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Open access Original research
Applicability of five nutritional BMJ Open: first published as 10.1136/bmjopen-2021-057765 on 27 May 2022. Downloaded from
screening tools in Chinese patients
undergoing colorectal cancer surgery: a
cross- sectional study
Bingxin Xie , Yefei Sun, Jian Sun, Tingting Deng, Baodi Jin, Jia Gao
To cite: Xie B, Sun Y, Sun J, ABSTRACT STRENGTHS AND LIMITATIONS OF THIS STUDY
et al. Applicability of five Objectives To identify the most appropriate nutritional
nutritional screening tools in risk screening tool for patients undergoing colorectal ⇒ As far as we know, it was the first time that five
Chinese patients undergoing cancer surgery, five nutritional screening tools, including nutrition screening tools have been used simultane-
colorectal cancer surgery: a the Nutritional Risk Screening 2002 (NRS 2002), ously to evaluate the nutritional risk at admission in
cross- sectional study. BMJ Open Short Form of Mini Nutritional Assessment (MNA- SF), patients with colorectal cancer in China.
2022;12:e057765. doi:10.1136/ Malnutrition Universal Screening Tool (MUST), Malnutrition ⇒ For the first time, we compared the diagnostic val-
bmjopen-2021-057765 ue of five nutritional screening tools simultaneously
Screening Tool (MST) and Nutritional Risk Index (NRI), were
► Prepublication history and employed to evaluate the nutritional risk at admission and based on the occurrence of short-term postopera -
additional supplemental material short- term clinical outcome prediction. tive complications of grade Ⅱ or above.
for this paper are available Design A cross- sectional study. ⇒ Patient selection bias may be present since patients
online. To view these files, Setting A comprehensive affiliated hospital of a university with operable colorectal cancer who decided not to
please visit the journal online in Shenyang, Liaoning Province, China. have surgery and patients receiving cancer treat-
(http://dx.doi.org/10.1136/ ment prior to admission were excluded.
bmjopen-2021-057765). Participants 301 patients diagnosed with colorectal
cancer were continuously recruited to complete the study ⇒ Given that the data originate from a single research
Received 28 September 2021 from October 2020 to May 2021. centre, the universality of the results is limited.
Accepted 12 May 2022 Primary and secondary outcome measures Within 48
hours of hospital admission, five nutritional screening tools
were used to measure the nutritional risk and to determine its burden is expected to increase by 60%
their relationship with postoperative short- term clinical to >2.2 million new cases and >1.1 million http://bmjopen.bmj.com/
outcomes. 1
Results The nutritional risk assesed by the five tools cancer deaths by 2030. Patients with CRC
ranged from 25.2% to 46.2%. Taking the Subject Global often suffer from intestinal dysfunction due
Assessment as the diagnostic standard, MNA- SF had to chronic blood loss, cancer ulceration,
the best consistency (κ=0.570, p<0.001) and MST had surgery and chemoradiotherapy, resulting in
the highest sensitivity (82.61%). Multivariate Logistic decreased digestive and absorption functions,
regression analysis after adjusting confounding factors abnormal nutrition metabolism or intestinal
showed that the NRS 2002 score ≥3 (OR 2.400, 95% CI obstruction. Related studies revealed that
1.043 to 5.522) was an independent risk factor for approximately 40%–65% of patients with CRC on January 7, 2023 by guest. Protected by copyright.
postoperative complications and was the strongest were diagnosed with malnutrition at various
predictor of postoperative complications (area under the 2 3
stages of the disease. Unfortunately, one
curve 0.621, 95% CI 0.549 to 0.692). The scores of NRS 4
study reported that 50% of patients with CRC
2002 (r=0.131, p<0.001), MNA- SF (r=0.115, p<0.05) suffer from weight loss and 20% of patients
and NRI (r=0.187, p<0.05) were poorly correlated with with CRC are diagnosed with malnutrition
the length of stay. There was no correlation between the on admission to a hospital, which suggested
five nutritional screening tools and hospitalisation costs that preoperative malnutrition is common in
© Author(s) (or their (p>0.05).
employer(s)) 2022. Re- use Conclusions Compared with the other four nutritional patients with CRC. Malnutrition can have a
permitted under CC BY- NC. No screening tools, we found that NRS 2002 is the most negative impact on the prognosis of patients
commercial re- use. See rights with CRC by reducing the response and toler-
and permissions. Published by appropriate nutritional screening tool for Chinese patients
BMJ. with colorectal cancer. ance to cancer treatment and increasing
5 6
Gastrointestinal Surgery, The the risk of postoperative complications.
First Hospital of China Medical Another study demonstrated that nutritional
University, Shenyang, Liaoning, INTRODUCTION risk screening may be able to predict mortality
China Colorectal cancer (CRC) is the third most and morbidity following CRC surgery.7 More-
Correspondence to common cancer and the fourth-leading cause over, malnutrition also increases the length
Yefei Sun; yfsun@ cmu. edu. cn of cancer- related deaths worldwide, and of hospital stay, disease burden and impacts
Xie B, et al. BMJ Open 2022;12:e057765. doi:10.1136/bmjopen-2021-057765 1
Open access
8 9 10 11 history, etc) and disease-related data (such as medical BMJ Open: first published as 10.1136/bmjopen-2021-057765 on 27 May 2022. Downloaded from
the quality of life. Even some studies revealed that
the lack of adequate nutritional screening tools was diagnosis, pathological stages, surgical methods, comor-
even considered as one of the reasons for not starting bidities, etc) were collected by trained investigators. Five
nutritional support. Therefore, identifying patients with nutritional screening tools were used to evaluate the
malnutrition or nutritional risk, and those who would nutritional risk of the patients within 48 hours after admis-
benefit from specific nutritional support, are critical in sion. Clinical outcomes (including complications, length
reducing the risk of surgical complications, improving of hospital stay and hospitalisation costs) were observed
clinical outcomes and reducing medical expenses. and recorded within 1 month after surgery. The severity
There are a variety of nutritional screening tools, such of postoperative complications was classified according
to Clavien- Dindo16
as Nutritional Risk Screening 2002 (NRS 2002), Short and the postoperative complications
Form of Mini Nutritional Assessment (MNA- SF), Malnu- recorded in this study were grade II or above. To ensure
trition Universal Screening Tool (MUST), Malnutrition standardisation of the screening, all researchers partici-
Screening Tool (MST), Nutritional Risk Index (NRI) pated in a training session before the study began.
and so on. Most of these nutrition screening tools belong
to universal screening tools, and it has not been deter- Nutrition risk screening tools
17
mined which is the best for patients with CRC. Subjective The NRS 2002 was proposed by the European Society
Global Assessment (SGA) has been tested and validated for Parenteral and Enteral Nutrition in 2002 based on 128
in different clinical environments, and it is usually used clinical randomised trials and recommended as one of
as a criterion for comparing different nutrition screening the primary screening tools for nutritional risk. This tool
12 13 contains a disease severity score, a nutritional impairment
tools and verifying new assessment tools. However,
because SGA is a subjective tool, its application requires score and an age score. The total score ranges from 0 to 7.
trained professionals, and the investigation time of using A total score ≥3 indicates nutritional risk, while a score <3
SGA is 2–3 times longer than that of other tools, which indicates well- nourished, and the nutritional assessment
hinders its use in clinical practice.14 15 Therefore, in this is repeated weekly. Finally, the NRS 2002 score ≥3 was
study, we investigated the prevalence of nutritional risk defined as a nutritional risk in this study.
18
in patients undergoing CRC surgery by using five nutri- The MNA- SF is the short form of MNA, and it is
tional screening tools, to compare whether they are suffi- designed especially for the elderly. It contains six ques-
cient to evaluate the nutritional risk and predict clinical tions selected from MNA. These questions are about
outcomes of patients undergoing CRC surgery. recent weight loss, changes in appetite, mobility, psycho-
logical stress, neuropsychological problems and body
METHODS mass index (BMI). The scores of each question ranged
Study design from 0 to 3, and the total score is 14. According to the
This cross-sectional study was conducted at the First score, the patients are divided into three groups: good http://bmjopen.bmj.com/
Hospital of China Medical University. Patients were nutrition group (12–14 points), malnutrition risk group
initially diagnosed with CRC and underwent surgery (8–11 points) and malnutrition group (≤7 points). In this
between October 2020 and May 2021. Other inclusion study, MNA- SF ≤11 was defined as nutritional risk.
19
criteria were age ≥18 years old, no tumour intervention MUST score is calculated by patient’s BMI, unplanned
such as surgery, chemoradiotherapy and biological immu- weight loss during the previous 3–6 months, and any
notherapy before admission, no serious dysfunction of acute disease which the patient found it almost impos-
important organs such as heart, liver, lung and kidney, sible to eat for more than 5 days. The summed scores were
clear consciousness, and complete case data. The exclu- divided into 3 degrees: 0 is at low risk of malnutrition, on January 7, 2023 by guest. Protected by copyright.
sion criteria were patients with systemic oedema, ascites, score 1 is at moderate risk of malnutrition, and score 2 is
severe diarrhoea or dehydration, patients with other at high risk of malnutrition. In our study, patients with a
consumptive diseases (such as severe liver and kidney score of ≥1 were classified as nutritional risk.
20
disease, hyperthyroidism, pulmonary tuberculosis, severe MST is a simple, valid and reliable nutritional
20
digestive system diseases, etc), patients receiving enteral screening tool designed by Ferguson et al to identify
or parenteral nutrition support, and patients requiring patients at nutrition risk. The MST involves two ques-
a stay in bed strictly during hospitalisation. The study is tions: recent unconscious weight loss and reduced oral
in line with the principles of the Declaration of Helsinki. intake (secondary to poor appetite). According to the
The survey was conducted within the first 48 hours after total score, the patients are divided into two groups:
admission. malnutrition risk (MST score ≥2) and no malnutrition
Patients and public involvement risk (MST score <2). MST proved to have good sensitivity
21 22
Patients or the public were not involved in the design, and specificity in adult inpatients, but relatively few
studies have been conducted in cancer patients.23–25 In
conduct, reporting or dissemination of this study. this study, MST ≥2 was defined as nutritional risk.
26
Data collection NRI is a nutritional risk index based on serum
On admission, demographic data (such as age, sex, albumin concentration and weight loss rate. Its formula is:
payment methods, smoking history, alcohol consumption NRI=1.519 × [serum albumin(gm/dL)]+0.417× (current
2 Xie B, et al. BMJ Open 2022;12:e057765. doi:10.1136/bmjopen-2021-057765
Open access
weight/usual weight). According to the NRI score, a RESULTS BMJ Open: first published as 10.1136/bmjopen-2021-057765 on 27 May 2022. Downloaded from
score ≥100 is well nourished, 97.5–100 is mild malnour- Characteristics of the study population
ished, 83.5–97.5 is moderately malnourished, and <83.5 is In this study, the nutritional risk of 301 patients with CRC
severely malnourished. In this study, the value of NRI<100 was examined within 48 hours of being admitted. The
was defined as a nutritional risk, and the value of NRI average age (mean±SD) was 62.78±10.56 years (range
≥100 was defined as good nutrition. from 24 to 87). A total of 123 cases (40.9%) were women,
and 178 cases (59.1%) were men. Patients with a monthly
Reference standard: SGA income of between 1000 and 3000 Ren Min Bi accounted
Nutritional risk of the participants was measured using for the largest proportion of 60.5%. Married patients had
13 27 the highest proportion, up to 86.1%. 136 patients (45.2%)
the assessment tool SGA including weight, diet,
activity, gastrointestinal symptoms, stress response, muscle were diagnosed with CRC and 165 (54.8%) were diag-
consumption, subcutaneous fat changes and other eight nosed with rectal cancer. Patients who had comorbidities
items. The assessment results for each item are divided accounted for 38.2%. The mean BMI was 23.70±3.11 kg/
2
into three grades A, B and C. When five or more items m (range from 16.98 to 37.11). 27.6% of the patients had
are screened as grade A, it means well-nourished, and grade Ⅱ or above complications within 1 month after the
when more than five items are screened as grade B or C, operation. The mean length of hospitalisation was 19.
it is suggested that it is moderate (or suspected) or severe 20±6. 69 days (range from 9 to 53). The mean hospitalisa-
malnutrition. In this study, we classified the evaluation tion cost was 75472.81±22 048.11 Ren Min Bi (range from
results (B/C) of SGA as nutritional risk and used it as the 16 985.00 to 262111.00). The specific data of the patients
gold standard of nutritional screening for comparative are shown in table 1.
analysis with the other five nutritional screening tools. Evaluation results of five nutritional screening tools
The introduction of the nutritional screening tools Table 2 lists the evaluation results and comparative anal-
used in this study is summarised in online supplemental ysis of five nutritional screening tools. The incidence
table 1. of nutritional risk classified by the NRS 2002, MNA- SF,
Sample size and statistical analysis MUST, MST, NRI and SGA was 41.5%, 46.2%, 39.5%,
28 30.6%, 25.2% and 43.5%, respectively. The tool with the
The minimum sample size was 89 patients with 36.2% highest level of consistency with the results of SGA was
postoperative complications in patients with CRC MNA- SF (κ=0.570, p<0.001), and the tool with the lowest
(p=0.362, α=0.05 and d=0.1). The definitive sample level of consistency were NRI (κ=0.250, p<0.001). Taking
size for this study was 301 cases. Statistical analysis was the SGA as the benchmark, MST has the highest sensi-
conducted using SPSS V.26.0 software for Windows. tivity of 82.61%, with a specificity of 73.68%, a positive
The counting data were described by frequency and predictive value of 58.02% and a negative predictive value http://bmjopen.bmj.com/
percentage. Independent t- test and Pearson’s χ2 test of 90.59%. The NRI showed the lowest sensitivity, 60.00%,
(or Fisher’s exact test) were applied to the appropriate with a specificity of 73.68%, a positive predictive value of
comparison of variables. For continuous variables, we 58.02% and a negative predictive value of 74.12%.
used the Kolmogorov- Smirnov test to verify the normality
of the data distribution. For normally distributed vari- Logistic regression analysis of postoperative complications
ables, mean and SD is reported, non- normal distributions The univariate analysis was performed on the charac-
are described by median and IQR. Mann-Whitney U test teristics of patients and five nutritional screening tools,
was performed for continuous variables and ordered with statistically significant variables (p<0.05) as indepen- on January 7, 2023 by guest. Protected by copyright.
categorical variables that do not follow the normal distri- dent variables, and with the occurrence of postoperative
bution. The Cohen’s kappa coefficient was calculated complications of grade Ⅱ and above as dependent vari-
to determine diagnostic concordance between the five ables, and the multivariate logistic regression model was
nutritional screening tools and the diagnostic criteria for used for further analysis. The results showed that only
the malnutrition of SGA. The sensitivity, specificity, posi- NRS 2002 (≥3 points) (OR 2.400, 95% CI 1.043 to 5.522)
tive predictive value and negative predictive value of each was independently associated with the postoperative
nutritional screening tool were calculated by standard complications of grade Ⅱ or above (table 3).
formula, respectively. Univariate analysis and multivariate
logistic regression analyses were performed to identify the Predictive value of five nutritional screening tools for
risk factors associated with postoperative complications complications
in patients with CRC. Receiver operating characteristic The ROC curve showed that the area under the curve
(ROC) curves of the five screening tools were also used (AUC) of the NRS 2002 and SGA were significantly larger
to evaluate the ability to accurately predict the postoper- than those of other tools, which suggested that NRS 2002
ative complications of grade Ⅱ or above. The correlations and SGA were similar in detecting postoperative compli-
between five nutritional screening tools and length of stay cations and were the strongest predictors of postopera-
(LOS) and cost of hospitalisation were evaluated by the tive complications in patients with CRC (AUC, 0.892
Pearson test. A p<0.05 was deemed statistically significant. and AUC, 0.885, respectively). The MST did not have a
Xie B, et al. BMJ Open 2022;12:e057765. doi:10.1136/bmjopen-2021-057765 3
Open access
Table 1 Characteristics of the study population (p<0.05). In addition, the five nutritional screening tools BMJ Open: first published as 10.1136/bmjopen-2021-057765 on 27 May 2022. Downloaded from
Variable N=301 were not correlated with hospitalisation expenses.
Age (years) 62.78±10.56(24–87)
<60 100 (33.2) DISCUSSION
≥60 201 (66.8) It is well known that patients with digestive system
Gender tumours are often accompanied by different levels of
Male 178 (59.1) nutritional risk or malnutrition, especially for patients
with CRC, most of whom have been in the middle or
Female 123 (40.9) advanced stage of cancer when diagnosed. A simple and
Monthly income (RMB) feasible nutritional screening tool with high sensitivity,
<1000 53 (17.6) strong specificity and accurate prediction of postopera-
1000–3000 129 (42.9) tive clinical outcomes will be an essential choice. In this
3001–5000 85 (28.2) study, when patients were admitted to the hospital for the
5001–10000 29 (9.6) first CRC surgery, the prevalence of nutritional risk for
patients ranged from 25.2% to 46.2%, which is diagnosed
>10 000 5 (1.7) by five different nutritional screening tools. According
Marital status to the SGA criteria, 43.5% of patients with CRC were at
Spinsterhood 1 (0.3) nutritional risk. This result was consistent with the find-
29–31
Married 259 (86.1) ings from other studies in similar patient groups,
Divorced 12 (4.0) which suggested that the results of this study reflect the
Widowed 29 (9.6) nutritional risk of patients with CRC in clinical practice.
However, our study showed that MNA- SF seemed to iden-
Diagnosis tify more patients at nutritional risk than other nutri-
Colon cancer 136 (45.2) tional risk screening tools, which was consistent with the
32 33
Rectal cancer 165 (54.8) results of Baek and Heo and Zhang et al. In their study,
Operation MNA- SF showed high sensitivity compared with nutri-
Laparoscopy 235 (78.1) tional risk screening tools such as NRS 2002 and MUST,
which can also explain this finding in our study. The
Open 66 (21.9) NRI appeared to underestimate the nutritional risk of
Comorbidity patients with CRC when compared with NRS 2002, SGA
Yes 115 (38.2) and PG- SGA in recent similar studies.9 34 A retrospective
34
No 186 (61.8) study of nutritional screening in 80 patients undergoing http://bmjopen.bmj.com/
BMI (mean±SD) (range) 23.70±3.11(16.98–37.11) radical surgery for gastric cancer showed that the prob-
Complication (≥II) ability of nutritional risk measured by NRI at admission
was 31% (the cut- off value of NRI score was 100), which
Yes 83 (27.6) was relatively close to our results. Another prospective
No 218 (72.4) 9
multicentre study showed that the probability of devel-
LOS (days±SD) (range) 19.20±6.69(9- 53) oping nutritional risk in patients with metastatic CRC
Hospitalisation cost 75472.81±22 048.11(16 985.00– measured by NRI was 56% (the cut-off value of NRI score
262111.00) was 97.5), significantly higher than 25.2% in our study. on January 7, 2023 by guest. Protected by copyright.
Values are mean±SD (with ranges in brackets) or n (%), This can be related to the different patient inclusion
respectively. criteria and different cut- off ranges of the NRI score in
BMI, body mass index; LOS, length of stay; RMB, Ren Min Bi. different studies. Second, the characteristics of different
hospitals and different patient populations may also be
the reason for this difference.
predictive value for postoperative complications (AUC, In addition, we found that the MNA-SF ( κ=0.570,
0.497). Furthermore, the NRS 2002 (59.03%) and SGA p<0.001) had the best consistency with the SGA through
(59.04%) presented the highest sensitivity, and the MST the Kappa consistency test. While the target population
35
presented the lowest (30.12%) as shown in figure 1 and in this study was different from Joaquín et al, the same
table 4. conclusion was drawn. The tool of the worst consistency
with SGA was the NRI (κ=0.250, p<0.001), which was
Association of five screening tools with LOS and hospital inverse with the results of a similar previous study (κ=0.564,
15
costs p<0.001). This is a prospective study from Taiwan, China,
Table 5 showed the Pearson correlation coefficients with a small sample size (n=45) and a long history. The
between the scores of the five nutritional screening nutritional risk of patients may have changed dramatically
tools and LOS and hospitalisation cost. LOS was poorly because of regional and temporal differences, which may
correlated with the scores of NRS 2002, MNA- SF and NRI be one of the reasons for the differing results between
4 Xie B, et al. BMJ Open 2022;12:e057765. doi:10.1136/bmjopen-2021-057765
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