Ann Surg Oncol
https://doi.org/10.1245/s10434-018-6342-8
ORIGINAL ARTICLE – GASTROINTESTINAL ONCOLOGY
Impact of Malnutrition After Gastrectomy for Gastric Cancer
on Long-Term Survival
Keiichi Fujiya, MD1, Taiichi Kawamura, MD, PhD1, Katsuhiro Omae, BS2, Rie Makuuchi, MD, PhD1,
Tomoyuki Irino, MD, PhD1, Masanori Tokunaga, MD1, Yutaka Tanizawa, MD, PhD1, Etsuro Bando, MD, PhD1,
and Masanori Terashima, MD, PhD, FACS1
1
Division of Gastric Surgery, Shizuoka Cancer Center, Shizuoka, Japan; 2Clinical Research Promotion Unit, Shizuoka
Cancer Center, Shizuoka, Japan
ABSTRACT
Background. Preoperative malnutrition can worsen mor-
bidity and mortality; however, the role of postgastrectomy
nutritional status remains unclear. Our purpose was to
clarify whether malnutrition after gastrectomy could pre-
dict long-term survival.
Methods. Patients with pathological stage I, II, and III
gastric cancer who underwent gastrectomy between 2002
and 2013 were included. The nutrition risk index (NRI)
was evaluated before and at 1, 3, 6 and 12 months after
gastrectomy. The patients were divided into normal
(NRI [ 97.5) or malnutrition (NRI B 97.5) groups, and we
compared the correlations of clinicopathological charac-
teristics, surgical treatment, and overall survival between
the two groups.
Results. Among the 760 participants, patients in the mal-
nutrition group were significantly older and had higher
incidences of comorbidity and advanced cancer than the
patients in the normal group. Multivariate analysis showed
that overall survival was poorer in the malnutrition group
before gastrectomy [hazard ratio (HR) 1.68] and at
1 month (HR 1.77), 3 months (HR 2.18), 6 months (HR
1.81) and 12 months (HR 2.17) after gastrectomy (all
p \ 0.01). Malnutrition at 1 and 3 months after
Electronic supplementary material The online version of this
article (https://doi.org/10.1245/s10434-018-6342-8) contains supple-
mentary material, which is available to authorized users.
Ó Society of Surgical Oncology 2018
First Received: 21 August 2017
M. Terashima, MD, PhD, FACS
e-mail: m.terashima@scchr.jp
gastrectomy was significantly associated with poor cause-
specific survival. Total gastrectomy, preoperative malnu-
trition, older age, and adjuvant chemotherapy were
independent risk factors of postoperative malnutrition at
12 months postgastrectomy.
Conclusions. Malnutrition before gastrectomy and at 1, 3,
6 and 12 months after gastrectomy significantly and
adversely affects overall survival. Nutritional interventions
to lessen the impact of postoperative malnutrition offer
hope for prolonged survival.
Keywords Albumin
Body weight
Elderly
Gastric cancer is the fifth most common malignancy
worldwide.1 Although the ability of gastrectomy to effec-
tively cure gastric cancer has improved, postoperative
problems related to quality of life and functional and
nutritional status persist.2,3 Nutritional status deteriorates
after surgery, because surgery, especially gastrectomy,
often leads to decreased food intake and reduced body
weight.2 These serious changes in nutritional status are
associated with marked deterioration in quality of life.4–6
Quick recovery from surgical stress and maintaining good
nutritional status are important to a healthy and active life.7
Many studies have reported that preoperative malnutri-
tion is correlated with surgical morbidity.8,9 Nutritional
status reflects the ability to resist infection and heal tissues,
and perioperative malnutrition can attenuate the systemic
immune system.10 Moreover, preoperative poor nutritional
status is related to increased risk of both cancer recurrence
and noncancer death.11–13
Relieving preoperative malnutrition is difficult in the
short term under advanced cancers. Many studies have
reported the inconsistent efficacy of preoperative nutri-
tional intervention.14,15 After surgery, however, long-term

nutritional intervention can be performed under cancer-free
conditions, highlighting the importance of postoperative
nutritional status evaluation.
It is unknown how secondary malnutrition status caused
by gastrectomy affects human physiology. Postgastrectomy
malnutrition may increase the risk of death or cancer
recurrence; however, there is no solid evidence that mal-
nutrition after gastrectomy associates with poor
survival.16,17 After gastrectomy for gastric cancer, appetite
and food intake decline, especially during the first
3 months after surgery; nutritional status takes up to 1 year
to recover.18 Nutritional status within 1 year after gas-
trectomy varies; therefore, appropriate time points for
detecting postgastrectomy malnutrition should be investi-
gated, assuming that postgastrectomy malnutrition is linked
to poor survival.
We evaluated the nutritional status of patients who
received gastrectomy for gastric cancer using the nutrition
risk index (NRI), before gastrectomy and at 1, 3, 6 and
12 months after gastrectomy, to clarify whether post-gas-
trectomy nutritional status is associated with long-term
survival.19
METHODS
Patients
We selected patients from a prospectively maintained
database. All patients were required to have undergone
elective and curative gastric resection (R0 surgery) for stage
I–III primary gastric cancer at the Shizuoka Cancer Center
between September 2002 and June 2013. We included 760
patients whose body weight and serum albumin were mea-
sured preoperatively, were followed up for more than
12 months after gastrectomy, did not have any other type of
cancer, and did not receive chemotherapy, radiation, or any
other treatment for gastric cancer before surgery. Data col-
lection and analysis were approved by the institutional
review board of the Shizuoka Cancer Center (Approval no.
28-J113-28-1-3). Gastrectomy and lymph node dissection
were performed according to the Japanese gastric cancer
treatment guidelines.20 Pathological tumor depth, nodal
status, and surgical curability were determined according to
the Union for International Cancer Control (UICC) TNM
Classification of Malignant Tumors criteria.21 Histological
type was classified according to the Japanese Gastric Cancer
Association classification of gastric carcinoma.22
Nutritional Assessment
Nutritional assessment was performed using NRI before
gastrectomy and at 1, 3, 6, and 12 months after gastrectomy.
K. Fujiya et al.
Body weight and serum albumin were measured at each
assessment, and NRI was calculated using the following
formula: NRI = (1.519 9 serum albumin, g/L) ? (41.7 9
current weight/usual weight).19 Malnutrition was defined by
an NRI score B 97.5 according to several past reports.23,24
Patients with an NRI score [ 97.5 or B 97.5 were catego-
rized into the normal and malnutrition groups, respectively.
Usual body weight was defined as the patient’s stable main-
tained body weight before gastrectomy, which was assessed
by their interview.
Comparison Between the Normal Nutrition
and Malnutrition Groups
Preoperative clinical characteristics, pathological find-
ings, and short-term outcomes were evaluated and
compared between the normal and malnutrition groups
based on the NRI cutoff point. Grouping was performed
using the NRI at five time points as follows: before gas-
trectomy and at 1, 3, 6 and 12 months after gastrectomy.
Patients who died or had gastric cancer recurrence at by the
time of NRI assessment were excluded (Fig. 1). Overall
survival (OS) and cause-specific survival (CSS) were
compared between the groups. OS was evaluated as the
time taken to death or censored day (last follow-up day or
last follow-up day before being lost to follow-up) from
each time point when NRI was measured. CSS was defined
as death from gastric cancer, and censor of CSS was
defined as death from any cause other than gastric cancer,
last follow-up day, or last follow-up day before being lost
to follow-up.
760 patients before gastrectomy
760 patients at 1 month after gastrectomy
11 patients died
1 patient had recurrence of gastric cancer
748 patients at 3 months after gastrectomy
3 patients died
745 patients at 6 months after gastrectomy
23 patients died
1 patient had recurrence of gastric cancer
721 patients at 12 months after gastrectomy
FIG. 1 Flowchart of enrolled patients before surgery and at 1, 3, 6
and 12 months after gastrectomy
Malnutrition After Gastrectomy and Survival
Statistical Analysis
All continuous variables are presented as the median and
25th and 75th percentiles. Statistical analyses were per-
formed using Fisher’s exact test and the Mann–Whitney
U test. Survival data were analyzed using the Kaplan–
Meier method, and the log-rank test was used to compare
the two groups. Independent prognostic factors were
identified by univariate and multivariate analyses using the
Cox proportional hazards model. The factors contributing
to malnutrition at 12 months after gastrectomy were iden-
tified by multivariate logistic regression analysis. A two-
sided p value \ 0.05 was considered statistically signifi-
cant. All statistical analyses were conducted using R
Statistics version 3.2.0 (R Foundation, Vienna, Austria).
RESULTS
Patient Characteristics
Body weight and serum albumin were initially measured
in 760 patients before gastrectomy. Twelve patients died or
had recurrence of gastric cancer within 3 months after
gastrectomy, reducing the study group to 748 patients.
Additionally, 3 and 24 patients died or had recurrence
within 6 and 12 months after gastrectomy, respectively.
This further reduced the study group to 745 patients at
6 months and 721 patients at 12 months after gastrectomy.
The median total follow-up period was 59.6 months. Fig-
ure 2 summarizes the changes in NRI before and after
gastrectomy. The median preoperative NRI was 105.9,
which was the highest of any measurement time point. The
median NRI decreased to 99.4 by 3 months after gastrec-
tomy but then gradually recovered to 100.9 by 12 months.
110
105
NRI
100
95
90
0 2 4 6 8 10
Month
FIG. 2 Changes in NRI over time from before to after gastrectomy.
The points indicate the median. The I bar indicates the 25th and 75th
percentiles. The dotted line indicates the NRI of 97.5. NRI nutrition
risk index
The participant characteristics according to nutritional
status before gastrectomy and at 12 months after gastrec-
tomy are shown in Table 1. Before gastrectomy, 661
patients (87.0%) were considered to have a normal nutri-
tional status, whereas 99 (13.0%) were considered
malnourished. However, by 12 months after gastrectomy,
the proportion of patients had changed to 498 (69.1%) and
223 (30.9%), respectively. Patients in the malnutrition
group were significantly older, with a higher proportion of
comorbidity and more advanced cancer stage than those in
the normal group, both before and after gastrectomy. The
rate of postoperative complications of Clavien–Dindo
grade II or higher was 28.1% in the preoperative normal
group and 40.4% in the preoperative malnutrition group.
Malnutrition at 1, 3, 6 and 12 months after gastrectomy
was found in 65.9, 56.0, 53.5 and 45.9% of patients with
postoperative complications, respectively.
Comparison of Long-Term Survival Between Groups
Before Gastrectomy
The Kaplan–Meier survival curves shows significantly
poor OS [hazard ratio (HR) 2.65, p \ 0.001] and CSS (HR
2.07, p = 0.008) in the patients who were malnourished
before gastrectomy (Supplementary Fig. 1). Multivariate
analysis showed preoperative malnutrition as an indepen-
dent risk factor for OS (HR 1.68, p = 0.009) but not CSS
(HR 1.21, p = 0.496; Table 2).
Comparison of Long-Term Survival between Groups
after Gastrectomy
Figure 3 presents the Kaplan–Meier survival curves
according to nutritional status at 1, 3, 6 and 12 months after
gastrectomy, showing significantly poorer OS in the mal-
nutrition group than in the normal group. Multivariate
analysis showed that malnutrition at each time point after
gastrectomy was significantly associated with poor OS
(Table 2). Age, comorbidity, and pathological stage were
also independent prognostic factors for OS at 12 months
after gastrectomy (Supplementary Table 1).
Figure 4 demonstrates CSS according to nutritional
status at 1, 3, 6, and 12 months after gastrectomy. Mal-
nutrition at each time point after gastrectomy was
significantly related to poor CSS. Multivariate analysis
showed that malnutrition at 1 and 3 months after gastrec-
tomy was significantly associated with poor CSS; however,
12
no significant association was found between malnutrition
and CSS at 6 and 12 months (Table 2).
Of the 632 patients in the normal nutrition group before
gastrectomy who did not die or have a recurrence within
12 months after gastrectomy, 175 patients (27.7%) devel-
oped malnutrition at 12 months. Among patients in the
 K. Fujiya et al.

TABLE 1 Comparison of preoperative clinical characteristics and surgical and pathological findings between the normal and malnutrition
groups before gastrectomy and at 12 months after gastrectomy
Before gastrectomy 12 months after gastrectomy
Normal Malnutrition p Normal Malnutrition p
(n = 661) (n = 99) (n = 498) (n = 223)

Age (years) \ 0.001 \ 0.001

Median 66 73 65 71
25th and 75th percentiles 59–73 68–77 58–71 64–76
Sex 0.165 0.49
Male 447 74 335 156
Female 214 25 163 67
ECOG performance status 0.031 0.683
0–1 655 95 4 3
2–4 6 4 494 220
Comorbidity 0.023 0.019
338 63 249 133
Surgical procedure \ 0.001
Distal gastrectomy – – 376 107
Proximal gastrectomy – – 18 11
Total gastrectomy – – 104 105
Histological type 0.334 0.809
Differentiated 319 53 246 113
Undifferentiated 342 46 252 110
Primary tumor \ 0.001 0.001
T1 332 25 266 85
T2 97 4 68 31
T3 135 32 95 56
T4 97 38 69 51
Regional lymph nodes \ 0.001 \ 0.001
N0 368 33 298 95
N1 132 20 89 57
N2 72 20 52 31
N3 89 26 59 40
Pathological stage \ 0.001 \ 0.001
I 345 25 281 85
II 177 24 119 69
III 139 50 98 69
Adjuvant chemotherapy \ 0.001
– – 178 112
ECOG Eastern cooperative oncology group

preoperative normal nutrition group, malnutrition at
12 months after gastrectomy was an independent prog-
nostic factor for OS (HR 2.11, p = 0.002), but not CSS
(HR 1.37, p = 0.350).
Patients with postoperative complications showed a
significantly poorer OS than those without postoperative
complications (Supplementary Table 2). Among patients
with and without postoperative complications, the malnu-
trition group, both before gastrectomy and after
gastrectomy had a significantly poorer OS than that in the
normal group.
Cause of Death
Of the 59 patients in the malnutrition group at
12 months after gastrectomy (n = 223) who died, the
causes of death were gastric cancer (n = 25), pneumonia
(n = 10), other cancer (n = 5), and cerebrovascular
Malnutrition After Gastrectomy and Survival

TABLE 2 Summary of relationship between long-term survival and malnutrition before gastrectomy and at each time point after gastrectomy from
multivariate analyses
95% CI
Hazard ratio Lower Upper p

Overall survival
Before gastrectomy
Malnutrition 1.68 1.14 2.48 0.009
Age [ 75 years 2.37 1.83 3.06 \ 0.001
Undifferentiated type 1.50 1.06 2.13 0.023
Stage II/III 2.82 1.9 4.18 \ 0.001
1 month after gastrectomy
Malnutrition 1.77 1.22 2.56 0.002
Age [ 75 years 2.26 1.74 2.93 \ 0.001
Undifferentiated type 1.56 1.09 2.22 0.015
Stage II/III 2.68 1.79 3.99 \ 0.001
3 months after gastrectomy
Malnutrition 2.18 1.49 3.21 \ 0.001
Age [ 75 years 2.03 1.54 2.67 \ 0.001
Stage II/III 2.37 1.57 3.57 \ 0.001
6 months after gastrectomy
Malnutrition 1.81 1.23 2.65 0.002
Age [ 75 years 2.10 1.59 2.78 \ 0.001
Stage II/III 2.38 1.57 3.6 0.004
12 months after gastrectomy
Malnutrition 2.17 1.43 3.29 \ 0.001
Age [ 75 years 2.04 1.48 2.83 \ 0.001
Comorbidity 1.91 1.25 2.93 0.003
Stage II/III 2.29 1.30 4.01 0.004
Cause-specific survival
Before gastrectomy
Malnutrition 1.21 0.69 2.13 0.496
Age [ 75 years 2.10 1.44 3.05 \ 0.001
Undifferentiated type 1.65 1.01 2.7 0.045
Stage II/III 24.56 7.7 78.26 \ 0.001
1 month after gastrectomy
Malnutrition 1.73 1.06 2.83 0.030
Age [ 75 years 1.92 1.32 2.79 \ 0.001
Undifferentiated type 1.74 1.06 2.87 0.030
Stage II/III 22.10 6.9 70.82 0.004
3 months after gastrectomy
Malnutrition 1.98 1.20 3.28 0.008
Age [ 75 years 1.74 1.16 2.59 0.007
Stage II/III 20.69 6.45 66.37 0.004
6 months after gastrectomy
Malnutrition 1.28 0.77 2.13 0.334
Age [ 75 years 1.81 1.20 2.74 0.004
Stage II/III 21.55 6.7 69.25 \ 0.001
12 months after gastrectomy
Malnutrition 1.37 0.77 2.44 0.289
Age [ 75 years 1.94 1.17 3.24 0.011
Stage II/III 27.70 6.17 124.41 \ 0.001
 K. Fujiya et al.

1.0
FIG. 3 Overall survival curves
for patients in the normal and
malnutrition groups after

0.8
gastrectomy. Overall survival

Overall survival
according to nutrition status a at

0.6
1 month after gastrectomy (HR
2.62, 95% CI 1.87–3.67;

0.4
p \ 0.001), b at 3 months after
gastrectomy (HR 3.18, 95% CI

0.2
2.23–4.54; p \ 0.001), c at
6 months after gastrectomy (HR (a)

0.0
2.73, 95% CI 1.91–3.89;
p \ 0.001) and d at 12 months 0 1 2 3 4 5 6 7 8 9 10
after gastrectomy (HR 2.98, N at risk Time to Event (Years)
95% CI 2.02–4.39; p \ 0.001) Normal 473 465 455 406 313 139 69 28 15 7 6
Malnutrition 287 272 254 218 175 100 49 29 17 10 5

1.0
0.8
Overall survival
0.6
0.4
0.2

(b)
0.0

0 1 2 3 4 5 6 7 8 9 10
N at risk
Time to Event (Years)
Normal 473 468 456 408 315 129 61 29 12 8 6
Malnutrition 275 262 244 201 156 78 42 22 13 8 5
1.0
0.8
Overall survival
0.6
0.4
0.2

(c)
0.0

0 1 2 3 4 5 6 7 8 9 10
N at risk Time to Event (Years)
Normal 477 472 454 384 290 98 45 24 10 7 6
Malnutrition 268 252 233 194 160 68 42 22 13 9 5
1.0
0.8
Overall survival
0.6
0.4
0.2

(d)
0.0

0 1 2 3 4 5 6 7 8 9 10
N at risk Time to Event (Years)
Normal 498 492 464 363 228 82 45 20 10 8 8
Malnutrition 223 211 187 146 106 53 42 13 8 4 3
Malnutrition After Gastrectomy and Survival

1.0
FIG. 4 Cause-specific survival
curves for patients in the normal

Cause-specific survival
and malnutrition groups after

0.8
gastrectomy. Cause-specific
survival according to nutrition

0.6
status a at 1 month after
gastrectomy (HR 2.59, 95% CI

0.4
1.64–4.09; p \ 0.001), b at
3 months after gastrectomy (HR

0.2
2.95, 95% CI 1.84–4.74;
p \ 0.001), c at 6 months after (a)

0.0
gastrectomy (HR 2.08, 95% CI
0 1 2 3 4 5 6 7 8 9 10
1.30–3.33; p = 0.002) and d at N at risk Time to Event (Years)
12 months after gastrectomy Normal 473 465 455 406 313 139 69 28 15 7 6
(HR 2.06, 95% CI 1.20–3.54; Malnutrition 287 272 254 218 175 100 49 29 17 10 5
p = 0.009)

1.0
Cause-specific survival
0.8
0.6
0.4
0.2
(b)
0.0

0 1 2 3 4 5 6 7 8 9 10
Time to Event (Years)
N at risk
Normal 473 468 456 408 315 129 61 29 12 8 6
Malnutrition 275 262 244 201 156 78 42 22 13 8 5
1.0
0.8
Cause-specific survival
0.6
0.4
0.2

(c)
0.0

0 1 2 3 4 5 6 7 8 9 10
N at risk
Time to Event (Years)
Normal 477 472 454 384 290 98 45 24 10 7 6
Malnutrition 268 252 233 194 160 68 42 22 13 9 5
1.0
Cause-specific survival
0.8
0.6
0.4
0.2

(d)
0.0

0 1 2 3 4 5 6 7 8 9 10
N at risk
Time to Event (Years)
Normal 498 492 464 363 228 82 36 20 10 8 8
Malnutrition 223 211 187 146 106 53 26 13 8 4 3

disorder (n = 5). Of the 45 patients in the normal group at
12 months after gastrectomy (n = 498) who died, the
causes of death were gastric cancer (n = 28), pneumonia
(n = 2), other cancer (n = 4), and cerebrovascular disor-
der (n = 2). There were significant differences in the
numbers of deaths due to gastric cancer, pneumonia, and
cerebrovascular disorder between the two groups.
Predictive Factors for Malnutrition at 12 Months
after Gastrectomy
We performed multivariate logistic regression analysis
for risk factors contributing to the occurrence of malnu-
trition at 12 months after gastrectomy (Supplementary
Table 3). Total gastrectomy (HR 3.16), preoperative mal-
nutrition (HR 2.23), older age (HR 2.06), and adjuvant
chemotherapy (HR 1.93) were independent risk factors for
malnutrition. Among the preoperative normal nutrition
group, independent risk factors for malnutrition at
12 months after gastrectomy were total gastrectomy (HR
3.27), older age (HR 2.19), and adjuvant chemotherapy
(HR 2.70).
DISCUSSION
We showed that preoperative and post-gastrectomy
malnutrition at 1, 3, 6 and 12 months after gastrectomy
were associated with poor long-term survival. Postopera-
tively, gastrectomy is closely associated with reduced food
intake and 5–15% body weight loss.25 Patients with mild-
to-moderate malnutrition and a stable general condition
may be followed up without special nutritional interven-
tion. However, our results indicate that special attention to
postoperative malnutrition is warranted, because short- to
medium-term postoperative malnutrition may cause sys-
temic immune system attenuation, leading to increased
cancer recurrence, infectious disease, and death.10,26
Malnutrition causes immune dysfunction, including
infections, enteropathy, and inflammation.10 Nutrient defi-
ciencies influence T-cell metabolism via cytoplasmic
nutrient sensors, including AMP-activated protein kinase,
which regulates cell survival, and mammalian target of
rapamycin serine/threonine kinase complex.27,28 Environ-
mental enteric dysfunction in malnourished individuals
also affects the immune system.29 Several mechanisms
have been proposed, including (a) impairment of the barrier
by intestinal villous architecture to prevent pathogen
translocation into tissues, (b) development of altered
nutrient-sensing pathways, such as aryl hydrocarbon
receptor and retinoic acid receptor signaling in gut-asso-
ciated lymphoid tissue, and (c) mechanical gut tissue
damage releasing host-derived immune-activating damage-
K. Fujiya et al.
associated molecular patterns and upregulating epithelial
repair.29–31
Postoperative nutritional status is decreased at 1 month
after gastrectomy and can take up to 12 months to
recover.18 Malnutrition at 1 month after gastrectomy is
inevitable because of acute surgical stress and abrupt
changes to dietary habits and lifestyle, after which the
general condition and nutritional status gradually recover
to normal. However, around one-third of patients who
undergo gastrectomy suffer from malnutrition until
12 months postoperatively. Persistent postoperative mal-
nutrition is frequently found in patients who undergo total
gastrectomy and those who are older, and these could be
candidates for aggressive nutritional intervention. How-
ever, the effects of perioperative nutritional intervention on
the prevention of body weight loss and muscular weakness
are unclear.14,15,32,33 Previous reports have found a rela-
tionship between preoperative malnutrition and poor
survival, which is consistent with our results obtained with
any patients and suitable nutrition assessment method.12,34
The relationship between postoperative nutritional status
and long-term survival remains unclear. Previous studies
reported that body weight loss at 6 and 12 months after
gastrectomy is predictive of poor long-term survival.16,17
However, these reports did not adjust for covariates
affecting nutritional status and used body weight only as a
measure of nutritional assessment. Malnutrition has con-
founding negative survival factors, such as elderly status,
comorbidity, and advanced malignant stage.25,35,36 There-
fore, we conducted multivariate analyses for survival
outcomes at each time point using NRI. Unlike previous
studies, we excluded patients who died or had gastric
cancer recurrence by the time of nutritional assessment to
evaluate accurately postgastrectomy malnutrition.
We revealed relationships between poor survival and
malnutrition before and at 1, 3, 6 and 12 months after
gastrectomy. Malnutrition at 1 and 3 months was related to
gastric cancer-related death. Previous studies have reported
that patients are uniquely susceptible to metastases for-
mation in the immediate postoperative period.26,37,38
Surgical stress impairs natural killer (NK) cell activity,
which are cytotoxic lymphocytes of the innate immune
system involved in controlling cancer growth and metas-
tases.39,40 Low NK activity perioperatively is associated
with a higher rate of cancer recurrence and mortality.41,42
Therefore, immune dysfunction due to surgical stress, with
the added challenge of malnutrition, may increase the risk
of cancer recurrence in the early postoperative period.
Conversely, malnutrition at 12 months after gastrectomy is
associated with noncancer death, especially from pneu-
monia. Gastrectomy patients are at high risk of sarcopenia,
which contributes to impaired respiratory function and
occurrence of pneumonia.43 Among patients with
Malnutrition After Gastrectomy and Survival
preoperative normal nutrition, as well as all patients,
postoperative malnutrition was an independent risk factor
for survival.
In this study, patients with preoperative malnutrition
showed high rates of postoperative complications, as in
previous reports.44,45 Postoperative complications have
been linked to poor survival.46 To eliminate the adverse
survival effects of postoperative complications, we com-
pared survival between the normal and malnutrition groups
among patients with and without postoperative complica-
tions and revealed that malnutrition was a risk factor for
survival irrespective of postoperative complications.
NRI is widely used as a beneficial perioperative nutri-
tional screening tool for postoperative complications,
length of hospital stay, or survival.44,45,47,48 A recent study
has shown the utility of NRI for nutritional status for
5 years after curative gastrectomy for gastric cancer.49
Outpatients can routinely measure nutrition status, because
NRI is a simple and objective indicator that combines body
weight loss with serum albumin level that can be measured
at every outpatient visit and does not require computed
tomography or bioelectrical impedance analyzer.50,51
Based on regular follow-up of nutrition status using NRI,
indication for nutritional intervention or its suitable timing
may be decided in future studies. Reduction in serum
albumin is related to metabolic conditions, infection, and
inflammation.52 However, serum albumin or BMI alone
underestimate the prevalence of malnutrition.53 Therefore,
we used NRI, which combines serum albumin and body
weight change. NRI also has shown correlations with
inflammatory and metabolic markers.54
This study has some limitations. First, it was retro-
spective and single-centered and, thus, was susceptible to
the inherent problems of such design features. Second, we
could not completely adjust for the negative survival
impact of patient backgrounds in the malnutrition group.
Third, we excluded patients with gastric cancer recurrence,
because cancer environment may evoke malnutrition.
However, there is a possibility that potential micrometas-
tasis causes malnutrition and is linked to a poor survival
effect of malnutrition.
CONCLUSIONS
Malnutrition before gastrectomy and at 1, 3, 6 and
12 months after gastrectomy are independent prognostic
factors. Patients who receive total gastrectomy and adju-
vant chemotherapy and the elderly are at high risk of
postoperative malnutrition. In the future, suitable nutri-
tional interventions should be assessed for their potential to
prolong survival in gastric cancer patients undergoing
gastrectomy.
ACKNOWLEDGEMENTS This research was supported in part
by the National Cancer Center Research and Development Fund (29-
A-3).
DISCLOSURES The authors declare that they have no conflicts of
interest.
ETHICAL STANDARDS All procedures followed were in
accordance with the ethical standards of the responsible committee on
human experimentation (institutional and national) and with the
Helsinki Declaration of 1964 and later versions.
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