Originally published as JCO Early Release 10.1200/JCO.2003.08.091 on July 21 2003

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Are Older French Patients As Willing As Older American Patients to Undertake Chemotherapy?

From the H. Lee Moffitt Cancer Center and Research Institute and the University of South Florida, Tampa, FL; the Lyon University, Centre Léon-Bérard, and Hôpital Antoine Charial, Lyon, France; and the Centre de Soins Continus (Cesco), University of Geneva, Switzerland.

Address reprint requests to Martine Extermann, MD, Senior Adult Oncology Program; Moffitt Cancer Center; 12902 Magnolia Dr, Tampa, FL 33612; e-mail: extermann{at}moffitt.usf.edu.

	ABSTRACT

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION APPENDIX REFERENCES

 
Purpose: A view often held in Europe is that older Europeans are less willing than older Americans to undertake chemotherapy. This study assesses whether this view is valid.

Patients and Methods: Three-hundred twenty outpatients aged 70 years and older were interviewed via anonymous questionnaires: French patients with and without cancer and American patients with and without cancer. The response rate was 61% (195 of 320 questionnaires). Ages ranged from 70 to 95 years (29% aged 80 years and older). Two scenarios were presented: a strong chemotherapy (platinum/taxane combination–like) and a milder chemotherapy (weekly vinorelbine–like). The options were to refuse chemotherapy or to accept for a threshold chance of cure, of life prolongation, or of symptom relief. Functional status, education, self-rated health, and depression were controlled for.

Results: French noncancer patients (34%) were less willing to accept the strong chemotherapy than French cancer patients (77.8%), American noncancer patients (73.8%), and American cancer patients (70.5%) (P < .001 for each pair). This was also true for the moderate chemotherapy (67.9% v 100%, 95.2%, and 88.5%, respectively; P < .001). Age and sex did not correlate with response, but self-rated health, cancer status, and nationality did. Thresholds varied from patient to patient.

Conclusion: Whereas older French people without cancer are more reluctant than older Americans to envision chemotherapy, older cancer patients in both countries have the same amenability to treatment. Chemotherapy options should be fully discussed with older cancer patients, given that most are willing to consider them.

	INTRODUCTION

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HALF OF all cancers occur in patients older than 70 years. Chemotherapy given alone or as part of a combined treatment regimen is often among their management options, and it is well tolerated in many elderly patients with cancer. Counseling by primary physicians and oncologists is influenced by assumptions about the willingness of the older patient to undergo various treatments. However, little information is available that focuses on the influence of age and culture on patient decision-making about cancer treatment.

In an American study,¹ no difference in the acceptance of chemotherapy was observed between older and younger cancer patients, but they differed in their willingness to exchange survival for current quality of life. In another American study,² patients older than 60 years tended to have higher thresholds of acceptance for chemotherapy. In a British study, cancer patients (median age, 60 years) were more likely than people without cancer to choose an intensive chemotherapy for a minimal chance of benefit.³ A Norwegian study found the same trend in younger patients, but older patients were more conservative.⁴ It is not clear whether these different results are due to variances in study design (eg, sample selection or regimen description) or to social or cultural differences. There is sparse evidence that European patients differ from their American counterparts on certain aspects. In a survey of British and American cancer patients with an average age of 51 and 57 years, respectively,⁷ American patients wanted more information about disease and treatment compared with the British patients. However, the study did not investigate further patient preferences for specific treatments. To our knowledge, no study has been published that compares the treatment preferences of elderly cancer patients in the United States with those in European countries.

A direct study of the willingness of elderly patients to undergo chemotherapy is critical. In the aforementioned studies, patient preferences were different from those of physicians, nurses, and caregivers and were also influenced by age.^3,4 However, physicians have a strong influence on their patients’ treatment choices. In a study by Newcomb and Carbone,⁵ the most common reasons for not selecting specific treatments were physician recommendations and the desire for more comprehensive treatment. If physicians have an inaccurate perception of the willingness of elderly patients to undertake chemotherapy, they might not refer patients to oncologists, they might reject potentially useful treatment options, or they might propose futile treatments.^5,8 A general impression among physicians, particularly those in Europe, is that attitudes among elderly cancer patients regarding chemotherapy in the United States differ from those in Europe. In the experience of the investigators, many European physicians apply a "corrigendum" to American literature toward less aggressiveness in older patients, with therapeutic consequences.⁶ Studies show that the willingness of a substantial number of younger patients to undertake treatment is within the range of what can be offered^3,4,8 and higher than that of the general population. Is the same true for older patients? If so, to what extent? Answers to these questions could influence not only physician appraisal of the literature and thus referral practices and/or proposed treatments,^5,6,8 but also policy making (eg, developing geriatric oncology units, more objective ground for discussions between geriatricians and oncologists), timing of discussion for living wills, physician and public education, and design of treatment guidelines using results of studies from different countries.

We designed this cross-national study to compare the differences, if any, in the willingness to undergo chemotherapy between elderly American and French cancer and noncancer patients. Our hypothesis was that whereas a cultural difference might be seen between American and French noncancer patients, this difference might be narrower between cancer patients from those countries.

	PATIENTS AND METHODS

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION APPENDIX REFERENCES

 
Subjects
The study sample consisted of four groups of 80 patients 70 years and older. The two cancer outpatient groups were recruited from the Senior Adult Oncology Program (SAOP) at the H. Lee Moffitt Cancer Center in Tampa, Florida, and the SAOP at the Centre Léon-Bérard in Lyon, France. A consecutive sample of patients treated between 1999 and 2000 for solid or hematologic tumor, regardless of tumor stage and pathologic type, was selected. A consecutive sample of geriatric outpatients without cancer history (except for skin cancer) was recruited from the outpatient geriatric clinics at the University of South Florida in Tampa and at the Hôpital Antoine Charrial in Lyon. All four sites are academic centers that provide tertiary care. A general exclusion criterion was medical diagnosis of dementia (Diagnostic and Statistical Manual of Mental Disorders, 4) as identified from medical records.

Questionnaires
Our cross-sectional study compared patient responses to an anonymous questionnaire in which two chemotherapy regimens were described, along with their respective side effects. (See Appendix.) The first regimen was described as a "strong chemotherapy" and was based on a platinum/taxane–like combination. The second chemotherapy was described as a "mild chemotherapy" and was based on a weekly vinorelbine–like regimen. The framing was negative to positive (ie, describing the side effects, and then asking for the expected benefit), in keeping with the format used by most similar studies.^2–4 After reading about the side effects of the treatment, patients were asked to express their willingness to undertake the treatment under varying chances of cure, prolongation of survival, and symptom relief. They were asked to specify the minimal benefit that would make the hypothetical treatment acceptable. They also had the option of refusing the treatment altogether. This method has been successfully applied in other studies.^3,4 The outcome measures were the willingness to accept each chemotherapy regimen and the expected minimal benefits. The questionnaire was designed in American English and translated to standard French. We used a forward translation by a bilingual physician in Tampa (M.E.) and a review by another bilingual physician in French-speaking Switzerland (G.Z.). All American patients and most French cancer patients received the questionnaire by mail. Because some cultural concerns about potential reactions of the patients arose in Lyon, a research nurse gave the questionnaire to the remainder of the cancer patients and the geriatric patients when they arrived for an outpatient visit, to allow feedback. In all cases, patients answered the questionnaire anonymously with no health professional present. Duric and Stockler⁹ recently showed that results about the willingness of cancer patients to receive treatment are consistent across methods.

We controlled for several potential confounding factors. Functional status was assessed with the self-reported Lawton’s 9-item Instrumental Activities of Daily Living Scale¹⁰ and the Eastern Cooperative Oncology Group (ECOG) Performance Status.¹¹ We screened for depression using the Geriatric Depression Scale (Short Form).¹² All instruments were presented in French or English according to patient population. Self-rated health was rated on a four-point Likert scale, from poor to excellent. The correlation between depression and self-rated health is not equivalent across cultures, thus requiring a separate rating.^13,14 For example, in the Seven Countries Study, respondents in Italy admitted more frequently than those in Finland to being depressed but reported better self-rated health.¹⁴ The following information was also collected: marital status, education, presence of a caregiver, tumor type, and previous treatment (eg, surgery, chemotherapy, radiation therapy).

Statistical Analysis
Assuming that 95% of patients would respond to items regarding minimal percentages of chances of cure and symptom relief with answers between 10% and 90%, we estimated the standard deviation to be 20%. To have 80% power for a pooled t test if the difference in means was 20%, we needed 24 patients per group. With the asymptotic relative efficiency of the Wilcoxon rank sum test relative to the t test being at least 0.86, the number of patients needed per group was 28 (24 divided by 0.86). The response rate was approximately 50% in published studies.^3,4 We assumed a conservative 35% response rate. Thus, a sample size of 80 patients per group was chosen.

Descriptive data regarding patients’ demographic and health characteristics were summarized and compared with ² tests and one-way analysis of variance (ANOVA).

The percentages of patients who accepted treatment in the two countries were compared in the cancer and noncancer groups separately, using ² tests. The Bonferroni adjustment was made in accordance with the four pairwise comparisons, giving a threshold for significance of 0.0125 (0.05/4). If the difference was significant between two groups, the patient characteristics of those who accepted the regimen and those of rejected the regimen were compared by country or cancer status. Variables that correlated (P < .1) at the univariate level were entered into separate logistic regression models to determine the independent factors associated with the acceptance of strong and moderate chemotherapy. Threshold values of benefit for patients who accepted treatment were compared with a Wilcoxon rank sum test. We performed all analyses using the Statistical Package for the Social Sciences software, version 10.1 (SPSS Inc, Chicago, IL).

Ethical Considerations
This project was approved by the institutional review board of the University of South Florida. In Lyon, the Protocol Review Commission of the Centre Léon-Bérard and the Hospital Antoine Charrial considered the protocol to fall in the exempt-from-review category. The questionnaires included an institutional review board–approved information letter, and the return of the questionnaires was considered to mean patient consent to the study.

	RESULTS

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION APPENDIX REFERENCES

 
The questionnaires were completed by 195 patients (61%). The response rates per group were as follows: American cancer patients, 78% (n = 62); American noncancer patients, 54% (n = 43); French cancer patients, 45% (n = 36); and French noncancer patients, 68% (n = 54) (P < .01). This level of response is similar to that obtained by the most cited comparative questionnaire studies in the field.^3,4 Since this was an anonymous survey, no systematic attempt was made to analyze differences between responders and nonresponders.

Table 1 presents the patients’ characteristics. The average age of all 195 patients was 77 years (range, 70 to 95 years). Because several characteristics were statistically different among the groups, the influence of these imbalances on study outcome was carefully analyzed with multivariate logistic regression models.

	DISCUSSION

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION APPENDIX REFERENCES

Another striking element is the high level of willingness to consider chemotherapy. Elderly patients in both countries want chemotherapy to be an available option. However, it should also be noted that the expected benefit was, on average, high, despite a wide variability in threshold. In this risk scenario, the patients in our survey appeared to have used as a group a two thirds to one-third rule—that is, a two-thirds chance of benefit for a one-third risk of no benefit. Interestingly, similar mean thresholds were observed for survival and symptom relief (Table 4). This latter point would indicate that older patients highly value symptom relief as an outcome from chemotherapy, an important consideration in the palliative setting. This result is similar to those observed by Bremnes et al.⁴ Conversely, Slevin et al³ observed a higher threshold for palliative effects than for curative effects. Nevertheless, the threshold expressed as a group by the patients in our survey is often beyond what is achievable in many settings.

So do our results mean that most elderly patients should receive chemotherapy, since most are willing to consider it under proper conditions? Or do they mean that most elderly patients should not receive chemotherapy, given that the thresholds expressed here are for the most part in a range beyond what chemotherapy is able to achieve?

To interpret this study correctly, several points must be taken into account. First, our study was designed to be biased against chemotherapy in order to have a conservative threshold: negative-positive framing, 6 months’ duration of chemotherapy, and no cancer-related survival specified. In other words, at the end of this study, we wanted to be able to state with reasonable confidence that at least a certain percentage of elderly patients was willing to envision chemotherapy and that the average benefit requested was, at highest, another given percentage. This approach was deemed to be the most likely to be sensitive to global cultural differences, the main end point of this study, in simple case scenarios. This study was not designed to address the impact of more favorable presentations of the treatment, such as the ones discussed below.

As a second point, in real situations, elderly patients regularly accept chemotherapies for much lower benefit thresholds than those presented in this study. There may be several reasons for this difference. One is a difference in the framing of the questions. The most common approach used in clinics is a threat (eg, "Your cancer cannot be cured"), response ("But we can try to control it for a while with chemotherapy"), risks ("Here are the side effects"), and benevolent conclusion ("I believe it is your best option") framing. Another possibility is that clinicians may present benefit information in a two-thirds to one-third format, such as, "If I give you chemotherapy for your metastatic colon cancer, there is a one-third chance of shrinking it, a one-third chance of stabilizing it, and a one-third chance that it may not respond." Physicians also gain acceptance from patients by promising early stopping in case of toxicity or noneffect.

A third point is that the decision-making literature shows that older patients are not unique in expecting high benefits from their chemotherapy. A study conducted in patients with advanced ovarian cancer (median age 55 years) showed that patients had overly high expectations concerning their chemotherapy. Nevertheless, chemotherapy was providing an improvement in their quality of life despite low response rates.¹⁶ Physicians are not immune to hope, but whether their estimates of treatment benefit are accurate is a matter of controversy.^15,17 In this setting, tools that allow an objective estimate of benefits can help the discussion, especially when such tools are available in a format designed for the elderly.⁸

A fourth comment is that because our patient populations were being treated in academic centers, the observation might arise that they were more willing to undertake treatment. Silvestri et al² studied lung cancer patients from three practice settings: an academic center, two veterans’ hospitals, and two private practices. The patients who tended to be most eager to undergo treatment were those treated in private practices, whereas those in the academic center were the most reluctant. Our response rate was approximately two thirds of patients contacted. Although we did not attempt to assess the characteristics of nonresponders, anecdotal feedback suggests they were at both ends of the spectrum of willingness. Because our data are consistent with other studies in the field, we believe that a major selection bias is unlikely. Furthermore, as we took the precaution of assessing several health variables, we can characterize positively the type of patients who answered our questionnaires. Therefore, we believe that, within the limits imposed by the method itself, our results can be extrapolated to the general oncogeriatric population.

Additional investigation will be needed to further understand the decision-making process in older cancer patients. However, at this point, we can already state the following: neither in France nor in the United States should information about the option of chemotherapy, curative or palliative, be withheld from elderly patients on the assumption that they would not be willing to consider it. This study demonstrated this assumption to be false. It also demonstrated that French and American cancer patients share similar thresholds in their expectations of a curative or palliative effect from chemotherapy. Whether each patient will or will not judge the benefit to be worth the toxicity is to be established in a shared and objective decision-making process, given the wide interindividual variations observed in our cohort.

Our study is the first of its kind to control for several confounding variables. This proved helpful in that it allowed us to analyze the differences between French geriatric noncancer patients and the other groups as not being due to age or sex, but to self-rated health and nationality or culture. As a group, the French patients rated their health as worse than that of the American patients. Part of this may be explained by functional status, but undeniable differences exist between cultures regarding self-rated health, even after adjustment for functional variables.¹⁴ Because this is a major influence in decision making, this aspect warrants further research and offers a potential for intervention. For example, the design of our study did not consider detailed assessments of comorbidities and illness experience (cancer included). These previous experiences likely had some influence in shaping the decisions of both geriatric and cancer patients and would be a rich field of research.

Our finding that oncologic groups in both countries were similarly willing to undertake chemotherapy suggests that the types of regimen offered to patients on both continents should be similar. Our study also challenges the assumption that there is generally less willingness by elderly French (and, most likely, other European) cancer patients to accept side effects and risks of treatment. The lesser willingness of French geriatric patients compared to their American counterparts likely reflects a cultural phenomenon. It is therefore interesting to note that a life-threatening disease makes these cultural differences disappear.

In summary, chemotherapy options should not be withheld from discussion with older patients. To the contrary, benefits and risks should be presented as objectively as possible and the patient’s opinion sought in the decision-making process. In applying the results of studies conducted in other countries to clinical practice, physicians should assume an equal willingness of older American and French patients—and likely also other European patients—to consider chemotherapy.

	APPENDIX

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION APPENDIX REFERENCES

 
The following were questions posed by the questionnaire:

Scenario #1: Strong chemotherapy

Suppose that you have a cancer that can be treated with a strong chemotherapy for 6 months.

This chemotherapy would take a whole day every month to give, as an outpatient. It would make you tired and make you lose your hair for the duration of the treatment. It would make you nauseated for some days. It may cause you diarrhea, muscle aches, tingling, or numbness in your fingers. It would increase your risk of bleeding or infection. There is a fairly high risk that you may need antibiotics in a hospital for several days. To reduce that risk, you would receive injections under the skin for 1 week after each chemotherapy (in the outpatient clinic or at home).

What is the MINIMUM benefit for which you would accept this chemotherapy? Please answer all three points.

1. A. . . . . . . . . . . % chance of curing your cancer (1% to 100%)

2. A prolongation of your survival of (check one)

1 month 3 months 6 months 9 months 1 year 15 months 18 months 21 months 2 years

3. A. . . . . .% chance of reducing symptoms from your tumor (such as pain, loss of appetite, being tired) (1% to 100%)

or 4. I would never accept such a chemotherapy whatever the benefit

Scenario #2: Mild chemotherapy

Suppose now that you have a cancer that can be treated with a milder chemotherapy for 6 months.

This chemotherapy would take one hour every week. It may make you tired the day after the chemotherapy, rarely more. You would keep your hair. You may have a bit of nausea, easily controlled with pills. You may experience mouth sores or diarrhea. You may experience an increased risk of bleeding or infection, but these risks are moderate. Your risk of needing hospitalization for antibiotics would be low.

What is the MINIMUM benefit for which you would accept this chemotherapy? Please answer all three points.

1. A. . . . . . . . . . . % chance of curing your cancer (1% to 100%)

2. A prolongation of your survival of (check one)

1 month 3 months 6 months 9 months 1 year 15 months 18 months 21 months 2 years

3. A. . . . . . . % chance of reducing symptoms from your tumor (such as pain, loss of appetite, being tired) (1% to 100%)

or 4. I would never accept such a chemotherapy whatever the benefit

	ACKNOWLEDGMENTS

 
We thank Linda Stenglein for her editorial assistance. We also thank all the participants who helped us improve our knowledge of decision-making by senior persons.

	REFERENCES

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION APPENDIX REFERENCES

 
1. Yellen SB, Cella DF, Leslie WT: Age and clinical decision making in oncology patients. J Natl Cancer Inst 86:1766–1770, 1994[Abstract/Free Full Text]

2. Silvestri G, Pritchard R, Welch HG: Preferences for chemotherapy in patients with advanced non-small cell lung cancer: A descriptive study based on scripted interviews. BMJ 317:771–775, 1998[Abstract/Free Full Text]

3. Slevin ML, Stubbs L, Plant HJ, et al: Attitudes to chemotherapy: Comparing views of patients with cancer with those of doctors, nurses, and general public. BMJ 300:1458–1460, 1990[Abstract/Free Full Text]

4. Bremnes RM, Andersen K, Wist EA: Cancer patients, doctors and nurses vary in their willingness to undertake cancer chemotherapy. Eur J Cancer 31:1955–1959, 1995[CrossRef]

5. Newcomb PA, Carbone PP: Cancer treatment and age: Patient perspectives. J Natl Cancer Inst 85:1580–1584, 1995

6. Benjamin RS, Rouëssé J, Bourgeois H, et al: Should patients with advanced sarcomas be treated with chemotherapy? Eur J Cancer 34:958–965, 1998[CrossRef][Medline]

7. Newall DJ, Gadd EM, Priestman TJ: Presentation of information to cancer patients: A comparison of two centres in the UK and USA. Br J Med Psychol 60:127–131, 1987

8. Extermann M, Balducci L, Lyman GH: What threshold for adjuvant therapy in older breast cancer patients? J Clin Oncol 18:1709–1717, 2000[Abstract/Free Full Text]

9. Duric V, Stockler M: Patients’ preferences for adjuvant chemotherapy in early breast cancer: A review of what makes it worthwhile. Lancet Oncol 2:691–697, 2001[CrossRef][Medline]

10. Lawton MP: Scales to measure competence in everyday activities. Psychopharm Bull 24:609–614, 789–791, 1988[Medline]

11. Zubrod CG, Schneiderman M, Frei E, et al: Appraisal of methods for the study of chemotherapy in man: Comparative therapeutic trial of mustard and triethylene thio-phosporamide. J Chron Dis 11:7–33, 1960

12. Sheikh JJ, Yesavage JA. Geriatric Depression Scale (GDS): Recent evidence and development of a shorter version, in Brink TL (ed): Clinical Gerontology: A Guide to Assessment and Intervention. New York, NY, Haworth Press, 1986, pp 165–173

13. Extermann M, Aapro M: International issues, in Hunter CP, Johnson KA, Muss HB (eds): Cancer in the Elderly. New York, NY, Marcel Dekker, 2000, pp 459–476

14. Jylhä M, Guralnik JM, Ferrucci L, et al: Is self-rated health comparable across cultures and genders? J Gerontol 53B:144–152, 1988

15. Rajagopal S, Goodman PJ, Tannock IF: Adjuvant chemotherapy for breast cancer: Discordance between physicians’ perception of benefit and the results of clinical trials. J Clin Oncol 12:1296–1304, 1994[Abstract/Free Full Text]

16. Doyle C, Crump M, Pintilie M, et al: Does palliative chemotherapy palliate? Evaluation of expectations, outcomes, and cost in women receiving chemotherapy for advanced ovarian cancer. J Clin Oncol 19:1266–1274, 2001[Abstract/Free Full Text]

17. Loprinzi CL, Thomé SD: Understanding the utility of adjuvant systemic therapy for primary breast cancer. J Clin Oncol 19:972–979, 2001[Abstract/Free Full Text]

Submitted August 14, 2002; accepted February 20, 2003.

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