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ORIGINAL ARTICLE
Year : 2020  |  Volume : 16  |  Issue : 7  |  Page : 1678-1685

Effect of oral supplements on the nutritional status of nasopharyngeal carcinoma patients undergoing concurrent chemotherapy: A randomized controlled Phase II trial


1 Radiotherapy Division, Department of Oral and Maxillofacial-Head Neck Oncology, Shanghai Ninth People's Hospital, College of Stomatology, Shanghai Jiao Tong University School of Medicine; National Clinical Research Center for Oral Diseases; Shanghai Key Laboratory of Stomatology, Shanghai Research Institute of Stomatology, Shanghai, China
2 Department of Nutrition, Fudan University Shanghai Cancer Center, Shanghai, China
3 Biostatistics Office of Clinical Research Center, Shanghai Ninth People's Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China

Date of Submission05-Mar-2020
Date of Decision13-Jul-2020
Date of Acceptance25-Oct-2020
Date of Web Publication9-Feb-2021

Correspondence Address:
Guopei Zhu
Radiotherapy Division, Department of Oral and Maxillofacial-Head Neck Oncology, Shanghai Ninth People's Hospital, College of Stomatology, Shanghai Jiao Tong University School of Medicine, 639 Zhizaoju Road, Shanghai, 200011
China
Yiqun Ling
Department of Nutrition, Fudan University Shanghai Cancer Center, Shanghai, No. 270, Dong'an Road, Shanghai 200032
China
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/jcrt.JCRT_273_20

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 > Abstract 


Objectives: The objectives of this study were to prospectively compare individualized dietary counseling with or without oral nutritional supplements (ONSs) in nasopharyngeal carcinoma (NPC) patients undergoing concurrent chemoradiotherapy (CCRT) in a Phase II, randomized trial.
Materials and Methods: Between June 2014 and August 2016, Stage II–IVb NPC patients were randomly enrolled. The primary endpoint was change in body weight between during CCRT, and the secondary endpoints were change in body mass index (BMI) and fat-free mass index (FFMI).
Results: Fifty-two patients were randomized; 19 patients in the control group and 23 in the ONS group were eligible for analysis. Weight, BMI, and body composition parameters significantly decreased from baseline to week 6. FFMI was significantly better in patients with ONS intake >2/3 planed than the control group (P = 0.028). Weight and BMI maintenance was slightly better in patients with total intake >2/3 planed (P = 0.170 and P= 0.229, respectively). The mean Patient-Generated Subjective Global Assessment score was also better in the ONS group at the end of CCRT (P = 0.053).
Conclusions: ONSs with individualized dietary counseling may be beneficial in patients with enough intake, and further prospective studies with large groups of patients are warranted.

Keywords: Body composition, fat-free mass index, malnutrition, nasopharyngeal carcinoma, oral supplement


How to cite this article:
Dou S, Ding H, Jiang W, Li R, Qian Y, Wu S, Ling Y, Zhu G. Effect of oral supplements on the nutritional status of nasopharyngeal carcinoma patients undergoing concurrent chemotherapy: A randomized controlled Phase II trial. J Can Res Ther 2020;16:1678-85

How to cite this URL:
Dou S, Ding H, Jiang W, Li R, Qian Y, Wu S, Ling Y, Zhu G. Effect of oral supplements on the nutritional status of nasopharyngeal carcinoma patients undergoing concurrent chemotherapy: A randomized controlled Phase II trial. J Can Res Ther [serial online] 2020 [cited 2021 Mar 8];16:1678-85. Available from: https://www.cancerjournal.net/text.asp?2020/16/7/1678/308764

Shengjin Dou and Huiping Ding contributed equally





 > Introduction Top


Malnutrition is very common in nasopharyngeal carcinoma (NPC) patients undergoing radiotherapy (RT) or concurrent chemoradiotherapy (CCRT) in consequence of dysphagia, mucositis,[1] nausea, and other treatment-related toxicities.[2],[3],[4],[5] Malnutrition is associated with lower physical functioning, lower immune status, more severe toxicities,[6] treatment interruption, lower chemotherapy response rates, hospital readmission, impaired quality of life (QoL), and increased mortality.[7],[8],[9],[10] Although the international guidelines recommend early nutritional support in the presence of nutritional risk,[11] the best type of nutritional intervention for NPC patients undergoing CCRT is still unclear. Individualized dietary counseling showed beneficial effects in nutritional intake, nutritional status, and QoL in head-and-neck cancer patients undergoing RT or CCRT-treatment;[7] oral nutritional supplements (ONSs) was most acceptable in Chinese NPC patients. Previous nutritional intervention trials in head-and-neck cancer patients have been conducted on small samples and did not clarify the role of ONSs. Accordingly, although current guidelines recommend ONS associated with dietary counseling for head-and-neck cancer patients undergoing RT or CCRT as Grade A,[11] the efficacy of this nutritional intervention still needs to be evaluated in randomized clinical trials for Chinese NPC patients. Therefore, we prospectively conducted a randomized trial that administered individualized dietary counseling with or without ONS in NPC patients undergoing CCRT.


 > Materials and Methods Top


Patient selection

Between June 2014 and August 2016, patients with histologically confirmed, Stage II–IVb (7th American Joint Committee on Cancer/Union for International Cancer Control staging system) NPC, eligible for CCRT, with or without induction chemotherapy were randomly enrolled in Fudan University Shanghai Cancer Center and Shanghai Ninth People's Hospital, Shanghai Jiaotong University School of Medicine. Other inclusion criteria included an age of 18–70 years and Karnofsky Performance Status of at least 70%. Adequate hematologic, hepatic, and renal functions were also required. Exclusion criteria were as follows: distant metastases, another noncured cancer except for a basocellular carcinoma of the skin, a prior radio(chemo)therapy treatment within the last 6 months, active intestinal comorbidity or a known eating disorder precluding adequate dietary intake or absorption, diagnosis of heart failure, uncontrolled diabetes, (severe) dementia, pregnancy or lactation, and known allergy for oral supplements. Informed consent was obtained from all included patients. The study was approved by the institutional review boards of all participating centers.

At baseline, patient characteristics, including age, sex, primary site of cancer, stage, type of chemotherapy, and performance status, were recorded. The nutritional assessment, including body weight, body mass index (BMI), and subjective global assessment (SGA) of nutritional status, was undertaken before the commencement of CCRT. Then, a 15–30-min evaluation and nutritional counseling were performed every 2 weeks throughout the 6-week CCRT period by the same oncology fellow-in-training who was supervised by an attending physician specialized in clinical nutrition. At each evaluation, weight measurement with the same scales, SGA, severity of mucositis, amount of oral intake, and interruption of RT and/or chemotherapy as a result of toxicity were recorded. Dietary intake was assessed by diet histories at each visit. The information obtained was used to determine whether estimated oral intake was <50% of energy requirement, in which case enteral feeding would be recommended to the patients.

Study design

This is a multicenter, open-labeled, randomized, Phase II trial in accordance with the Helsinki Declaration and the good clinical practice guidelines. Randomization was performed at the time of enrollment to the control group or the ONS group with the use of randomization lists generated by the statistician. To minimize the difference of nutritional intake of patients in the two groups, all patients will receive individualized dietary counseling from specialized nutrition doctors during CCRT. Patients in the ONS group were asked to consume Healing Element (Methuselah Medical Technology [Shanghai] Co., Ltd), 25 g t. i. d., from treatment initiation to the end of week 2. Considering the decreasing daily oral nutrition intake caused by increasing acute radiation toxicities after week 2, we increased the supplement intake to 50 g t. i. d. until the end of treatment. The nutritional composition of Healing Element is listed in [Table S1]. Patients were asked to return all unconsumed sachets for calculation of total dietary supplement intake.



Counseling consists of stimulating a sufficient protein and energy intake, based on the current European Society for Clinical Nutrition and Metabolism (ESPEN) guidelines for protein and energy.[11] The criterion for sufficient protein intake is at least 1.0 g/kg body weight.[12] Furthermore, patients are advised to use at least 25 g of proteins per meal. This evenly distributed ingestion of protein throughout the day is expected to maximally stimulate muscle protein synthesis.[13]

The standard oncologic therapy regimen included CCRT with cisplatin/nedaplatin and radiation therapy according to the center's current practice. In brief, RT consisted of a median total dose of 66 Gy in single fractions of 1.8–2.0 Gy daily.

Outcome measurement

All patients were assessed at baseline and every week during the course of CCRT by the same specialized nutrition doctor. Nutritional assessment measurements (body weight, BMI, and body composition) were assessed every week. The Patient-Generated (PG) SGA was assessed every other week. The scored PG-SGA was completed as described by Ottery.[14] Each patient was classified as well nourished (SGA-A), moderately or suspected of being malnourished (SGA-B), or severely malnourished (SGA-C). In addition, a mean PG-SGA score was calculated. Weight was measured without shoes and while wearing light clothing. To do the body composition analysis, a multifrequency bioelectrical impedance analyzer, InBody S10 Biospace device (Biospace Co, Ltd, Korea/Model JMW140), was used according to the manufacturer's guidelines. Body cell mass (BCM), fat-free mass (FFM), skeletal muscle mass (SM), and phase angle (PA) were obtained using the InBody software. FFM was converted to fat-free mass index (FFMI) by dividing them by the square of height (m2). Acute toxicities were defined as occurring within 90 days of treatment completion. The Common Terminology Criteria for Adverse Events v3.0 were used to evaluate the acute toxicities.

Endpoints and statistical analysis

The primary endpoint was the difference in percentage body weight loss during CCRT between the ONS group and the control group. Patient weights at the start and end of treatment were used to calculate percentage body weight loss during treatment. The secondary outcomes of this study were the change of BMI, FFMI, PG-SGA score, SM, BCM, and PA comparing the ONS group with the control group. Patients treated with chemoradiation therapy without ONS in the previous study lost a mean of 10.7% (standard deviation [SD] = 6.5) of their body weight,[15] and we assumed a loss of 6.0% (SD = 4.0) in the ONS group patients. To detect such a difference, a minimum of 21 patients (type I error 5% and power 80%) was required in each arm. After adjustment by approximately 20% for dropout, a total sample size should be 52 patients (26 pairs).

For descriptive analysis, continuous variables are presented as the mean and SD or as median and interquartile range when appropriate. Categorical variables are presented as frequencies. The Chi-square test was used to detect statistical differences in proportions. The Shapiro–Wilk test was used to test the normality of data distribution. For the outcome analysis, changes of numerical data were analyzed with paired t-test. Repeated-measures analysis of variance (repeated-measures ANOVA) was used for the comparisons of all outcome measures at different time points. All statistical analysis was performed using SPSS software (IBM SPSS Statistics for Windows, version 18.0; SPSS Institute, IBM, US). A two-sided P < 0.05 was considered statistically significant.


 > Results Top


Patient and tumor characteristics

Among 60 residents, 58 met the selection criteria, and among them, 52 agreed to participate in the study and were randomized. Seven patients in the control group and three patients in the ONS group withdrew from the study because they refused to nutritional status assessment. All remaining 19 and 23 individuals completed the study.

A total of 42 patients were recruited for this study comprising 33 men and 9 women, of whom median age was 47 years old. The distribution of patients in the two hospitals was 30 and 12 patients, respectively. The general characteristics of the 42-patient study population are summarized in [Table 1].
Table 1: The clinical characteristics of two groups

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Nutritional status between the oral nutritional supplement and control groups

Over time, weight, BMI, and body composition parameters (FFMI, SM, and BCM) significantly decreased from baseline to week 6 [Table 2], with a decrease of 5.69%–16.00% and 5.13%–10.08% in the above parameters in two groups, respectively. The decreases in weight, BMI, and body composition parameters (FFMI, SM, BCM, and PA) in the ONS group did not differ significantly from that of the control group [Figure 1]. However, the ONS group had a significant better BMI maintenance in the first 2 weeks (P = 0.024).
Figure 1: Comparison of change in weight, BMI, and body composition parameters (FFMI, SM, BCM, and PA) during CCRT between the ONS group and the control group, and there was no significant difference between the two groups. Abbreviations: BMI = Body mass index, FFMI = Fat-free mass index, SM = Skeletal muscle mass, BCM = Body cell mass, PA = Phase angle, CCRT = Concurrent chemoradiotherapy, ONS = Oral nutritional supplement

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Table 2: Change of different nutritional status of the two group during concurrent chemoradiotherapy

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Nutritional supplement intake in the oral nutritional supplement group

A comparison of patients' total ONS intake in the ONS group between actual and planed is illustrated in [Figure S1]. The actual ONS intake rate in the first 2 weeks was 87.2%–89.5%. Due to the acute toxicities of CCRT, especially oral mucositis increased to Grade III–IV after week 3, the total ONS intake rate in the ONS group decreased to only 40.5%–63.6% of planed in week 3 to week 6 [Figure S1], which may be responsible for the low nutritional status in the ONS group.



Nutritional status in patients with enough supplement intake

Weight and BMI: From baseline to week 6, the weight and BMI in both the groups decreased, but weight and BMI maintenance was slightly better in patients with total intake >2/3 planed, though did not differ significantly (P = 0.170 and P = 0.229, respectively) [Figure 2]a and [Figure 2]b.
Figure 2: Comparison of nutritional status between patients enough supplement intake in the ONS group and the control group. (a and b) weight and BMI maintenance was slightly better though did not differ significantly (P = 0.170 and P = 0.229, respectively). (c and d) FFMI and SM were significant better (P = 0.028 and P = 0.018, respectively). (e and f) BCM and PA also reached marginal difference (P = 0.061 and P = 0.074, respectively). Abbreviations: ONS = Oral nutritional supplement, BMI = Body mass index, FFMI = Fat-free mass index, SM = Skeletal muscle mass, BCM = Body cell mass, PA = Phase angle

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Body composition parameters: Over time, FFMI and SM were significantly better in patients with ONS intake >2/3 planed than the control group (P = 0.028 and P = 0.018, respectively). The change of BCM and PA also reached marginal difference (P = 0.061 and P = 0.074, respectively) [Figure 2]c,[Figure 2]d,[Figure 2]e,[Figure 2]f.

Patient-Generated Subjective Global Assessment score

The PG-SGA scores of both the groups at all time points are presented in [Figure 3]. Compared with baseline, patients with Stage C significantly increased in both the groups during CCRT (P = 0.000 and P = 0.000, respectively), implying decreased status in both the groups [Figure 3]a. On the other hand, the difference of mean PG-SGA score between the ONS group and the control group increased gradually over time [Figure 3]b. The mean PG-SGA scores of the ONS and the control group patients at baseline were 4.14 ± 3.97 and 3.91 ± 2.66, respectively, which rose to 16.60 ± 6.33 and 21.33 ± 4.00 at the end of CCRT (P = 0.053) [Figure 3]b.
Figure 3: PG-SGA scores during CCRT between the ONS group and the control group. (a) Compared with baseline, patients with Stage C significantly increased in both the groups during CCRT (P = 0.000 and P = 0.000, respectively). (b) The difference of mean PG-SGA score between the two groups increased gradually over time, which reaches a significant difference at the end of CCRT (P = 0.053). Abbreviations: CCRT = Concurrent chemoradiotherapy, ONS = Oral nutritional supplement, PG-SGA = Patient-Generated Subjective Global Assessment

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Toxicity

The acute toxicities experienced during chemoradiotherapy are listed in [Table 3]. Most commonly observed grade III–IV toxicity was grade III-IV oral mucositis. There was no difference in acute toxicities between the two groups.
Table 3: Acute adverse events during concurrent chemoradiotherapy

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 > Discussion Top


In this randomized controlled study, we compared ONS and dietary counseling to dietary counseling alone for effects on nutritional status in NPC patients undergoing CCRT. We demonstrated a significant difference in FFMI and SM between patients with enough oral supplement intake and the control group, and the mean PG-SGA score at week 6 was significantly better in the ONS group. To our knowledge, this is the first randomized controlled trial showing the beneficial effects of ONS on nutritional status in Chinese NPC patients during multimodality treatment.

Results suggest a better BMI maintenance in the first 2 weeks from baseline in the ONS group, when the overall intake was about 85%–90% of planed. What deserves to be mentioned more is that ONS was beneficial only when the total intake was >2/3 planed. The total ONS intake rate in the ONS group decreased to only about 40%–60% of planed in week 3 to week 6 [Figure S1], which was cause by the acute toxicities of CCRT, such as dysphagia, mucositis, nausea, vomit weakness, and other treatment-related adverse events, especially oral mucositis and dysphagia. Thus, how to ensure enough ONS intake from week 3 is the key point for patients undergoing CCRT. One method utilized to combat insufficient intake is enteral feeding via nasogastric (NG) or percutaneous endoscopic gastrostomy (PEG) tubes. PEG is both safe and efficacious in arresting weight loss and maintaining nutrition in patients undergoing surgery and/or chemoradiotherapy for head-and-neck cancer.[16] In contrast to NG, PEG may be more efficient and would not increase mucositis for head-and-neck cancer patients undergoing RT, while NG may be associated with better long-term swallow outcomes.[17],[18] Although NG and PEG may be more beneficial help to keep a better nutritional status, treatment acceptance is a big problem for us to overcome.

While the body composition parameters, such as FFMI and SM, showed a significant difference in patient with enough oral supplement intake, the BMI and body weight still did not reach the border of difference, which may demonstrate that body composition parameters may have better sensitivity in nutritional assessment. Bioelectrical impedance analysis (BIA) has been validated for the assessment of body composition and nutritional status in a variety of patient populations.[19],[20] It is an easy-to-use, noninvasive, and reproducible technique. The technique measures the impedance of the body to a small applied electric current and uses the impedance data, together with an appropriate model to generate body composition parameters including BCM, FFM, and SM.[21] Moreover, a recent study by Rondel et al.[22] showed that only the ESPEN diagnostic criteria including FFMI were predictive for both three-months and one-year survival in hospitalized patients, which suggested that including the FFMI had additional value and highlighted the importance of the BIA measurement. BIA should be increasingly implemented in nutritional assessment.

The study also has some limitations. (a) The sample size of this study is relatively small, which means that results for clinical outcomes must be interpreted with caution, with a large-scale trial required to determine and quantify the clinical benefit from the intervention. (b) The proportion of withdrawal and noncompliance to the treatment regimen in this study was a bit high due to severe acute toxicities, such as oral mucositis and dysphagia. (c) Although dietary counseling was done every week, diets and health conditions of participants may vary among families.


 > Conclusions Top


In this study, we have shown that ONSs with individualized dietary counseling may be beneficial in patients with enough supplement intake for NPC patients during concurrent chemotherapy, which require confirmation in a larger Phase III trial.

Acknowledgment

Healing Element was kindly provided by methuselah medical technology.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
 > References Top

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Paddon-Jones D, Rasmussen BB. Dietary protein recommendations and the prevention of sarcopenia. Curr Opin Clin Nutr Metab Care 2009;12:86-90.  Back to cited text no. 13
    
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Ottery FD. Definition of standardized nutritional assessment and interventional pathways in oncology. Nutrition 1996;12:S15-9.  Back to cited text no. 14
    
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Lee H, Havrila C, Bravo V, Shantz K, Diaz K, Larner J, et al. Effect of oral nutritional supplementation on weight loss and percutaneous endoscopic gastrostomy tube rates in patients treated with radiotherapy for oropharyngeal carcinoma. Support Care Cancer 2008;16:285-9.  Back to cited text no. 15
    
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Burney RE, Bryner BS. Safety and long-term outcomes of percutaneous endoscopic gastrostomy in patients with head and neck cancer. Surg Endosc 2015;29:3685-9.  Back to cited text no. 16
    
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Goff D, Coward S, Fitzgerald A, Paleri V, Moor JW, Patterson JM. Swallowing outcomes for patients with oropharyngeal squamous cell carcinoma treated with primary (chemo) radiation therapy receiving either prophylactic gastrostomy or reactive nasogastric tube: A prospective cohort study. Clin Otolaryngol 2017;42:1135-40.  Back to cited text no. 18
    
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Władysiuk MS, Mlak R, Morshed K, Surtel W, Brzozowska A, Małecka-Massalska T. Bioelectrical impedance phase angle as a prognostic indicator of survival in head-and-neck cancer. Curr Oncol 2016;23:e481-7.  Back to cited text no. 20
    
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Kyle UG, Bosaeus I, de Lorenzo AD, Deurenberg P, Elia M, Gomez JM, et al. Composition of the EWG. Bioelectrical impedance analysis--part I: Review of principles and methods. Clin Nutr 2004;23:1226-43.  Back to cited text no. 21
    
22.
Rondel AL, Langius JA, de van der Schueren MA, Kruizenga HM. The new ESPEN diagnostic criteria for malnutrition predict overall survival in hospitalised patients. Clin Nutr 2018;37:163-8.  Back to cited text no. 22
    


    Figures

  [Figure 1], [Figure 2], [Figure 3]
 
 
    Tables

  [Table 1], [Table 2], [Table 3]



 

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