1310 Articles | JNCI Vol. 100, Issue 18 | September 17, 2008
Colon cancer is the most common gastrointestinal malignancy and
the second-leading cause of cancer death in the United States ( 1 ).
Approximately 80% of colon cancer patients present with resect-
able, localized disease, and in these patients, nodal metastases have
long been recognized as the most important factor predicting
long-term survival ( 1 , 2 ). Nodal involvement is an important deter-
minant in the decision to administer adjuvant chemotherapy, and
with the demonstration over the last decade of highly effective
systemic therapies for colon cancer, it is essential to ensure that all
patients who would benefit from such treatment receive counsel-
ing concerning these therapies and have access to them ( 3 ).
Numerous studies have shown an improvement in disease-
specifi c and overall survival when increasing numbers of lymph
nodes are examined for colon cancer ( 4 – 13 ). The improvement in
outcomes is probably due in part to stage migration or more accu-
rate staging that allows for increased utilization of adjuvant che-
motherapy. The adequacy of lymph node examination for colon
cancer may alternatively be a proxy for other factors that account
for the improvement in outcomes, such as overall surgical tech-
nique and cancer surveillance activities ( 14 ). The suggestion that
there is a direct therapeutic benefi t from a more complete lymph-
adenectomy is controversial ( 14 ).
There has been a considerable effort to determine the minimum
number of nodes that need to be evaluated to deem a patient free of
nodal metastases with reasonable certainty. Estimates have varied
from 6 to 40 lymph nodes ( 5 , 9 , 11 – 15 ); however, numerous studies and
consensus guidelines have suggested that examination of 12 regional
lymph nodes is a reasonable minimum for adequate nodal evaluation
for colon cancer ( 5 , 9 , 11 – 20 ). Despite these fi ndings, population-based
assessments have shown that the majority of patients in the United
States do not have 12 or more nodes examined ( 21 , 22 ).
Affiliations of authors: Cancer Programs, American College of Surgeons,
Chicago, IL (KYB, AKS, DPW, TRR, CYK); Department of Surgery, Feinberg
School of Medicine, Northwestern University, Chicago, IL (KYB, DJB, MST,
DPW); Department of Surgery, Evanston Northwestern Healthcare,
Evanston, IL (MST, DPW); Department of Surgery, University of California,
Los Angeles and VA Greater Los Angeles Healthcare System, Los Angeles,
CA (CYK) .
Correspondence to: Karl Y. Bilimoria, MD, MS, Cancer Programs, American
College of Surgeons, 633 North St Clair Street, 25th Floor, Chicago, IL 60611
(e-mail: email@example.com ).
See “Funding” and “Notes” following “References.”
© The Author 2008. Published by Oxford University Press. All rights reserved.
For Permissions, please e-mail: firstname.lastname@example.org.
Lymph Node Evaluation as a Colon Cancer Quality
Measure: A National Hospital Report Card
Karl Y. Bilimoria , David J. Bentrem , Andrew K. Stewart , Mark S. Talamonti , David P. Winchester ,
Thomas R. Russell , Clifford Y. Ko
Background Examination of 12 or more regional lymph nodes for colon cancer is associated with improved staging
and survival, and the National Quality Forum recently endorsed lymph node examination for colon cancer
as a quality surveillance measure. However, information regarding the extent of hospital compliance with
the 12-node measure in the United States is lacking.
Methods From the National Cancer Data Base, 1296 hospitals that performed 156 789 colectomies in 1996 – 1997 and
2004 – 2005 were identified, and rates of hospital-level compliance (defined as examination of ≥ 12 nodes in
≥ 75% of patients) in these two time periods were compared. Multivariable models were developed to
determine if hospital type, volume, or differences in case mix were associated with 12-node measure
compliance. All statistical tests were two-sided.
Results In 1996 – 1997, 15% of hospitals were compliant with the 12-node measure; in 2004 – 2005 the percentage of
compliant hospitals had increased to 38%. From 1996 – 1997 to 2004 – 2005, 12-node measure compliance
increased at 980 hospitals, remained unchanged at 6 hospitals, and decreased at 310 hospitals. In 2004 –
2005, National Cancer Institute – designated Comprehensive Cancer Centers were more frequently compli-
ant with the 12-node measure than other academic hospitals, Veterans ’ Administration hospitals, or
community hospitals (78.1% versus 52.4%, 53.1%, and 33.7%, respectively, all P < .001), even after adjust-
ment for differences in characteristics of the colon cancer patients at these hospitals.
Conclusions This study provides a national report card of nearly 1300 hospitals showing that more than 60% of institu-
tions failed to achieve a compliance benchmark for the 12-node measure. Considerable improvement is
needed in colon cancer nodal evaluation in the United States.
J Natl Cancer Inst 2008;100: 1310 – 1317
JNCI | Articles 1311
Although a recent and controversial study comparing survival
of colorectal cancer patients based on the hospitals ’ lymph node
examination rates has questioned whether the 12-node measure
improves survival and is an indicator of hospital quality ( 23 – 25 ),
the American College of Surgeons (ACoS), American Society of
Clinical Oncology (ASCO), and the National Comprehensive
Cancer Network (NCCN) harmonized a quality measure requir-
ing resection and pathological examination of 12 or more lymph
nodes for colon cancer ( 16 , 26 , 27 ). Subsequently, the National
Quality Forum (NQF) endorsed the 12-node measure for quality
surveillance ( 28 ). A large, national health-care insurer, United
Healthcare, is already basing referral recommendations for colec-
tomy on a one-time requirement that surgeons provide pathology
reports demonstrating examination of 12 or more lymph nodes for
However, the level of national compliance with the 12-node
measure at the hospital level is unknown. The objective of this
study was to create a national report card of hospital compliance
with the 12-node measure over time by 1) assessing performance
rates according to hospital type and volume, 2) determining what
proportion of hospitals are compliant with the 12-node measure,
and 3) evaluating the association of hospital type and volume with
institutional compliance with the 12-node measure. We hypothe-
sized that the number of hospitals compliant with the 12-node
measure had increased over time and that National Cancer
Institute – designated Comprehensive Cancer Centers (NCI – CCCs)
and high-volume hospitals were more likely to be compliant than
other hospital types.
Data Acquisition and Patient Selection
The National Cancer Data Base (NCDB) is a program of the
ACoS, the Commission on Cancer (CoC), and the American
Cancer Society ( 29 ) that has been collecting data on newly diag-
nosed cancers since 1985 and contains information on over 21
million patients. All CoC-approved hospitals must report all their
cancer cases to the NCDB annually. Based on national incidence
estimates from the American Cancer Society, the NCDB has been
estimated to capture approximately 67% of all new colon cancers
annually ( 1 , 29 ).
One of the fi rst recommendations to examine 12 or more lymph
nodes was put forth by the American Joint Committee on Cancer
(AJCC) in 1997 in the fi fth edition of the Cancer Staging Manual
( 17 ). This recommendation was followed by similar ones from
numerous other major oncology organizations over the next
3 years ( 17 ). Thus, we sought to compare nodal evaluation between
patients diagnosed between January 1, 1996, and December 31,
1997 (prior to the AJCC ’ s recommendation) and patients diagnosed
between January 1, 2004, and December 31, 2005 (most recent data
available). Patients who had a diagnosis of colon cancer in 1996 –
1997 and 2004 – 2005 were identifi ed from the NCDB. We limited
the study to patients who underwent a colectomy for adenocarci-
noma of the colon, excluding patients who had local procedures (eg,
polypectomy) ( 30 , 31 ). Patients were also excluded if they were <18
years old, had nonepithelial lesions, presented with distant metasta-
ses (AJCC Stage IV), had a reported history of prior malignancy, or
had undergone neoadjuvant therapy. Patients were also excluded if
they had undergone surgery at a hospital other than the reporting
facility. Appendiceal, rectal, and rectosigmoid junction cancers
were not included in this study. The inclusion and exclusion criteria
used in this study are identical to those specifi ed in the 12-node
measure by the ACoS, NCCN, ASCO, and NQF. From the
patient-level analytic cohort, patients were aggregated to create a
hospital-level dataset. This study was approved by the Northwestern
University Institutional Review Board.
Hospitals were examined by type and volume. The categories for
the hospital-type variable were NCI – CCC (n = 32), other academic
institutions (academic but not NCI – CCC, n = 231), Veterans ’
Administration (VA) centers (n = 49), and community hospitals (n =
984). The National Cancer Institute designates hospitals as
Comprehensive Cancer Centers based on clinical care, research, and
community outreach criteria. Hospitals in the NCDB are broadly
classified by the CoC into academic and community hospitals ( 32 ).
To be considered as academic, hospitals must be primarily affiliated
with teaching and research institutions, meet annual case volume
requirements, fulfill criteria regarding the capacity to provide a wide
range of cancer-specific services and specialists, meet specified clini-
cal trial accrual standards, perform a range of quality improvement
activities (convening cancer committees and multidisciplinary tumor
CONTEXT AND CAVEATS
Although examination of 12 or more regional lymph nodes in
patients diagnosed with colon cancer is associated with improved
survival, the extent to which hospitals comply with the 12-node
measure was unknown.
Rates of hospital compliance with the 12-node measure (defined as
examination of 12 or more nodes in 75% or more of patients) in
1996 – 1997 and 2004 – 2005 were determined from the National
Cancer Data Base. Logistic regression models were used to deter-
mine associations of hospital characteristics with compliance.
Although the percentage of hospitals compliant with the 12-node
measure increased over time, only 38% of hospitals were
compliant in 2004 – 2005. National Cancer Institute – designated
Comprehensive Cancer Centers and academic hospitals were
more likely than community hospitals to be in compliance with the
Improvement is needed in nodal evaluation of colon cancer
patients in the United States.
The authors only had access to data from hospitals approved by
the Commission on Cancer, which may have biased estimates of
compliance at community hospitals.
From the Editors
1312 Articles | JNCI Vol. 100, Issue 18 | September 17, 2008
boards, carrying out specified annual quality assessment and
improvement projects, and instituting a cancer registry quality con-
trol plan), and offer community outreach programs. A hospital’s
compliance with these standards is reassessed every 3 years through
an on-site evaluation. VA hospitals are those operated by the
Veterans ’ Health Administration. Procedure volume quartiles were
calculated separately for 1996 – 1997 and 2004 – 2005 by ranking all
hospitals in order of increasing mean annual hospital volume of col-
ectomies, and whole-number cut points were chosen that most
closely categorized hospitals into four equal groups.
Only hospitals that reported to the NCDB in both time periods
were included in the hospital-level dataset. Variables representing
the characteristics of an individual hospital included median num-
ber of nodes examined; proportion of patients having at least 12
nodes examined; mean annual hospital colectomy volume; median
age of study patients; percent of study patients per hospital who are
female and nonwhite; and percent of study patients with right-sided
colon cancers, high-grade tumors, and T1, T2, T3, or T4 lesions.
The unit of analysis was the hospital for all analyses in this study.
Adequate lymph node evaluation was defi ned as examination of 12
or more nodes based on consensus guidelines and the specifi cations
for the 12-node measure ( 16 , 26 – 28 ). To measure hospital perfor-
mance with respect to the 12-node measure, we calculated the pro-
portion of patients who had at least 12 nodes examined per hospital
per time period. Thus, performance was defi ned as the proportion of
patients per hospital who had at least 12 nodes examined. A bench-
mark for performance was derived by calculating the mean perfor-
mance level with the 12-node measure for the top-performing
quartile of hospitals in 2004 – 2005. This level, 75%, was considered
the benchmark for compliance. Thus, a hospital was considered com-
pliant with the 12-node measure if examination of at least 12 nodes
occurred for at least 75% of patients at that hospital. Due to statistical
variation, hospitals were considered “statistically compliant” if the
upper limit of the 95% confi dence interval (CI) of the estimate of
their performance rate was greater than or equal to 75%.
Multiple logistic regression models were developed to evaluate the
association of hospital characteristics and compliance with the 12-
node measure. The dependent variable was statistical compliance
(ie, the upper limit of the 95% CI for the estimate of performance
was greater than or equal to 75%) versus non – statistical compli-
ance with the 12-node measure. Variables were introduced into the
model in a forward stepwise fashion and included the hospital-level
characteristics calculated for sex (percent female), median age
(continuous), race/ethnicity (percent nonwhite), T stage (percent
with T1, T2, T3, or T4), tumor grade (percent with poorly differ-
entiated tumors), lesion location along the colon (percent with
right-sided tumors), and hospital type and volume. Hospital type
(NCI – CCC, other academic, VA, or community hospitals) and
volume (as both a continuous and a categorical [quartiles] variable)
were examined separately. Odds ratios with 95% CIs were calcu-
lated and converted to relative risks (RRs) with 95% CIs ( 33 ).
Differences in case mix and 12-node measure performance by
hospital type and volume were compared using analysis of vari-
ance. Median lymph node counts by hospital type and volume were
compared with the Mann – Whitney test. Differences in mean per-
formance rates over time were compared with t tests. The chi-
square test was used to compare compliance by hospital type and
volume. The Bonferroni method was used to correct for multiple
comparisons. The threshold for statistical signifi cance was set at
.05. All P values were based on two-sided tests. Statistical analyses
were performed using SPSS, version 14 (SPSS Inc., Chicago, IL).
Patient and Hospital Characteristics
From the NCDB, we identified 74 669 patients with a diagnosis of
colon cancer in 1996 – 1997 and 82 120 with a diagnosis of colon
cancer in 2004 – 2005 who underwent a colectomy and met the
inclusion criteria for this study. For each time period, the records
for patients were aggregated into a hospital-level file consisting of
1296 hospitals ( Table 1 ). Of these hospitals, 32 (2.5%) were NCI –
CCCs, 231 (18%) were other academic institutions (academic but
not NCI – CCC), 49 (3.8%) were VA medical centers, and 984
(76%) were community hospitals. Hospital characteristics accord-
ing to type and volume derived from data from patients in this
study are described in Table 1 .
Change in Nodal Evaluation Over Time
The median number of nodes examined was calculated for all hos-
pitals and by institution type and volume ( Table 2 ). The median
number of nodes examined per hospital increased from 10 in 1996 –
1997 to 12 in 2004 – 2005 ( P < .001). Increases in the median number
of nodes examined were seen irrespective of hospital type and vol-
ume, with the largest absolute median increase observed for NCI –
CCCs and VA hospitals (increase = 4.5 nodes for both NCI – CCCs
[from 11.5 to 16 nodes] and VA hospitals [from 8.5 to 13 nodes]).
Hospital performance rates were calculated with respect to the
12-node measure as the proportion of patients per hospital who
had at least 12 nodes examined ( Table 2 ). From 1996 – 1997 to
2004 – 2005, the mean hospital performance rate in the United
States increased from 39.8% to 53.8% ( P < .001 based on t test).
An increase was observed in NCI – CCCs, other academic institu-
tions, VA hospitals, and community hospitals, as well as for all
hospital volume quartiles. The largest absolute increase in perfor-
mance rates was observed for NCI – CCCs (20.2%, Table 2 ), and
the smallest absolute increase was observed for community hospi-
tals (13.7%). From 1996 – 1997 to 2004 – 2005, 12-node measure
performance increased at 980 hospitals, remained unchanged at
6 hospitals, and decreased at 310 hospitals.
Based on the statistically derived benchmark for hospital perfor-
mance, a hospital was considered compliant with the 12-node
measure if at least 12 nodes were examined in 75% or more of
patients. A hospital was considered statistically compliant if the
upper limit of the 95% CI for the estimate of performance was
greater than or equal to 75%. In 1996 – 1997, 51 hospitals (3.9%)
were compliant with the 12-node measure and 195 hospitals
(15.0%) were statistically compliant with the measure ( Figure 1, A ,
Table 3 ). In 2004 – 2005, 222 hospitals (17.5%) were compliant with
the 12-node measure and 504 hospitals (38.9%) were statistically
compliant ( Figure 1, B , Table 3 ). From 1996 – 1997 to 2004 – 2005,
JNCI | Articles 1313
282 hospitals (21.8%) improved their performance enough to
become statistically compliant with the 12-node measure.
In 1996 – 1997, statistical compliance with the 12-node measure
was observed at 15.6% of NCI – CCCs, 16.9% of other academic
institutions, 22.4% of VA centers, and 14.2% of community hospi-
tals. In 2004 – 2005, 78.1% of NCI – CCCs, 52.4% of other academic
institutions, 53.1% VA centers, and 33.7% of community hospitals
were statistically complaint ( P < .001 for all hospital types in compari-
son with NCI – CCCs [Figure 1, C] based on chi-square tests), and
corresponding absolute differences between the two time periods
were 62.5%, 35.5%, 30.7%, and 19.5%, respectively. The absolute
improvement in the proportion of compliant hospitals was 21.0% at
highest volume, 17.0% at high-volume, 23.4% at moderate-volume,
and 15.6% at low-volume hospitals ( Table 3 ).
Factors Associated With Compliance
A multivariable logistic regression model was developed to examine
the association of hospital factors and statistical compliance with the
12-node measure while adjusting for differences in hospital colon can-
cer patient populations ( Table 4 ). Hospital type was the factor most
strongly associated with statistical compliance. Compared with com-
munity hospitals, NCI – CCCs (RR = 2.22, 95% CI = 1.65 to 2.60),
Table 2 . Hospital-level median lymph node counts and 12-node performance rates: 1996 – 1997 versus 2004 – 2005*
Lymph nodes examined, median (IQR) Hospital performance rate, %
1996 – 1997 2004 – 20051996 – 19972004 – 2005
Median IQRMedianIQR P value † Median IQR MedianIQR P value †
Hospital type ‡
NCI – CCC
108.0 – 10.0 12.0 * 10.0 – 15.0 <.00139.8 40.7 – 66.953.8 * 26.1 – 53.6 <.001
10.0 – 14.0
9.0 – 13.0
6.0 – 10.0
7.0 – 12.0
14.5 – 20.0
11.5 – 20.0
10.0 – 16.5
10.0 – 19.5
45.6 – 56.0
45.1 – 49.3
29.3 – 40.1
36.8 – 39.2
66.9 – 75.2
58.7 – 63.1
45.7 – 57.9
50.4 – 53.0
9.0 – 13.0
8.0 – 12.0
7.0 – 12.0
7.0 – 11.0
12.0 – 16.0
10.0 – 15.5
10.0 – 15.0
9.0 – 13.5
42.3 – 45.9
39.2 – 43.0
36.0 – 40.3
33.7 – 38.4
60.1 – 63.4
52.6 – 57.0
50.9 – 55.3
43.2 – 48.1
* Performance rate is the percentage of patients per hospital who had at least 12 nodes examined. IQR = interquartile range; NCI – CCC = National Cancer Institute
Comprehensive Cancer Center; VA = Veterans ’ Administration.
† In comparison with 1996 – 1997 using Mann – Whitney test for median node counts and analysis of variance for performance rates.
‡ NCI – CCCs are designated by the NCI. Other academic hospitals are designated as academic centers by the Commission on Cancer but do not include
NCI – CCCs. VA hospitals include those facilities operated by the Veterans’ Health Administration. Community hospitals are designated by the Commission on
Cancer as nonteaching/research institutions.
Table 1 . Hospitals and their colon cancer patient characteristics by hospital type and volume (2004 – 2005) *
Hospital type † Hospital volume quartiles
NCI – CCC
(28 – 42 cases/y)
(17 – 27 cases/y)
No. of hospitals
Female patients (%)
Median age (years)
Right side (%)
* Hospital characteristics derived from data from patients in this study. NCI – CCC = National Cancer Institute Comprehensive Cancer Center; VA = Veterans’ Administration.
† NCI – CCC are designated by the NCI. Other academic hospitals are designated as academic centers by the Commission on Cancer but do not include NCI – CCCs.
VA hospitals include those facilities operated by the Veterans ’ Health Administration. Community hospitals are designated by the Commission on Cancer as
‡ P < .05 in comparison with NCI – CCCs or highest volume hospitals using analysis of variance for mean percentages and Mann – Whitney for medians.
1314 Articles | JNCI Vol. 100, Issue 18 | September 17, 2008
other academic institutions (RR = 1.53, 95% CI = 1.30 to 1.75), and
VA hospitals (RR = 1.90, 95% CI = 1.27 to 2.40) were more likely to
be statistically compliant with the 12-node measure. Average annual
hospital colectomy volume was also examined, but volume was not
statistically significantly associated with 12-node measure compliance,
either as a continuous or as a categorical variable ( Table 4 , Figure 3 ).
The expected values for performance (ie, the predicted rate of
examination of at least 12 nodes) from the regression model were
used to assess compliance with the 12-node measure. Adjustment
for differences in colorectal cancer patient populations between
hospitals did not result in any additional hospitals becoming compli-
ant with the 12-node measure (the expected value for performance
did not increase above the compliance threshold for any hospital).
Moreover, the expected values were relatively unaffected for all
hospitals by adjustment for patient characteristics (data not shown).
In examining treatment of colon cancer patients who underwent
colectomy at 1296 hospitals using data from the NCDB, we found
that although the proportion of compliant hospitals (those that
examined at least 12 lymph nodes in at least 75% of patients)
increased considerably from 1996 – 1997 to 2004 – 2005, the major-
ity of hospitals failed to comply with the 12-node measure. To our
knowledge, this is the first study to examine the 12-node measure
at the hospital level and provide a hospital report card for regional
lymph node evaluation for colon cancer in the United States.
Prior studies conducted at the level of individual patients have
demonstrated that only approximately 37% to 50% of colon can-
cer patients in the United States have 12 or more nodes
Figure 1 . Hospital 12-node measure performance. Dots and gray bars
represent estimates for percentage of patients with 12 or more nodes
examined in a given hospital, with 95% confi dence intervals.
The horizontal line represents the 75% benchmark for compliance. A )
All hospitals, 1996 – 1997. B ) All hospitals, 2004 – 2005. C ) National
Cancer Institute – designated Compre hensive Cancer Centers,
2004 – 2005.
Figure 2 . Change in individual hospitals ’ performance rates with the
12-node measure from 1996 – 1997 to 2004 – 2005 at National Cancer
Institute – designated Comprehensive Cancer Centers (NCI – CCCs). Each
gray circle represents one of the 32 (NCI – CCCs) in this study.
JNCI | Articles 1315
examined ( 21 , 34 ). At the hospital level, we found that the overall
performance rate (proportion of patients at a hospital who had at
least 12 nodes examined) increased by a statistically signifi cant
extent from 1996 – 1997 to 2004 – 2005. This increase was observed
regardless of hospital type or volume. This improvement is pre-
sumably due to multiple factors that have increased awareness of
the importance of lymph node examination for colon cancer. Nodal
evaluation is likely to improve further with the recent development
of a 12-node measure by multiple national oncology organizations
and as physicians and hospitals recognize that a requirement to
examine 12 or more nodes may affect referral and reimbursement.
The primary objective of this study was to determine the num-
ber of hospitals that are compliant with the 12-node measure. We
considered a hospital statistically compliant if the upper limit of
the 95% CI for the estimate of its performance was greater than or
equal to 75% to preclude categorizing hospitals as noncompliant
simply based on statistical variation. The percentage of statistically
compliant hospitals increased from 15.0% in 1996 – 1997 to 38.9%
in 2004 – 2005. Overall, national compliance with a 12-node mea-
sure remains low, possibly because some question whether the 12-
node measure is important for staging and is an indicator of
hospital quality. However, the increase in performance over time,
particularly at NCI – CCCs, is encouraging and demonstrates that
improved compliance with the 12-node measure is feasible.
In examining the association of hospital factors with compli-
ance with the 12-node measure, we found that the rate of statistical
compliance for NCI – CCCs (78%) was higher than that for other
hospital types. Previous studies have shown that colon cancer
patients treated at high-volume specialized cancer centers have
better long-term outcomes (eg, recurrence and survival) than those
Table 4 . Hospital factors associated with 12-node measure statistical compliance (2004 – 2005) *
(95% CI) P value
Adjusted RR †
(95% CI) P value
Hospital type ‡
NCI – CCC
Hospital volume (quartiles)
2.32 (1.79 to 2.65)
1.55 (1.34 to 1.76)
1.57 (1.15 to 1.98)
2.22 (1.65 to 2.60)
1.53 (1.30 to 1.75)
1.90 (1.27 to 2.40)
1.19 (0.98 to 1.40)
0.98 (0.79 to 1.19)
1.10 (0.90 to 1.32)
1.21 (0.99 to 1.44)
1.02 (0.82 to 1.24)
1.16 (0.94 to1.38)
* Hospitals were considered statistically compliant if the upper limit of the 95% confidence interval of the estimate of their performance rate (proportion of
patients with 12 or more nodes examined) was greater than or equal to 75%. RR = relative risk; CI = confidence interval; NCI – CCC = National Cancer Institute
Comprehensive Cancer Center; VA = Veterans’ Administration.
† Multivariable logistic regression model evaluating the association between hospital type/volume and compliance with the 12-node measure while adjusting for
sex, age, race/ethnicity, lesion location along the colon, T classification, and tumor grade. Hospital type and hospital volume were examined in separate models.
Relative risk >1.0 indicates a higher likelihood of compliance with the 12-node measure.
‡ NCI – CCCs are designated by the NCI. Other academic hospitals are designated as academic centers by the Commission on Cancer, but do not include NCI –
CCCs. VA hospitals include those facilities operated by the Veterans ’ Health Administration. Community hospitals are designated by the Commission on Cancer
as nonteaching/research institutions.
Table 3 . Hospital-level compliance with the 12-node measure: 1996 – 1997 versus 2004 – 2005 *
Compliant hospitals † Statistically compliant hospitals ‡
1996 – 1997, No. (%)2004 – 2005, No. (%)1996 – 1997, No. (%) 2004 – 2005, No. (%)
NCI – CCC
Hospital volume (quartiles)
51 (3.9) 222 (17.1) 195 (15.0) 504 (38.9)
* NCI – CCCs are designated by the NCI. Other academic hospitals are designated as academic centers by the Commission on Cancer, but do not include
NCI – CCCs. VA hospitals include those facilities operated by the Veterans ’ Health Administration. Community hospitals are designated by the Commission on
Cancer as nonteaching/research institutions. NCI – CCC = National Cancer Institute Comprehensive Cancer Center; VA = Veterans ’ Administration.
† Estimate of hospital performance rate (ie, percentage of patients with 12 or more nodes examined) is at least 75%.
‡ Upper limit of the 95% confidence interval for estimate of hospital performance rate is at least 75%.
1316 Articles | JNCI Vol. 100, Issue 18 | September 17, 2008
treated at low-volume community hospitals ( 35 , 36 ). Better lymph
node examination rates at NCI – CCCs and other academic hospi-
tals may in part explain this disparity.
Because hospitals care for varying proportions of elderly
patients and those with left-sided tumors, both of which are associ-
ated with lower nodal counts, it has been suggested ( 37 ) that a 12-
node measure that compares hospitals must adjust for differences
in the patient populations at various hospitals and hospital types.
To examine the effect of patient characteristics on the rate of
lymph node examination, the predicted rates were calculated as a
function of the multivariable logistic regression model. We found
that patient characteristics did not affect the proportion of hospi-
tals meeting the compliance benchmark. Thus, these differences
among hospitals do not appreciably affect evaluation of compliance
rates, and comparing hospitals without adjustment for case mix is
likely appropriate. Moreover, adjustment for differences in patient
populations is, in principle, not needed for process measures,
because adherence with the measure is either met or not met.
The large number of hospitals in the United States that are not
compliant with the 12-node measure may indicate to some that 12
lymph nodes is not an appropriate threshold for a quality indicator
for colon cancer because it is either not attainable or unimportant.
The rate of adherence with a requirement to evaluate 12 regional
lymph nodes is dependent on the extent of surgical resection, the
thoroughness of pathological examination, and multiple patient fac-
tors ( 38 – 40 ). However, large institutions and entire geographic
areas have been able to dramatically improve nodal examination
rates for colon cancer. In a study of eight NCCN hospitals, Rajput
et al. ( 41 ) found that during 2005 – 2006, 89% of colectomy patients
had 12 or more nodes examined. Similarly, emphasizing the impor-
tance of nodal evaluation has resulted in a substantial improvement
in lymph node examination in the Canadian province of Ontario
( 42 ). If large institutions or an entire province can improve lymph
node examination rates, then it is likely that evaluation of 12 nodes
is a reasonable benchmark for colon cancer, and increasing aware-
ness of the importance of nodal evaluation through multidisciplinary
initiatives can improve lymph node examination for colon cancer.
Hospital-specifi c performance for the 12-node measure will be
reported to all 1450 individual facilities currently reporting to the
NCDB. The reporting process is meant to increase awareness of
the importance of adequate nodal evaluation and allow institutions
to privately compare their performance with a large national sam-
ple of hospitals. Hospitals with outlying nodal evaluation rates can
be identifi ed and notifi ed so that these centers can initiate internal
quality improvement initiatives.
The potential limitations of this study should be noted. First,
there is considerable statistical variation in 12-node measure perfor-
mance rates among extremely low-volume hospitals, and an argu-
ment could be made to exclude hospitals that performed a small
number of colectomies per year. However, when we excluded very
low – volume hospitals, the proportion of compliant hospitals did not
change substantially (data not shown). Second, only hospitals
approved by the CoC report to the NCDB. These hospitals may
exhibit a higher level of specialization than institutions that are not
approved by the CoC. Thus, if all hospitals in the United States
were examined, the differences in 12-node measure compliance
between NCI – CCCs and community hospitals would likely be aug-
mented. Finally, the benchmark for compliance of 75% was derived
statistically by calculating the mean performance rate of hospitals in
the top quartile of lymph node examination rates in 2004 – 2005.
Some have suggested that the quality threshold should be the per-
formance rate of the hospitals in the 90th percentile ( 43 ). Although
there are numerous methods to derive quality benchmarks, 75%
serves as a statistically derived, conservative, and achievable starting
point. Establishment of a benchmark should be considered an itera-
tive process as hospitals improve and science progresses.
This study presents a hospital report card for regional lymph node
examination for colon cancer in the United States. Nearly two-thirds
of hospitals failed to meet the benchmark for compliance with the
measure in 2004 – 2005. Considerable improvement in lymph node
examination rates is needed, irrespective of hospital type. The mea-
sure may be used to assess physicians and/or hospital performance in
the future, and a surveillance period will allow hospitals to focus on
the issue and improve their performance before they may be held
accountable. The 12-node measure offers an opportunity to improve
the quality of care for colon cancer patients in the United States.
1. Jemal A , Siegel R , Ward E , et al . Cancer statistics, 2008 . CA Cancer J Clin .
2008 ; 58 ( 2 ): 71 – 96 .
2. Dukes C . The classifi cation of cancer of the rectum . J Pathol Bacteriol .
1932 ; 25 : 325 – 332 .
3. Benson AB III . New approaches to the adjuvant therapy of colon cancer .
Oncologist . 2006 ; 11 ( 9 ): 973 – 980 .
4. Berger AC , Sigurdson ER , LeVoyer T , et al . Colon cancer survival is
associated with decreasing ratio of metastatic to examined lymph nodes .
J Clin Oncol . 2005 ; 23 ( 34 ): 8706 – 8712 .
5. Caplin S , Cerottini JP , Bosman FT , Constanda MT , Givel JC . For
patients with Dukes ’ B (TNM Stage II) colorectal carcinoma, examination
of six or fewer lymph nodes is related to poor prognosis . Cancer . 1998 ;
83 ( 4 ): 666 – 672 .
6. Chen SL , Bilchik AJ . More extensive nodal dissection improves survival
for stages I to III of colon cancer: a population-based study . Ann Surg .
2006 ; 244 ( 4 ): 602 – 610 .
7. Cianchi F , Palomba A , Boddi V , et al . Lymph node recovery from colorec-
tal tumor specimens: recommendation for a minimum number of lymph
nodes to be examined . World J Surg . 2002 ; 26 ( 3 ): 384 – 389 .
8. Cserni G , Vinh-Hung V , Burzykowski T . Is there a minimum number of
lymph nodes that should be histologically assessed for a reliable nodal stag-
ing of T3N0M0 colorectal carcinomas? J Surg Oncol . 2002 ; 81 ( 2 ): 63 – 69 .
Figure 3 . Scatterplot showing relationship between annual average
colectomy volume and hospital 12-node measure performance.
JNCI | Articles 1317
9. Goldstein NS . Lymph node recoveries from 2427 pT3 colorectal resec-
tion specimens spanning 45 years: recommendations for a minimum
number of recovered lymph nodes based on predictive probabilities . Am J
Surg Pathol . 2002 ; 26 ( 2 ): 179 – 189 .
10. Johnson PM , Porter GA , Ricciardi R , Baxter NN . Increasing negative
lymph node count is independently associated with improved long-term
survival in stage IIIB and IIIC colon cancer . J Clin Oncol . 2006 ; 24 ( 22 ):
3570 – 3575 .
11. Le Voyer TE , Sigurdson ER , Hanlon AL , et al . Colon cancer survival
is associated with increasing number of lymph nodes analyzed: a second -
ary survey of intergroup trial INT-0089 . J Clin Oncol . 2003 ; 21 ( 15 ):
2912 – 2919 .
12. Prandi M , Lionetto R , Bini A , et al . Prognostic evaluation of stage B colon
cancer patients is improved by an adequate lymphadenectomy: results of a
secondary analysis of a large scale adjuvant trial . Ann Surg . 2002 ;
235 ( 4 ): 458 – 463 .
13. Swanson RS , Compton CC , Stewart AK , Bland KI . The prognosis of
T3N0 colon cancer is dependent on the number of lymph nodes exam-
ined . Ann Surg Oncol . 2003 ; 10 ( 1 ): 65 – 71 .
14. Chang GJ , Rodriguez-Bigas MA , Skibber JM , Moyer VA . Lymph node
evaluation and survival after curative resection of colon cancer: systematic
review . J Natl Cancer Inst . 2007 ; 99 ( 6 ): 433 – 441 .
15. Joseph NE , Sigurdson ER , Hanlon AL , et al . Accuracy of determining
nodal negativity in colorectal cancer on the basis of the number of nodes
retrieved on resection . Ann Surg Oncol . 2003 ; 10 ( 3 ): 213 – 218 .
16. National Comprehensive Cancer Network (NCCN) . ASCO/NCCN
Quality Measures: Breast and Colorectal Cancers . http://www.nccn.org/
professionals/quality_measures/default.asp . Accessed April 26, 2007 .
17. American Joint Committee on Cancer . Cancer Staging Manual . 5th ed.
Chicago, IL : Springer ; 1997 .
18. Hammond ME , Fitzgibbons PL , Compton CC , et al. College of American
Pathologists Conference XXXV: solid tumor prognostic factors-which,
how and so what? Summary document and recommendations for imple-
mentation. Cancer Committee and Conference Participants . Arch Pathol
Lab Med . 2000 ; 124 ( 7 ): 958 – 965 .
19. Nelson H , Petrelli N , Carlin A , et al . Guidelines 2000 for colon and rectal
cancer surgery . J Natl Cancer Inst . 2001 ; 93 ( 8 ): 583 – 596 .
20. National Comprehensive Cancer Network (NCCN). Clinical Practice
Guidelines in Oncology: Colon Cancer Version 1 . 2008 ;
21. Baxter NN , Virnig DJ , Rothenberger DA , Morris AM , Jessurun J , Virnig
BA . Lymph node evaluation in colorectal cancer patients: a population-
based study . J Natl Cancer Inst . 2005 ; 97 ( 3 ): 219 – 225 .
22. Bilimoria KY , Stewart AK , Palis BE , Bentrem DJ , Talamonti MS , Ko CY .
Adequacy and importance of lymph node evaluation for colon cancer in
the elderly . J Am Coll Surg . 2008 ; 206 ( 2 ): 247 – 254 .
23. Wong SL , Ji H , Hollenbeck BK , Morris AM , Baser O , Birkmeyer JD .
Hospital lymph node examination rates and survival after resection for
colon cancer . JAMA . 2007 ; 298 ( 18 ): 2149 – 2154 .
24. Bilimoria KY , Stewart AK , Edge S , Ko CY . Lymph node examination
rate, survival rate, and quality of care in colon cancer . JAMA . 2008 ; 299 ( 8 ):
896 – 897 .
25. Peters E , Nagtegaal I , van de Velde C , Krieken J . Lymph node examina-
tion rate, survival rate, and quality of care in colon cancer . JAMA . 2008 ;
299 ( 8 ): 896 – 897 .
26. American Society of Clinical Oncology (ASCO) . ASCO-NCCN Quality
Measures . http://www.asco.org/portal/site/ASCO/menuitem.
5d1b4bae73a 9104ce277e89a320041a0/?vgnextoid = 1b08fcd4eb46c0-
10VgnVCM100000ed730ad1RCRD . Accessed April 26, 2007 .
27. Commission on Cancer (CoC) . National Quality Forum Endorsed
Commission on Cancer Measures for Quality of Cancer Care for Breast
and Colorectal Cancers . http://www.facs.org/cancer/qualitymeasures.
html . Accessed April 26, 2007 .
28. National Quality Forum Endorses Consensus Standards for Diagnosis and
Treatment of Breast & Colorectal Cancer . http://22.214.171.124/pdf/
news/prbreast-colon03-12-07.pdf . Accessed December 27, 2007 .
29. Bilimoria KY , Stewart AK , Winchester DP , Ko CY . The National Cancer
Data Base: a powerful initiative to improve cancer care in the United
States . Ann Surg Oncol . 2008 ; 15 ( 3 ): 683 – 690 .
30. Standards of the Commission on Cancer Volume II: Registry Operations and
Data Standards . Commission on Cancer ; 1998
31. Facility Oncology Registry Data Standards . Chicago, IL : Commission on
Cancer ; 2004 .
32. Commission on Cancer: Program Standards . Chicago, IL : American College
of Surgeons ; 2006 .
33. Zhang J , Yu KF . What’s the relative risk? A method of correcting the
odds ratio in cohort studies of common outcomes . JAMA . 1998 ; 280 ( 19 ):
1690 – 1691 .
34. Bilimoria KY , Palis B , Stewart AK , et al . Impact of tumor location
on nodal evaluation for colon cancer . Dis Colon Rectum . 2008 ; 51 ( 2 ):
154 – 161 .
35. Schrag D , Cramer LD , Bach PB , Cohen AM , Warren JL , Begg CB .
Infl uence of hospital procedure volume on outcomes following surgery for
colon cancer . JAMA . 2000 ; 284 ( 23 ): 3028 – 3035 .
36. Rogers SO Jr , Wolf RE , Zaslavsky AM , Wright WE , Ayanian JZ . Relation
of surgeon and hospital volume to processes and outcomes of colorectal
cancer surgery . Ann Surg . 2006 ; 244 ( 6 ): 1003 – 1011 .
37. Baxter N , Rosen L . Open letter to the National Quality Forum regarding the
12 Node Measure on behalf of the American Society Colon and Rectal Surgeons .
2007 ; http:// www.qualityforum.org/pdf/cancer . Accessed March 13, 2008 .
38. Rieger NA , Barnett FS , Moore JW , et al . Quality of pathology reporting
impacts on lymph node yield in colon cancer . J Clin Oncol . 2007 ; 25 ( 4 ): 463
author reply 463 – 464 .
39. Simunovic M , Baxter NN . Lymph node counts in colon cancer surgery:
lessons for users of quality indicators . JAMA . 2007 ; 298 ( 18 ): 2194 – 2195 .
40. Ostadi MA , Harnish JL , Stegienko S , Urbach DR . Factors affecting the
number of lymph nodes retrieved in colorectal cancer specimens . Surg
Endosc . 2007 ; 21 ( 12 ): 2142 – 2146 .
41. Rajput A , Skibber JM , Engstrom PF , et al . Meeting the 12 lymph node
benchmark in colorectal cancer surgery: a comparison of NCCN and
SEER data . J Clin Oncol . 2007 ; 25 ( 18S ): 4015 .
42. Cancer Care Ontario . http://www.cancercare.on.ca/ . Accessed May 23, 2007 .
43. Weissman NW , Allison JJ , Kiefe CI , et al . Achievable benchmarks of care:
the ABCs of benchmarking . J Eval Clin Pract . 1999 ; 5 ( 3 ): 269 – 281 .
American College of Surgeons, Clinical Scholars in Residence program (to
K.Y.B.) ; American Cancer Society (ACS IRG 93-037-12 to D.J.B.) ; National
Cancer Institute (NCI-60058-NE to C.Y.K.) .
The funding sources had no role in the design of the study; the collection,
analysis, and interpretation of the data; the decision to submit the manuscript
for publication; and the writing of the manuscript.
Manuscript received February 28 , 2008 ; revised June 27 , 2008 ; accepted
July 16 , 2008 .