Current Problems in Cancer 45 (2021) 100638

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Current Problems in Cancer

journal homepage: www.elsevier.com/locate/cpcancer

Nutritional assessment and risk factors

associated to malnutrition in patients with
esophageal cancer
Jingjing Cao a, Hongxia Xu b, Wei Li c, Zengqing Guo d, Yuan Lin e,
Yingying Shi f, Wen Hu g, Yi Ba h, Suyi Li i, Zengning Li j,
Kunhua Wang k, Jing Wu l,m, Ying He n, Jiajun Yang o, Conghua Xie p,
Fuxiang Zhou p, Xinxia Song q, Gongyan Chen r, Wenjun Ma s,
Suxia Luo t, Zihua Chen u, Minghua Cong v, Hu Ma w,
Chunling Zhou x, Wei Wang y, Qi Luo z, Yongmei Shi aa, Yumei Qi bb,
Haiping Jiang cc, Wenxian Guan dd, Junqiang Chen ee, Jiaxin Chen ff,
Yu Fang gg, Lan Zhou hh, Yongdong Feng ii, Rongshao Tan jj,
Junwen Ou kk, Qingchuan Zhao ll, Jianxiong Wu mm, Xin Lin b,
Liuqing Yang nn, Zhenming Fu oo, Chang Wang c, Li Deng c,
Tao Li pp,1,∗∗∗, Chunhua Song qq,1,∗∗, Hanping Shi rr,1,∗ , The
Investigation on Nutrition Status and Clinical Outcome of Common
Cancers (INSCOC) Group, Chinese Society of Nutritional Oncology
a
Department of Preventive Medicine, Heze Medical College, Heze, Shandong 274000, China
b
Department of Nutrition, Daping Hospital & Research Institute of Surgery, Third Military Medical University,
Chongqing 400042, China
c
Cancer Center of the First Hospital of Jilin University, Changchun, Jilin 130021 China

✩
This work was financially supported by Chinese Society for Oncological Nutrition & Supportive Care; The National
Key Research and Development Program (2017YFC1309200); Support program for scientific and technological innova-
tion talents of Henan Universities (19HASTIT005); Medical Science and Technology Key Projects of Henan Province and
Zhengzhou (192102310 088, SBGJ2018089, 19A320 0 0820);The National Natural Science Foundation of China (U1604168).
✩✩
Conflicts of Interest: The authors declare that they have no competing interests.
∗
Correspondence to: Hanping Shi, Departments of Gastrointestinal Surgery and Department of Clinical Nutrition, Bei-
jing Shijitan Hospital, Capital Medical University, No. 10 Tieyi Road Haidian Dist, Beijing 10 0 038, China.
∗∗
Correspondence to: Chunhua Song, Department of Epidemiology and Statistics, College of Public Health, Zhengzhou
University, Zhengzhou, Henan 450 0 01, China.
∗∗∗
Correspondence to: Tao Li, Department of Radiotherapy, Sichuan Cancer Hospital & Institute, Sichuan Cancer Center,
School of Medicine, University of Electronic Science and Technology of China, Chengdu, Sichuan 610041, China.
E-mail addresses: litaoxmf@126.com (T. Li), sch16@zzu.edu.cn (C. Song), shihp@ccmu.edu.cn (H. Shi).
1
Hanping Shi, Chunhua Song, and Tao Li contributed equally to this work.

https://doi.org/10.1016/j.currproblcancer.2020.100638
0147-0272/© 2020 Elsevier Inc. All rights reserved.
2 J. Cao, H. Xu and W. Li et al. / Current Problems in Cancer 45 (2021) 100638

d
Department of Medical Oncology, Fujian Cancer Hospital, Fujian Medical University Cancer Hospital, Fuzhou,
Fujian 350014, China
e
Department of Gastrointestinal Surgery, Affiliated Tumor Hospital of Guangxi Medical University, Nanning,
Guangxi 530021, China
f
Department of Surgery, The First Affiliated Hospital of SunYat-sen University, Guangzhou, Guangdong 510080,
China
g
Department of Clinical Nutrition, West China Hospital of Sichuan University, Chengdu, Sichuan 610041, China
h
Department of Gastrointestinal Oncology, Tianjin Medical University Cancer Institute and Hospital, National
Clinical Research Center for Cancer, Tianjin Key Laboratory of Cancer Prevention and Therapy, Tianjin 300060, China
i
Department of Nutrition and Metabolism of Oncology, Affiliated Provincial Hospital of Anhui Medical University,
Hefei, Anhui 230031, China
j
Department of Clinical Nutrition, The First Hospital of Hebei Medical University, Shijiazhuang, Hebei 050031, China
k
Department of Gastrointestinal Surgery, Institute of Gastroenterology, The First Affiliated Hospital of Kunming
Medical University, Kunming, Yunnan 650032, China
l
Zhongshan Chenxinghai Hospital (Affiliated Zhongshan Chenxinghai Hospital of Guangdong Medical University),
Zhongshan, Guangdong 528400, China
m
Department of Clinical Nutrition, The First People’s Hospital of Kashi, Xinjiang 844000, China
n
Department of Clinical Nutrition, Chongqing General Hospital, Chongqing 400014, China
o
Department of Colorectal and Anal Surgery, Huizhou Municipal Central Hospital, Huizhou, Guangdong 516001,
China
p
Department of Radiation and Medical Oncology, Zhongnan Hospital of Wuhan University, Wuhan, Hubei 430071,
China
q
Department of Oncology, Xingtai People’s Hospital, Hebei Medical University, Xingtai, Hebei 054031, China
r
The First Department of the Tumor Hospital of Harbin Medical University, Harbin, Heilongjiang 150085, China
s
Department of Nutrition, Guangdong General Hospital, Guangdong Academy of Medical Sciences, Guangzhou,
Guangdong 510080, China
t
Department of Oncology, Affiliated Cancer Hospital of Zhengzhou University and Henan Cancer Hospital,
Zhengzhou, Henan 450008, China;
u
Department of General Surgery, Xiangya Hospital, Central South University, Changsha, Hunan 410008, China
v
Comprehensive Oncology Department, Cancer Hospital, Chinese Academy of Medical Sciences, Beijing 100021,
China
w
Department of Oncology, Affiliated Hospital of Zunyi Medical University, Zunyi, Guizhou 563000, China
x
The Fourth Affiliated Hospital, Harbin Medical University, Harbin, Heilongjiang 150001, China
y
Cancer Center, The First People’s Hospital of Foshan, Foshan, Guangdong 528000, China
z
Department of Gastrointestinal Tumor Surgery, The First Affiliated Hospital, Xiamen University, Xiamen, Fujian
361003, China
aa
Department of Nutrition, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200025,
China
bb
Department of Nutrition, Tianjin Third Central Hospital, Tianjin 300170, China
cc
Department of Surgery, The First Affiliated Hospital of Jinan University, Guangzhou, Guangdong 510632, China
dd
Department of General Surgery, Nanjing Drum Tower Hospital, The Affiliated Hospital of Nanjing University
Medical School, Nanjing, Jiangsu 210008, China
ee
Department of Gastrointestinal Surgery, First Affiliated Hospital of Guangxi Medical University, Nanning, Guangxi
530021, China
ff
Department of Radiation and Medical Oncology, People’s Hospital of Guangxi Zhuang Autonomous Region,
Nanning, Guangxi 530021, China
gg
Department of Clinical Nutrition, Peking University Cancer Hospital and Institute, Beijing 100142, China
hh
Department of Nutrition, Third Affiliated Hospital of Kunming Medical College, Tumor Hospital of Yunnan
Province, Kunming, Yunnan 650118, China
ii
Department of Surgery, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology,
Wuhan 430030, China
jj
Department of Nutrition, Guangzhou Red Cross Hospital, Guangzhou, Guangdong 510220, China
kk
Department of Clinical Nutrition, Clifford Hospital, Guangzhou University of Chinese Medicine, Guangzhou,
Guangdong 510632, China
ll
Department of Digestive Diseases, Xijing Hospital, Fourth Military Medical University, Xi’an, Shanxi 710032, China
mm
Department of Hepatobiliary Surgery, National Cancer Center/Cancer Hospital, Chinese Academy of Medical
Sciences and Peking Union Medical College, Beijing 100021, China
nn
Department of Gastrointestinal Surgery/Clinical Nutrition, Beijing Shijitan Hospital, Capital Medical University,
The 9th Clinical College, PKU. No.10 Tieyi Road, Haidian Dist, Beijing 100038, China
oo
Cancer Center, Renmin Hospital of Wuhan University, Wuhan, Hubei 430060, China
pp
Department of Radiotherapy, Sichuan Cancer Hospital & Institute, Sichuan Cancer Center, School of Medicine,
University of Electronic Science and Technology of China, Chengdu, Sichuan 610041, China
qq
Department of Epidemiology and Statistics, College of Public Health, Zhengzhou University, Zhengzhou 450001,
Henan, PR China
 J. Cao, H. Xu and W. Li et al. / Current Problems in Cancer 45 (2021) 100638 3

rr
Department of Gastrointestinal Surgery/Clinical Nutrition, Beijing Shijitan Hospital, Capital Medical University, The
9th Clinical College, PKU. No. 10 Tieyi Road, Haidian Dist, Beijing 100038, China

a b s t r a c t

Introduction: Esophageal cancer is the fourth most common cause of cancer death in China. Patients with
esophageal cancer are more likely to suffer from malnutrition. The purpose of this study is to assess nu-
tritional status of patients with esophageal cancer from multiple perspectives and analyze the risk factors.
Methods: A total of 1482 esophageal cancer patients were enrolled in the study. We investigated the Scored
Patient Generated Subjective Global Assessment (PG-SGA) scores, NRS-2002 scores, Karnofsky performance
status scores, anthropometric, and laboratory indicators of patients. Unconditional logistic regression anal-
ysis was applied to identify the risk factors of nutritional status. Results: PG-SGA (≥4) and NRS-2002 (≥3)
showed the incidence of malnutrition were 76% and 50%, respectively. In the patients with PG-SGA score
≥4, the proportion of patients who did not receive any nutritional support was 60%. The incidence of mal-
nutrition in females was significantly higher than that in males. Besides, abnormality rates of Red blood
cell (P < 0.001), MAC (P = 0.037), and MAMC (P < 0.001) in males was significantly higher than that in fe-
males, while abnormality rates of TSF (P < 0.001) was lower than that in females. After adjusted with the
other potential risk factors listed, unconditional logistic regression analysis indicated smoking (odds ratio:
2.868, 95% confidence interval: 1.660-4.954), drinking (OR: 1.726, 95% CI: 1.099-2.712), family history (OR:
1.840, 95% CI: 1.132-2.992), radiotherapy or chemotherapy (OR: 1.594, 95% CI: 1.065-2.387), and pathologi-
cal stage (OR: 2.263, 95% CI: 1.084-4.726) might be the risk factors of nutritional status, while nutritional
support can reduce the risk of malnutrition. Conclusion: Effective nutritional risk assessment methods and
nutritional intervention measures can be adopted according to the research data to improve quality of life
of esophageal cancer patients.
© 2020 Elsevier Inc. All rights reserved.

a r t i c l e i n f o

Keywords: Esophageal cancer; Nutrition status; Nutritional support; Risk factor; PG-SGA

Introduction

Esophageal cancer is the sixth most common malignant tumor and the fourth most com-
mon cause of cancer death in China.1 It is estimated that about 375,0 0 0 Chinese will die from
Esophageal cancer in 2015, accounting for 13.3% of all cancer deaths.2
Influenced by the disease itself and the treatment of cancer, the nutritional problems of pa-
tients with malignant tumors are more serious. Malnutrition has been shown to have negative
effect on cancer patients, such as reducing the tolerance and efficacy of their treatment,3 in-
creasing the risk for clinical and surgical complications,4 and lengthening hospital stay with a
concomitant increase in health care costs.5 It is estimated that 10%-20% of cancer patients die
from malnutrition, not cancer itself.6 Esophageal cancer, as a kind of upper gastrointestinal can-
cer, directly affects the intake of food and has a higher risk of malnutrition. Most of the patients
diagnosed with esophageal cancer are advanced, about 40%-60% of the patients were malnour-
ished at the time of admission.7 Progressive dysphagia8 and significant weight loss9 are the
typical symptomatic presentation of advanced esophageal cancer patients and concurrent radio-
therapy and chemotherapy is an effective way of esophageal cancer treatment.10 The character-
istics of esophageal cancer make patients with esophageal cancer are more likely to suffer from
malnutrition.
The importance of nutritional status of cancer patients is widely recognized, and vari-
ous methods to assess nutritional status of patients are emerging. The Patient Generated
4 J. Cao, H. Xu and W. Li et al. / Current Problems in Cancer 45 (2021) 100638

Subjective Global Assessment (PG-SGA) is a specific nutritional assessment and screening tool for
cancer patients, it is significantly associated with subjective and objective parameters and widely
recognized method of assessing nutritional status.11 NRS-2002 is a nutritional risk screening
method recommended by the European Society of Parenteral Nutrition (ESPEN) for hospitalized
patients12 and the Karnofsky performance status (KPS) available to monitor the variation in vi-
tality and dependence levels can also reflect the nutritional status of cancer patients to a certain
extent.13 Besides, anthropometry and laboratory examinations can provide objective measure-
ments to reflect the nutritional status of cancer patients.
Studies confirmed that understanding the nutritional status of patients and implementing
nutritional intervention can improve the quality of life and reduce the risk of malnutrition.
However, no single method or indicator can accurately assess the overall nutritional status of
patients. Up to now, study on comprehensive assessment of nutritional status of patients with
esophageal cancer has not yet been found. In the current study, we attempt to evaluate the
nutritional status of patients with esophageal cancer from multiple perspectives. The PG-SGA,
NRS-2002, and KPS scores of 1482 esophageal cancer patients were estimated and classic an-
thropometric and laboratory indicators that can reflect the nutritional status of patients were
collected. In addition, unconditional logistic regression analysis was carried out to identify the
factors that might affect nutritional risk of esophageal cancer patients.

Materials and Methods

Subjects

In the cross-sectional study, a total of 1482 esophageal cancer patients in 72 hospitals in

China came from a Program on Nutrition Status and its Clinical Outcome of Common Cancers
supported by Chinese Society for Oncological Nutrition & Supportive Care in 2013. All partici-
pants followed strict inclusion and exclusion criteria: (1) age ≥18 years; (2) pathology diagnosed
with esophageal cancer; (3) conscious, and no communication disorders; (4) informed consent;
(5) deem the patients as 1 case when he hospitalized more than 2 times during our investiga-
tion; (6) without organ transplantation. Informed consent was obtained from each participant.
The study was approved by the ethical review committee of X Committee for Medical and Health
Research Ethics.

Nutritional Assessment

PG-SGA, NRS-2002, and Karnofsky Performance Status

Referring to the operation standard produced by the American Academy of Nutrition and Di-
etetics, we used the PG-SGA method to assess nutritional risk in patients with esophageal can-
cer.14 The subjects were divided into 4 groups according to their PG-SGA scores: those with 4-8
point require an intervention by a dietitian with clinical symptom survey; those with ≥9 point
urgently need to improve symptom management and nutritional support treatment. NRS-2002
was also used to assess the nutritional risk of esophageal cancer patients. In addition, we evalu-
ated the KPS of patients with esophageal cancer. The KPS uses a score from 0% to 100%. A score
of 100% indicates full capacity to perform normal daily activities without clinical evidence of dis-
ease and without physical dependence, and a score of 0% indicates death.15 The KPS score 70%
was as a cutoff to define the impossibility of maintaining independent individual daily activities
and needing direct care to maintain life.16

Anthropometric and Laboratory Indicators

Anthropometric and laboratory examination variables were collected by investigators with
unified training for the standardized techniques for interview and measurement. Height and
 J. Cao, H. Xu and W. Li et al. / Current Problems in Cancer 45 (2021) 100638 5

weight (0.1-kg precision) were measured without heavy clothing and shoes using a standard sta-
diometer by trained observers. Mid-arm circumference (MAC) was measured to the nearest 0.5
cm midway between the acromion and the olecranon and circumference of calf was assessed
at the thickest part of the calf with a flexible anthropometric tape. Triceps skin fold (TSF) was
determined with skin fold thickness meter and grip strength of subdominant hand was deter-
mined with dynamograph. Body mass index (BMI) is calculated as follows: weight divided by
the square of height (kg/m2 ). Mid-arm muscle circumference (MAMC) is calculated as follows:
MAC minus 3.14 times TSF (cm). Laboratory variables include: albumin, prealbumin, transferrin,
C-reactive protein, hemoglobin, total lymphocyte, and red blood cell.

Diagnosis of Malnutrition
In the study of the influencing factors of malnutrition, the diagnosis standard of malnutrition
adopts the standard recommended by The European Society of Clinical Nutrition and Metabolism
(ESPEN) in 2015.17

Data Collection
The demographic data and potential esophageal cancer risk factors were collected face-to-
face by trained physicians. The detailed information include age, gender, smoking (more than
100 cigarettes in total), drinking (at least once a week), types of medical insurance, occupation,
permanent residence, nationality, education level, complicated with chronic diseases, family his-
tory of cancer, pathological stage, and radiotherapy or chemotherapy.

Statistical Analysis

For quantitative variables, arithmetic mean ± standard deviation or median (upper quartile-
lower quartile) were presented, and Student’s t test was used to analyze differences between
men and women. For categorical variables, constituent ratio (percentages) was presented, and
chi-squared test was used to analyze differences between men and women. Unconditional logis-
tic regression analysis was conducted to identify malnutrition risk factors of esophageal cancer
with adjustments of the other potential influence factors. Statistical analysis was conducted with
SPSS 22.0 software and a 2-side P value with a level of less than 0.05 was significant.

Results

The Characteristics of Esophageal Cancer Patients

A total of 1482 esophageal cancer patients were included in the study, of which 273(18.42%)
were females and 1209 (81.58%) were males with a mean age of 62.68 ± 10.91 years. There
were 35.09% (519) esophageal cancer patients with moderately malnourished status (scores 4-
8), 46.93% (694) with severely malnourished status (score≥9), 11.49% (170) with suspicious mal-
nourished status (scores 2-3), and only 6.49% (96) with well-nourished status (scores 0-1). We
observed 613(41.39%) patients received either radiotherapy or chemotherapy and 840 esophageal
cancer patients could be confirmed pathological stage (328 cases with stage III esophageal can-
cer, 258 with IV, 148 with II, 104 with I). The nutritional support of the subjects was as follows:
67% esophageal cancer patients did not receive any nutritional intervention, 19% of patients re-
ceived parenteral nutrition (PN) support, 9% received enteral nutrition (EN) support, and 5% re-
ceived both enteral and PN support. The factors that might affect the nutritional status of pa-
tients (smoking, drinking, types of medical insurances, occupations, permanent residential, na-
tionality, education levels, complicated with chronic diseases, family history, and pathological
stage) were showed in Table 1.
6 J. Cao, H. Xu and W. Li et al. / Current Problems in Cancer 45 (2021) 100638

Table 1
The characteristics of esophageal cancer patients.

Variables N (%)

Age 62.68 ± 10.91

Gender
Male 1209 (81.58)
Female 273 (18.42)
Smoking
Yes 903 (60.93)
No 579 (39.07)
Drinking
Yes 575 (38.80)
No 907 (61.20)
Types of medical insurance
Urban medical insurance 583 (40.10)
Commercial medical insurance 14 (0.96)
Rural cooperative medical insurance 690 (47.46)
Self-paid medical 167 (11.48)
Occupations
Staff 131 (8.85)
Worker 112 (7.56)
Farmer 650 (43.89)
Retirees and others 588 (39.70)
Permanent residence
Capital city 180 (12.29)
Prefecture level cities 205 (13.99)
County-level city 145 (9.90)
Rural areas 935 (63.82)
Nationality
Han 970 (90.90)
Uygur 45 (4.22)
Zhuang 22 (2.06)
Mongolian 10 (0.94)
Other ethnic groups 20 (1.88)
Education levels
Primary school and below 689 (46.52)
Junior middle school 450 (30.38)
Senior high school 243 (16.41)
University degree or above 99 (6.69)
PG-SGA score
0-1 96 (6.49)
2-3 170 (11.49)
4-8 519 (35.09)
≥9 694 (46.93)
Complicated with chronic diseases
Yes 395 (26.67)
No 1086 (73.33)
Family history
Yes 243 (16.41)
No 1238 (83.59)
Pathological stage
1 104 (12.41)
2 148 (17.66)
3 328 (39.14)
4 258 (30.79)
Radiotherapy or chemotherapy
Yes 613 (41.39)
No 868 (58.61)
 J. Cao, H. Xu and W. Li et al. / Current Problems in Cancer 45 (2021) 100638 7

Table 2
PG-SGA, Karnofsky and NRS-2002 scores of esophageal cancer patients.

Scores N Mean ± standard deviation Males Females P

PG-SGA 1479 8.651 ± 5.095

≥4 1130 (0.76) 909 (0.75) 221 (0.81) 0.037
<4 349 (0.24) 298 (0.25) 51 (0.19)
Karnofsky 1480 84.277 ± 14.07
≥70 1364 (0.92) 1118 (0.93) 246 (0.98) 0.24
<70 116 (0.08) 90 (0.07) 26 (0.02)
NRS-2002 1476 2.42 ± 1.639
≥3 731 (0.50) 576 (0.48) 155 (0.60) 0.006
<3 745 (0.50) 628 (0.52) 117 (0.40)
∗
There were significant differences among the 3 methods in judging nutritional risk of patients (P < 0.001).

Table 3
Laboratory parameters in esophageal cancer patients.

Parameters Median (quartile Abnormality rate

(unit) N range) P
Males Females

Albumin (g/L) 1444 38.30 0.25 0.19 0.041

(35.00-41.50)
Prealbumin (g/L) 881 0.19 (0.14-0.24) 0.88 0.92 0.22
Transferrin (g/L) 133 2.00 (1.71-2.37) 0.32 0.3 0.91
C-reactive protein (mg/L) 372 5.31 (2.00-15.17) 0.37 0.25 0.10
Hemoglobin (g/L) 1449 122.00 0.41 0.34 0.18
(110.0 0-134.0 0)
Total lymphocyte (109 /L) 1451 1.37 (0.96-1.91) 0.22 0.25 0.21
Red blood cell (1012 /L) 1449 4.06 (3.63-4.43) 0.76 0.52 <0.001

Reference range of albumin: ≥35 g/L; reference range of prealbumin: ≥0.28 g/L; reference range of transferrin: ≥1.8
g/L; reference range of C-reactive protein: ≤8 mg/L; reference range of hemoglobin: male ≥120 g/L, female ≥110 g/L;
reference range of total lymphocyte: 0.8-4∗ 109 /L; reference range of red blood cell: ≥male 4.5∗ 1012 /L, female ≥4.0∗ 1012 /L.

PG-SGA, Karnofsky, and NRS-2002 Scores of Esophageal Cancer Patients

Table 2 showed the PG-SGA, Karnofsky, and NRS-2002 scores of esophageal cancer patients.
The average PG-SGA score in patients with esophageal cancer was 8.651 ± 5.095. The results
showed that 76% of esophageal cancer patients are malnourished (PG-SGA≥4) and the incidence
of malnutrition in males was significantly higher than that in females. The average level of
Karnofsky score of the subjects was 84.277 ± 14.07, and there was no statistical difference in
the proportion of people with Karnofsky score<70 between different genders. We evaluated the
NRS-2002 scores of esophageal cancer patients, and found the proportion of patients needing
nutritional intervention (NRS-2002 ≥3) was 50% and the proportion of women needing nutri-
tional intervention (NRS-2002 ≥3) was higher than that of men.

Laboratory Parameters in Esophageal Cancer Patients

Table 3 shows the levels of albumin, prealbumin, transferrin, C-reactive protein, hemoglobin,
total lymphocyte, and red blood cell in patients with esophageal cancer. Average level and vari-
ation degree are expressed by median and quartile spacing, respectively. The prealbumin levels
(0.19 g/L) in patients with esophageal cancer were lower than normal (0.28-0.36 g/L). Although
the levels of transferrin, hemoglobin, and red blood cell were within the normal range, they
were on the low side. In addition, the abnormal rates of these indicators for men and women
were calculated, respectively. The abnormal rate of prealbumin is the highest. For most of the
indicators, the abnormal rates of men were higher than that of women, and chi-square test
8 J. Cao, H. Xu and W. Li et al. / Current Problems in Cancer 45 (2021) 100638

Table 4
The anthropometric parameters of esophageal cancer patients.

Parameters (unit) N Mean ± standard deviation Males Females P

Weight loss in a month (≥5%, kg) 1423 1.600 ± 3.275 0.26 0.20 0.09
Weight loss in 6 months (≥10%, kg) 1042 4.120 ± 5.373 0.51 0.51 0.99
BMI (kg/m2 ) 1471 20.973 ± 3.340 0.22 0.25 0.28
MAC (cm) 1436 25.188 ± 3.542 0.42 0.35 0.043
MAMC (cm) 1419 21.504±3.834 0.63 0.49 <0.001
TSF (mm) 1433 11.971 ± 6.659 0.44 0.58 <0.001
Grip strength of subdominant hand (kg) 1377 24.443 ± 10.131 0.63 0.67 0.21
Circumference of calf (left, cm) 1366 31.583 ± 4.031 0.18 0.32 <0.001

Reference range of BMI for adults in China: ≥18.5 kg/m2 ; reference range of MAC: male ts in 5 cm, female ≥23.22
cm; reference range of MAMC: male ≥22.77 cm, female ≥20.88 cm; reference range of TSF: male ≥7.47 mm, female
≥13.77 mm; reference range of grip strength of subdominant hand: male r29.6 kg, female n18.6 kg; reference range of
circumference of calf (cm): ≥29 cm.

Table 5
The nutritional support in esophageal cancer patients.

Nutrition Total Male Female PG-SGA≥4

support (%) (%) (%)
Total (%) Male (%) Female (%)

No 959 (66.69) 787 (67.32) 172 (63.94) 671 (60.94) 545 (61.72) 126 (57.80)
Yes
PN 272 (18.91) 214 (18.31) 58 (21.56) 246 (22.34) 191 (21.63) 55 (25.23)
EN 131 (9.11) 108 (9.24) 23 (8.55) 120 (10.90) 98 (11.10) 22 (10.09)
EN and PN 76 (5.29) 60 (5.13) 16 (5.95) 64 (5.82) 49 (5.55) 15 (6.88)

showed that the abnormal rate of albumin (P = 0.041) and red blood cell (P < 0.001) in males
was significantly higher than that in females.

Anthropometric Parameters of Esophageal Cancer Patients

The anthropometric parameters of esophageal cancer patients were displayed in Table 4.

Twenty-six percent of male patients and 20% of female patients lose more than 5% of their body
weight in a month. No matter in males and females, almost half of the patients lost more than
10% of their body weight in 6 months. No significant differences were observed in the propor-
tion of weight loss between men and women. MAMC, BMI, MAC, and TSF of esophageal cancer
patients were at a low borderline level. Moreover, there were significant differences between
men and women in MAC, MAMC, TSF, and circumference of calf.

Nutritional Support in Patients With Esophageal Cancer

Nutritional support in patients with esophageal cancer was showed in Table 5. We observed
that 67% esophageal cancer patients did not receive any nutritional intervention. 19% of patients
received PN support, 9% received EN support, and 5% received both EN and PN support. In addi-
tion, in the patients with PG-SGA score ≥4, the proportion of patients who did not receive any
nutritional support was still as high as 60%.

The Association Between Influence Factors and Malnutrition

The distributions of potential risk factors in malnutrition group and nonmalnutrition group
were displayed in Table 6. Statistical analysis showed that there were significant differences in
 J. Cao, H. Xu and W. Li et al. / Current Problems in Cancer 45 (2021) 100638 9

Table 6
The association between influence factors and nutritional risk in esophageal cancer patients.

Variables Non Malnutrition Pa Pb OR (95% CI)

malnutrition (%)
(%)

Age
≤65 681 (75.84) 217 (24.16) 0.043 0.205 1
>65 411 (71.11) 167 (28.89) 1.320 (0.859-2.029)
Gender
Male 894 (74.19) 311 (25.81) 0.727 0.152 1
Female 199 (73.16) 73 (26.84) 1.614 (0.839-3.103)
Smoking
No 438 (75.91) 139 (24.09) 0.181 <0.001 1
Yes 655 (72.78) 245 (27.22) 2.868 (1.660-4.954)
Drinking
No 694 (74.95) 232 (25.05) 0.289 0.018 1
Yes 399 (72.41) 152 (27.59) 1.726 (1.099-2.712)
Types of medical insurance
Urban medical insurance 426 (73.70) 152 (26.30) 0.787 0.407 1
Rural cooperative medical insurance 510 (74.56) 174 (25.44) 0.751 0.914 (0.527-1.588)
Others 129 (72.07) 50 (27.93) 0.307 1.428 (0.721-2.831)
Occupations
Staff 102 (77.86) 29 (22.14) 0.599 0.531 1
Worker 80 (72.07) 31 (27.93) 0.941 0.964 (0.371-2.504)
Farmer 472 (72.84) 176 (27.16) 0.754 0.870 (0.364-2.080)
Retirees and others 439 (74.79) 148 (25.21) 0.301 0.672 (0.316-1.427)
Permanent residential
Capital city 121 (67.22) 59 (32.78) 0.085 0.337 1
Prefecture level cities 154 (75.12) 51 (24.88) 0.251 0.643 (0.302-1.366)
County-level city 115 (79.31) 30 (20.69) 0.075 0.426 (0.167-1.089)
Rural areas 692 (74.33) 239 (25.67) 0.180 0.632 (0.324-1.236)
Nationality
Han 699 (72.21) 269 (27.79) 0.944 0.821 1
Other ethnic groups 69 (71.88) 27 (28.12) 1.084 (0.54-2.174)
Education levels
Primary school and below 504 (73.36) 183 (26.64) 0.903 0.555 1
Junior middle school 335 (74.61) 114 (25.39) 0.991 1.003 (0.619-1.624)
Senior high school 179 (73.66) 64 (26.34) 0.659 0.867 (0.459-1.636)
University degree or above 75 (76.53) 23 (23.47) 0.178 0.519 (0.200-1.349)
Family history
No 917 (74.19) 318 (25.81) 0.944 0.014 1
Yes 175 (72.61) 66 (27.39) 1.840 (1.132-2.992)
Complicated with chronic diseases
No 789 (72.92) 293 (27.08) 0.117 0.166 1
Yes 304 (76.96) 91 (23.04) 0.724 (0.458-1.144)
Radiotherapy or chemotherapy
No 490 (76.09) 154 (23.91) 0.106 0.023 1
Yes 603 (72.39) 230 (27.61) 1.594 (1.065-2.387)
Pathological stage
Ⅰ 88 (83.81) 17 (16.19) 0.038 0.139 1
Ⅱ 114 (77.03) 34 (22.97) 0.302 1.552 (0.674-3.575)
Ⅲ 229 (70.25) 97 (29.75) 0.030 2.263 (1.084-4.726)
Ⅳ 189 (73.26) 69 (26.74) 0.074 1.987 (0.935-4.222)
Nutritional support
No 601 (69.64) 262 (30.36) <0.001 <0.001 1
Yes 462 (80.63) 111 (19.37) 0.443 (0.296-0.661)
a
Two-sided chi-square test, P < 0.05 was considered to be statistically significant.
b
P value of logistic regression analysis with adjusted for the other variables listed in the table.
10 J. Cao, H. Xu and W. Li et al. / Current Problems in Cancer 45 (2021) 100638

age (P = 0.043), pathological stage (P = 0.038) and nutritional support (P < 0.001) distributions
between the 2 groups. After adjusted for the other potential risk factors listed, new significant
associations between malnutrition and several factors were detected: the results revealed a sig-
nificant higher nutritional risk in the participant with smoking (OR: 2.868, 95% CI: 1.660-4.954),
drinking (OR: 1.726, 95% CI: 1.099-2.712), family history (OR: 1.840, 95% CI: 1.132-2.992) and
radiotherapy or chemotherapy (OR: 1.594, 95% CI: 1.065-2.387). In addition, after adjusted for
the other factors listed, pathological stage Ⅲ (OR: 2.263, 95% CI: 1.084-4.726) and nutritional
support (OR: 0.443, 95% CI: 0.296-0.661) were still significantly associated with malnutrition.

Discussion

The PG-SGA was recommended as a nutritional screening tool specifically for oncology pa-
tients.18 It could detect subtle changes in nutritional risk in a short time and most of PG-SGA
can be done by patients alone.19 It was widely recognized that PG-SGA was a quick, valid, and
reliable nutrition risk screening tool. In a previous article, we evaluated the nutritional risk of
16 common malignant tumors in 23904 cancer patients by PG-SGA methods and the results
showed malnutrition risk is highest in patients with esophageal cancer (8.6 ± 5.1) among those
common malignant tumors except for pancreatic cancer(10 ± 6.0).14 A study evaluated nutrition
status of 63 Vietnamese patients with esophageal cancer and reported the mean ± standard
deviation of PG-SGA score was 9.88 ± 4.41.20 The McGill Cancer Nutrition and Rehabilitation
(CNR) assessed the nutritional status of patients with gastroesophageal cancer, the median score
of PG-SGA was12.0 (2–24).21 The higher PG-SGA scores in several studies indicated poor nutri-
tional status in patients with esophageal cancer. In the current study, we found 35.09% (519)
esophageal cancer patients were moderately malnourished (scores 4-8) and 46.93% (694) were
severely malnourished (score≥9), and only 6.49% (96) with well-nourished status (scores 0-1).
ESPEN recommends nutritional support for patients with NRS-2002 ≥3. NRS-2002 has been
applied into nutritional risk screening for patients with many tumors, and it suggest NRS-2002
can provide a reasonable and effective basis for the clinical nutritional support.22 Wang’s study
reported a 65% incidence of nutritional risk in 160 esophageal cancer patients aged over 6023
and another study identified 44.8% esophageal cancer patients at nutritional risk.24 In this study,
about 50% of Esophageal Cancer patients were considered to be in the risk of nutrition with
NRS-2002 ≥3 and the proportion of patients in nutritional risk is higher in women than in men.
In previous studies, we also found that women’s nutritional status is worse than men’s in some
malignant tumors, such as gastric cancer and liver cancer, including esophageal cancer.14 Some
studies have focused on the effect of gender on nutritional status. A study from Lao PDR found
women had lower intake than men for almost all nutrients and age groups.25 In addition, nu-
trient insufficiencies were higher among pregnant and lactating women than other adult men
and women.25 The latest WHO estimates show that the prevalence of underweight in women is
higher than in men.26 On the other hand, changes in many diets have led to excessive weight
gain in men and women, especially in women. Prevalence of overweight and obesity were re-
spectively 5% and 8.5% among men and 9.5% and 12.5% among women.27 These might partly
explain the higher nutritional risk of women.
Anthropometric and laboratorial parameters have been widely used in a number of studies to
indicate nutritional status. The prevalence of malnutrition varies with different nutrition assess-
ment methods. Poziomyck’s study28 showed the mean BMI of 74 patients with foregut tumors
was 22.9 ± 4.4 kg/m2 and weight loss were associated with mortality. A clinical study revealed
43.8% of Esophageal Cancer patients were underweight according to BMI and revealed 29.7% of
undernourished patients by MAC.20 Silva et al reported the prevalence of malnutrition in 43
esophageal and gastric cancer patients was 86.1% according to the SGA, however, the overall
prevalence of malnutrition, as defined by BMI, TSF, MAC, and MAMC, was 48.8%, 41.9%, 72.1%,
and 74.4%, respectively. In addition, they found the MAC, MAMC, and HGS were different be-
tween nourished (SGA A) and severely malnourished (SGA C) patients.29 Takeda et al and Ibuki
et al tested the serum albumin, C-reactive protein, and hemoglobin in patients with esophageal
 J. Cao, H. Xu and W. Li et al. / Current Problems in Cancer 45 (2021) 100638 11

cancer, and found albumin and C-reactive protein might be related to better prognosis.30 , 31 In
our study, we detected high abnormal rate of indicators, of which the abnormal rate of prealbu-
min was as high as 88%. Similar to previous studies, we found that although these classical mea-
surements showed a significant correlation with nutritional status, Esophageal Cancer patients
had also most of anthropometric and laboratorial parameters within normal range, indicating
that general parameters may not reliably discriminate nutritional features indeed.
Nutritional support could reduce the nutritional risk of cancer patients and improve their
quality of life, including esophageal cancer. Cong’s study concluded reasonable nutritional inter-
vention could provide positive effects in esophageal cancer patients undergoing chemoradiother-
apy on maintaining their nutrition status.32 Another study showed nutritional support before
surgery can facilitate the nutritional status of esophageal cancer patients and decrease the aver-
age hospitalization and hospitalization cost.23 For patients with esophageal cancer after surgery,
early EN support can reduce the incidence of serious complications and maintain better nu-
tritional status than PN support.33 PN may be considered when EN is insufficient to maintain
nutritional status. A previous study did not recommend total PN support for all of patients with
gastrointestinal lymphoma as the practice of prophylactic total PN and bowel rest was asso-
ciated with higher infection risk and longer hospitalization.34 At present, there are few reports
about the nutritional support rate of esophageal cancer patients. For the 1482 esophageal cancer
patients in our study, only 479 (33%) patients received nutritional support. Of all patients receiv-
ing nutritional support, about 73% (348) had to receive parenteral nutritional support. Even in
malnourished patients (A strict diagnostic standard for malnutrition recommended by ESPEN),
the nutritional support rate of patients with esophageal cancer was only 43%. Considering about
76% of patients with PG-SGA≥4, the nutritional support rate of patients with esophageal cancer
is too low. Therefore, timely assessment of nutritional status of patients with esophageal cancer
and active nutritional intervention measures are very urgent.
Nutritional status of patients with esophageal cancer can be affected by many factors. Pre-
vious studies suggested that the nutritional risk of patients with malignant tumor is gradually
deteriorating with age for most of the malignant tumor.14 Similarly, our study showed higher
age increases nutritional risk in patients with esophageal cancer. However, after adjusted for
the other potential risk factors listed, no significant correlation between age and the risk of
malnutrition in patients with esophageal cancer was found. Differences in sample size and nu-
trition assessment methods may lead to this conflicting outcome. The majority of patients with
esophageal cancer are males, but there was no significant difference in the nutritional risk be-
tween male and female esophageal cancer patients, which was consistent with Wang’s results.24
In our previous study, we observed the associations between nutritional risk of malignant tu-
mor patient and different demographic characteristics.14 Few studies have focused on the rela-
tionship between demographic characteristics and nutritional status in patients with esophageal
cancer. However, in the current study, no association was found between the risk of malnutrition
and demographic characteristics in patients with esophageal cancer. A study from Switzerland
showed that active smoking and excessive alcohol consumption were associated with the oc-
currence of severe complications of esophageal cancer.35 Similarly, our results suggested that
smoking and drinking were risk factors for malnutrition in patients with esophageal cancer. Be-
side, radiotherapy or chemotherapy and higher pathological stages might lead to malnutrition in
esophageal cancer patients.
Several strengths and limitations of the study are as follows. This is a large-scale survey
of nutritional status of common cancer supported by Chinese Society for Oncological Nutrition
& Supportive Care. Up to now, more than 25,0 0 0 questionnaires on common cancer patients
from 72 first-class hospitals in China were collected. During the whole process of this investiga-
tion, strict quality control was adopted to reduce bias: pathologically confirmed patients, unified
training clinicians and double data entry. Meanwhile, some limitations cannot be ignored. No
single method or indicator can comprehensively assess the nutritional status of patients. In this
cross-sectional study, we only describe the nutritional status of patients with esophageal cancer
12 J. Cao, H. Xu and W. Li et al. / Current Problems in Cancer 45 (2021) 100638

from multiple perspectives, the clinical outcomes of the patients will be followed up and the
association between clinical outcomes and nutritional risk will be explored further.
In conclusion, our findings support a higher nutritional risk in patients with esophageal can-
cer, especially in women. Considering the poor nutritional status of patients with esophageal
cancer and the low nutritional support rate in clinic, we call for more attention to the nutri-
tional status of patients with esophageal cancer. Effective nutritional risk assessment methods
and nutritional intervention measures can be adopted according to the research data to improve
the clinical therapeutic effect and quality of life of esophageal cancer patients.

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