Oral chemotherapy and patient perspective in solid tumors: a national survey by the Italian association of medical oncology

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1 TJ ISSN Tumori 2015; 00(00): DOI: /tj Original Research Article Oral chemotherapy and patient perspective in solid tumors: a national survey by the Italian association of medical oncology Gaetano Aurilio 1, Stefania Gori 2, Franco Nolè 1, Giancarlo Pruneri 3, Francesca Coati 4, Valter Torri 5, Gianluigi Lunardi 2, Francesco Atzori 6, Nicla La Verde 7, Giuseppe Luigi Banna 8, Antonio Rossi 9, Lucia Del Mastro 10, Francesca Di Fabio 11, Ilaria Marcon 12, Vittorio Gebbia 13, Fotios Loupakis 14, Laura Orlando 15, Libero Ciuffreda 16, Placido Amadio 17, Gabriele Luppi 18, Stefania Redana 19, Gianfranco Filippelli 20, Annalisa Gentile 21, Elena Collovà 22 1 Medical Oncology, European Institute of Oncology, Milan - Italy 2 Department of Oncology, Sacro Cuore-Don Calabria Hospital, Verona - Italy 3 Division of Pathology and Laboratory Medicine, European Institute of Oncology, University of Milan School of Medicine, Milan - Italy 4 Medical Oncology, Sacro Cuore-Don Calabria Hospital, Verona - Italy 5 Oncology Department, Institute of Pharmacology Research Mario Negri, Milan - Italy 6 Medical Oncology, University Hospital, Cagliari - Italy 7 Department of Oncology, AO Fatebenefratelli e Oftalmico, Milan - Italy 8 Division of Medical Oncology, Cannizzaro Hospital, Catania - Italy 9 Division of Medical Oncology, S.G. Moscati Hospital, Avellino - Italy 10 Sviluppo Terapie Innovative, IRCCS AOU San Martino, Genova - Italy 11 Medical Oncology, Policlinico S.Orsola-Malpighi, Bologna - Italy 12 Medical Oncology, Ospedale di Circolo e Fondazione Macchi, Varese - Italy 13 Medical Oncology, Università di Palermo, Palermo - Italy 14 Medical Oncology, Polo Oncologico-Azienda Ospedaliero-Universitaria Pisana, Pisa - Italy 15 Medical Oncology & Breast Unit, Antonio Perrino Hospital, Brindisi - Italy 16 S.C. Oncologia Medica, A.O.U. Città della Salute e della Scienza-Molinette, Torino - Italy 17 S.C. Oncologia Medica, ARNAS Garibaldi, Catania - Italy 18 Day Hospital Oncologico, Azienda Ospedaliero-Universitaria, Modena - Italy 19 Oncologia Medica, FPO-IRCCS Università di Torino, Candiolo, Torino - Italy 20 Oncologia Medica, P.O. di Paola-A.S.P. di Cosenza, Paola, Cosenza - Italy 21 Medical Oncology, Ospedale Civile Spirito Santo, Pescara - Italy 22 Division of Medical Oncology, Hospital of Legnano, Legnano, Milan - Italy Abstract Aim: To assess patient perception toward oral chemotherapy for solid tumors, the Italian Association of Medical Oncology performed a large multi-institutional national survey. Methods: A 17-item anonymous questionnaire including 7 general and 10 investigational questions with free-text, single-choice, or multiple-choice answers was administered. Analysis of response distribution according to predefined factors was described by summary measures and conducted by χ 2 test and other nonparametric tests. Results: From January to June 2010, 581 patients completed the questionnaire; data of 404 patients constituted the final study sample. Three groups could be distinguished according to treatment: IV chemotherapy (IV group, n = 313), oral chemotherapy (oral group, n = 48), or combined therapy (combined group, n = 43). Thirty-one (72%) patients in the combined group and 187 (60%) in the IV group expressed preference for oral therapy (p = 0.028). Limitations in family and work commitment were more frequently perceived by patients on IV than oral chemotherapy (147 (47%) vs 14 (29%) patients, p<0.05, and 134 (43%) vs 11 (23%) patients, p<0.05). A total of 134 (43%) patients on IV chemotherapy versus 15 (31%) patients in the oral group did not point out any limitation for number of tablets per day (p = 0.004). Conclusions: We observed a propensity from the patient perspective in favor of oral chemotherapy that was considered to have a lower impact on family and work commitments than IV chemotherapy. The treatment that patients were taking when the questionnaire was administered likely influenced their perception and related results. Keywords: IV chemotherapy, Oral chemotherapy, Patient perspective, Questionnaire, Treatment Accepted: June 8, 2015 Published online: July 2, 2015 Corresponding author: Gaetano Aurilio, MD, PhD European Institute of Oncology Medical Oncology Via G. Ripamonti, Milan, Italy Introduction One-quarter of the anticancer therapies currently under investigation are oral agents (1). The availability of the oral pharmaceutical form of a cytotoxic drug (alternatively to its IV form) or of new molecules exclusively available as oral formulation can represent an advantage for both patients and oncologists. Several studies have reported that most patients prefer oral to IV therapy (2, 3) for reasons related

2 2 Patient perspective and oral chemotherapy to convenience, home treatment, and needle avoidance, although a minority of patients consider IV therapy more effective (4). An all-oral chemotherapy or coupling oral with IV treatments may contribute to improve quality of life (QoL), representing a useful therapeutic approach for patients with cancer. In daily oncology practice, patient preference for oral or IV therapy is sometimes disregarded. Twelves et al (5) demonstrated that preference rates for oral agents versus IV chemotherapy turned from 95% pretreatment to 65% posttreatment, suggesting that patient perception may conceivably change upon oral treatment. Nevertheless, patient compliance with oral treatments remains to be fully elucidated, with figures ranging from 20% to 100% (6-8). On these grounds, in 2010 the Oral Therapy Task Force formed by the Italian Association of Medical Oncology (AIOM) launched a large national survey to assess patient perception and attitude toward oral chemotherapy. Materials and methods The study was evaluated and approved by the Institutional Review Board of the AIOM. Nineteen oncology units well-distributed throughout the country were identified (north: 10; center, south, and isles: 9). A 17-item anonymous questionnaire with single- and multiplechoice questions was administered by each unit to patients treated for solid tumors with oral, IV, or oral plus IV chemotherapy (see Appendix). Informed consent was obtained from each patient who agreed to fill in the questionnaire anonymously. Seven questions on general sample characteristics and 10 investigational questions were answered independently by each patient. All questionnaires were sent to the central collection unit in order to code and analyze the data. Description of questionnaire Questions about age, sex, education, and region (from Q1 to Q4) were distributed as multiple-choice questions admitting only a single answer, while a free-text answer was required for the primary disease (Q5). The 2 items on past and present chemotherapy types (Q6, Q7) were multiple-choice questions admitting multiple answers. Q8, Q11, and Q15 were conceived only for patients on IV chemotherapy; Q9, Q10, Q12, and Q13 for patients on either IV or oral chemotherapy; Q14 for patients on oral therapy; and Q16 and Q17 for patients on either oral or combined therapy. Items Q8, Q12, Q15, Q16, and Q17 were multiple-choice questions admitting only a single answer; Q10, Q11, Q13, and Q14 were multiple-choice questions admitting multiple answers. Statistical analysis Information collected through the questionnaire was entered and coded as numerical code through Stata-12 software dataset. All free-text responses were independently reviewed by 2 of the authors (G.A. and F.C.) in order to ensure a representative but not redundant coding. Multiple-choice questions admitting multiple answers were analyzed as single questions per each possible answer, and an answer was considered not affirmative when the related option button was not clicked on. Three final analysis groups were identified in order to have consistent (present and previous) experience about each type of therapy formulation: patients with only oral chemotherapy experience, patients with only IV chemotherapy, and patients receiving concomitant IV and oral treatments. Investigational questions were analyzed and compared by cross-tabulation tables. Chi-square or Fisher exact tests for categorical variables were used to evaluate any differences among answer proportions of analyzed groups. Fisher exact test was used in place of chi-square test when at least one of the expected frequencies was <1 or when more than 20% of expected frequencies were 5. Results A total of 581 patients completed the questionnaire from January to June 2010, 404 of whom represented the final study population split into 3 patient groups as described above. Forty-eight patients were treated with oral chemotherapy only (oral group), 313 patients with IV chemotherapy only (IV group), and 43 patients with concomitant IV and oral treatment (combined group). The combined group was selected from a mixed group of 165 patients, 43 of whom were on concomitant IV and oral chemotherapy (combined group), 58 on IV chemotherapy with previous oral therapy, and 64 on oral chemotherapy with previous IV therapy. These last 2 groups (122 patients) were not included in the analysis since it was not possible to clearly identify the overall treatment experience when the questionnaire was administered (Tab. I). The 3 groups finally included in the analysis were compared across the investigational questions. General questions Most of the patients were over 55 years of age (68%) (Q1) and female (53%) (Q2); about 22% had completed primary school, two thirds had received middle school or high school education, and 12% had graduated (Q3); 37% of patients came from the north, 37% from the south and isles, and 18% from the center of the country (7% not specified) (Q4); gastrointestinal and breast diseases were the most frequent tumors (Q5); most of the patients had previously experienced IV chemotherapy and were still receiving IV chemotherapy when the questionnaire was administered (Q6 and Q7) (Tab. II). TABLE I - Prior therapy experience of final analysis groups No. (total n = 404) Prior therapy experience IV None Oral Mixed IV Oral Combined

3 Aurilio et al 3 TABLE II - General questions Investigational questions No. (total n = 581) Percentage Q1: Age, y < > Q2: Sex Female Male Q3: Education Primary Secondary Graduate Q4: Geographic region North Italy Central Italy South Italy/isles Not specified 41 7 Q5: Primary cancer Breast Gastrointestinal Lung Others Not specified Q6: Received treatments Surgery 409/ IV chemo 461/ Oral chemo/ht 212/ RT 199/ Q7: Ongoing treatments IV chemo 415/ Oral chemo/ht 292/ RT 19/581 3 Chemo = chemotherapy; HT = hormonal therapy; RT = radiation therapy. Q1-Q5: only one item could be ticked off; Q6, Q7: more than one item could be ticked off. Question 8: If the treatment that you are currently getting is intravenous, which one would you choose if your oncologist offered you the same drug orally? Among the 313 patients on IV therapy, 60% (187 patients) responded that they would switch to oral therapy, while 34% (107 patients) preferred to maintain IV therapy (6% of missing answers). Thirty-one (72%) patients in the combined group expressed preference in favor of oral therapy vs 187 (60%) patients in the IV group (p = 0.028). In most cases, the preference for oral treatment was due to a feeling of convenience (64%, n = 120). The reasons for IV preference among the abovementioned 107 patients were mostly associated with low toxicity with previous therapy (21%), oral intake believed to be difficult (16%), and perception of greater efficacy/disease control of IV vs oral administration (21%). Question 9: Which of the following activities are mainly affected by the current therapy? Daily life activities were assessed in this item, comparing the IV group (n = 313) to the oral group (n = 48). A sizeable proportion of patients felt limited in their family and work commitments: 47% and 31% on IV and oral therapies for family, and 43% and 23% for work commitment, respectively (p<0.05). Of note, 20% of patients from both groups had limitations in their hobbies and sexual activities. Question 10: What would be the potential advantages of switching from intravenous therapy to an oral formulation of the same drug? The explanations in favor of oral treatment were no need for central venous access and fewer working days lost for patients and their family (p<0.01). In detail, 33.9% (n = 106) of patients on IV therapy vs 8.3% (n = 4) of patients on oral therapy considered avoidance of placement of a central venous access advantageous (p<0.001); 23% vs 6.3% (p = 0.008) and 30.7% vs 12.5% of patients (p = 0.009) underlined that fewer working days would be lost, respectively. Question 10 vs Question 8 Potential advantages of oral therapy (Q10) were compared between the 2 groups preferring IV or oral therapy (Q8) (Fig. 1). Meaningful differences (p<0.01) were detected for taking home (51.4% IV vs 80.8% oral therapy, p<0.001), no need for central venous access (24.3% vs 41.2%, p = 0.004), fewer hospital accesses (26.2% vs 55.6%, p<0.001), and fewer working days lost for both patients and their families (14% vs 29.4%, p = 0.003, and 21.5 vs 37.4%, p = 0.005, respectively). Question 11: Which factors do you believe important to switch from an intravenous therapy to an oral therapy, if this opportunity is available? Seventy percent of patients considered oral and IV therapy as equally effective; 43% of patients believed that toxicity would not be higher for oral than IV therapy. Question 11 vs Question 8 The results of Q11 were compared among patient preference groups (Q8) (Fig. 2). A statistically significant difference (p<0.01) was observed for the following characteristics: efficacy at least equal to IV therapy (50.5% IV vs 85% oral preference), efficacy superior to IV therapy (31.8 vs 16%), and toxicity not greater than IV therapy (33.6 vs 50.8%). Question 12: If you received an oral therapy, how many tablets would you be willing to take per day? There was a significant difference (p = 0.004) between the IV and oral therapy groups: 43% of patients on IV therapy did not claim any limitation regarding the number of tablets per day; the limit of 4-6 tablets per day expressed by patients on oral therapy would seem to be the largest contributor to the significant difference (Fig. 3).

4 4 Patient perspective and oral chemotherapy Fig. 1 - Advantages of oral therapy (Q10) versus the 2 groups of IV or oral preference (Q8). *p<0.01. Fig. 2 - Results of Q11 compared among patient preference groups (Q8). *p<0.01. Fig. 3 - Maximum number of tablets per day in intravenous group and oral group. Question 13: What aspects do you feel connected to the maximum number of tablets per day? Intake in relation to meals and therapy-related side effects were the most common concerns within the oral therapy group versus the IV group (25% vs 9%, p = 0.002, and 29% vs 15%, p = 0.012, respectively). Question 14: Which of the following activities would be most affected if you switched from the oral to the intravenous formulation of the same drug? This analysis was restricted to the oral therapy group (n = 48). The results demonstrated that patients most commonly perceived family and work activities would be affected (42% and 25% of patients, respectively). Question 15: How many drugs are you currently taking, apart from chemotherapy and endocrine therapy? This item focused on the IV group (n = 313) and examined non-cancer-specific treatments. Fifty-five percent of patients took no more than 3 drugs and 20% between 4 and 6 drugs. Comparison between Q15 and Q12 showed that concomitant treatments were not considered a significant limitation to the intake of oral chemotherapy (Fisher exact test 0.576). Question 16: If you take an oral chemotherapy, has your oncologist explained to you the possible interactions with the drugs that you usually take? This item considered patients in the oral (n = 48) and combined therapy groups (n = 43), exploring the attitude of oncologists to explain the possible interactions between oral chemotherapy and noncancer agents. The results showed that 85% of oncologists detailed potential drug-drug interactions. Question 17: If you take an oral chemotherapy, has your oncologist given you the appropriate information to pass on to your general practitioner? The same population analyzed in Q16 was the focus of this item. Seventy-nine percent of the patients answered that the oncologist provided the appropriate information to pass on to their general practitioners. Discussion In the present study, we interrogated for the first time Italian patients attitudes towards different methods of taking medications, providing evidence that oral administration was preferred to IV. Oral chemotherapy regimens have emerged to be as effective as IV regimens, leading to an increase in use. Over time, the development of oral drugs has resulted in changes in patients quality of life as well as in the modality of patient management by the oncology team (information on side effects, treatment of toxicity) and in the organization of all outpatient oncologic activities. Many potential advantages have been associated with oral therapy, including convenience and ease of administration (particularly important when patients require prolonged treatment), the opportunity for home-based therapy, which increases infusion-free survival, no need to place central or peripheral venous access and infusion, potential use of fewer resources, and cost reduction. However, several aspects need to be elucidated. In our analysis, among the 313 patients receiving IV chemotherapy, 60% would have preferred taking the same therapy orally, and 31 out of 43 (72%) patients in the combined group favored oral therapy (Q8). However, the availability of both IV and oral formulations for the same drug is currently limited.

5 Aurilio et al 5 The propensity towards oral therapy was not affected by the number of tablets per day, as reported by 43% of the patients in the IV therapy group (Q12). Along this line, the intake in relation to meals and therapy-related side effects were the factors that most influenced the maximum number of tablets tolerated per day (Q13). The intake of oral chemotherapy was not affected by concomitant non-cancer-related drugs (Q15). Interestingly, IV chemotherapy mainly affected patients commitment to family and work (Q9), and the possibility of oral intake was perceived as supportive to work commitments, both for the patients and their family (Q10). Our survey provides evidence that, when asked to consider switching from IV to oral therapy, most of the patients felt the 2 methods of administration were similar in terms of efficacy and toxicity (Q11). Almost half of the patients receiving oral therapy alone stated that shifting to IV formulation would mainly impact on family, rather than professional commitments, emphasizing patient perception to engage their families (Q14). It has to be underlined that administering the questionnaire while patients were already receiving a specific treatment may have influenced patients perception and related answers, thus representing a potential flaw of the present study; likewise, we did not collect detailed clinical-pathologic characteristics of tumors, and the stage of disease may have affected patients social activities. It is worth emphasizing that oncologists provided information about drug-drug interactions to patients and their general practitioners in most cases (Q16, Q17), an attitude possibly improving adherence to (or compliance with) oral chemotherapies. Interactions with other drugs, even unrelated to cancer, and toxicity should be carefully addressed in order to appropriately manage home therapies. Along this line, health staff (doctors, nurses, hospital pharmacists) must be trained to provide patients with appropriate explanations regarding the administration route, timing, intake modalities, and toxicity management. Likewise, educating patients may prevent a number of potential problems including underdosing or overdosing. In this regard, it is important for cancer teams to have ad hoc meetings with patients, ensuring day-long availability for both physical and telephone examinations. It has been reported that adherence is not a consistent finding, ranging from 20% to 100% in different studies (6), and adherence-oriented research is considerably limited. These data point towards the need for prospective clinical trials designed to comparatively investigate the efficacy of oral and IV chemotherapy and assess patient perception and attitude, such as the Twelves et al (5) study and PISCES trial (9). To this aim, an educative AIOM-sponsored study promoting adherence in patients treated with oral therapies is ongoing. The project is also evaluating the role of nurses in helping patients to make informed decisions and to acquire a role as active partners. Acknowledgment The authors thank the Associazione Italiana Oncologia Medica for the conception and design of the research. Disclosures Financial support: None. Conflict of interest: None. References 1. Banna GL, Collovà E, Gebbia V, et al. Anticancer oral therapy: emerging related issues. Cancer Treat Rev. 2010;36(8): Liu G, Franssen E, Fitch MI, Warner E. Patient preferences for oral versus intravenous palliative chemotherapy. J Clin Oncol. 1997;15(1): Borner MM, Schoffski P, de Wit R, et al. Patient preference and pharmacokinetics of oral modulated UFT versus intravenous fluorouracil and leucovorin: a randomised crossover trial in advanced colorectal cancer. Eur J Cancer. 2002;38(3): Catania C, Didier F, Leon ME, et al. Perception that oral anticancer treatments are less efficacious: development of a questionnaire to assess the possible prejudices of patients with cancer. Breast Cancer Res Treat. 2005;92(3): Twelves C, Gollins S, Grieve R, Samuel L. A randomised crossover trial comparing patient preference for oral capecitabine and 5-fluorouracil/leucovorin regimens in patients with advanced colorectal cancer. Ann Oncol. 2006;17(2): Partridge AH, Avorn J, Wang PS, Winer EP. Adherence to therapy with oral antineoplastic agents. J Natl Cancer Inst. 2002; 94(9): Escalada P, Griffiths P. Do people with cancer comply with oral chemotherapy treatments? Br J Community Nurs. 2006; 11(12): Foulon V, Schöffski P, Wolter P. Patient adherence to oral anticancer drugs: an emerging issue in modern oncology. Acta Clin Belg. 2011;66(2): Escudier B, Porta C, Bono P, et al. Randomized, controlled, double-blind, cross-over trial assessing treatment preference for pazopanib versus sunitinib in patients with metastatic renal cell carcinoma: PISCES Study. J Clin Oncol. 2014;32(14):

6 6 Patient perspective and oral chemotherapy Appendix Questionnaire 1. How old are you? (single answer admitted) 55 years years <40 years 2. Which is your sex? (single answer admitted) Females Men 3. Which is your education level? (single answer admitted) Middle school High school Primary school University degree 4. Where are you from? (single answer admitted) Northern Italy Southern Italy/Islands Central Italy 5. Which is your primary disease? (free text answer) 6. Which kind of treatment did you previously receive for your disease? (multiple answers admitted) Intravenous therapy Oral therapy None therapy 7. What treatment are you getting now? (multiple answers admitted) Intravenous therapy Oral therapy None therapy 8. If the treatment that you are currently getting is intravenous, which one would you choose if your oncologist offered you the same drug orally? (single answer admitted) Oral Intravenous 9. Which of the following activities are mainly affected by the current therapy? (multiple answers admitted) Work commitment Family commitment Hobby Sexual activity Other 10. What would be the potential advantages of switching from intravenous therapy to an oral formulation of the same drug? (multiple answers admitted) Taking home No need for central venous access Less access to hospital Fewer working days lost for myself Fewer working days lost for my family members Fewer money lost (travel and other support) 11. Which factors do you believe important to switch from an intravenous therapy to an oral therapy, if this opportunity is available? (multiple answers admitted) Efficacy al least equal to intravenous therapy Toxicity not superior to intravenous therapy Efficacy superior to intravenous therapy 12. If you received an oral therapy, how many tablets would you be willing to take per day? (single answer admitted) 1-3 tab/die 4-6 tab/die No limit 13. What aspects do you feel connected to the maximum number of tablets per day? (multiple answers admitted) Maximum number of doses per day (1-2-3 times a day) Intake in relation to meals Taking other drugs Inability to take large tablets Disorders related to therapy Efficacy of the therapy on my symptoms (before or fasting) It does not depend of any of these factor 14. Which of the following activities would be most affected if you switched from the oral to the intravenous formulation of the same drug? (multiple answers admitted) Work commitment Family commitment Hobby Sexual activity Other 15. How many drugs are you currently taking, apart from chemotherapy and endocrine therapy? (single answer admitted) none 1-3 drugs 4-6 drugs >6 drugs 16. If you take an oral chemotherapy, has your oncologist explained to you the possible interactions with the drugs that you usually take? (single answer admitted) Yes No 17. If you take an oral chemotherapy, has your oncologist given you the appropriate information to pass on to your general practitioner? (single answer admitted) Yes No

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