic irradiation was finally halted in the 1940s, almost four decades after Friedländer irradiated the first patient. In the first edition of his radiology textbook in 1945,16 John Caffey, MD, a pioneer in pediatric radiology, proclaimed that “a causal relationship between hyperplasia of the thymus and sudden unexplained death has been completely refuted. … [I]rradiation of the thymus … is an irrational procedure at all ages.”16

More than 10,000 deaths caused by thyroid cancer resulted from this treatment.7

Rudolf Virchow, the father of cellular pathology, a man who stood at the top of the academic medical world for 50 years, was one of those who endorsed the mistaken therapy.7 Virchow, the man who first explained the pathophysiology of pulmonary embolus, the man who named leukemia, and a founder of social medicine, got it wrong!17

A Cautionary Tale: Fat

Perhaps there is no better modern medical example of our capacity for serious error than the fact that we have given the wrong dietary advice since shortly after President Eisenhower’s heart attack in 1955. Not only has our advice been wrong, it has been dangerously wrong.18

As in the case of the supposed thymic disorders, once again a mistake has led to great harm.

Ancel Keys, PhD, a physiologist, studied the American and European diets after World War II. He studied the epidemiology of cardiovascular disease (CVD) and noted that American business executives had high rates of CVD,19,20 whereas the heart disease rates in postwar Europe had fallen sharply, presumably from reduced food supplies. He postulated that the different rates of CVD were owing to markedly different rates of dietary fat consumption. Keys was convinced that dietary fat led to elevated cholesterol levels, which then caused CVD.21 Keys presented his diet-heart hypothesis to the World Health Organization in 1955. His research was epidemiologic and could only prove an association, not causality. But Keys was a convincing salesman at a time when the country was searching for solutions to prevent the sudden deaths resulting from this newly recognized killer. In January 1961, Keys became a cultural hero, his picture gracing the cover of Time Magazine, and the diet-heart hypothesis was accepted.22

In 1978, Keys published his data in support of dietary fat as the cause of CVD, in the Seven Countries Study.23 Unfortunately, he excluded data from 15 countries and 4 indigenous tribes that did not fit well with his hypothesis.24

While Keys was proposing dietary fat as the cause of CVD, Brown and Goldstein were advancing our understanding of cholesterol and fatty acid metabolism, work for which they received the Nobel Prize in 1985.25 Working with skin cells from patients with a rare genetic disorder, familial hypercholesterolemia, Brown and Goldstein25 demonstrated the presence of the low-density lipoprotein (LDL) cholesterol receptor. Patients with the disorder lacked the normal number of receptors, had high serum cholesterol levels, and had a risk of heart attack early in life. The new knowledge seemed to fit well with Keys’ “dietary fat hypothesis” as the cause of CVD. Because LDL cholesterol correlated with the risk of CVD and dietary fat increased blood LDL cholesterol levels, it seemed logical to conclude that dietary fat was the cause of CVD.

Once again, incomplete knowledge led to the pursuit of a dangerous path. In the dietary guidelines case, epidemiologic research that showed an association was wrongly assumed to prove causality. In addition, the contrary evidence to Keys’ diet-heart hypothesis was ignored. There never was any association between dietary fat and all-cause mortality. Certainly, if dietary fat was the cause of CVD, one would expect such an association. In the single randomized controlled trial that compared a 10% saturated fat intake vs a diet with unrestricted saturated fat, the subjects with low-fat intake had a higher death rate due to all causes, including heart disease.26

In 1977, the McGovern Commission, chaired by then Senator George McGovern, issued dietary guidelines in keeping with the diet-heart hypothesis.27 Decades later, we have continued to follow these guidelines.28 Americans have been repeatedly told to consume no more than 30% of total calories from fat and no more than 10% from saturated fat.28

When the food companies responded to the guidelines by removing the fat from food, the taste went with it. The solution: add sugar, and lots of it. This worked well economically, as the invention of high-fructose corn syrup provided an endless supply of cheap sugar. The result of admonishing people to eat less fat was that sugar consumption skyrocketed.24,29,30 This substitution of sugar for fat has been the major driver of the diabetes epidemic31,32,33 and has played a key role in causing coronary heart disease,34-36 strokes,37 fatty liver disease,38 obesity,39 hypertension,40 and some cancers.41 In addition, as Americans began avoiding fat, they also increased their intake of simple starches. Like sugar, diets high in refined starches are associated with an increased risk of obesity, CVD, and Type 2 diabetes.42-44

Now the so-called “French paradox” makes sense.45,46 People in France consume high rates of fat but do not have correspondingly high rates of CVD. It isn’t a paradox. There simply is no connection between CVD and dietary fat.

Many physicians continue to warn their patients to avoid dietary fat despite accumulating evidence showing that unrefined carbohydrates cause metabolic syndrome and its related illnesses. In 2015, the Dietary Guidelines Advisory Committee Report47 for the first time started to change course and to exonerate fat and saturated fat. Instead, the report focuses our attention on fructose and other simple carbohydrates as the real culprits of diet-related illnesses. It took 100 years for the faux thymic conditions to be understood to be a gross medical error. How many more years will it take before we correct our mistaken dietary advice?

Embracing Professional Humility

During a leadership training session that I attended, a National Aeronautics and Space Administration (NASA) scientist explained that the July 1969 Apollo Mission to the moon was on the ideal flight path only 3% of the time. Great achievements depend not on perfection, but on our ability to quickly notice when we are off course and to make adjustments.

As a profession, we have failed miserably to notice that we were terribly off course in both the fictitious thymus diseases tragedy and the dietary guideline mishap. In the first instance, the error persisted for more than 100 years, in the second, many decades. In each case, innumerable people were harmed, and many died.

To prevent similar tragedies in the future, we will need a cultural shift in medicine. Coulehan48 has critiqued our present medical culture as “characterized by arrogance and entitlement.” Berger49 pointed out that the arrogance goes beyond the individual physician and is systemic:

The physician has become a “provider” and the patient a “health consumer.” This distancing of the doctor from the patient breeds a kind of “system arrogance,” in which the patient is no longer seen as a human being but simply as a job to be done cost-effectively.

The late Franz Ingelfinger,50 former editor of the New England Journal of Medicine, stated: “Efficient medical practice, I fear, may not be empathic medical practice, and it fosters, if not arrogance, at least the appearance of arrogance.”

If the toxin is professional arrogance, the antidote is professional humility.

One area in health care in which we have witnessed a cultural shift is in our understanding of how to provide competent care to patients from different backgrounds. Tervalon and Murray-Garcia51 have challenged us to go beyond “cultural competency” and to embrace “cultural humility.” They explain:

… cultural competence in clinical practice is best defined not by a discrete endpoint but as a commitment and active engagement in a lifelong process that individuals enter into on an ongoing basis with patients, communities, colleagues, and with themselves. ... It is a process that requires humility as individuals continually engage in self-reflection and self-critique as lifelong learners and reflective practitioners.

The underlying principle is that, given the great diversity of cultural practices and beliefs, humility is the appropriate mindset. Practitioners should be humble enough “to say that they do not know when they truly do not know and to search for and access resources … .”51 The practitioner is both a teacher and a student.

This model holds for the general practice of medicine as well. Humility is both a personal virtue and a professional necessity. Personal humility is essential for good doctoring.52-55 Professional humility promotes the questioning of medical dogma, leading to the scientific testing of hypotheses.

William Osler,56 considered by many the father of American Medicine, addressed the question of humility in a 1906 lecture to medical students at the University of Minnesota:

In these days of aggressive self-assertion, when the stress of competition is so keen and the desire to make the most of oneself so universal, it may seem a little old-fashioned to preach the necessity of this virtue, but I insist for its own sake and for the sake of what it brings, that a due humility should take the place of honour on the list [of virtues] … since with it comes not only reverence for truth, but also proper estimation of the difficulties encountered in our search for it. …
[T]his grace of humility is a precious gift.

The more humble the medical profession is, the more likely we will avoid costly errors.

To facilitate this cultural shift, we will need to unlearn old behaviors and replace them with new ones. This will require a major re-education effort for those already in practice, and the development of a robust curriculum to reach those in training. To be successful, we will need to have an impact on all layers of the medical hierarchy, including nonphysician health care workers, students, physicians-in-training, and those in positions of authority.

Our aim must be to create a safe learning environment where questions and alternative points of view are encouraged. The curriculum in medical and allied health professional schools should include courses on medical history, highlighting past medical errors, and stressing the importance of questioning current medical practice.57 Medical and allied health professional students should be required to research an area of medical care to determine if current practices are consistent with the latest medical science.

Continuing medical education courses should be developed to reach those who have already completed their formal medical education. When it became clear that physicians in practice were not well educated in end-of-life care and in pain management, training in both areas became mandatory for medical license renewal. We can do the same for professional humility.

It will be crucial to this effort for the leaders in American medicine to embrace this cultural shift. Those in authority must be open to new ideas, even if those ideas challenge paradigms associated with their own success. Medical students and physicians-in-training will find it much easier to raise important questions if they feel encouraged to do so.

Would the terrible health outcomes from thymus irradiation have been avoided if a medical student had felt empowered to ask, “Dr Virchow, are we sure that the thymus gland is abnormally enlarged in infants with SIDS?”

Disclosure Statement

The author(s) have no conflicts of interest to disclose.

Acknowledgements

The author thanks Vivien Feyer for editorial assistance and Charlie Clements, MD, for suggesting the inclusion of the Helicobacter pylori story.

Kathleen Louden, ELS, of Louden Heatlh Communications provided editorial assistance.

How to Cite this Article

Ritterman JB. To err is human: Can American medicine learn from past mistakes? Perm J 2017;21:16-181. DOI: https://doi.org/10.7812/TPP/16-181.

References
1.    Marshall BJ, Warren RM. Unidentified curved bacilli in the stomach of patients with gastritis and peptic ulceration. Lancet 1984 Jun 16;1(8390):1311-5. DOI: https://doi.org/10.1016/S0140-6736(84)91816-6.
    2.    Ahmed N. 23 years of the discovery of Helicobacter pylori: Is the debate over? Ann Clin Microbiol Antimicrob 2005 Oct 31;4:17. DOI: https://doi.org/10.1186/1476-0711-4-17.
    3.    Tannenbaum J. Delayed gratification: Why it took everybody so long to acknowledge that bacteria cause ulcers. Journal of Young Investigators [Internet] 2005 Feb [cited 2017 Mar 6]. Available from: www.jyi.org/issue/delayed-gratification-why-it-took-everybody-so-long-to-acknowledge-that-bacteria-cause-ulcers/.
    4.    Linder D. The trial of Gallileo [Internet]. Kansas City, MO; University of Missouri Kansas City Law School; 2002 [cited 2017 Mar 20]. Available from: http://law2.umkc.edu/faculty/projects/ftrials/galileo/galileoaccount.html.
    5.    Planck M. Scientific autobiography and other papers. New York, NY: Philosophical Library; 2007 Dec.
    6.    Azoulay P, Fons-Rosen C, Graff Zivin JS. Does science advance one funeral at a time? [Internet]. Cambridge, MA: National Bureau of Economic Research; 2015 [cited 2017 Mar 20]. Available from: www.nber.org/papers/w21788.
    7.    Sapolsky RM. Poverty’s remains. The Sciences 1991 Sep-Oct;31(5):8-10.
    8.    Jacobs MT, Frush DP, Donnelly LF. The right place at the wrong time: Historical perspective of the relation of the thymus gland and pediatric radiology. Radiology 1999 Jan;210(1):11-6. DOI: https://doi.org/10.1148/radiology.210.1.r99ja4511.
    9.    Mitchell AG, Brown EW. The clinical implications of the thymus and status thymico-lymphaticus. Ann Intern Med 1934 Dec;8(6):669-77. DOI: https://doi.org/10.7326/0003-4819-8-6-669
    10.    Wilson DS. Status thymicolymphaticus; presentation and discussion of a case. Curr Res Anesth Analg 1950 Nov-Dec;29(6):356-8. DOI: https://doi.org/10.1213/00000539-195011000-00061.
    11.    Friedländer A. Status lymphaticus and enlargement of the thymus: With report of a case successfully treated by the x-ray. Arch Pediatr 1907; 24:490-501.
    12.    Duffy BJ Jr, Fitzgerald PJ. Thyroid cancer in childhood and adolescence: A report of 28 cases. Cancer 1950 Nov;3:1018-32. DOI: https://doi.org/10.1002/1097-0142(1950)3:6%3C1018::AID-CNCR2820030611%3E3.0.CO;2-H.
    13.    Hildreth NG, Shore RE, Dvoretsky PM. The risk of breast cancer after irradiation of the thymus in infancy. N Engl J Med 1989 Nov 9; 321(19):1281-4. DOI: https://doi.org/10.1056/NEJM198911093211901.
    14.    Hildreth NG, Shore RE, Hemplemann LH, Rosenstein M. Risk of extrathyroid tumors following radiation treatment in infancy for thymic enlargement. Radiat Res 1985 Jun;102(3):378-91. DOI: https://doi.org/10.2307/3576713.
    15.     Adams MJ, Dozier A, Shore RE, et al. Breast cancer risk 55+ years after irradiation for an enlarged thymus and its implications for early childhood medical irradiation today. Cancer Epidemiol Biomarkers Prev 2010 Jan;19(1):48-58. DOI: https://doi.org/10.1158/1055-9965.EPI-09-0520.
    16.    Caffey J. Pediatric x-ray diagnosis. Chicago, Ill: Year Book; 1945. p 344-5.
    17.    Schultz M. Rudolf Virchow. Emerg Infect Dis 2008 Sep;14(9):1480-1. DOI: https://doi.org/10.3201/eid1409.086672.
    18.    Ritterman J. Correcting four decades of the wrong dietary advice. JAAPA 2016 Jul;29(7):1-3. DOI: https://doi.org/10.1097/01.jaa.0000484299.50943.55.
    19.    Blackburn H. Famous polemics on diet-heart theory [Internet]. Twin Cities, MN: University of Minnesota; 2012 Oct 15 [cited 2017 Mar 14]. Available from: www.epi.umn.edu/cvdepi/essay/famous-polemics-on-diet-heart-theory/.
    20.    Keys A, Taylor HL, Blackburn H, Brozek J, Anderson JT, Simonson E. Coronary heart disease among Minnesota business and professional men followed fifteen years. Circulation 1963 Sep;28:
381-95. DOI: https://doi.org/10.1161/01.CIR.28.3.381.
    21.    Harcombe Z, Baker JS, Cooper SM, et al. Evidence from randomised controlled trials did not support the introduction of dietary fat guidelines in 1977 and 1983: A systematic review and meta-analysis. Open Heart 2015 Jan 29;2(1):e000196. DOI: https://doi.org/10.1136/openhrt-2014-000196. Erratum in: Open Heart 2015 Feb 20;2(1):e000196. DOI: https://doi.org/10.1136/openhrt-2014-000196corr1.
    22.    Andrade J, Mohamed A, Frohlich J, Ignaszewski A. Ancel Keys and the lipid hypothesis: From early breakthroughs to current management of dyslipidemia. B C Med J 2009 Mar;51(2):66-72.
    23.    Keys A. Coronary heart disease in seven countries. I. The study program and objectives. Circulation 1970 Apr;41(4 Suppl):I1-8.
    24.    Lustig RH. Fat chance: Beating the odds against sugar, processed food, obesity, and disease. New York, NY: Hudson Street Press; 2013. p 110-1.
    25.    Brown MS, Goldstein JL. A receptor-mediated pathway for cholesterol homeostasis. Science 1986 Apr 4;232(4746):34-47. DOI: https://doi.org/10.1126/science.3513311.
    26.    DiNicolantonio JJ. The cardiometabolic consequences of replacing saturated fats with carbohydrates or Ω-6 polyunsaturated fats: Do the dietary guidelines have it wrong? Open Heart 2014 Feb 8;1(1):e000032. DOI: https://doi.org/10.1136/openhrt-2013-000032.
    27.    Staff of the Select Committee on Nutrition and Human Needs, United States Senate. Dietary goals for the United States, 2nd edition. Washington, DC: US Government Printing Office; 1977.
    28.    US Department of Health and Human Services and US Department of Agriculture. 2015-2020 dietary guidelines for Americans, 8th Edition [Internet]. Washington, DC: US Department of Health and Human Services; 2015 Dec [cited 2017 Mar 20]. Availble from: http://health.gov/dietaryguidelines/2015/guidelines/.
    29.    Dugan A. Americans still avoid fat more than carbs [Internet]. Washington, DC: Gallop; 2014 Jul 29 [cited 2015 Jul 9]. Available from: www.gallup.com/poll/174176/americans-avoid-fat-carbs.aspx.
    30.    Chanmugam P, Guthrie JF, Cecilio S, Morton JF, Basiotis PP, Anand R. Did fat intake in the United States really decline between 1989-1991 and 1994-1996? J Am Diet Assoc 2003 Jul;103(7):867-72. DOI: https://doi.org/10.1016/s0002-8223(03)00381-x.
    31.    DiNicolantonio JJ, O’Keefe JH, Lucan SC. Added fructose: A principal driver of type 2 diabetes mellitus and its consequences. Mayo Clin Proc 2015 Mar;90(3):372–81. DOI: https://doi.org/10.1016/j.mayocp.2014.12.019.
    32.    Palmer JR, Boggs DA, Krishnan S, Hu FB, Singer M, Rosenberg L. Sugar-sweetened beverages and incidence of type 2 diabetes mellitus in African American women. Arch Intern Med 2008 Jul 28;168(14):1487-92. DOI: https://doi.org/10.1001/archinte.168.14.1487.
    33.    Schulze MB, Manson JE, Ludwig DS, et al. Sugar-sweetened beverages, weight gain, and incidence of type 2 diabetes in young and middle-aged women. JAMA 2004 Aug 25;292(8):927-34. DOI: https://doi.org/10.1001/jama.292.8.927.
    34.    Fung TT, Malik V, Rexrode KM, Manson JE, Willett WC, Hu FB. Sweetened beverage consumption and risk of coronary heart disease in women. Am J Clin Nutr 2009 Apr;89(4):1037-42.
DOI: https://doi.org/10.3945/ajcn.2008.27140.
    35.    de Koning L, Malik VS, Kellogg MD, Rimm EB, Willett WC, Hu FB. Sweetened beverage consumption, incident coronary heart disease, and biomarkers of risk in men. Circulation 2012 Apr 10;125(14):1735-41. DOI: https://doi.org/10.1161/CIRCULATIONAHA.111.067017.
    36.    Yang Q, Zhang Z, Gregg EW, Flanders WD, Merritt R, Hu FB. Added sugar intake and cardiovascular diseases mortality among US adults. JAMA Intern Med 2014 Apr;174(4):516-24. DOI: https://doi.org/10.1001/jamainternmed.2013.13563.
    37.    Larsson SC, Akesson A, Wolk A. Sweetened beverage consumption is associated with increased risk of stroke in women and men. J Nutr 2014 Jun;144(6):856-60. DOI: https://doi.org/10.3945/jn.114.190546.
    38.    Basaranoglu M, Basaranoglu G, Bugianesi E. Carbohydrate intake and nonalcoholic fatty liver disease: Fructose as a weapon of mass destruction. Hepatobiliary Sur Nutr 2015 Apr;4(2):109-16. DOI: https://doi.org/10.3978/j.issn.2304-3881.2014.11.05.
    39.    Woodward-Lopez G, Kao J, Ritchie L. To what extent have sweetened beverages contributed to the obesity epidemic? Public Health Nutr 2011 Mar;14(3):499-509. DOI: https://doi.org/10.1017/S1368980010002375.
    40.    Jalal DI, Smits G, Johnson RJ, Chonchol M. Increased fructose associates with elevated blood pressure. J Am Soc Nephrol 2010 Sep;21(9):1543-9. DOI: https://doi.org/10.1681/ASN.2009111111.
    41.    Inoue-Choi M, Robien K, Mariani A, Cerhan JR, Anderson KE. Sugar-sweetened beverage intake and the risk of type I and type II endometrial cancer among postmenopausal women. Cancer Epidemiol Biomarkers Prev 2013 Dec;22(12):2384-94. DOI: https://doi.org/10.1158/1055-9965.EPI-13-0636.
    42.    Sharman MJ, Kraemer WJ, Love DM, et al. A ketogenic diet favorably affects serum biomarkers for cardiovascular disease in normal-weight men. J Nutr 2002 Jul;132(7):1879-85.
    43.    Volek JS, Phinney SD, Forsythe CE, et al. Carbohydrate restriction has a more favorable impact on the metabolic syndrome than a low fat diet. Lipids 2009 Apr;44(4):297-309. DOI: https://doi.org/10.1007/s11745-008-3274-2.
    44.    Volek JS, Fernandez ML, Feinman RD, Phinney SD. Dietary carbohydrate restriction induces a unique metabolic state positively affecting atherogenic dyslipidemia, fatty acid partitioning, and metabolic syndrome. Prog Lipid Res 2008 Sep;47(5):307-18. DOI: https://doi.org/10.1016/j.plipres.2008.02.003.
    45.    Renaud S, de Lorgeril M. Wine, alcohol, platelets, and the French paradox for coronary heart disease. Lancet 1992 Jun 20;339(8808):1523-6. DOI: https://doi.org/10.1016/0140-6736(92)91277-f.
    46.    Criqui MH, Ringel BL. Does diet or alcohol explain the French paradox? Lancet 1994 Dec 24-31;344(8939-8940):1719-23. DOI: https://doi.org/10.1016/s0140-6736(94)92883-5.
    47.    Dietary Guidelines Advisory Committee. Scientific report of the 2015 Dietary Guidelines Advisory Committee. Advisory report to the Secretary of Health and Human Services and the Secretary of Agriculture [Internet]. Rockville, MD: Office of Disease Prevention and Health Promotion; 2015 Feb [cited 2017 Mar 6]. Available from: www.health.gov/dietaryguidelines/2015-scientific-report/.
    48.    Coulehan J. “A gentle and humane temper”: Humility in medicine. Perspect Biol Med 2011 Spring;54(2):206-16. DOI: https://doi.org/10.1353/pbm.2011.0017.
    49.    Berger AS. Arrogance among physicians. Acad Med 2002 Feb;77(2):145-7. DOI: https://doi.org/10.1097/00001888-200202000-00010.
    50.    Ingelfinger FJ. Arrogance. N Engl J Med 1980 Dec 25;303(26):1507-11. DOI: https://doi.org/10.1056/NEJM198012253032604.
    51.    Tervalon M, Murray-García J. Cultural humility versus cultural competence: A critical distinction in defining physician training outcomes in multicultural education. J Health Care Poor Underserved 1998 May;9(2):117-25. DOI: https://doi.org/10.1353/hpu.2010.0233.
    52.    Mahant S, Jovcevska V, Wadhwa A. The nature of excellent clinicians at an academic health science center: A qualitative study. Acad Med 2012 Dec;87(12):1715-21. DOI: https://doi.org/10.1097/acm.0b013e3182716790.
    53.    Chou CM, Kellom K, Shea JA. Attitudes and habits of highly humanistic physicians. Acad Med 2014 Sep;89(9):1252-8. DOI: https://doi.org/10.1097/acm.0000000000000405.
    54.    Wear D. On outcomes and humility. Acad Med 2008 Jul;83(7):625-6. DOI: https://doi.org/10.1097/acm.0b013e318178379f.
    55.    DuBois JM, Kraus EM, Mikulec AA, Cruz-Flores S, Bakanas E. A humble task: Restoring virtue in an age of conflicted interests. Acad Med 2013 Jul;88(7):924-8. DOI: https://doi.org/10.1097/acm.0b013e318294fd5b.
    56.    Osler W. Aequanimitas, with other addresses to medical students, nurses and practitioners of medicine. Philadelphia, PA: P. Blakiston’s Son and Co; 1905. p 39.
    57.    Sokol DK. Perspective: Should we amputate medical history? Acad Med 2008 Dec;83(12):1162-4. DOI: https://doi.org/10.1097/acm.0b013e31818c6610.
 

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Circulation

25,000 print readers per quarter, 7,628 eTOC readers, and in 2016, 1.4 million page views on TPJ articles in PubMed from a broad international readership.

Letters

Articles, editorials, letters to the editor, and other material represent the opinion of the authors. Send your comments to permanente.journal@kp.org.


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