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European Journal of Clinical Nutrition (2005) 59, 35–40
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ORIGINAL COMMUNICATION
Prognostic significance of Subjective Global
Assessment (SGA) in advanced colorectal cancer
D Gupta1*, CA Lammersfeld1, PG Vashi1, J Burrows1, CG Lis1 and JF Grutsch1
1
Cancer Treatment Centers of Americas at Midwestern Regional Medical Center, Zion, IL, USA
Objective: To evaluate the prognostic significance of Subjective Global Assessment (SGA) in advanced colorectal cancer and
create statistically distinct prognostic groups of colorectal cancer patients based on clinical and nutritional variables.
Design: A retrospective clinical epidemiologic study.
Setting: A private tertiary care American Cancer Center.
Subjects: In total, 234 colorectal cancer patients aged 29–82 y treated at Cancer Treatment Centers of America at Midwestern
Regional Medical Center between January 1995 and March 2001.
Intervention: SGA Questionnaire. SGA A—well nourished; SGA B—moderately malnourished; and SGA C—severely
malnourished. Malnutrition was defined as either SGA B or SGA C.
Results: The prevalence of malnutrition in this patient population, as determined by SGA, was 52% (113/217). The median
survival of patients with SGA A was 12.8 months (95% CI; 9.1–16.5), those with SGA B was 8.8 months (95% CI; 6.7–10.9) and
those with SGA C was 6 months (95% CI; 3.9–8.1); the difference being statistically significant at P ¼ 0.0013. Regression tree
analysis identified prior treatment history, lactate dehydrogenase (LDH) and SGA to be important predictors of survival for our
patient cohort. Patients with no prior treatment history (newly diagnosed disease), low LDH scores, and SGA A had the best
overall survival of 40.4 months (95% CI; 30.45–50.4), whereas patients with prior treatment history (progressive disease), high
LDH scores, and SGA B/C had the worst overall survival of 4.5 months (95% CI; 2.22–6.76).
Conclusion: The SGA provides useful prognostic information in patients with advanced colorectal cancer.
Sponsors: Cancer Treatment Centers of America.
European Journal of Clinical Nutrition (2005) 59, 35–40. doi:10.1038/sj.ejcn.1602029
Published online 14 July 2004
Keywords: advanced colorectal cancer; subjective global assessment; nutritional assessment; prognostic significance; survival
Introduction
Colorectal cancer is the second leading cause of cancer death
in the United States (Hawk et al, 2002). Despite significant
advances in early diagnosis and treatment, 5-y survival rates
for stages III and IV colorectal cancer remain poor. Various
clinical, biochemical and histological prognostic factors for
*Correspondence: D Gupta, Cancer Treatment Centers of America at
Midwestern Regional Medical Center, 2610 N Sheridan Road, Zion, IL
60099, USA.
E-mail: [email protected]
Guarantor: D Gupta.
Contributors: DG was the main author of the manuscript, initiated the
study, collected, analyzed and interpreted data. PGV supervised the
project and assisted in interpretation of results. CAL and JB assisted in
writing the manuscript. CGL initiated the study and assisted in
writing and interpretation. JFG supervised the project and assisted
with the statistical analysis.
Received 4 November 2003; revised 10 May 2004; accepted 11 June 2004;
published online 14 July 2004
advanced colorectal cancer have been identified. Tumor
stage has proved to be the most decisive prognostic factor in
both univariate and multivariate analyses (Lindmark et al,
1994; D’Eredita et al, 1996; Heys et al, 1998). Other
prognostic factors for colorectal cancer include age, tumor
grade, tumor size and location, symptom duration, and
vascular and neural invasion. More recently, other prognostic factors have been identified including carcinoembryonic
antigen (CEA), carbohydrate antigen 19-9 (CA 19-9), serum
albumin, alkaline phosphatase, lactate dehydrogenase
(LDH), aspartate aminotransferase, gamma-glutamyl-transpeptidase, and performance status (Chang et al, 1989; Kouri
et al, 1992; Steinberg et al, 1992; Wang et al, 2002; Yuste et al,
2003).
Although such factors do provide useful prognostic
information, many of these factors cannot favorably influence survival. As a result, an urgent need exists to identify
those prognostic factors that are modifiable. Intervention
SGA and survival in colorectal cancer
D Gupta et al
36
directed at such factors could possibly lead to improved
survival. Nutritional status is one such factor. However, the
evidence documenting its prognostic significance in colorectal cancer remains sparse. In part, this is due to the
difficulty of measuring nutritional status in a valid and
reliable manner.
Historically, nutritional status has been evaluated by
various objective measures including anthropometric and
laboratory measurements (eg weight change, arm muscle
circumference, triceps skinfold thickness, serum albumin,
transferrin assays and nitrogen balance studies). Some of
these objective measures such as serum albumin are likely to
be influenced by many non-nutritional factors (Bauer et al,
2002; Carney & Meguid, 2002; Waitzberg & Correia, 2003).
The interpretation of these measures is often difficult
because non-nutritional factors, such as hydration state
and disease process, can obscure the effects of actual nutrient
deprivation (Detsky et al, 1984). Furthermore, some objective
indicators such as serum albumin have long half-lives, thus,
assessing changes in the nutritional status over a short
period of time is challenging. Moreover, in the clinical
setting, these methods are not ideal because they are time
consuming and require well-trained staff. In an effort to
overcome the problems of traditional nutritional assessment,
an easy-to-use, inexpensive, and noninvasive clinical instrument has been developed—the subjective global assessment
(SGA).
The SGA is a clinical technique that combines data from
subjective and objective aspects of medical history (weight
change, dietary intake change, gastrointestinal symptoms,
and changes in functional capacity) and physical examination (loss of subcutaneous fat, muscle wasting, ankle or sacral
edema and ascites) (Detsky et al, 1987). After evaluation,
patients are categorized into three distinct classes of nutritional status; well nourished (SGA A), moderately malnourished (SGA B) and severely malnourished (SGA C). The SGA
has been validated in a number of diverse patient populations including cancer patients (Enia et al, 1993; Ek et al,
1996; Jones et al, 1997; Duerksen et al, 2000; Sacks et al, 2000;
Thoresen et al, 2002). It has also been correlated with a
number of objective nutritional assessment indicators,
morbidity, mortality, and quality of life (QoL) measures
(Detsky et al, 1987; Hirsch et al, 1991; Hasse et al, 1993;
Ferguson et al, 1999a, b; Persson et al, 1999; Bauer et al,
2002).
The scored patient-generated subjective global assessment
(PG-SGA) is a further modification of the SGA and has been
specifically developed for patients with cancer. (Ottery, 1994,
1996). Unlike the SGA, which is categorical in nature, the
PG-SGA measures nutritional status on a continuous scale,
thus allowing for the detection of subtle changes in
nutritional status over a short period of time. The higher
the PG-SGA score, the greater the risk of malnutrition. Also,
unlike the SGA, which must be completed entirely by the
health professional, much of the PG-SGA can be completed
by the patient.
European Journal of Clinical Nutrition
Although extensive research has been conducted on the
validation of the SGA, a relatively small body of evidence
exists regarding its use as a prognostic indicator in patients
with cancer. To the best of our knowledge, no studies
conducted to date have evaluated the prognostic significance of the SGA in advanced colorectal cancer.
The primary objective of this study is to evaluate the
prognostic significance of the SGA in patients with advanced
(stages III and IV) colorectal cancer. The secondary objective
is to create statistically distinct prognostic groups of colorectal cancer patients based on clinical and nutritional
variables.
Patients and methods
Patients
A retrospective chart review was performed on a consecutive
series of 234 stages III and IV colorectal cancer patients
treated at Cancer Treatment Centers of America (CTCA) at
Midwestern Regional Medical Center (MRMC) between
January 1995 and March 2001. The patients were identified
from the MRMC tumor registry. Data were collected on a
wide range of variables including demographic (age, sex);
tumor-related (grade, stage, size, site); clinical (duration of
symptoms, metastatic sites, lymph node involvement,
comorbidities); prior treatment history (newly diagnosed vs
progressive disease); laboratory (blood counts, tumor markers, serum enzymes) and nutritional (SGA, serum albumin,
body mass index).
The SGA and the scored PG-SGA were used to assess
nutritional status; however, for the purpose of this study
only the SGA ratings were used. All patients in this study
were scheduled for a consultation with a dietitian. Prior to
each consultation, a dietitian reviewed the patient’s history
from the medical record and verified the patient’s current
weight. During the consultation, the dietitians reviewed the
SGA instrument with the patient to obtain answers to all the
questions. The dietitians also completed a physical exam
paying particular attention to loss of subcutaneous fat,
muscle wasting, presence of ankle and sacral edema and
ascites. After the consultation, the dietitians ranked the
patient’s nutritional status as well nourished (SGA A),
moderately malnourished (SGA B) or severely malnourished
(SGA C) as described by Detsky et al (1987). For the purpose
of this analysis, malnutrition was defined as either SGA B or
SGA C.
This study was approved by the Institutional Review Board
at the Midwestern Regional Medical Center.
Statistical methods
All data were analyzed using SPSS 11.0 (SPSS Inc., Chicago,
IL, USA). Patient survival was defined as the time interval
between the first date of patient visit to the hospital and date
of death from any cause or date of last contact/last known to
be alive. The Kaplan–Meier or product-limit method was
SGA and survival in colorectal cancer
D Gupta et al
37
used to calculate survival. The log-rank test statistic was used
to evaluate the equality of survival distributions across
different strata.
A wide range of demographic, clinical, pathological, and
serological factors were evaluated for patient survival in a
univariate analysis. Kaplan–Meier survival curves were constructed for each variable and the corresponding log-rank
scores and P-values were also determined.
The method of recursive partitioning or regression trees
was used to identify distinct prognostic categories of the
patient population. The variable with the highest log-rank
score was used to sequentially bifurcate the patient population into two mutually exclusive groups. This process was
repeated until no variable achieved statistical significance at
Pr0.05. This analysis strategy allows for identification of a
large number of prognostic groups, each containing only a
small number of patients. There are several advantages to
this approach. First, the scale of measurement is arbitrary,
except that a monotonic relationship must be assumed
between covariates and survival. Second, this technique
allows us to classify patients into mutually exclusive groups,
that can be easily described and understood (Green et al,
2003).
Results
At the time of this analysis, 200 patients had expired and 34
were lost to follow-up. In all, 133 patients (56.8%) were male
and 101 (43.2%) were female. The mean age was 58.4 y
(s.d. ¼ 10.6; range 29–82 y). A total of 170 (72.6%) patients
had been diagnosed and treated outside of our hospital and
63 (26.9%) were newly diagnosed. Moderately differentiated
tumors were the most common type (70.1%) followed by
poorly differentiated (18.4%) and well-differentiated (7.3%)
tumours. All patients had a histologically confirmed diagnosis of stages III or IV colorectal cancer. A total of 95
(40.6%) had stage III disease and 139 (59.4%) had stage IV.
All tumors were adenocarcinomas. The prevalence of malnutrition in this patient population, as determined by SGA,
was 52% (113/217). Table 1 shows the characteristics of our
patient cohort in greater detail.
Table 2 shows the univariate survival analysis of different
prognostic factors. The variables have been rank-ordered
based on their statistical strength of association with
survival. Prior treatment history was most strongly associated with survival (log-rank ¼ 53.1, P-valueo0.0001) and
was therefore the first variable to split our patient population
into two mutually exclusive groups: patients with progressive disease and those with newly diagnosed disease. The
SGA was also found to be significantly associated with
survival on univariate analysis (Figure 1). The median
survival of patients with SGA A was 12.8 months (95% CI;
9.1–16.5), those with SGA B was 8.8 months (95% CI; 6.7–
10.9) and those with SGA C was 6 months (95% CI; 3.9–8.1),
the difference being statistically significant at P ¼ 0.0013.
Table 1
patients
Baseline characteristics of 234 stage III/IV colorectal cancer
(A) Characteristic
Categories
Sex
Male
Female
Expired
censored (lost to
follow-up)
Progressive disease
Newly diagnosed
Unknown
Stage III
Stage IV
Well
Moderate
Poor
Unknown
Right sided
Left sided
A
B
C
Unknown
Vital status
Prior treatment
history
Tumor stage at
diagnosis
Tumor grade at
diagnosis
Tumor site
Subjective global
assessment
Number
Percent (%)
133
101
200
34
56.8
43.2
85.5
14.5
170
63
1
95
139
17
164
43
10
89
145
104
75
38
17
72.6
26.9
(B) Characteristic
Mean
s.d.
Age (y)
Albumin (g/dl)
Total protein (g/dl)
Hemoglobin (g/dl)
Body mass index (kg/
m2)
Lactate
dehydrogenase (U/l)
Carbohydrate
antigen 19-9 (IU/ml)
Carbohydrate
antigen 72-4 (ng/ml)
Carcinoembryonic
antigen (ng/ml)
58.4
3.5
6.6
11.8
26.4
10.6
0.62
1.4
1.9
5.7
40.6
59.4
7.3
70.1
18.4
4.2
38
62
44.4
32.1
16.2
7.2
Range
29–82
1.8–4.9
0.2–8.8
5–16.1
4.9–46.4
1222.8
1565.9
129–10 212
1342.5
3977.7
0–25 704
72.4
329.9
1–3450
629.9
1619.6
0.5–13 191
Table 2 Univariate analysis of prognostic factors of 234 stage III/IV
colorectal cancer patients
Variable
Prior treatment history
Lactate dehydrogenase
Carbohydrate antigen 19-9
Number of prior chemo regimens
Hemoglobin
Carbohydrate antigen 72-4
Subjective global assessment
Stage at diagnosis
Carcinoembryonic antigen
Albumin
Total protein
Tumor grade
Tumor location
Number of positive lymph nodes
Body mass index
Age
Sex
Log-rank score
P-value
53.1
44.5
41.47
31.82
20.59
19.31
13.36
13.02
12.95
11.61
6.88
3.3
3.2
2.1
0.38
0.18
0.01
o0.0001
o0.0001
o0.0001
o0.0001
o0.0001
o0.0001
0.0013
0.0003
0.0003
0.0007
0.0087
0.192
0.0742
0.3431
0.539
0.675
0.942
European Journal of Clinical Nutrition
SGA and survival in colorectal cancer
D Gupta et al
38
Discussion
Figure 1
Survival stratified by SGA categories (N ¼ 234).
Some other variables that were found to have a statistical
association with survival were tumor stage, serum LDH,
CA 19-9 and CA 72-4, serum albumin, total protein and
CEA. Age, tumor grade, and tumor location were not
found to have a statistically significant association with
survival.
Figure 2 shows the recursive-partitioning model that was
constructed based on the strength of association of different
prognostic variables with survival. It shows the variable splitpoints that were used to divide our patient cohort into
statistically distinct and mutually exclusive groups. We
found that for both previously treated and newly diagnosed
patients, LDH had the highest statistical strength of association with survival (P-valueo0.0001 for both previously
treated and newly diagnosed patients). Further analysis
showed the SGA to be most strongly associated with survival
(P-value ¼ 0.01 for previously treated patients with high LDH
levels and 0.0003 for newly diagnosed patients with low LDH
levels). The analysis stopped at the SGA because no other
variable was found to be statistically significantly associated
with survival beyond that point.
Table 3 shows six (6) statistically distinct prognostic classes
of our patient cohort. This classification scheme was derived
from the final recursive-partitioning tree. Patients with no
prior treatment history, low LDH scores, and SGA A had the
best overall survival of 40.4 months (95% CI; 30.45–50.4),
whereas patients with prior treatment history (progressive
disease), high LDH scores, and SGA B/C had the worst overall
survival of 4.5 months (95% CI; 2.22–6.76).
European Journal of Clinical Nutrition
According to the National Cancer Institute’s ‘Nutrition in
Cancer Care’ guidelines, timely identification and treatment
of nutrition problems may improve cancer patients’ prognosis by helping the patient gain or maintain weight,
improving the patient’s response to therapy, and reducing
the complications of treatment (http://www.cancer.gov/
cancerinfo/pdq/supportivecare/nutrition). However, the
published literature documenting the prognostic significance of nutritional status in patients with advanced cancer
remains sparse. Moreover, nutritional status has traditionally
been assessed by anthropometric and laboratory measures,
which are costly, time consuming, and difficult to perform.
Therefore, we examined the prognostic significance of an
easy-to-use and inexpensive clinical technique called the
SGA in patients with advanced colorectal cancer.
In this study, we found that SGA A (well-nourished status)
vs SGA B/C (moderate-to-severe malnourished status) identified patients with better survival outcomes. We found that
the SGA provides useful prognostic information in patients
with advanced colorectal cancer and thereby, deserves
serious attention in cancer treatment settings. In a clinical
setting, the SGA is invaluable in identifying malnourished
patients in a quick and noninvasive manner. Moreover, the
simplicity of use of the SGA also enables health professionals
other than oncologists to accurately assess the patients’
nutritional status.
We also identified and described the distinct prognostic
categories of patients with advanced colorectal cancer. This
information could be of great value to clinicians in
predicting the prognosis of a patient at admission and
deciding upon subsequent treatment intervention. It also
highlights the importance of assessing nutritional status of
cancer patients early on in their treatment cycle.
Another finding of this study was the identification of
LDH as a useful prognostic indicator. Several studies have
reported the prognostic significance of LDH in patients with
metastatic colorectal cancer (Chang et al, 1989; Kemeny et al,
1989; Steinberg et al, 1992; Fountzilas et al, 1996). Indeed,
one study (Kemeny & Braun, 1983) described the importance
of LDH as an independent predictor of survival in advanced
colorectal carcinoma. Our findings are consistent with these
studies. In our regression tree analysis, LDH was the second
variable to influence survival for both previously treated and
newly diagnosed patients.
The strength of this study lies in its adequate statistical
power. A large sample size of 234 patients with survival
information available for 85.4% (200) patients provides
adequate power to effectively identify the true prognostic
effect of the variables studied. Only 14.6% (34) patients were
lost to follow-up in our study.
The recursive partitioning analytic methodology used in
this study has some drawbacks. For example, the precise
split-points identified for our data set may not be duplicated
in other similar data sets. As a result, this exploratory
data analysis approach needs to be validated in other
SGA and survival in colorectal cancer
D Gupta et al
39
Figure 2 Recursive partitioning tree. Variable split-points that were used to divide the patient cohort into statistically distinct and mutually
exclusive groups.
Table 3 Prognostic classes of 234 stage III/IV colorectal cancer patients
No.
Strata
N
Median survival (in months)
95% CI
1
2
3
4
5
6
No treatment history, low LDH, and SGA A
No treatment history, low LDH, and SGA B/C
No treatment history and high LDH
Prior treatment history and low LDH
Prior treatment history, high LDH, and SGA A
Prior treatment history, high LDH, and SGA B/C
16
20
22
75
40
46
40.4
32.8
10.8
13.7
7.4
4.5
30.45–50.4
5.9–59.61
0–22.5
9.94–17.5
5.21–9.72
2.22–6.76
LDH—lactate dehydrogenase; SGA—Subjective Global Assessment.
independent but similar data sets before it can be considered
valid and reliable. Despite these limitations, recursive
partitioning provides an effective way to classify patients
into distinct and easily understood prognostic groupings. We
also think that restricting the analysis to newly diagnosed
patients (patients with no prior treatment history) would
have been more accurate, since it would have allowed for
evaluation of true overall survival time, that is, time from the
date of diagnosis to the date of death. However, doing so
would have caused a significant reduction in the sample size.
In our study, the survival time was calculated from the day of
first visit at our hospital because the SGA information was
not available at the time of diagnosis for previously treated
patients. This drawback emphasizes the need for conducting
European Journal of Clinical Nutrition
SGA and survival in colorectal cancer
D Gupta et al
40
prospective studies having nutritional information available
since the date of diagnosis. This study, because of its
retrospective nature, relies on data not primarily meant for
research. The SGA, being a subjective method, relies on the
observer’s ability to collect and interpret information, and as
a result, is likely to suffer from observer bias. No assessment
of inter-rater reliability of the users of the SGA was made in
this study. This bias, however, was minimized by restricting
the use of the SGA to well-trained dietitians with an expertise
in the use of this clinical instrument. This study did not
evaluate the effectiveness of nutritional intervention on
survival and future prospective studies should attempt to
address this important research question.
In summary, this study has identified the SGA as a useful
prognostic indicator in patients with advanced colorectal
cancer. However, the importance of the SGA as an independent prognostic indicator needs to be established in
subsequent studies. This study provides a good starting
point for future research in that direction.
Acknowledgements
This study was funded by Cancer Treatment Centers of
America.
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