Background: For patients with breast cancer treated with certain chemotherapy regimens, taste disorders associated with those regimens can negatively affect quality of life.
Objectives: This study evaluated the effects of taste disorder–related education on meal satisfaction and sense of taste in Japanese women with breast cancer undergoing chemotherapy.
Methods: A sample of 53 newly diagnosed women with breast cancer scheduled for chemotherapy treatment were randomly assigned to the control or intervention (nurse-provided education about chemotherapy-associated taste disorders) group. Meal satisfaction and sense of taste were assessed using a visual analog scale.
Findings: The proportions of patients with meal dissatisfaction and impaired sense of taste were lower in the intervention group than in the control group. Although meal dissatisfaction and impaired sense of taste recovered in the intervention group two months after protocol completion, they did not recover in the control group. Providing education to women with breast cancer scheduled for chemotherapy treatment can affect patients’ experience of treatment-associated taste disorders.
Taste disorder (TD), a possible adverse effect experienced by patients with cancer treated with certain chemotherapies (Wagland et al., 2016), is caused by injury to the taste buds (Epstein et al., 2016; Nagraj et al., 2014). A cross-sectional study reported that the prevalence of TDs among patients with colon cancer, breast cancer, lung cancer, and lymphoma were 78%, 68%, 67%, and 67%, respectively (Ponticelli et al., 2017). Certain chemotherapy regimens are associated with various taste dysfunctions, such as hypogeusia (decline in taste sensitivity), hypergeusia (increase in taste sensitivity), and ageusia (lack of taste sensitivity) (IJpma et al., 2015; Sozeri & Kutluturkan, 2015). Chemotherapy-associated TDs (CATDs) can begin when a patient first receives treatment or immediately after treatment begins; they can persist during treatment cycles and eventually resolve within a few months to a year after completing the regimen (Boltong et al., 2014; de Vries, Boesveldt, et al., 2018; de Vries, Winkels, et al., 2018; Marinho et al., 2017).
About 50% of patients with breast cancer experience TDs. Taxane regimens are associated with TDs (Amézaga et al., 2018; Campagna et al., 2018). One study’s results suggested that patients with breast cancer and a TD can experience lower quality of life than those without a TD (de Vries, Boesveldt, et al., 2018). CATDs can adversely affect nutritional status, which can then affect physical, psychological, and social status (de Vries, Boesveldt, et al., 2018).
Rehwaldt et al. (2009) evaluated whether patients who were educated about TDs could better cope with them. They developed a taste suggestion sheet to educate patients with cancer who were prescribed chemotherapy. More than 70% of the study participants responded that the education was helpful. Another study found that instructing patients with breast cancer about the adverse effects of chemotherapy (e.g., anorexia, nausea, vomiting) before treatment reduced the frequency of negative effects (Williams & Schreier, 2004). In addition, patients with cancer were reported to want information about such adverse effects before deciding to undergo chemotherapy (Piredda et al., 2008).
Educating patients about CATDs before starting treatment may help them cope with TDs (Williams & Schreier, 2004). The aim of this study was to evaluate the effects of TD-related education on meal satisfaction and sense of taste in a sample of Japanese women with breast cancer undergoing chemotherapy.
This was an interventional, multicenter, randomized study that recruited outpatients scheduled to receive breast cancer treatment at seven Japanese hospitals (six in Hiroshima and one in Hakodate) from June 2014 to December 2017.
The inclusion criteria were women who were newly diagnosed with breast cancer; were aged 20 years or older; were scheduled to receive neoadjuvant or adjuvant chemotherapy with an anthracycline- and taxane-based regimen; had an Eastern Cooperative Oncology Group performance status score of 0 to 1; and had no preexisting problems with their sense of taste, oral cavity, swallowing, or communication. The exclusion criteria were as follows: stage IV (according to the TNM [tumor, node, metastasis] staging system) or recurrent breast cancer; a history of receiving other chemotherapy regimens for cancer; a history of radiation therapy in the oral cavity or salivary gland area; a history of surgery in the oral cavity; a history of zinc administration for idiopathic TDs; severe renal dysfunction; hemolysis; severe liver dysfunction; diabetes; psychiatric disorder; and oral cavity cancer.
In accordance with the Declaration of Helsinki, this study was approved by the institutional review board of Hiroshima University. Physicians identified potential study patient participants. Nurses then followed up with patients, explaining the study. If a patient agreed to participate, nurses obtained informed consent.
An education booklet was developed to instruct the intervention group (IG) (see Figure 1). It was produced based on previous studies of CATDs (Hong et al., 2009; Rehwaldt et al., 2009; Speck et al., 2013). It was reviewed by three patients with breast cancer who had experienced CATDs but were not enrolled in this study. During the three-week review process, one reviewer suggested making the booklet easier to read. Based on their experiences, two reviewers commented about food used to counterbalance for TDs. Owing to reviewer comments, elusive words were changed to increase patient understanding, and sentences relating to food to counterbalance for TDs were added. The modified booklet was then reviewed by a certified oncology nurse, a breast surgeon, and a nutritionist.
Anthracycline chemotherapy regimens were administered as follows: epirubicin and cyclophosphamide (60–90 mg/m2 and 600 mg/m2, respectively, administered on the first day); doxorubicin and cyclophosphamide (50–60 mg/m2 and 600 mg/m2, respectively, administered on the first day); 5-fluorouracil, epirubicin, and cyclophosphamide (500 mg/m2, 90–100 mg/m2, and 500 mg/m2, respectively, administered on the first day); and cyclophosphamide, doxorubicin, and 5-fluorouracil (500 mg/m2, 50–60 mg/m2, and 500 mg/m2, respectively, administered on the first day). Each regimen was repeated every 21 days for up to four cycles.
Taxane chemotherapy regimens were administered as follows: weekly paclitaxel (80–100 mg/m2 administered on days 1, 8, and 15) repeated every three to four weeks for up to four cycles and docetaxel (75 mg/m2 administered on day 1) repeated every 21 days for up to four cycles. Anthracycline- and taxane-based regimens are usually administered to women with breast cancer as the sequential first or second half of chemotherapy. Each treatment is administered for up to four cycles, and both regimens can be delivered as the first half of breast cancer chemotherapy. In addition, all patients with breast cancer received antiemetic agents before chemotherapy.
After participants were consented for the study, they were randomly assigned to groups; the control group (CG) or IG. The CG received the chemotherapy regimen as prescribed, standard side effect management, and standard nursing care. The IG received the chemotherapy regimen as prescribed, standard side effect management, and nursing care, as well as the education intervention.
The intervention included nurse-provided education (review of the booklet) for about 30 minutes before the patient started the chemotherapy regimen. The nurse also supported patients during the treatment period. During each regimen’s second cycle, the nurse conducted TD evaluations, in which each patient was asked about TDs throughout the treatment period. The nurse instructed patients on how to manage TDs based on the booklet contents. Patients in the CG and IG received treatment doses optimized to produce minimal adverse effects. Although patients were treated at different hospitals, all patients in the IG received the same support.
Data Sources and Measurement
Demographic and clinical data were obtained from patients’ medical records. Questionnaires on meal satisfaction and sense of taste were completed by all patients before starting chemotherapy. Because patients with breast cancer recovered their sense of taste by day 15 of each chemotherapy cycle, additional questionnaires were completed for each cycle and midway through the treatment period. All patients answered the same questionnaires two months after completing chemotherapy.
Patients were monitored for the following five adverse effects associated with meal satisfaction and sense of taste in women undergoing chemotherapy: oral mucositis, oral pain, anorexia, nausea, and vomiting. The severity of these negative effects were assessed and categorized from grades 1 to 5 using the Common Terminology Criteria for Adverse Events (CTCAE), version 4.0 (National Cancer Institute, 2017); a higher CTCAE grade indicates more severe adverse events, and patients with grades 3 or greater were considered to have severe chemotherapy-associated adverse events. In addition, patients’ meal satisfaction and sense of taste were assessed using a visual analog scale (VAS) that tested as valid and reliable (Stubbs et al., 2000). The VAS in this study was a 10 cm straight line denoting 0 points on the left end and 100 points on the right. Regarding meal satisfaction, a VAS score of 0 points meant that eating was enjoyable, and that of 100 points indicated that eating was unenjoyable owing to taste changes. Regarding sense of taste, a VAS score of 0 points indicated that the taste had not changed, and that of higher values indicated a worsened sense of taste. The VAS scores were classified into four stages, as follows: no change (0–9 points), mild (10–39 points), moderate (40–69 points), and severe (70–100 points). Patients were considered to have taste disorders when their VAS scores for meal satisfaction or sense of taste were 10 points or greater.
Analyses were performed using IBM SPSS Statistics, version 21.0. Descriptive statistics were calculated for clinical characteristics. For assessment of differences between groups, chi-square test was used for categorical data, and the t test or Mann–Whitney U test following the Kolmogorov–Smirnov test was used for continuous data, as appropriate. Means and standard deviations (SDs) of meal satisfaction and sense of taste VAS scores were calculated. To compare meal satisfaction and sense of taste between groups, the Friedman test with Bonferroni correction was used, because the data distribution was not Gaussian. Using a post-hoc test, changes in meal satisfaction and sense of taste at each time point from baseline were assessed. Patients who could not continue chemotherapy or had incomplete questionnaire-related data were excluded. The sample size was determined based on previous study sample sizes and calculations using Stata, version 15.1 (Steinbach et al., 2009) (p = 0.5; power = 0.8). The significance levels were set at p < 0.05, and all analyses were two-tailed.
Eighty-seven outpatients with breast cancer participated in this study. Of the 45 patients in the CG, 6 dropped out during chemotherapy and an additional 14 were excluded because of missing questionnaire data. Of the 42 patients in the IG, 6 dropped out during chemotherapy; of the 36 who completed the study protocol, 8 were excluded because of missing questionnaire data. Data were analyzed from 25 patients from the CG and 28 patients from the IG.
The patients’ clinical characteristics are shown in Table 1. The mean patient age was 50.1 years (SD = 10.3), with no differences between the IG and CG (p = 0.919). The most prevalent TNM clinical stage in the IG and CG was stage II (46% and 48%, respectively); the proportions of TNM clinical stages were not significantly different between the two groups (p = 0.76). The chemotherapy regimens and schedules were also not significantly different between the two groups (IG: p = 0.487, CG: p = 0.884).
Chemotherapy-Associated Adverse Effects
Thirty-six percent of patients experienced severe chemotherapy-associated adverse effects (IG: 32%, CG: 40%). The highest proportions of severe oral mucositis after each cycle in the IG and CG were 14% and 12%, respectively. Despite the high frequency of severe oral mucositis, few patients experienced severe oral pain (IG: 4%, CG: 8%). In addition, severe anorexia was observed in 7% and 12% of patients in the IG and CG, respectively. No patients experienced severe nausea in either group. In addition, no patients in the IG experienced severe vomiting, although 8% of patients in the CG did.
Meal Satisfaction and Sense of Taste
Meal satisfaction and sense of taste worsened immediately after starting treatment, and CATDs occurred during the first regimen. Meal satisfaction and sense of taste temporarily recovered at the midpoint of the chemotherapy regimen break but worsened again after commencing the second regimen (see Table 2).
Forty-seven of the 53 participants (89%) experienced meal dissatisfaction (i.e., VAS score of 10 points or greater) during the protocol. In the IG, 6 of 28 participants (21%) did not have meal dissatisfaction (i.e., VAS score less than 10 points) during the protocol, and all patients in the CG experienced meal dissatisfaction (p < 0.001). VAS scores for meal satisfaction recovered two months after completing chemotherapy in the IG, but scores were still higher (indicating less satisfaction) in the CG.
Forty-nine of the 53 participants (93%) experienced impaired sense of taste (i.e., VAS score of 10 points or greater) during the protocol. Four of the 28 IG participants (14%) did not show an impaired sense of taste during the protocol, but all CG participants did (p < 0.001). The VAS scores for sense of taste recovered at the midpoint (chemotherapy break) in the IG but remained significantly higher in the CG. In addition, sense of taste recovered to the baseline level two months after completing chemotherapy in the IG but remained impaired at that time point in the CG.
This study investigated the effect of education on CATDs in Japanese women receiving treatment for breast cancer. Meal satisfaction and sense of taste worsened after the start of chemotherapy in both groups; however, TD in IG participants recovered two months after completing chemotherapy, whereas that in CG participants did not. The results suggest that providing TD education to patients with breast cancer receiving chemotherapy can affect their TD experience.
The incidence rate of TDs in the study was about 90%, which was higher than that reported in previous studies of patients with cancer receiving chemotherapy (Ponticelli et al., 2017) but similar to those in a study of patients with breast cancer receiving chemotherapy (Amézaga et al., 2018). This study’s findings suggest that providing patients with information about adverse effects before starting chemotherapy may help them prepare for these effects and subsequently mitigate their distress. Therefore, providing patients with sufficient information about coping with TDs before starting chemotherapy may prevent or ameliorate the effects of such disorders and enhance patients’ abilities to perform self-care to lessen the effects of TDs. TDs tend to be overlooked as an adverse effect because they may be overlooked by physicians (Galizia et al., 2018).
The results indicate that CG participants had not recovered from TDs two months after completing chemotherapy. A possible reason is that the ability to perform self-care was lower in CG participants because they could not compensate for taste changes during chemotherapy; the IG received more self-care support for taste changes (Wang et al., 2019). In addition, most patients with cancer who develop TDs rarely report it to medical staff (de Vries et al., 2016). Patients receiving chemotherapy are already under a significant amount of stress that can be difficult for family and friends to understand (Da Mata Tiezzi et al., 2017). Because TDs have adverse effects to physical and psychological quality of life, education may play a pivotal role in ameliorating not only TDs, but also psychological distress (de Vries, Boesveldt, et al., 2018; Ponticelli et al., 2017).
Studies have shown the efficacy of managing patients’ adverse effects during chemotherapy using the Internet (Basch et al., 2016; Denis et al., 2017). Even if patients’ TDs are mild, using the Internet to obtain information that helps patients cope with their needs may be an effective management approach. The authors used a booklet to provide information about CATDs. Meal dissatisfaction may be mitigated further if a computer or targeted website is used to provide specific information to help patients reduce their distress.
Participants were required to respond to questionnaires concerning meal satisfaction and sense of taste as experienced during the previous two weeks on day 15 of each chemotherapy cycle; this time point was chosen after patients appeared to start recovering from adverse effects of treatment by that time, which would make them more amenable to completing the questionnaire. However, this may have resulted in over- or underestimation of TD severity, because responses were based on recalling their distress. Future studies should consider more appropriate time points for collecting data.
The IG received standard care, education, and instruction by a trained nurse using a specially prepared booklet, and the CG received only standard care. However, some CG participants may have obtained information about TDs on their own. Because patients can easily research their symptoms using the Internet and networks for patients with cancer, those who are able can readily seek out useful information. Because of the nature of the hospital nurses’ behaviors, some CG participants may have received specific care for TDs from the nurses when required. Participants were newly diagnosed with breast cancer and had received neither neoadjuvant nor adjuvant chemotherapy as a first half of chemotherapy. Because the chemotherapy period was six months, participants may have preferred to simply tolerate their changes in taste rather than perform self-care. In addition, because anthracycline-based chemotherapy induces other somatic symptoms that can cause severe distress, participants may have had difficulty performing self-care. Although antiemetic medications administered before chemotherapy may have distorted the frequency of side effects during chemotherapy (particularly for nausea and vomiting), the standards of care were not changed for this study for ethical reasons. In addition, this study did not evaluate which TD types, such as hypogeusia, hypergeusia, and ageusia, occurred during treatment. Regarding ethnic dietary differences, no studies have directly compared differences of TDs among different ethics diets, such as diets in Japan and the United States. Because the diets of Japanese and U.S. populations are different, ethnic differences may also pertain to the most suitable intervention methods. The number of patients analyzed was lower than the number of patients calculated as necessary for power of 0.8; therefore, there may be statistical errors in this study. Further studies are needed to overcome these limitations.
In this sample of Japanese women with breast cancer who received chemotherapy, participants reported CATDs (i.e., meal dissatisfaction and an impaired sense of taste); however, TDs were ameliorated in the IG more than in the CG. Education and instruction by nurses before chemotherapy may be useful for the management of CATDs in this population.
About the Author(s)
Sanae Asano, RN, MHS, is a PhD student and Hiroyuki Sawatari, PhD, is an assistant professor in the Department of Health Care for Adults, both in the Graduate School of Biomedical and Health Sciences at Hiroshima University; Hideko Mentani, RN, MSN, is a nursing teacher at Shimizugaoka Senior High School in Hiroshima; Yuko Shimada, RN, is an oncology certified nurse at Higashihiroshima Medical Center in Hiroshima; Michie Takahashi, RN, is an oncology certified nurse at Hakodate Gryoukaku Hospital in Hokkaido; Kazumi Fudano, RN, MSN, is a certified nurse specialist in cancer and head nurse at Hiroshima Red Cross Hospital and Atomic-Bomb Survivors Hospital; Keiko Sasaki, RN, is an oncology certified nurse at Hiroshima City Asa Citizens Hospital; Mayumi Niitani, RN, PhD, is an associate professor in the Department of Nursing in the Faculty of Nursing at Yasuda Women’s University in Hiroshima; Kazuaki Tanabe, MD, PhD, is a professor in the Department of Health Care for Adults in the Graduate School of Biomedical and Health Sciences at Hiroshima University; and Tsuyoshi Kataoka, MD, PhD, is a surgical doctor at Hiroshima Kosei Hospital, all in Japan. The authors take full responsibility for this content. This work was supported by the public benefit trust Fumiko Yamaji specialty nursing education research subsidy fund (#26-5). The article has been reviewed by independent peer reviewers to ensure that it is objective and free from bias. Sawatari can be reached at email@example.com, with copy to CJONEditor@ons.org. (Submitted August 2019. Accepted December 5, 2019.)
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