Skip to main content

Advertisement

ADVERTISEMENT

Empirical Studies

Providing Weight Loss Support to Patients Who Are Obese in Preparation for Colorectal Cancer Surgery to Reduce Surgical Site Infection Risk: A Mixed-methods Study

June 2020

Abstract

Obesity increases the risk of surgical site infections (SSIs) after colorectal cancer surgery, but strategies to support weight loss in obese patients who have colorectal cancer have not been established. PURPOSE: This mixed-methods study, using retrospective and prospective data, aimed to explore inhibitors and facilitators of preoperative weight loss in obese patients with colorectal cancer and the potential impact of preoperative weight loss support on SSIs. METHODS: Patients with a body mass index (BMI) of ≥ 25 kg/m2 were eligible to participate in the weight loss support program. Patient demographic, history, surgical, and outcomes variables were abstracted from the records. Five (5) nurses who provided weight loss support participated in a focus group interview method to explore weight loss inhibitory and promotional factors. Descriptive statistics and qualitative analysis methods were used to examine the data. RESULTS: Twenty-six (26) patients participated in the program for a mean of 45.5 days (SD ± 25.3). Body weight decreased from 79.8 kg (SD ± 15.6) to 75.7 kg (SD ± 14.3), and BMI decreased from 30.4 kg/m² (SD ± 4.7) to 29.4 kg/m² (SD ± 5.0) (P < .05). The average weight loss percentage was 4.9% (SD ± 3.4). In 14 patients, the weight loss percentage was 5% or more. SSIs occurred in 5 of 26 patients (19.2%). Additionally, 4 of 26 patients (15.4%) who had 8.8% or more weight loss did not manifest SSIs. Previous weight loss before the preoperative surgery visits, lack of motivation for weight loss, and time and duration required for weight loss were identified as inhibitory factors, whereas history of successful weight loss experience, knowledge acquisition, family support, and reduced knee and lower back pain were identified as promotional factors for weight loss. CONCLUSION: Patients in this program lost weight prior to colorectal surgery. Research to further explore the safety and effects of preoperative weight loss in obese patients with colorectal cancer as well as inhibitory and promotional factors for participation and success is needed. 

Introduction

A large epidemiological study of obesity involving 68.5 million people in 195 countries by the Global Burden of Disease 2015 Collaborators et al1 reported that an estimated 603.7 million adults were obese in 2015, and body mass index (BMI) ≥ 25 kg/m2 increased the risk of dying of obesity-related diseases. In 2017, approximately 152 100 Japanese patients were diagnosed with colorectal cancer, making the colon the most common cancer site.2 Obesity and lack of exercise are risk factors for colorectal cancer development, and the Centers for Disease Control and Prevention (CDC) Guidelines for the Prevention of Surgical Site Infection3 have shown that obesity increases the risk of surgical site infections (SSIs).

According to the CDC,4 a literature review reported that even a small weight loss of 5%–10% of an obese individual’s body weight may provide health benefits such as improvements in blood pressure, blood cholesterol, and blood glucose levels. A prospective cohort and case–control study by Latham et al,5 which included 1000 cardiovascular patients undergoing cardiac surgery, reported a 2.76-fold increase in the risk of SSIs when postoperative blood glucose levels were ≥ 200 mg/dL as well as an association between SSIs and elevated blood glucose levels within 48 hours after surgery. In addition, persistent hyperglycemia prior to surgery lowers immune defense mechanisms and increases the risk of infection. Reduced neutrophil migration and phagocytic activity due to hyperglycemia affects SSI and prolonged wound healing. Therefore, preoperative glycemic control is necessary. However, to date, there have been no studies investigating the effects of diet and exercise on preoperative weight loss in obese colorectal cancer patients and SSIs, and no studies on nurses’ support regarding how it relates to preoperative weight loss. Based on these findings, the authors examined a preoperative weight loss support strategy to reduce the risk of SSIs in obese patients with colorectal cancer.

In 2017, our medical institution’s outpatient services (which prepares patients for surgery) created a perioperative management team composed of a colorectal surgeon, nurses, a nutritionist, and a physiotherapist to provide support for patients with concurrent cancer and obesity to safely lose weight, with a goal of 5%–10% weight loss before surgery. Obesity is defined as a BMI of ≥ 25 kg/m2 by the Japan Society for the Study of Obesity.6 Nurses preparing outpatients for surgery (hereafter “nurses”) provide an orientation about preoperative weight loss support to patients and their family members, verify weight loss progress, and perform follow-ups. Coordination among the perioperative management teams enables patients to receive dietary guidance by a nutritionist and exercise guidance by a physiotherapist, with the goal of improving the diet and exercise habits of obese patients before surgery. This mixed-methods study, using retrospective and prospective data, aimed to explore inhibitors and facilitators of preoperative weight loss in obese patients with colorectal cancer and the potential impact of preoperative weight loss support on SSIs.

Methods

Study design and sample. This study involved 5 nurses who provided preoperative weight loss support from January 2017 to March 2019 to outpatients as preparation for non-emergency laparoscopic surgery for colorectal cancer at a surgical preparation outpatient clinic at the National Cancer Center Hospital East, Kashiwa, Japan. This study used a mixed research (exploratory) design method.

Overview of preoperative weight loss support. Patients with colorectal cancer were eligible to receive preoperative weight loss support if they had Tumor, Lymph, Node, Metastasis-Union for International Cancer Control (TNM-UICC) stage 0 to IIIb disease, were diagnosed as needing weight loss support, were 20 to 80 years of age and did not require emergency surgery, had a BMI of ≥ 25 kg/m2, and subsequently underwent elective laparoscopic surgery for colorectal cancer. Exclusion criteria for participation in the program were as follows: patients receiving chemotherapy or radiation therapy, terminal cancer, diabetes with a hemoglobin A1c (HbA1c) level ≥ 8.0%, chronic renal failure requiring dialysis (an organic complication of heart failure), severe arrhythmia, and a history of mental illness treatment. In addition, to be eligible to participate the surgeon needed to determine that the patients enrolled in the preoperative weight loss support program had no problems regarding nutritional status and locomotor function.

Preoperative weight loss support was provided on an outpatient basis 1 week after the initial outpatient consultation, whereby nurses preparing outpatients for surgery distributed documents and explained the details of preoperative weight loss support to consenting patients. Thereafter, a physiotherapist from the rehabilitation department physically assessed the patients and guided them on slow jogging for 60 minutes per day to achieve a modified Borg scale of 5–6 (Figure 1). A nutritionist provided dietary guidance to outpatients 1 week after the initial consultation, following the guidance from the rehabilitation department, and the patients were provided dietary guidance and exercise forms to record their meals and exercise. Instructions on how to complete the forms were provided. The guidance contents included information about weight loss and SSI prevention, a list of specific quantities for designated nutritional amounts, discussion points to correct patients’ current diets, and important considerations for daily diet. The target balance for protein, fats, and carbohydrates was determined based on the amounts recommended by the Ministry of Health, Labour and Welfare in 2015.7 

In the present study, the weight loss period was evaluated from the week after the first visit to the surgery preparation outpatient clinic until the day of admission (the day before surgery). Weight loss duration was defined as the period from 1 week after the initial outpatient consultation in preparation for surgery to the day of hospital admission. Nutrition and exercise guidance was provided for 30 minutes every 2 weeks for each patient from the initial outpatient consultation in preparation for surgery to the day of hospital admission. Nurses performed follow-up of the patients during the outpatient period until surgery; shared information with the physician, nutritionist, and physiotherapist; and recorded weight loss progress in the patient’s electronic health record.

Data collection. Data regarding the attributes of patients who underwent non-emergency surgery for colorectal cancer after preoperative weight loss support were retrospectively collected from the medical records. Data from patients who participated between January 2017 and March 2019 were retrieved. The demographic variables for patients who participated in preoperative weight loss support were as follows: age, sex, history of smoking, comorbidities, cancer staging (TNM-UICC), preoperative weight loss support period, and length of postoperative hospital stay (days). The surgical variables were information regarding surgical site, length of surgery, and estimated amount of blood loss. Preoperative blood testing (day of admission) encompassed serum albumin, HbA1c, total cholesterol, and triglyceride levels.

The completion rate was defined as the proportion of patients who—upon consulting the outpatient services in preparation for surgery and receiving preoperative weight loss support from the physician, nurse, nutritionist, and physiotherapist—jogged for 60 minutes per day and recorded their meals and exercise preoperatively. For the weight loss percentage, the patient’s height and weight before weight loss support were measured at the time of the initial outpatient consultation in preparation for surgery, and their weight was measured upon the completion of the preoperative weight loss support on the day of admission (preoperative). 

Surgical site infections. The surgeon used and documented the diagnosis based on CDC criteria.4

Focus group interview. The overt and hidden opinions of nurses regarding preoperative weight loss support were evaluated prospectively using the focus group interview8 method, which was semi-structured. Inclusion criteria were nurses in the preoperative outpatient surgery who provided preoperative weight loss support to the patient. 

After obtaining informed consent, interviews were recorded using a digital voice recorder. The group interview was conducted on March 5, 2019, at outpatient services for surgery preparation.

Using open-ended questions, the focus group interview method is a means of discussion involving study participants whereby unedited remarks are organized, and hidden information as well as needs and opinions can be identified. Compared with individual interviews, focus group interviews create group dynamics among the participants, thereby aiding in identifying the hidden opinions of individual participants who may not be aware of their actual feelings. In the present study, the purpose, methods, and interview content were described for all participants, and the authors verified that participants were willing to discuss their opinions. The focus group interview method required 60 minutes for completion, with the principal researcher serving as the interviewer.

Interview guide. An interview guide was created and implemented to obtain detailed information on preoperative weight loss support from nurses. The interview was composed of the following questions: 

• How did you motivate patients for preoperative weight loss support?

• How did you support patients with regard to meal management and exercise implementation?

• What differences were found between patients who lost weight and those who did not?

• What difficulties did you experience during preoperative weight loss support?

Data analysis

Quantitative data. The incidence rate of SSIs was calculated using the number of patients with SSIs after selected operations divided by the total number of selected operations performed times 100. Weight changes were determined using the following calculations:

• Degree of weight loss: weight after the completion of preoperative weight loss support (preoperative) minus weight prior to entering preoperative weight loss support

• Weight loss percentage: degree of weight loss divided by weight prior to entering preoperative weight loss support times 100

Descriptive statistics were also used for study participants’ attributes, surgical variables, and preparatory blood tests.

The basic attributes of nurses and patients who received preoperative weight loss support are presented as the mean (SD). Patients’ body weight and BMI before and after preoperative weight loss support were compared using a paired t-test. A P value of < .05 was considered statistically significant. Data analysis of quantitative variables was performed in SPSS Statistics 24.0.

Qualitative data. Using the verbatim records, a qualitative content analysis was performed following the Mayring9 technique. The authors created verbatim records and repeatedly read the narrated content to provide an overall outline. The inhibitory and promotional factors for weight loss were analyzed by summarizing the content analysis and explanatory content analysis, as proposed by Mayring.9 Descriptions expressed by an interpretation definition were extracted to avoid losing the context and then summarized into a sentence. While comparing the analysis theme of each sentence, the authors rephrased the sentence to precisely express the content and defined it as an analysis unit. These exact words or phrases were placed in an Excel data file, and the code was generated.

In the first step, the investigator independently classified the codes derived into categories and grouped the conceptually linked words or phrases within these categories. In the second step, similar content within coded units was summarized and set as context units. In the last step, the investigator created a code, a subcategory, and a definition for each category. To ensure the robustness of the study, an expert in qualitative research supervised the analysis process to ensure consistency and confirmability.

Ethical considerations. Before the interview, participants were instructed in writing regarding the study objectives, including the voluntary aspect of participation as well as matters regarding privacy protection, and written informed consent was obtained. The researchers informed the subject nurses that they could suspend or stop study participation at any time. In addition, the research representative explained in writing that the recorded tapes used in the interviews would be discarded by the research representative after the study was completed. The study was conducted with the approval of the ethical review board of the National Cancer Center Hospital East, Kashiwa, Japan.

Results

Patient demographics and clinical characteristics. Twenty-six (26) patients met the inclusion and exclusion criteria of this study and underwent non-emregency colorectal cancer surgery after preoperative weight reduction assistance. The study consisted of 15 (57.7%) male and 11 (42.3%) female participants, and their mean age was 60.6 (SD ± 12.4) years (Table 1). HbA1c was 6.2% (SD ± 0.6). Demographic and clinical characteristics of patients who received preoperative weight loss support are presented in Table 2.

Program completion and weight loss. The completion rate of preoperative weight loss support was 100%. The mean weight of the 26 patients was 79.8 kg (SD ± 15.6) at the time of the initial outpatient consultation in preparation for surgery (before preoperative weight loss support) and 75.7 kg (SD ± 14.3) at the time of hospital admission (after preoperative weight loss support) (P < .05) (Table 3). BMI was 30.4 kg/m² (SD ± 4.7) before preoperative weight loss support and 29.4 kg/m² (SD ± 5.0) after preoperative weight loss support (P < .05) (Table 3). Overall, the average percent weight loss was 4.9% (SD ± 3.4) (Table 2). 

The weight loss percentage was 5% or more in 14 patients (53.8%) and less than 5% in 12 patients (46.2%). The average weight loss duration was 45.5 days (SD ± 25.5); during this period, no adverse effects of weight loss were reported. The average amount of weight loss was 4.1 kg (SD ± 3.2). Two (2) patients had a weight gain of 0.5 kg and 1.5 kg, respectively.

Weight loss and SSIs. SSIs were observed in 5 of 26 patients (19.2%) who received preoperative weight loss support. They included superficial incisional SSI in 1 patient (20%), deep incisional SSI in 1 patient (20%), and organ/space SSI in 3 patients (60%). Four (4) patients (15.4%) achieved a weight loss percentage of 8.8%–10.8% and did not exhibit SSI (Table 4). The weight loss percentage was 3.4% (SD ± 3.7) for the SSI group and 5.0% (SD ± 3.2) for the non-SSI group. The maximum value of HbA1c in patients with SSIs was 8.1%, and the minimum value was 5.8%.

Attributes of nurses who provided preoperative weight loss support. Five (5) subjects were women with 17.6 years (SD ± 2.4) of nursing experience and 2.8 years (SD ± 1.8) of experience in preparing outpatients for surgery.

Inhibitory factors of weight loss. For factors that inhibited patient weight loss, the authors extracted 7 subcategories in the following 3 categories: 1) weight loss that occurred prior to outpatient examination in preparation for surgery, 2) lack of motivation for weight loss, and 3) time and duration required for weight loss (Table 5). Inhibitory and promotional factors of weight loss were cited by the nurses and reflected conversations they had with patients. The notations for interview results are as follows: subcategories are in quotation marks (“ ”), and citations are in italics.

Under the first category of inhibitory factors (ie, weight loss that occurred prior to outpatient examination in preparation for surgery), two subcategories were extracted: 1) “already received dietary guidance for diabetes treatment” and 2) “striving to lose weight on one’s own prior to examination at outpatient services.” Nurses used the following patient quotes to illustrate these two subcategories, respectively:

• “I don’t need this guidance because I have already heard it as guidance for diabetes.” 

• “I’d like to lose weight in my own way. I will take care of myself.” 

Lack of motivation for weight loss was another category of inhibitory factors. In this category, we extracted the following two subcategories: “difficulty accepting cancer” and “difficulty losing weight.” The patients were in a mental state wherein they could not accept the fact that they had colorectal cancer and experienced difficulty losing weight preoperatively. Consequently, nurses experienced difficulty in motivating patients to lose weight and reported the following observations:

• Although I’d try to somehow explain with a sense of “I’m sorry but…,” some patients did not completely accept the disease, which makes it difficult for them to accept the idea that they need to go on a diet. 

• While I am sure they are aware that they need to accept the fact that they have cancer, I feel that a little more time is required. I felt that it was extremely difficult to be directly involved with the patient and to motivate them. 

Time and duration required for weight loss. In this category, patients had “concern that the outpatient examination time will be prolonged.” In terms of achieving weight loss in a short period, “weight loss plateau” was observed, whereas “limitation to the frequency of outpatient follow-up preparation for surgery” was perceived as a problem by the nurses and patients, as shown in the following quote:

It takes quite a bit of time. After testing, patients come to the outpatient services to prepare for surgery and after being examined by the doctor; they come back, which alone is quite a time commitment. In addition, consultations with the departments of rehabilitation and nutrition take at least 30 min each, which together take about 1 hour. Therefore, as expected, the patients cannot be convinced that this guidance is worthwhile. 

Weight loss promotional factors. For the categories of factors that promote patient weight loss, we extracted 9 subcategories in the following 4 categories: 1) successful weight loss experience, 2) acquisition of knowledge about obesity and postoperative complications, 3) family support, and 4) alleviation of knee pain and low back pain (Table 5).

Successful weight loss experience. In this category, we extracted the following two subcategories: “history of regaining weight following weight loss,” and “previous experience dieting.” Furthermore, the motivation provided by nurses on an outpatient basis in preparation for surgery helped patients understand dietary management and exercise implementation, as shown by the following report of a nurse:

• There was a young obese woman who, amazingly, lost 10 kg on her own by dieting, but still, she rebounded, and the doctor asked her to attend guidance to lose weight. She said, “I have to try because I’ve already lost weight once,” and she was really motivated; she undertook the nutrition and rehabilitation support without a hitch.

Acquisition of knowledge about obesity and postoperative complications. In this category, physicians and nurses provided explanations to the patients about the relationship between postoperative complications and obesity and incorporating diet management and exercise habits into one’s lifestyle. The following feedback from nurses reflects the words of patients and also suggests that the diet and exercise diary, changes in muscle mass, and HbA1c results improved motivation by demonstrating the effects of weight loss:

• From the day of receiving guidance, patients changed, so when they came for their follow-up 2 weeks later, I looked at the completed diary, and as expected, find that many patients had stopped snacking and were engaged in appropriate exercise. 

• Being involved in helping patients prepare for surgery independently through diet, rather than leaving everything up to the doctor’s treatment, means that they can receive surgery safely, which makes the patients try hard to prepare for surgery, and the fact that they look forward to surgery with motivation.

Family support. Family support for preoperative weight loss was another supporting factor, and the subcategories were “participation in preoperative weight loss support at the request of the spouse” and “dietary management by the spouse.” The latter was performed by recording a diet and exercise diary and cooking at home. Nurses reported:

• Patients who lost weight were often those who had someone to provide support. 

Alleviation of knee and low back pain. Patients had “awareness of knee pain and low back pain” caused by obesity and experienced an increase in muscle mass from exercising with “pain relief from weight loss.” Therefore, they understood the importance of weight loss. The following reflects nurses’ recall of patient interactions: 

• The patient understood, saying “My knees hurt” and “My lower back hurts,” and so “I have to lose more weight.” 

• I said, “Just as they say, losing weight lowers the burden on my body.” 

Discussion

According to the results of the present study, no patient experienced weight loss-related adverse events during the weight loss period, and the completion rate of preoperative weight loss support was 100%, indicating that preoperative weight loss can be executed safely. 

A report by the American Cancer Society that evaluated the scientific evidence and best clinical practice related to optimal nutrition and physical activity after a cancer diagnosis found that in obese individuals undergoing cancer treatment, weight loss of up to 1 kg per week or 5%–10% of weight loss can be beneficial to health, even when the weight loss to ideal weight is not achieved.10 The rate of SSI in this study was 19.2%, which is higher than the Japanese Ministry of Health, Labor and Welfare’s report on SSI surveillance (10.6% for colon surgery and 13.4% for rectal surgery).11 This may have been influenced by the fact that this study included only obese patients, suggesting that obesity does increase SSI risk. Weight loss percentage was 3.4% in the SSI group and 5.0% in the non-SSI group; no SSIs occurred in patients who had a weight loss of more than 8.8%. 

Promotional and inhibitory factors in preoperative weight loss support. In the present study, the weight loss percentage was 5% or more in 14 patients (53.8%), showing that preoperative weight loss is possible; support to improve the weight loss percentage requires further investigation. However, the experience of successful weight loss provided hope for weight loss effects and results. 

The acquisition of knowledge about obesity and postoperative complications enabled the “incorporation of diet and exercise habits into one’s lifestyle.” Family support and reduced knee and low back pain were also cited as promotional factors for weight loss. Weight loss inhibitory factors included weight loss that had already occurred before outpatient examination in preparation for surgery, a lack of motivation for weight loss as a result of the diagnosis or difficulty losing weight in the past, and “concern that the outpatient examination time will be prolonged.” The duration of preoperative weight loss support was short at 45.5 days; therefore, the authors believe that the time and duration required for weight loss were perceived to be an issue by both patients and nurses. 

Although there have been no previous studies on the control factors of preoperative weight loss support, the results of this study suggest that one of the factors inhibiting weight loss (time and duration required to lose weight) should be supported by diet management and exercise so that weight loss can be safely achieved before surgery.

In addition, nutritional guidance was conducted by a dietitian, exercise guidance by a physiotherapist, and follow-up by a surgeon to prevent patients’ nutritional status and motor function from deteriorating. However, in the future, the safety of preoperative weight loss should be verified by measuring body composition at the start of weight loss, just before surgery, preoperatively, and postoperatively. Prospective studies involving larger populations are needed to explore the potential effects of preoperative weight loss support on SSIs in patients with colorectal cancer. 

Limitations

The present study is the first, to the authors’s knowledge, to investigate the preoperative weight loss support of nurses preparing outpatients with colorectal cancer for surgery; however, the study had a small sample size, and patient variables and outcomes data were collected retrospectively. Additionally, weight loss inhibitory and promotional factors need to be verified by interviewing patients who have received preoperative weight loss support. 

Conclusions

In this mixed-methods research study, the authors interviewed 5 nurses who provided preoperative weight loss support to outpatients with a BMI ≥ 25 kg/m2 who were scheduled for non-emergency colorectal cancer surgery. The body weight and BMI of 26 patients significantly decreased compared with baseline values. The weight loss percentage was lower in the SSI onset group than in the non-SSI group. Results suggest that preoperative weight loss support may have a potential impact on SSI. Interviews with nurses who provided weight loss support showed several inhibitory and weight loss promotional factors that require further exploration.

Acknowledgments

The authors acknowledge the nurses and surgeons of the National Cancer Center Hospital East, Kashiwa, Japan, who participated in the data collection for this study. All authors participated in writing the manuscript and approved the final version. All authors read and approved the final manuscript. This project was supported by the Health Labour Sciences Research Grant (2016–2018).

Affiliations

Dr. Nakagawa is a professor, School of Nursing, Takarazuka University, Kita Ward, Osaka City, Japan. Dr. Tanaka is a professor emeritus, University of Tsukuba, Tsukuba, Ibaraki, Japan. Dr. Sasai is an assistant professor, Graduate School of Arts and Sciences, The University of Tokyo, Tokyo, Japan. Dr. Nishizawa is an attending surgeon, Department of Colorectal Surgery, National Cancer Center Hospital East, Kashiwa, Japan. Please address all correspondence to: Hiromi Nakagawa, PhD, School of Nursing, Takarazuka University, 1-13-16 Shibata, Kita-ku, Osaka City, Osaka Prefecture 530-0012, Japan; email: h-nakagawa@takara-univ.ac.jp.

References

1. GBD 2015 Obesity Collaborators, Afshin A, Forouzanfar MH, Reitsma MB, et al. Health effects of overweight and obesity in 195 countries over 25 years. N Engl J Med. 2017;377(1):13–27. doi:10.1056/NEJMoa1614362

2. Cancer Control and Information Services, National Cancer Center. がん統計. 最新ん統計. Ganjoho.jp. Updated May 7, 2020. https://ganjoho.jp/reg_stat/statistics/stat/summary.html

3. Mangram AJ, Horan TC, Pearson ML, Silver LC, Jarvis WR. Guideline for prevention of surgical site infection, 1999. Centers for Disease Control and Prevention (CDC) Hospital Infection Control Practices Advisory Committee. Am J Infect Control. 1999;27(2):97–132. 

4. Centers for Disease Control and Prevention. Losing Weight. Centers for Disease Control and Prevention. Updated February 4, 2020. https://www.cdc.gov/healthyweight/losing_weight/index.html#

5. Latham R, Lancaster AD, Covington JF, Pirolo JS, Thomas CS Jr. The association of diabetes and glucose control with surgical-site infections among cardiothoracic surgery patients. Infect Control Hosp Epidemiol. 2001;22(10):607–612. doi:10.1086/501830

6. Japan Society for the Study of Obesity. Guidelines for the Management of Obesity Disease 2016. Tokyo, Japan: Life Science Publishing; 2016.

7. Overview of Dietary Reference Intakes for Japanese (2015). Ministry of Health, Labour and Welfare. 2015. Accessed October 24, 2019. https://www.mhlw.go.jp/file/06-Seisakujouhou-10900000-Kenkoukyoku/Overview.pdf

8. Anme T, ed. Group Interview Methods in Human Services: The Development of Qualitative Research Methods Based on Scientific Grounds. Tokyo, Japan: Ishiyaku Publishers;2003.

9. Mayring P. Qualitative content analysis. In: Flick U, von Kardorff E, Steinke I, eds. A Companion to Qualitative Research. SAGE Publications; 2004:266–269.

10. Doyle C, Kushi LH, Byers T, et al. Nutrition and physical activity during and after cancer treatment: an American Cancer Society guide for informed choices. CA Cancer J Clin. 2006;56(6):323–353. doi:10.3322/canjclin.56.6.323

11. Japan Nosocomial Infections Surveillance. Annual Open Report 2017 (All Facilities). Japan Nosocomial Infections Surveillance. July 30, 2019. Accessed October 24, 2019. https://janis.mhlw.go.jp/english/report/open_report/2017/3/1/ken_Open_Report_Eng_201700_clsi2012.pdf

Advertisement

Advertisement

Advertisement