Nutrition and Cancer

ISSN: 0163-5581 (Print) 1532-7914 (Online) Journal homepage: http://www.tandfonline.com/loi/hnuc20

Associations Between Nutritional Parameters and

Clinicopathologic Factors in Patients with Gastric
Cancer: A Comprehensive Study

Adam Brewczyński, Beata Jabłońska & Krzysztof Pawlicki

To cite this article: Adam Brewczyński, Beata Jabłońska & Krzysztof Pawlicki (2017): Associations
Between Nutritional Parameters and Clinicopathologic Factors in Patients with Gastric Cancer: A
Comprehensive Study, Nutrition and Cancer, DOI: 10.1080/01635581.2017.1324993

To link to this article: http://dx.doi.org/10.1080/01635581.2017.1324993

Published online: 01 Jun 2017.

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NUTRITION AND CANCER
https://doi.org/10.1080/01635581.2017.1324993

Associations Between Nutritional Parameters and Clinicopathologic Factors in

Patients with Gastric Cancer: A Comprehensive Study

skia, Beata Jab»on
Adam Brewczyn
skab, and Krzysztof Pawlickic
a
Department of Radiotherapy Center of Oncology Maria Sk»odowska-Curie Memorial Cancer Center and Institute of Oncology, Gliwice, Poland;
b
Department of Digestive Tract Surgery, Medical University of Silesia, Katowice, Poland; cDepartment of Biophysics, Medical University of Silesia,
Katowice, Poland

ABSTRACT ARTICLE HISTORY

The aim of this study was to assess and analyze the nutritional status of gastric cancer (GC) patients. Received 27 July 2016
The analysis included 207 patients with GC treated in a large center of oncology. Patients were Accepted 5 April 2017
divided into two groups according to the cutoff value of the mean prognostic nutritional index
(PNI): those with a PNI < 52.78 and those with a PNI
52.78. The higher PNI was associated with
lower age and higher total protein and hemoglobin levels (P < 0.01). The total lymphocyte count
(P D 0.02), albumin, total protein and PNI (P < 0.01) were significantly higher in stable-weight
patients and lower in the group with weight loss > 10% (P D 0.000031). Body mass index (BMI) after
disease recognition, albumin and total protein (0.003) levels, total lymphocyte count, and PNI were
significantly lower in patients with nutritional risk. Significantly lower BMI before disease and BMI
after disease recognition were noted in smoking patients. Significantly higher total lymphocyte
count was observed in smoking patients (P < 0.01). Significantly lower PNI was noted in tumors
with lymph node metastasis (NC). G3 tumors were associated with the lowest total lymphocyte
count (P D 0.01). Assessment of nutritional status using PNI calculation should be the standard
management of patients with GC before treatment.

Introduction
Malnutrition is a common problem in cancer patients.
According to the literature, 30–50% of hospitalized
patients are malnourished. Malnutrition is reported in
about 84% of the cancer patients. Malnutrition negatively
influences patients’ prognosis and quality of life. About
20% of cancer patients die due to malnutrition, not
because of the cancer. In gastric cancer (GC) patients,
malnutrition is caused by insufficient food intake due to
lack of appetite, dysphagia, dyspeptic symptoms (epigas-
tric pain, nausea, vomiting), and impaired digestion and
absorption. It is also secondary to oncologic treatment
(surgery, chemotherapy, and radiotherapy) as well as hos-
pitalization of the patients. Proper assessment of nutri-
tional status allows the appropriate nutritional therapy in
order to support care of GC patients. To assess the nutri-
tional status both objective and subjective criteria are
used, including different, anthropometric, clinical, and
biochemical parameters (1,2).
The aim of the study was assessment and analysis of
nutritional status of patients with GC using selected
anthropometric, clinical, and biochemical parameters.
Methods
Patients
The analysis included 207 patients with GC treated in the
Center of Oncology (Gliwice, Poland). Assessment of
nutritional status was performed in patients at the time of
tumor diagnosis and histological confirmation prior to
treatment. There were 142 (68.6%) men and 65 (31.4%)
women with a mean age of 57.80 § 9.22 (25–74) yr in
the analyzed group. Inclusion criteria: primary GC, age
>18 yr, locally advanced cancer without distant metasta-
ses. Exclusion criteria: disseminated cancer, cancer
recurrence, incomplete demographic and clinical data.
Study Design
All patients were asked about deterioration of nutritional
status, body weight before disease and before treatment,
loss of body weight and food intake since the onset of
disease. Information on comorbidities (arterial hyperten-
sion, ischemic heart disease, type 1 and 2 diabetes
mellitus) and smoking (including the amount and dura-
tion of smoking and smoking cessation after diagnosis)

CONTACT Adam Brewczy
nski adam.brewczynski@io.gliwice.pl Department of Radiotherapy Center of Oncology Maria Sk»odowska-Curie Memorial
Cancer Center and Institute of Oncology, Gliwice Branch, Wybrze_ze Armii Krajowej 15 Street, 44-101 Gliwice, Poland.
© 2017 Taylor & Francis Group, LLC
2

A. BREWCZYNSKI ET AL.
was collected. The height and weight were measured, and
laboratory blood tests were performed. The selected
blood count parameters (hemoglobin and total lympho-
cyte count) and biochemical parameters (serum total
protein and albumin) were analyzed. The body mass
index (BMI) and weight loss during the course of the dis-
ease were calculated. The patients were divided into two
groups according to their BMI: into malnourished
patients (BMI < 18.5 kg/m2) and well-nourished patients
(BMI
18.5 kg/m2) (3). The nutritional risk according to
Nutritional Risk Screening 2002 (NRS 2002) was assessed
by the European Society of Parenteral and Enteral Nutri-
tion (4,5) . The Onodera’s nutritional prognostic index
(PNI) was calculated based on the serum albumin con-
centration and total lymphocyte count in the peripheral
blood by the formula: 10 £ level of albumin (g/dl) C
0.005 £ total lymphocyte count (/mm3) (6). The patients
were divided into two groups according to the cutoff
value of the mean PNI (52.78). The mean value of the
PNI (52.78) among the study population was set as the
border value, to divide high and low-PNI groups, in
order to perform statistical comparisons of clinicopatho-
logical findings between both groups. Clinicopathological
factors were compared between the two groups.
The tumor parameters such as general location (1.
cardia and the all stomach and 2. body or pylorus), and
detailed location (1. cardia 2. body 3. pylorus 4. whole
stomach 5. cardia and body 6. body and pylorus) were
assessed. The tumors were classified according to the
standard TNM system and histological type and grade.
The stage of GC was classified according to the 7th edi-
tion of the American Joint Committee on Cancer TNM
classification system: primary tumor depth (T), regional
lymph node metastasis (N), distant metastasis (M) (7).
T1-3 tumors invaded lamina propria, muscularis muco-
sae, or submucosa (T1), muscularis propria (T2), and
penetrated subserosal connective tissue without invasion
of visceral peritoneum or adjacent structures (T3). T4
tumors invaded serosa (visceral peritoneum) or adjacent
structures. N0 stages were without regional lymph node
metastasis, and NC (N1–N3) stages were with metastasis
in one or more regional lymph nodes. Tumor depth and
lymph node invasion were performed on the basis of
computed tomography of the abdomen.
Statistical Analysis
A statistical analysis of correlations between different
nutritional parameters (NRS 2002, BMI, total protein,
albumin and hemoglobin levels, total lymphocyte count
in the peripheral blood, PNI) and selected clinicopatho-
logic factors (age, gender, tumor location, histological
grade and clinical stage according to TNM classification)
was performed. The Kendall’s tau non-parametric test
was used to assess statistical correlations. Correlation
strength (as a correlation coefficient) and significance
(as a P value) were described. The categorical variables
were presented as numbers and percentages. Continuous
variables with normal distribution were expressed as the
means and standard deviations. A strength coefficient
(T) was calculated. The following interpretation of the
strength of correlation results was used: 0.00–0.30
(weak correlation), 0.31–0.50 (moderate correlation),
0.51–0.80 (strong correlation), and 0.81–1.00 (very
strong correlation).
Between-group (according to gender, weight loss,
BMI, NRS 2002, tumor location, clinical stage and histo-
pathology) comparisons were performed by one-way
analysis of variance for continuous variables (age, BMI,
total lymphocyte count, albumin, total protein, hemoglo-
bin levels, and PNI). Also, the Mann-Whitney U test was
used to evaluate associations between parameters of
nutritional status and selected clinicopathological varia-
bles. A P value of less than 0.05 was considered to be
statistically significant. The statistical analyses were per-
formed using the StatisticaÒ software program, version
12.0 (StatSoft).
Results
The general clinical characteristics of 207 patients are
presented in Table 1. The mean weight recorded before
treatment was 72.77 § 14.50 (45–115) kg. The mean
weight loss was 6.57 § 6.90 (¡16–35) kg and it was
noted within 3.46 § 4.65 (0–36) mo. BMI values before
disease and after disease recognition but before treat-
ment are presented in Table 1. It should be noted that in
the majority of patients, BMI exceeded 25 kg/m2. The
pathological tumor analysis is presented in Table 1. It
should be noted that the majority of the analyzed tumors
were T1-3 tumors and metastased to the lymph nodes.
In the analyzed material, most frequently tumor was
located within the body of the stomach. Adenocarcinoma
was the most frequent [96 (46.38%)] histopathological
type. Most of the tumors showed a low degree of histo-
logical differentiation (G3). The values of laboratory tests
are presented in Table 1. The values of PNI were mostly
in the range of 50–55 with a mean value 52.78. In the
study, most patients (over 70) were awarded 1 point in
NRS 2002. However, there was also a large number (76)
of patients with a score
3 in NRS 2002, indicating
a real nutritional risk that required nutritional
intervention.
A weak significant relationship between the NRS 2002
score and gender was noted in our patients. A female
gender was associated with a higher NRS 2002 score.
 NUTRITION AND CANCER 3

Table 1. The patients’ clinicopathological characteristics and (calculated after disease), and smoking was noted.
laboratory results. A higher BMI was associated with a lower nutritional
Demographic characteristics risk in NRS 2002. The initial BMI (calculated before dis-
Age (years) 57.80 § 9.22 (25–74)
ease) was positively correlated with age, final BMI (calcu-
Male/female 142 (68.6%)/65 (31.4%) lated after disease recognition), and comorbidities
Weight loss (%) (arterial hypertension, ischemic heart disease, diabetes).
Stable 63 (30.43%)
Weight loss  10% 65 (31.40%) Smoking was significantly associated with the lower
Weight loss > 10% 79 (38.17%) initial BMI in analyzed patients. The final BMI was posi-
BMI (kg/m2)
Before disease 27.77 § 4.64 (18.52–43.93) tively correlated with age, initial BMI, and comorbidities.
Before treatment 25.63 § 4.58 (16.05–38.97) Negative correlations between the final BMI and weight
NRS 2002 (points) 2.33 § 1.33 (1–5)
Arterial hypertension loss, NRS 2002 score, and smoking were reported. The
No 144 (69.57%) higher weight loss, NRS 2002, and smoking were associ-
Yes 63 (30.43%)
Ischaemic heart disease
ated with the lower final BMI.
No 177 (85.51%) The serum albumin level was negatively correlated
Yes 30 (14.49%) with age, general location, lymph node invasion, weight
Diabetes mellitus (type 1)
No 207 (100.00%) loss, and the NRS 2002 score. Higher age, body and pylo-
Yes 0 (0.00%) rus tumor location, lymph node invasion, higher weight
Diabetes mellitus (type 2)
No 178 (85.99%) loss and NRS 2002 scores were associated with the lower
Yes 29 (14.01%) serum albumin level in the analyzed patients. The serum
Smoking
No 119 (57.49%) level of total protein was positively correlated with the
Yes 88 (42.51%) final BMI, and negatively with weight loss and NRS 2002
Smoking cessation after recognition
No 188 (90.82%)
scores. Lower final BMI, and higher weight loss and NRS
Yes 19 (9.18%) 2002 scores were associated with lower total protein
Duration of smoking (years) 14.29 § 18.15 (0–63) level. Lower hemoglobin level correlated with the body
Number of cigarettes per day 7.38 § 6.04 (0–40)
Serum level of total protein (g/l) 69.74 § 5.4 (53–83) and pylorus tumor location and higher weight loss. The
Serum level of albumin (g/l) 42.77 § 4.31 (30.92–50.68) total lymphocyte count was positively correlated with
Hemoglobin level (g/dl) 12.94 § 2.29 (5.8–17.7)
Total lymphocyte count (/mm3) 2.00 § 0.72 (0.63–4.89) smoking, and negatively with general location, histologi-
PNI (prognostic nutritional index) 52.78 § 6.04 (37.17–65.22) cal grade, lymph node invasion, weight loss, and NRS
General tumor location
Cardia and all stomach 68 (32.85%) 2002 scores. The lower total lymphocyte count was
Body and pylorus 139 (67.15%) associated with no smoking, body and pylorus tumor
Detailed tumor location
Cardia 19 (9.18%)
location, higher histological grade, lymph node invasion,
Body 92 (44.44%) and higher weight loss and NRS 2002 scores. Lower PNI
Pylorus 17 (8.21%) was correlated with age, body and pylorus tumor loca-
All stomach 15 (7.25%)
Cardia and body 38 (18.36%) tion, lymph node invasion, higher weight loss and NRS
Body and pylorus 21 (10.15%) 2002 scores and smoking cessation. All significant corre-
Data not available 5 (2.41%)
Histopathological grading lations are presented in Table 2. Significantly higher age,
G1 9 (4.36%) weight loss, lymph node invasion, higher NRS 2002
G2 60 (28.98%)
G3 138 (66.66%) scores, smoking cessation, and more frequent location
Tumor depth (T) within all stomach and body and pylorus were observed
T1-3 199 (196.14%)
T4 8 (3.86%)
in the low-PNI group compared to the high-PNI group
Lymph node metastasis (N) (Table 3).
N0 95 (45.89%) The analyzed patients were divided into groups
NC 112 (54.11%)
according to gender, BMI, weight loss, NRS 2002 score,
Values are presented as means and standard deviations. BMI, body mass tumor location, and histopathological type and grade,
index; NRS 2002, Nutritional Risk Score 2002.
and PNI. The continuous variables (age, BMI, total lym-
phocyte count, albumin, total protein, hemoglobin levels,
A very significant and strong positive correlation and PNI) were compared. All results of this analysis are
between the NRS 2002 score and weight loss was presented in Table 4. The age, initial and final BMI,
observed. A higher weight loss was strongly associated albumin, total protein, hemoglobin levels, total lympho-
with a higher nutritional risk according to the NRS 2002 cyte count, and PNI were comparable in both gender
score. A positive correlation between the NRS 2002 score groups. Significant difference in final BMI between
and the tumor depth was reported. A negative correla- groups divided according to weight loss (P D 0.000005)
tion between the NRS 2002 score and the final BMI was noted. The highest final BMI was noted in patients
4

A. BREWCZYNSKI ET AL.

Table 2. Significant correlations between nutritional parameters Table 3. Comparison of low and high prognostic nutritional
and selected clinicopathological factors. index (PNI) groups according to selected clinicopathological
factors.
T P
PNI < 52.78 PNI
52.78 P
NRS 2002
Gender 0.155829 0.002075 Age (yr) 59.90 § 8.57 55.92 § 9.75 0.006955
Tumor depth (T) 0.116992 0.020787 Gender 67.53% M 69.88% M 0.634900
Weight loss 0.757294 0.000000 32.47% F 30.12% F
Final BMI ¡0.292512 0.000000 General location 37.66% (a) 27.71% (a) 0.046324
Final BMI (division into 2 groups) ¡0.114443 0.027661 62.34% (b) 72.29% (b)
Smoking ¡0.134944 0.008207 Detailed location 8.22% (1) 9.76% (1) 0.001035
Duration of smoking (yr) ¡0.147723 0.004477 34.25% (2) 56.10% (2)
Number of cigarettes per day ¡0.154783 0.002814 8.22% (3) 7.32% (3)
Initial BMI 15.07% (4) 2.44% (4)
Age 0.192281 0.000216 19.18% (5) 15.85% (5)
Initial BMI 0.668046 0.000000 15.07% (6) 8.54% (6)
Final BMI (division into 2 groups) 0.264441 0.000000 Tumor depth (T) 93.51% T1 97.59% T1 0.061160
NRS 2002 (division into 2 groups) 0.104443 0.044468 6.49% T2 2.41% T2
Arterial hypertension 0.266303 0.000000 Lymph node metastasis (N) 32.47% N1 56.63% N1 0.000005
Ischemic heart disease 0.157887 0.002456 67.53% N2 43.37% N2
Diabetes mellitus (type 2) 0.181268 0.000507 Weight loss
Smoking ¡0.224386 0.000019 1. Stable 19.72% 45.95% 0.000000
Duration of smoking ¡0.158701 0.002988 2. Weight loss  10% 28.17% 33.78%
Number of cigarettes per day ¡0.182035 0.000634 3. Weight loss > 10% 52.11% 20.27%
Final BMI Final BMI groups
Age 0.172001 0.000653 1. <18.5 2.94% 2.94% 1.0000
Weight loss ¡0.297637 0.000000 2.
18.5 97.06% 97.06%
Initial BMI 0.668046 0.000000 Initial BMI (kg/m2) 27.86 § 4.74 27.86 § 4.83 0.997227
NRS 2002 ¡0.292512 0.000000 Final BMI (kg/m2) 25.06 § 4.23 25.36 § 4.73 0.088124
NRS 2002 (division into 2 groups) ¡0.209113 0.000054 NRS 2002
Arterial hypertension 0.225777 0.000008 1. 30.00% 61.64% 0.000002
Ischemic heart disease 0.156614 0.001970 2. 17.14% 8.22%
Diabetes mellitus (type 2) 0.180598 0.000359 3. 12.86% 6.85%
Smoking ¡0.190715 0.000179 4. 38.57% 23.29%
Duration of smoking ¡0.130106 0.012038 5. 1.43% 0.00%
Number of cigarettes per day ¡0.141383 0.006202 NRS (division into groups)
Albumin level 1. <3 47.14% 69.86% 0.000043
Age ¡0.212734 0.000065 2.
3 52.86% 30.14%
Detailed location ¡0.151367 0.005187 Arterial hypertension 70.13% (N) 67.47% (N) 0.590471
Lymph node metastasis (N) ¡0.126013 0.018029 29.87% (Y) 32.53% (Y)
Weight loss ¡0.253166 0.000006 Ischemic heart disease 88.31% (N) 85.54% (N) 0.441821
NRS 2002 ¡0.192354 0.000653 11.69% (Y) 14.46% (Y)
NRS 2002 (division into 2 groups) ¡0.187400 0.000898 Diabetes mellitus (type 2) 85.71% (N) 87.95% (N) 0.534349
Total protein level 14.29% (Y) 12.05% (Y)
Weight loss ¡0.280670 0.000000 Smoking 63.16% (N) 54.32% (N) 0.095601
Final BMI 0.131288 0.017122 36.84% (Y) 45.68% (Y)
NRS 2002 ¡0.184031 0.000767 Smoking cessation 89.19% (N) 96.25% (N) 0.011699
NRS 2002 (division into 2 groups) ¡0.188980 0.000550 10.81% (Y) 3.75% (Y)
Hemoglobin level Serum level of total protein (g/l) 66.98 § 5.27 72.43 § 4.15 0.000000
Detailed location ¡0.126926 0.014899 Serum level of albumin (g/l) 39.78 § 3.32 45.54 § 3.10 0.000000
Weight loss ¡0.138455 0.010566 Hemoglobin level (g/dl) 11.91 § 2.26 13.93 § 1.75 0.000000
Total lymphocyte count Total lymphocyte count (/mm ) 3
1.57 § 0.45 2.40 § 0.66 0.000000
Detailed location ¡0.108444 0.037499 PNI 47.63 § 3.70 57.56 § 3.17 0.000000
Histopathological grade ¡0.177965 0.001015
Lymph node metastasis (N) ¡0.114430 0.025853 Coefficients are significant with P < 0.05000. T, Tau Kendall’s coefficient; BMI,
Weight loss ¡0.220702 0.000046 body mass index. M, male; F, female; (N), No; (Y), yes. (a). cardia and all
NRS 2002 ¡0.173198 0.001543 stomach; (b). body or pylorus (general location); (1) cardia; (2) body; (3)
NRS 2002 (division into 2 groups) ¡0.149437 0.006293 pylorus; (4) all stomach; (5) cardia and body; (6) body and pylorus (detailed
Smoking 0.178081 0.000611 location).
Duration of smoking 0.119852 0.024034
Number of cigarettes per day 0.162118 0.002129
Prognostic nutritional index with stable weight, and the lowest BMI was recorded in
Age ¡0.139782 0.008704 patients with weight loss of more than 10%. The initial
General location ¡0.136438 0.011752
Lymph node metastasis (N) ¡0.150507 0.004732 BMI was comparable in both groups. The total lympho-
Weight loss ¡0.302984 0.000000 cyte count was significantly highest in stable-weight
NRS 2002 ¡0.233567 0.000035
NRS 2002 (division into 2 groups) ¡0.217413 0.000117
patients and the lowest count was noted in patients with
Smoking cessation ¡0.109891 0.043119 weight loss of more than 10% (P D 0.02515). Also, albu-
T, Tau Kendall’s coefficient; BMI, body mass index; NRS 2002, Nutritional Risk
min (P D 0.000031) and total protein (P D 0.000022)
Score. Coefficients are significant with P < 0.05000. levels and PNI (P D 0.000025) were significantly highest
Table 4. Comparison of clinical and laboratory parameters between groups according to selected clinicopathological factors.
Initial BMI Final BMI TLC SAL STPL HL
Age (kg/m2) (kg/m2) (/mm3) (g/l) (g/l) PNI (g/dl)

Gender/P 0.093978 0.653124 0.357950 0.225953 0.806040 0.594321 0.412896 0.222562

Male 58.53 § 9.09 27.87 § 4.39 25.84 § 4.19 2.05 § 0.78 42.83 § 4.17 69.89 § 5.40 53.05 § 6.23 13.08 § 2.36
Female 56.21 § 9.36 27.52 § 5.23 25.16 § 5.36 1.90 § 0.57 42.65 § 4.65 69.41 § 5.43 52.20 § 5.60 12.62 § 2.13
Weight loss/P 0.686330 0.60805 0.000005 0.002515 0.000031 0.000022 0.000025 0.072000
1. Stable 57.29 § 9.18 26.97 § 3.97 27.97 § 3.94 1.26 § 0.79 44.04 § 3.76 71.53 § 5.25 55.10 § 4.97 13.36 § 2.10
2. 10% 56.59 § 10.26 26.50 § 4.37 25.25 § 4.45 1.89 § 0.60 43.68 § 3.81 70.39 § 3.94 53.18 § 5.02 12.93 § 2.16
3. >10% 58.04 § 9.01 28.53 § 5.17 23.97 § 4.35 1.80 § 0.73 40.65 § 4.23 67.07 § 5.51 49.79 § 6.62 12.33 § 2.59
BMI groups/P 0.122333 0.000014 0.000001 0.955629 0.651528 0.370622 0.722294 0.840446
1. <18.5 kg/m2 52.71 § 9.98 20.48 § 1.53 17.65 § 0.96 1.99 § 1.24 43.70 § 2.79 67.22 § 5.28 53.65 § 8.12 12.62 § 2.08
2.
18.5 kg/m2 58.19 § 9.09 28.08 § 4.47 25.78 § 4.28 1.97 § 0.71 42.72 § 4.27 69.65 § 5.34 52.55 § 6.04 12.86 § 2.35
NRS groups/P 0.909452 0.051143 0.002316 0.032189 0.005476 0.003751 0.001527 0.641191
1. <3 points 57.96 § 9.16 27.16 § 4.15 26.36 § 4.46 2.08 § 0.74 43.56 § 3.93 70.58 § 5.04 53.94 § 5.25 12.94 § 2.13
2.
3 points 58.12 § 9.10 28.57 § 5.15 24.25 § 4.27 1.82 § 0.67 41.54 § 4.60 68.01 § 5.60 50.70 § 6.71 12.76 § 2.57
AH groups/P 0.000029 0.000004 0.000100 0.691213 0.530682 0.965308 0.647986 0.474285
1. No 56.05 § 9.41 26.73 § 4.09 24.79 § 4.33 2.02 § 0.74 42.63 § 4.27 69.76 § 5.59 52.63 § 5.85 12.84 § 2.24
2. Yes 61.80 § 7.52 30.29 § 5.00 27.67 § 4.54 1.98 § 0.69 43.09 § 4.41 69.72 § 5.07 53.11 § 6.48 13.11 § 2.42
IHD groups/P 0.004953 0.014994 0.009154 0.130586 0.691948 0.931976 0.455491 0.624883
1. No 57.07 § 9.45 27.40 § 4.58 25.28 § 4.50 1.97 § 0.71 42.82 § 4.42 69.73 § 5.66 52.64 § 6.03 12.96 § 2.32
2. Yes 62.17 § 6.45 29.81 § 4.62 27.80 § 4.53 2.22 § 0.78 42.42 § 3.57 69.84 § 3.52 53.70 § 6.19 12.71 § 2.18
DM groups/P 0.000103 0.003750 0.005189 0.379783 0.808995 0.793544 0.539798 0.485403
1. No 56.81 § 9.29 27.34 § 4.48 25.24 § 4.55 1.99 § 0.70 42.80 § 4.35 69.70 § 5.49 52.67 § 5.84 12.98 § 2.38
2. Yes 63.90 § 6.19 30.25 § 4.96 27.86 § 4.15 2.13 § 0.83 42.54 § 4.15 70.01 § 5.04 53.54 § 7.35 12.63 § 1.74
Smoking groups/P 0.189222 0.001672 0.007802 0.008159 0.942778 0.721791 0.199562 0.732964
1. No 58.44 § 9.63 28.83 § 4.15 26.49 § 4.31 1.88 § 0.72 42.78 § 4.56 69.84 § 5.40 52.24 § 6.61 12.86 § 2.28
2. Yes 56.71 § 8.65 26.57 § 4.71 24.64 § 4.74 2.18 § 0.68 42.73 § 3.97 69.53 § 5.51 53.50 § 5.13 12.98 § 2.34
Smoking cessation/P 0.978174 0.398878 0.268887 0.451963 0.884972 0.568694 0.096901 0.238932
1. No 57.67 § 9.30 27.68 § 4.54 25.51 § 4.47 2.02 § 0.75 42.91 § 4.28 69.68 § 5.40 52.98 § 6.10 13.01 § 2.23
2. Yes 57.60 § 9.38 28.92 § 6.51 27.03 § 5.93 1.85 § 0.32 40.58 § 4.69 68.75 § 6.24 49.80 § 5.64 12.21 § 2.81
General location/P 0.660357 0.580459 0.192060 0.211325 0.488485 0.580490 0.137978 0.328918
Location (a) 58.21 § 10.28 27.50 § 4.66 25.01 § 4.05 1.91 § 0.74 42.43 § 4.69 69.43 § 5.61 51.76 § 6.50 12.70 § 2.27
Location (b) 57.60 § 8.68 27.91 § 4.65 25.95 § 4.81 2.05 § 0.71 42.94 § 4.13 69.91 § 5.30 53.27 § 5.77 13.06 § 2.31
Detailed location/P 0.716352 0.920704 0.616385 0.367957 0.038707 0.680538 0.96861 0.043176
Location (1) 60.42 § 9.33 27.44 § 4.45 25.78 § 3.77 2.07 § 1.00 44.22 § 3.71 70.99 § 3.59 53.63 § 6.16 13.84 § 2.21
Location (2) 57.02 § 9.49 27.64 § 5.00 26.03 § 5.20 2.06 § 0.66 43.62 § 3.91 70.14 § 5.48 54.01 § 5.31 13.10 § 2.44
Location (3) 59.23 § 7.31 28.56 § 4.40 25.96 § 4.59 2.21 § 0.58 42.20 § 6.30 68.29 § 6.13 53.21 § 7.71 13.98 § 1.43
Location (4) 59.07 § 6.08 27.77 § 2.18 23.60 § 2.18 1.95 § 0.55 39.77 § 3.10 68.46 § 4.59 49.51 § 4.02 11.56 § 2.25
Location (5) 57.50 § 11.74 27.47 § 5.28 25.29 § 4.46 1.82 § 0.66 42.65 § 4.89 69.41 § 6.05 51.82 § 6.99 12.54 § 2.12
Location (6) 57.33 § 6.78 28.75 § 4.39 25.83 § 4.36 1.82 § 0.72 41.88 § 3.67 69.74 § 4.40 51.12 § 6.06 12.66 § 2.26
Tumor depth/P 0.832846 0.796946 0.423544 0.443725 0.922031 0.747913 0.701381 0.162730
T1-3 57.83 § 9.31 27.75 § 4.72 25.69 § 4.65 2.01 § 0.72 42.76 § 4.36 69.77 § 5.42 52.82 § 6.06 12.89 § 2.30
T4 57.12 § 6.79 28.21 § 2.63 24.27 § 2.06 1.79 § 0.69 42.93 § 3.37 69.10 § 4.97 51.92 § 6.03 14.13 § 1.78
(Continued on next page)
NUTRITION AND CANCER
5
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A. BREWCZYNSKI ET AL.

Table 4. (Continued).
Initial BMI Final BMI TLC SAL STPL HL
Age (kg/m2) (kg/m2) (/mm3) (g/l) (g/l) PNI (g/dl)

Lymph node metastasis/P 0.396626 0.412173 0.146246 0.095387 0.070790 0.606738 0.019190 0.292065
N0 57.21 § 10.27 27.45 § 5.06 25.10 § 4.77 2.10 § 0.73 43.45 § 4.41 69.98 § 6.07 54.01 § 6.26 13.14 § 2.15
NC 58.30 § 8.23 28.04 § 4.26 26.10 § 4.37 1.92 § 0.70 42.21 § 4.17 69.55 § 4.79 51.77 § 5.69 12.77 § 2.40
Histological grade/P 0.043166 0.703021 0.867800 0.010141 0.317489 0.944785 0.785676 0.412589
G1 59.37 § 4.87 26.14 § 5.45 24.75 § 5.30 2.52 § 0.49 40.50 § 5.73 69.64 § 5.60 53.09 § 7.89 13.46 § 2.18
G2 59.98 § 7.51 27.78 § 4.97 24.75 § 4.90 2.21 § 0.86 42.29 § 3.94 69.89 § 5.14 53.33 § 6.75 12.53 § 2.39
G3 56.34 § 9.85 27.78 § 4.55 25.71 § 4.64 1.89 § 0.62 43.03 § 4.34 69.57 § 5.41 52.57 § 5.72 13.02 § 2.22

Statistical significance is defined by P < 0.05000.

BMI, body mass index; TLC, total lymphocyte count; SAL, serum albumin level; STPL, serum total protein level; PNI, prognostic nutritional index; HL, haemoglobin level;
M, male; F, female; N, no; Y, yes; AH, arterial hypertension; IHD, ischaemic heart disease; DM, diabetes mellitus (type 2).
(a) cardia and all stomach; (b) body or pylorus (general location);
(1) cardia; (2) body; (3) pylorus; (4) all stomach; (5) cardia and body; (6) body and pylorus (detailed location).

in stable-weight patients and lowest in the group with
weight loss > 10% (P D 0.000031). The age and initial
BMI were comparable in all groups divided according to
weight loss. Different variables were also compared in
groups divided according to final BMI, namely well
nourished (BMI
18.5 kg/m2) and malnourished (BMI
< 18.5 kg/m2). There was no significant difference in
laboratory nutritional parameters in both groups.
According to NRS 2002, patients were divided into two
groups depending on points number into <3 and
3
(nutritional risk) points. Both groups were comparable
according to age, initial BMI, and hemoglobin level. Sig-
nificant differences in other nutritional parameters were
observed in compared groups. The final BMI (P D
0.02316), albumin (P D 0.005476), total protein
(0.003751) levels, total lymphocyte count (P D
0.032189), and PNI (P D 0.001527) were significantly
lower in patients with nutritional risk. The analyzed
patients were divided into groups according to comor-
bidities (arterial hypertension, ischemic heart disease,
type 2 diabetes mellitus). The significantly higher age,
initial and final BMI were noted in patients with comor-
bidities compared to health groups. Nutritional parame-
ters were comparable in all groups. Significant
differences in BMI and total lymphocyte count were
recorded in patients groups divided according to smok-
ing status. Significantly lower initial BMI (P D 0.001672)
and final BMI (P D 0.007802) were noted in smoking
patients. Significantly higher total lymphocyte count was
observed in smoking patients (P D 0.008152). The other
parameters were comparable in both groups. There was
no significant difference in analyzed parameters in
patient groups divided according to smoking cessation.
In order to assess the relationship between tumor
characteristics and nutritional parameters, patients were
divided into groups according to tumor location and
staging, histological type and grade. The final BMI and
laboratory parameters (albumin, total protein, hemoglo-
bin, lymphocyte count, PNI) were higher in patients
with tumors located in gastric body or pylorus compared
to patients with tumors located in cardia and whole
stomach, but this difference was not statistically signifi-
cant. When the patients were divided into six groups
according to detailed location, statistically significant dif-
ference in albumin (P D 0.038707) and hemoglobin (P D
0.043176) levels were observed. The highest albumin
level was recorded in patients with tumors located in car-
dia, and the lowest one was in patients with tumors
located within all stomach. The highest hemoglobin level
was noted in patients with pyloric tumors, and the lowest
hemoglobin level was observed in patients with tumors
located within all stomach. According to tumor depth,
lower final BMI, total protein level, lymphocyte count,
NUTRITION AND CANCER 7
and PNI were reported in T4 compared to T1-3, but dif-
ferences were not statistically significant. Significantly
lower PNI (P D 0.019190) was noted in NC tumors with
lymph node metastasis. Also, not significantly lower lym-
phocyte count, albumin, total protein, and hemoglobin
were recorded in NC tumors. Statistically significant dif-
ferences in age and albumin level were observed between
compared groups divided according to histological type.
The significantly lowest age was noted in patients with
G3 tumors (P D 0.43166). G3 tumors were associated
with the lowest total lymphocyte count (P D 0.010141),
total protein level (P D 0.944785), and PNI (P D
0.785676) in the analyzed patients.
Two groups divided according to mean PNI were
compared in our work. This comparative analysis
revealed significant differences in age, total lymphocyte
count, albumin, and total protein and hemoglobin levels.
Higher PNI was associated with lower age (P D 006955),
and higher total protein (P D 0.000000) and hemoglobin
levels (P D 0.000000). Also, higher final BMI was
observed in the high-PNI group, but the difference was
not statistically significant (P D 0.088124). Both groups
were comparable according to histopathological type
and grade (P D 0.983593).
Discussion
Many publications have proved that malnutrition is
associated with poor prognosis in patients with cancer,
as a result of deterioration of their general health condi-
tion and more complications related to treatment. In GC
patients, a relationship between nutritional status and
prognosis has been reported (8,9). The negative impact
of malnutrition on the prognosis of cancer patients is
caused by a significant immune system dysfunction in
both the cellular and humoral immunity (10). Therefore,
assessment of nutritional status is very important
because it allows for selection or malnourished patients
with an increased nutritional risk and take appropriate
nutritional intervention in order to improve prognosis
and reduce complications (1,11–13).
In this study, we selected a few simple diagnostic tools
to determine the nutritional status of GC patients. The
weight loss in our GC patients was comparable to that
given in the literature (14). We noted a lower body
weight before treatment compared to that before the dis-
ease (mean difference was 6.57 § 6.90 kg). It should be
noted that the majority of patients were found to be
overweight or obese (BMI exceeded 25 kg/m2), which
may confirm the theory that obesity is a risk factor for
cancer development, including GC (15). The higher ini-
tial BMI was associated with higher age and comorbid-
ities (arterial hypertension, ischemic heart disease, and
8

A. BREWCZYNSKI ET AL.
type II diabetes). This observation confirms the associa-
tion of higher BMI with chronic diseases mentioned
above. Smoking was associated with lower BMI in the
analyzed patients. This result is in accordance with most
publications. Smoking is known to be associated with
oxidative stress, poor nutritional status, weight loss, and
increased mortality. According to the literature, it could
be associated with a poor taste and appetite, lower intake
of antioxidant fruits and vegetables and pro-inflamma-
tory effect of smoking. Therefore, the negative correla-
tion between smoking and nutritional status including
NRS 2002 noted in our material contrasts with the most
literature data (16–18). These results could be associated
with a lower initial BMI in smokers compared to non-
smokers, and lower weight loss. Also, it could be associ-
ated with the lower age of smokers compared to the age
of non-smokers. The other disturbance factors could
influence on the final NRS 2002.
In the analyzed group of patients, we recorded an
increased nutritional risk related to nutritional status in
NRS 2002 (
3 points) in 76 patients requiring nutri-
tional intervention. In the comparable number of
patients (more than 70) the nutritional risk according to
NRS 2002 was the lowest (1 point). Identification of
patients at increased nutritional risk is very important,
because the adverse effect of low NRS 2002 scores on
prognosis, survival, quality of life, and the incidence of
complications associated with treatment was demon-
strated in the literature (19–21).
In our study, blood test parameters including total
protein, albumin level, lymphocyte count and hemoglo-
bin level were analyzed. The appropriate level of albumin
in blood serum is essential for vital physiological func-
tions such as maintenance of normal serum osmolality,
tissue repair, transport of compounds, such as drugs and
nutrients and modulation of inflammatory response
(12,22). Therefore, hypoalbuminemia may cause an
increased incidence of postoperative complications fol-
lowing gastric resection, including anastomosis edema,
delayed healing and reduced therapeutic efficacy of drugs
and nutrients, and activation of inflammatory response.
As a result, low albumin levels may promote tumor
growth and infections that worsen the prognosis. The
lymphocyte count in the peripheral blood is second labo-
ratory parameter reflecting the immunological status and
degree of systemic inflammatory response (12,23,24). In
our study, PNI values were higher in comparison with
the majority of data published in the literature.
The PNI was originally introduced in 1980 by Buzby
et al. (25) (study involving 161 patients undergoing elec-
tive surgery) to evaluate the immunological and nutri-
tional aspects of patients undergoing surgical treatment of
diseases of the gastrointestinal tract. In 1984, Onodera
et al. (6) proposed a modified PNI calculated on the basis
of two factors: serum albumin and lymphocytes in the
peripheral blood. The authors claimed that the incidence
of postoperative complications was significantly higher in
patients with low PNI values. In 2014, Sun et al. (26) pub-
lished a comprehensive meta-analysis on the PNI. The
work included the analysis of 14 publications involving
3414 patients. The authors observed a significantly shorter
overall survival and a greater number of postoperative
complications in patients with low PNI, but did not report
a similar dependence for the cancer-specific survival.
Correlation between PNI and GC TNM classification (the
depth of invasion and metastasis to lymph nodes) was
also noted. Among the articles related to GC, authors
included the analysis of studies published by Nozoe et al.
(27): 248 patients, the cutoff value of PNI 49.7, Watanabe
(28): 99 patients, the cutoff value of PNI 44.7, Migita (29):
548 patients, the cutoff value of PNI 48. These cutoff val-
ues were determined based on an increased risk associated
with a higher incidence of postoperative complications in
patients undergoing gastrectomy. In the study by Migita
et al. (29), the mean PNI before surgery was 50.3 § 5.8
with a cutoff value 48. According to most studies, a PNI
value of 45 is considered an indicator of significant mal-
nutrition, but the optimal cutoff value remains unclear.
Nozoe et al. (27) divided 248 patients into two groups,
with high and low PNI, according to the average value of
PNI 49.7. The groups were compared according to differ-
ent clinicopathological factors. The authors observed that
the PNI was associated with tumor progression and
venous invasion. There was no correlation between the
value of PNI and gender, and a statistically significant dif-
ference in age between the compared groups was reported.
In the group with low PNI, the mean age (70.1 § 8.6) was
significantly higher compared to that in the high-PNI
group (64.4 § 11.1). Preoperative PNI was 29.8–65.8.
Jiang et al. (10) conducted a similar work, published in
2014, involving 386 GC patients undergoing total gastrec-
tomy. The authors compared two groups with high and
low PNI (cutoff value 46) values. In the group with low
PNI, they reported more patients aged> 65 yr and low
BMI < 18.5 compared with the high-PNI group. There
was no statistically significant difference between the
groups in terms of gender and location, and histopa-
thology of tumor. Correlation of PNI with tumor stage
in the TNM classification and incidence of postopera-
tive complications was observed. Our results were
similar to results mentioned above. In the analyzed
patients, PNI was also associated with lower age and
higher total lymphocyte count, albumin, total protein
and hemoglobin levels. A higher final BMI was also
observed in the high-PNI group, but the difference was
not statistically significant.

Sun et al. (12) published in 2015 a work based on the
study of 632 patients who underwent gastrectomy due to
GC and suggested additional factors useful for the assess-
ment of nutritional status and immune system. The
authors determined the cutoff value of PNI to be 48.2.
They suggested the so-called prognostic Canton score
including, PNI addition to other indicators such as the
neutrophil-lymphocyte ratio and platelet-lymphocyte
ratio. The authors also compared the two separated on
the basis of PNI group (of high and low PNI) according
to different factors. They reported a significantly higher
proportion of resectability and a higher level of albumin
in the high-PNI group.
In our material, the lower serum albumin and total
protein levels and the lower PNI values were significantly
associated with a higher age which confirms the litera-
ture data regarding a poor nutritional status in older
patients. According to the literature, age-related physio-
logical anorexia may predispose to protein-energy
undernutrition in older persons. In general, lean body
mass decreases with age, while body fat, increases. These
factors may decrease energy requirements and intake
(30,31). Therefore, a positive correlation between age
and BMI and negative correlation between age and
serum albumin, total protein levels and PNI were noted
in analyzed patients.
An interesting positive correlation between the total
lymphocyte count in the peripheral blood and smoking
status was observed in our material. Smoking was associ-
ated with the higher lymphocyte count in the analyzed
patients. It could be caused by the so-called persistent
polyclonal B-cell lymphocytosis in chronic smokers.
According to literature, persistent leucocytosis, neutro-
philia, and lymphocytosis (with increased T and B lym-
phocyte count) is a well-recognized phenomenon in some
chronic cigarette smokers (32–35). Therefore, the positive
correlation between the total lymphocyte count in the
peripheral blood and smoking in our patients was proba-
bly not associated with better nutritional status, but with
influence of smoking on immunological status in smokers.
Conclusion
Assessment of nutritional status using basic diagnostic
tools and PNI calculation should be the standard man-
agement of patients with GC before treatment in order
to improve the prognosis, quality of life, and reduce the
risk of complications.
Acknowledgments
The authors express their gratitude to the Associate Professor
Jerzy Wydma
nski for his permission to make use of the gastric
NUTRITION AND CANCER 9
cancer patients’ case records from the Radiotherapy Depart-
ment Gliwice Branch of Maria Sklodowska-Curie Memorial
Cancer Center, Poland.
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