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Journal of Clinical Oncology, Vol 23, No 25 (September 1), 2005: pp. 6256-6259 © 2005 American Society of Clinical Oncology. DOI: 10.1200/JCO.2005.04.019
To Feed or Not to Feed: Is That the Right Question?From the Mayo Clinic, Rochester, MN; and The University of Texas M.D. Anderson Cancer Center, Houston, TX Address reprint requests to Timothy Moynihan, MD, Mayo Clinic, 200 First St SW, Rochester, MN 55905; e-mail: moynihan.timothy{at}mayo.edu HERE’S THE CASE Mr. Smith was a 54-year-old man with advanced non–small-cell lung cancer who had received two cycles of systemic chemotherapy for metastatic disease. He decided to not have any further chemotherapy. He had significant anorexia and cachexia, having lost 10 pounds in the last 2 months despite the use of megestrol acetate. He emphasized that he was neither hungry nor thirsty. At the clinic visit, it was evident that his family was quite distressed by his situation and had been strongly encouraging the patient to eat. They asked his oncologist about a feeding tube. The situation in the office was clearly an emotional one. Nutrition at the end of life is an issue that is fraught with multiple sources of confusion, contradiction, myth, and emotion. Anorexia and cachexia in the context of a terminal illness form a poorly understood syndrome mediated by multiple factors, including proinflammatory cytokines (such as tumor necrosis factor, interleukin-6, and interleukin-8), hormonal disturbances, muscle proteolysis, and lipid alterations. The net effect is the break of the linkage between the intake of nutrition, the laying down of new tissues, and the maintenance of a healthy state. Cancer anorexia and cachexia is a topic of interest to numerous investigators in basic and clinical science. Unfortunately, it is clear that artificial nutrition, defined here as administration of nutrition via tubes placed into the gut (enteral) or vein (parenteral), will not reverse this syndrome. In addition, the means by which artificial nutrition is administered may produce serious adverse effects. Nutrition issues in patients with advanced cancer are often addressed as a part of palliative care. Palliative care, as defined by WHO,1 is "the total active care of patients whose disease is not responsive to curative treatment." This definition does not specifically include or exclude any type of therapy, such as artificial nutrition or hydration. Palliative care seeks to provide relief from symptoms caused by the terminal process and, in so doing, does not seek to hasten or postpone death. The essence of palliative care is to relieve suffering; it strives to minimize the adverse effects or complications of any medical procedures. One of the most important aspects of end-of-life palliative care is defining the patient's goals and balancing these goals with the medical realities of the situation and the patient's and family's desires. Thus, it is essential for the physician to weigh the risks of any proposed treatment against the potential gain. Managing patients with severe cachexia in the setting of advanced cancer is often challenging because this syndrome unmasks or accentuates one or more challenging aspects of caring for patients toward the end of life (Table 1).
From a legal perspective, most states consider artificial nutrition and hydration as no different from any other medical treatment,2 and, as such, these are generally regarded as extraordinary care.3 A patient's cultural or religious beliefs may play a crucial role in the decision-making process because some faith systems place any extension of survival ahead of quality of life, where much of Western medicine now places the most emphasis.4 The physician must ensure that the patient and the family are basing nutrition-related decisions on a realistic grasp of what artificial nutrition can and cannot accomplish and not on myths and emotions. Elegant care of the patient and family dealing with cancer cachexia toward the end of life requires a broad approach that addresses the following fundamental questions: What is happening to me? What is going to happen to me? What can be done to help?5 Most people have experienced changes in their weight directly in relation to the amount and type of food they consume. It is understandable, then, that patients and their loved ones find it puzzling when their physicians suggest that artificial feeding is unlikely to mitigate the problem of weight loss. To help patients and families understand cachexia and why nutritional support is usually not helpful, it is often useful to render the concept in familiar terms using a metaphor.6 An example of a metaphor for cachexia is the concept of a furniture factory where production is disturbed not by a lack of wood and raw materials (calories) but by a defect within the factory itself that prevents these raw materials from being made into furniture (lean body tissues). Once cachexia is understood, the next step is to review the underlying cause of the cachexia and the overall prognosis and treatment options for the cancer itself. Thereafter, the discussion can focus on all interventions that are being taken to improve the comfort and quality of life of the patient and to preserve dignity. Anorexia at the end of life may result from multiple disease processes, including dysphagia, chronic nausea, abnormal gut motility (from any of several pathologic processes), recurrent aspiration, pain, fear, and depression. Anorexia and cachexia caused by a terminal, irreversible, underlying disease process are unlikely to be reversed. Careful evaluation for other reversible causes of anorexia may lead to relatively straightforward symptom relief and, hence, relief of the anorexia. Pain, nausea, and depression can often be controlled by proper attention to these factors. An additional opportunity to help patients with cancer cachexia and anorexia and their families is for the physician to acknowledge that nurturing is an essential part of human existence and that feeding is a central part of human nurturing. When no longer able to provide sustenance, families can lose an important opportunity to support their loved one. This can cause considerable conflict between the patient and the family, with significant feelings of guilt on both sides. Although they often have only the best of intentions, family and friends sometimes blame the patient for the condition by saying or implying, "If only you'd eat, you'd get better." In this setting, the use of empathic listening skills and effective phrases in response to loss, fear, and unrealistic hopes is the key to effective counseling.7-9 Substituting other nurturing activities for feeding can help keep the family members involved in their loved one's care. Touching, massage, communicating, bathing, and mouth care may help fill the family's need to help nurture. Despite the broad approach to discussing the artificial nutrition issues described earlier, there are situations in which the clinician will need to provide some description of the relevant data regarding the expected risks and benefits of artificial nutrition. After all, artificial nutrition has been claimed to be useful for treating anorexia, reversing weight loss, alleviating fatigue, improving performance status, and improving survival. What are the data that support these claims? ANOREXIA The Oxford English Dictionary defines palliate as "to mitigate, alleviate, or give relief." Therefore, one must have a symptom for it to be relieved. For patients at the end of life, anorexia and cachexia are common. Anorexia is, by definition, a "loss of appetite." At times, but certainly not always, anorexia can be a bothersome symptom for patients. In this situation, the use of an orexigenic agent (such as megestrol acetate or a corticosteroid) to try to correct the anorexia is justified by extensive data demonstrating their utility in this situation.10 Corticosteroids may be used in patients with an expected survival of weeks or a few months, whereas progestational agents such as megestrol acetate are often thought to be better for patients who may survive longer. Nonetheless, a patient who is anorexic from the effects of a terminal disease may not be bothered by this symptom. In fact, many such patients tend to report a complete lack of hunger. McCann et al11 monitored 32 terminally ill patients for hunger and thirst during the final 6 months of their disease course. They found that 63% of patients (20 of 32 patients) never experienced hunger, and 34% (11 of 32 patients) had hunger only transiently at the beginning of the observation period. In the patients who did experience hunger, most were relieved with small amounts of oral intake. Similarly, 63% of the patients in this study denied thirst, and those who did experience thirst had their symptoms relieved with oral fluids, mouth care, ice chips, and lubrication of their lips. Sullivan12 found that, in many patients who did express hunger during their terminal illness, these symptoms tended to cease after only a few days of decreased intake. Kalk et al13 reported similar phenomena in healthy political prisoners who go on hunger strikes, for whom feelings of hunger and thirst tended to disappear after a few days of cessation of oral intake, although how this experience in healthy, highly motivated persons translates to end-of-life care is uncertain. WEIGHT LOSS What about the effect of enteral or parenteral nutrition on body mass in terminally ill patients? Both Nixon14 and Lundholm et al15 examined the use of artificial nutrition in terminal cancer patients. In both studies, there was no significant gain of lean body mass, although fat stores (as measured by triceps skinfold thickness) did increase marginally. Neither study suggested any improvement in the quality of life for patients receiving artificial nutrition. Loeser et al16 noted that, in patients with a variety of terminal diseases, enteral feedings did cause their weight to stabilize, but none of the patients showed any significant weight gain. It might be assumed that these patients, if they did not have an enteral tube placed, would have continued to lose weight at the same rate as before tube placement. However, this is not necessarily the case, and a randomized trial would be needed to clarify this issue. FATIGUE AND PERFORMANCE STATUS What about using artificial nutrition to treat fatigue and try to improve performance status? Although fatigue and a declining performance status are typical parts of the end of life, there are no data to suggest that artificial nutrition helps alleviate these symptoms. The study by Lundholm et al15 showed no improvement in fatigue in a randomized trial in which all patients received a cyclooxygenase inhibitor and erythropoietin (titrated to hemoglobin level) and were then randomly assigned to receive either oral nutrition as tolerated or artificial nutrition if weight loss and energy balance indicated a nutritional deficit. Another study by Pironi et al17 revealed that, when 164 patients received artificial nutrition, only 13 (8%) showed even a minimal improvement in their physician-rated Karnofsky performance status after nutritional intervention. It is not clear whether this percentage would have been any smaller if the patients had not received nutritional intervention. SURVIVAL Survival, which is easily measured, is clearly an important clinical outcome in most situations. For patients with anorexia and cachexia arising from a terminal illness, few data suggest a survival advantage for patients receiving artificial nutrition. The Lundholm et al15 study examined the effects of enteral and parenteral nutrition on terminally ill cancer patients. In an intent-to-treat analysis, there was no evidence of a survival advantage. However, a post hoc as-treated analysis suggested a minimal survival advantage for patients receiving artificial nutrition. This type of analysis increases the likelihood of bias in favor of those patients treated with artificial nutrition and makes drawing any conclusions from this subset analysis difficult. No differences in weight gain, energy, or performance status were noted between the two randomly assigned groups. There are also experimental animal data to address whether enteral or parenteral nutrition affect survival times. Some,18,19 although not all,20 animal experiments have demonstrated that hyperalimentation causes tumors to grow faster or animals to die sooner. This has been referred to as feeding the tumor. There have been no comparable studies in humans. It is clear that intravenous nutrition support can sometimes hasten death, particularly in the case of patients who are critically ill and receiving total parenteral nutrition.21,22 Additionally, the added work, typically requiring the time and effort of significant others, can preclude other appropriate care of the patient at home. Overall, physicians should feel comfortable informing the patient and family that there is no evidence to suggest that, in patients with cancer anorexia and cachexia, increased caloric intake will improve patient survival or quality of life. Therefore, family members should be encouraged to provide the patient with whatever nutrition he or she desires and is able to tolerate, but they should refrain from trying to force feed the patient. A FEW PATIENTS BENEFIT Although most patients with advanced, metastatic cancer will not derive any survival benefit from artificial nutrition, certain exceptions do occur. Patients with inoperable, malignant bowel obstruction, a lack of symptomatic involvement of critical organs (eg, brain, liver, or lung), a relatively indolent course of disease, and a good performance status can have prolonged survival with the use of enteral or parenteral nutrition.23,24 However, these patients represent a small subset of patients with advanced cancer. The use of artificial nutrition in patients with advanced malignancy should be considered only under exceptional circumstances. THE ROLE OF THE TIME-LIMITED THERAPEUTIC TRIAL OF ARTIFICIAL NUTRITION Despite the lack of proven benefit, artificial nutrition at the end of life will remain a sensitive topic for some patients and families. The most important question to ask in this situation is will artificial nutrition help accomplish the goals of the patient? If the physician's judgment is that artificial nutrition would not help achieve the goals of the patient, then the physician should explicitly recommend against this type of feeding. As Cassell25 has argued, to merely present patients with options from which to choose is insensitive to the fact that illness limits the patient's ability to appraise complex information and that a patient seeking the guidance of an authority is now forced to ascertain what the physician really thinks is best. However, if the physician believes that feeding has some potential benefit that outweighs the risks, then the judicious use of enteral or parenteral nutrition may be offered in the context of a time-limited therapeutic trial with clear goals and expectations. An open discussion and exploration of the financial implications of enteral or parenteral nutrition should also be included in the discussion of the risks versus benefits of feeding because insurance limitations may leave the patient and family bearing considerable costs. There are times when the patient or family members are entrenched in the view that feeding should be offered. In this context, it may be reasonable to acquiesce and proceed with a time-limited therapeutic trial. The physicians should clearly delineate to the patient and the family the goals of this therapeutic trial and set a firm date for re-evaluation of those goals, typically in 3 to 4 weeks. If the goals have been met by the trial (for example, improved energy or sense of well-being), it may be reasonable to continue therapy. If the goals have not been met, having agreed on specific criteria for discontinuing treatment can make this transition more acceptable to a patient and family. In this situation, a unified team approach that is individualized to each patient with predefined goals is essential. Ongoing communication between the patient, family members, and the health care team throughout the entire course of the illness, with an effort to prepare the patient and family for future complications, can help provide the best possible relief and prevention of suffering. BACK TO THE CASE After discussing with Mr. Smith and his family his goals for his own care, his current lack of symptoms, and the mechanics of administration of tube feedings, he clearly stated that he "never wanted to be hooked up to tubes." The family was counseled on how they might continue to nurture him in lieu of feedings by helping him with mouth care, bathing, dressing, transfers, massage, readings, and life review and leaving behind a legacy. The family used these approaches to remain intimately involved in his care during this time in hospice. The final 8 weeks of this patient's life were experienced as meaningful and dignified. Authors' Disclosures of Potential Conflicts of Interest The authors indicated no potential conflicts of interest.
NOTES Authors' disclosures of potential conflicts of interest are found at the end of this article. REFERENCES 1. WHO Expert Committee: Cancer Pain Relief and Palliative Care. Geneva, Switzerland, WHO, 1990, pp 11
2. Meisel A, Snyder L, Quill T: Seven legal barriers to end of life care: Myths, realities and grains of truth. JAMA 284:2495-2501, 2000 3. Rousseau P: Ethical and legal issues in palliative care. Primary Care 28:391-400, 2001[Medline] 4. Gordon M, Alibhai SMH: Ethics of PEG tubes: Jewish and Islamic perspectives. Am J Gastroenterol 99:1194, 2004[CrossRef][Medline]
5. Cohen JJ: Remembering the real questions. Ann Intern Med 128:563-566, 1998
6. Arroliga AC, Newman S, Longworth DL, et al: Metaphorical medicine: Using metaphors to enhance communication with patients who have pulmonary disease. Ann Intern Med 137:376-379, 2002
7. Quill TE, Arnold RM, Platt F: "I wish things were different": Expressing wishes in response to loss, futility, and unrealistic hopes. Ann Intern Med 135:551-555, 2001
8. Coulehan JL, Platt FW, Egener B, et al: "Let me see if I have this right": Words that help build empathy. Ann Intern Med 135:221-227, 2001
9. Back AL, Arnold RM, Quill TE: Hope for the best, and prepare for the worst. Ann Intern Med 138:439-443, 2003 10. Jatoi A, Kumar S, Sloan JA, et al: On appetite and its loss. J Clin Oncol 21:79-81, 2003 (suppl 9)
11. McCann RM, Hall WJ, Groth-Juncker A: Comfort care for terminally ill patients: The appropriate use of nutrition and hydration. JAMA 272:1263-1266, 1994 12. Sullivan R: Accepting death without artifical nutrition or hydration. J Gen Intern Med 8:220-224, 1993[Medline] 13. Kalk WJ, Felix M, Snoey ER, et al: Voluntary total fasting in political prisoners: Clinical and biochemical observations. S Afr Med J 83:391-394, 1993[Medline] 14. Nixon DW: Hyperalimentation in the undernourished cancer patient. Cancer Res 42:727s-728s, 1982 (suppl 2) 15. Lundholm K, Daneryd P, Bosaeus I, et al: Palliative nutritional intervention in addition to cyclooxygenase and erythropoietin treatment of patients with malignant disease: Effects on survival, metabolism and function. Cancer 100:1967-1977, 2004[CrossRef][Medline] 16. Loeser C, von Herz U, Küchler T, et al: Quality of life and nutritional state in patients on home enteral tube feeding. Nutrition 19:605-611, 2003[CrossRef][Medline] 17. Pironi L, Ruggeri E, Tanneberger S, et al: Home artificial nutrition in advanced cancer. J R Soc Med 90:597-603, 1997[Abstract] 18. Steiger E, Oram-Smith J, Miller E, et al: Effects of nutrition on tumor growth and tolerance to chemotherapy. J Surg Res 18:455-461, 1975[CrossRef][Medline] 19. Cameron IL, Pavlat WA: Stimulation of growth of a transplantable hepatoma in rats by parenteral nutrition. J Natl Cancer Inst 56:597-601, 1976 20. Daly JM, Copeland EM, Dudrick SJ: Effects of intravenous nutrition on tumor growth and host immunocompetence in malnourished animals. Surgery 84:655-658, 1978[Medline] 21. Marik PE, Pinsky M: Death by parenteral nutrition. Intensive Care Med 29:867-886, 2003[Medline] 22. Alverdy JC, Burke D: Total parenteral nutrition: Latrogenic immunosuppression. Nutrition 11:339-344, 1995[Medline] 23. Ripamonti C, Twycross R, Baines M, et al: Clinical practice recommendations for the management of bowel obstruction in patients with end stage cancer. Support Care Cancer 9:223-233, 2001[CrossRef][Medline]
24. Whitworth MK, Whitfield A, Holm S, et al: Doctor, does this mean I'm going to starve to death? J Clin Oncol 22:199-201, 2004
25. Cassell EJ: Consent or obedience? Power and authority in medicine. N Engl J Med 352:328-330, 2005 Submitted January 5, 2005; accepted June 2, 2005.
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Copyright © 2005 by the American Society of Clinical Oncology, Online ISSN: 1527-7755. Print ISSN: 0732-183X
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