You are on page 1of 11

Original Investigation | Gastroenterology and Hepatology

External Validation of the Oakland Score to Assess Safe Hospital Discharge


Among Adult Patients With Acute Lower Gastrointestinal Bleeding in the US
Kathryn Oakland, MD; Sandeepkumar Kothiwale, PhD; Tyler Forehand; Edmund Jackson, PhD; Cliff Bucknall, MD; Michael S. L. Sey, MD, MPH; Siddharth Singh, MD, MS;
Vipul Jairath, MD, PhD; Jonathan Perlin, MD

Abstract Key Points


Question Is the Oakland Score a valid
IMPORTANCE Lower gastrointestinal bleeding (LGIB), which manifests as blood in the colon or
tool for assessing the risk of adverse
anorectum, is a common reason for hospitalization. In most patients, LGIB stops spontaneously with
outcomes among a large population of
no in-hospital intervention. A risk score that could identify patients at low risk of experiencing
adult patients with acute lower
adverse outcomes could help improve the triage process and allow greater numbers of patients to
gastrointestinal bleeding in the
receive outpatient management of LGIB.
United States?

OBJECTIVE To externally validate the Oakland Score, which was previously developed using a score Findings In this prognostic study of
threshold of 8 points to identify patients with LGIB who are at low risk of adverse outcomes. 38 067 adult patients who were
hospitalized with acute lower
DESIGN, SETTING, AND PARTICIPANTS This multicenter prognostic study was conducted in 140 gastrointestinal bleeding, the Oakland
US hospitals in the Hospital Corporation of America network. A total of 46 179 adult patients (aged Score consistently identified patients
ⱖ16 years) admitted to the hospital with a primary diagnosis of LGIB between June 1, 2016, and who were at low risk of experiencing
October 15, 2018, were initially identified using diagnostic codes. Of those, 51 patients were excluded adverse outcomes. Extension of the
because they were more likely to have upper gastrointestinal bleeding, leaving a study population of Oakland Score threshold from 8 points
46 128 patients with LGIB. For the statistical analysis of the Oakland Score, an additional 8061 or lower to 10 points or lower for
patients were excluded because they were missing data on Oakland Score components or clinical assessing whether a patient can safely
outcomes, resulting in 38 067 patients included in the analysis. The study used area under the be discharged from the hospital could
receiver operating characteristic curves with 95% CIs for external validation of the model. Sensitivity detect more patients who have a low
and specificity were calculated for each score threshold (ⱕ8 points, ⱕ9 points, and ⱕ10 points). risk of experiencing adverse outcomes
Data were analyzed from October 16, 2018, to September 4, 2019. and potentially avoid hospitalization in
17.8% of patients whose conditions
MAIN OUTCOMES AND MEASURES Identification of patients who met the criteria for safe could safely be managed on an
discharge from the hospital and comparison of the performance of 2 score thresholds (ⱕ8 points vs outpatient basis.
ⱕ10 points). Safe discharge was defined as the absence of blood transfusion, rebleeding, hemostatic
Meaning The findings of this study
intervention, hospital readmission, and death.
suggest that adoption of the Oakland
Score into the triage process for patients
RESULTS Among 46 128 adult patients with LGIB, the mean (SD) age was 70.1 (16.5) years; 23 091
presenting to hospitals in the US could
patients (50.1%) were female. Of those, 22 074 patients (47.9%) met the criteria for safe discharge
reduce the rate of hospitalization among
from the hospital. In this group, the mean (SD) age was 67.9 (18.1) years, and 11 056 patients (50.1%)
patients with acute lower
were female. In the statistical analysis of the Oakland Score, which included only the 38 067 patients
gastrointestinal bleeding.
with complete data, the area under the receiver operating characteristic curve for safe discharge was
0.87 (95% CI, 0.87-0.87). An Oakland Score threshold of 8 points or lower identified 3305 patients
(8.7%), with a sensitivity and specificity for safe discharge of 98.4% and 16.0%, respectively. + Supplemental content
Extension of the Oakland Score threshold to 10 points or lower identified 6770 patients (17.8%), with Author affiliations and article information are
a sensitivity and specificity for safe discharge of 96.0% and 31.9%, respectively. listed at the end of this article.

CONCLUSIONS AND RELEVANCE In this study, the Oakland Score consistently identified patients
with acute LGIB who were at low risk of experiencing adverse outcomes and whose conditions could

(continued)

Open Access. This is an open access article distributed under the terms of the CC-BY License.

JAMA Network Open. 2020;3(7):e209630. doi:10.1001/jamanetworkopen.2020.9630 (Reprinted) July 7, 2020 1/11

Downloaded From: https://jamanetwork.com/ by a Non-Human Traffic (NHT) User on 12/05/2021


JAMA Network Open | Gastroenterology and Hepatology Validation of a Score to Assess Patients With Lower Gastrointestinal Bleeding

Abstract (continued)

safely be managed without hospitalization. The score threshold to identify low-risk patients could be
extended from 8 points or lower to 10 points or lower to allow identification of a greater proportion
of low-risk patients.

JAMA Network Open. 2020;3(7):e209630. doi:10.1001/jamanetworkopen.2020.9630

Introduction
Lower gastrointestinal bleeding (LGIB) is a common presentation in the emergency departments of
hospitals worldwide. In comparison with upper gastrointestinal bleeding (UGIB), LGIB is likely to have
a less severe course. Compared with patients with UGIB, patients with LGIB are less likely to present
with hemorrhagic shock or require red blood cell (RBC) transfusions or interventions to treat
bleeding, and in-hospital mortality rates among patients with LGIB are lower.1 Acute LGIB typically
presents with bright red rectal bleeding or blood clots from the rectum,1 whereas the presenting
features of UGIB include hematemesis, coffee-ground emesis, and melena. Unlike patients with
UGIB, for which risk stratification scores, such as the Rockall2 and Glasgow-Blatchford3 scores, are
used, patients with LGIB have no equivalent risk score tool available.
In 2016, the American College of Gastroenterology recommended that risk assessment be
performed but did not endorse the use of any single tool.4 Since the publication of this guideline, the
Oakland Score5 was developed within a nationally representative sample of patients in the United
Kingdom. Rather than calculating a risk score for death or inpatient intervention, the Oakland Score
was designed to identify patients who were at low risk of experiencing adverse outcomes and whose
conditions could safely be managed without hospitalization. Despite limited external validation of
the Oakland Score,5,6 national guidelines in the United Kingdom have recently recommended use of
the tool for the triage of patients with acute LGIB.7 Therefore, the aim of this study was to externally
validate the Oakland Score in a large population of patients with acute LGIB from the United States
and compare the performance of the Oakland Score at 2 score thresholds (ⱕ8 points vs ⱕ10 points).

Methods
Patients with acute LGIB were identified from 140 hospitals in the Hospital Corporation of America
(HCA) network across the United States. The study was approved by the HCA Research Review
Council. Written informed consent to use unidentified patient data for clinical improvement
purposes was obtained from all participants, as written informed consent is built into the overall
informed consent process when a patient agrees to receive treatment or diagnostic testing at any
HCA hospital. The study used data that are routinely collected for quality improvement purposes,
collected no patient identifiers, and involved no new clinical intervention. This study followed the
Transparent Reporting of a Multivariable Prediction Model for Individual Prognosis or Diagnosis
(TRIPOD) reporting guideline8 for prognostic studies.
Adult patients (aged ⱖ16 years) who were admitted to the hospital with acute LGIB between
June 1, 2016, and October 15, 2018, were identified retrospectively using codes from the
International Classification of Diseases, Tenth Revision, Clinical Modification (ICD-10-CM)9 that were
consistent with a primary diagnosis of LGIB (eMethods in the Supplement). In 2018, the HCA network
of US hospitals comprised 179 general and acute care hospitals in 20 states that delivered care to
patients who paid for care directly or through Medicare and Medicaid programs, managed care plans,
or private insurance. Clinical data from HCA facilities have been stored in a single data warehouse
since 2011. For each patient encounter, these data are automatically collected in real time from
electronic health records (EHRs) and consolidated in the data warehouse, from which longitudinal
EHRs for each patient can be extracted. These EHRs contain data on current hospitalizations as well

JAMA Network Open. 2020;3(7):e209630. doi:10.1001/jamanetworkopen.2020.9630 (Reprinted) July 7, 2020 2/11

Downloaded From: https://jamanetwork.com/ by a Non-Human Traffic (NHT) User on 12/05/2021


JAMA Network Open | Gastroenterology and Hepatology Validation of a Score to Assess Patients With Lower Gastrointestinal Bleeding

as comorbidities reported during previous health care events. Hospitals in the HCA network were
eligible to participate in the present study if they had an emergency department, routinely admitted
patients with emergency conditions, and had comprehensive EHRs to allow record linkage of clinical
outcomes.
Patients provisionally identified as having LGIB who received endoscopic hemostasis during
esophagogastoduodenoscopy (using Current Procedural Terminology [CPT] code 43255) were
excluded because they were more likely to have UGIB. Data on demographic characteristics,
comorbidities, medications, vital signs, blood test results, treatments, and outcomes were collected
for each patient. Heart rate (measured in beats per minute), systolic blood pressure (measured in
mm Hg), hemoglobin concentration (measured in g/L), platelet count (measured in 109/L), white
blood cell count (measured in 109/L), blood urea nitrogen level (measured in mg/dL), creatinine level
(measured in mg/dL), albumin level (measured in g/dL), and international normalized ratio were
extracted from the results of each patient’s first recorded set of vital signs and blood tests. Previous
hospital admission with LGIB was identified through ICD-10-CM codes for LGIB that were recorded at
any point in the patient’s longitudinal EHR.
Comorbidities were classified using codes from the International Classification of Diseases,
Ninth Revision, Clinical Modification (ICD-9-CM) that were consistent with cancer and cardiovascular,
renal, and liver diseases (eMethods in the Supplement). Patient receipt of oral antiplatelet or
anticoagulant medications was identified using the Standard Industrial Classification codes M9L and
M9P, and these data were extracted only if receipt of the medications appeared in the patient’s
regular medication records. To identify medical procedures received, the following CPT codes were
used: codes 45378 to 45398 for inpatient colonoscopy, code 36430 for RBC transfusion, code 37242
for mesenteric embolization, and codes specific to small bowel, colon, or rectum resection for
abdominal surgery for bleeding (full list of CPT codes available in eMethods in the Supplement).
The primary outcome was the composite outcome of safe discharge from the hospital,5 with
safe discharge defined as the absence of all of the following after hospital presentation: in-hospital
rebleeding (defined as a decrease in hematocrit concentrations of 20% or more after 24 hours of
clinical stability10); RBC transfusion; therapeutic colonoscopy, mesenteric embolization, or
laparotomy for bleeding; in-hospital death (all causes); and readmission with subsequent LGIB within
28 days. We were able to identify patients who were readmitted to the index hospital or another
hospital in the HCA network using ICD-10-CM codes (eMethods in the Supplement) but were not able
to detect patients who were readmitted to hospitals outside of the HCA network.

Oakland Score
The Oakland Score was originally derived from prospective data obtained from 2336 patients with
LGIB from 143 hospitals in the United Kingdom in 2015 (eMethods in the Supplement), with the aim
of identifying patients at low risk of experiencing adverse outcomes.5 The total score contains 7
variables (age, sex, previous hospital admission with LGIB, digital rectal examination results, heart
rate, systolic blood pressure, and hemoglobin concentration) and ranges from 0 to 35 points, with
higher scores indicating greater risk of experiencing an adverse outcome (Table 1).
Data on the Oakland Score variables were extracted from patient EHRs. Digital rectal
examination findings were not available, so this variable was omitted from the score calculations.
When calculating a total Oakland Score, hemoglobin concentration and systolic blood pressure are
assigned the highest point weightings (0-22 points and 0-5 points, respectively). Points ascribed to
digital rectal examination results are either 1 point if blood is present or 0 points if blood is absent.
The remaining variables were used to calculate an Oakland Score for each patient with LGIB.

Statistical Analysis
Any patients with missing data on score component variables or clinical outcomes were excluded
from the statistical analysis of the Oakland Score. The ability of the Oakland Score to predict
in-hospital rebleeding, RBC transfusion, therapeutic intervention to control bleeding, in-hospital

JAMA Network Open. 2020;3(7):e209630. doi:10.1001/jamanetworkopen.2020.9630 (Reprinted) July 7, 2020 3/11

Downloaded From: https://jamanetwork.com/ by a Non-Human Traffic (NHT) User on 12/05/2021


JAMA Network Open | Gastroenterology and Hepatology Validation of a Score to Assess Patients With Lower Gastrointestinal Bleeding

mortality, subsequent LGIB within 28 days, and the composite outcome of safe discharge was
assessed using area under the receiver operating characteristic (AUROC) curves and 95% CIs.
When assessing the performance of a risk score that is designed to identify low-risk patients,
sensitivity is the most important outcome.11 When clinicians make decisions about early discharge, it
is important that patients at high risk are not misclassified as low risk. Previous studies of patients
with UGIB have reported that a sensitivity of 95% or more can be used to identify optimal score
thresholds for low-risk patients whose conditions would be potentially suitable for outpatient
management.12 The sensitivity for safe discharge was calculated for point scores of 8 or lower, 9 or
lower, and 10 or lower, and the performance of these score thresholds was compared to identify
thresholds that would maintain a sensitivity of 95%. Statistical analysis was performed with Python
software (Python Software Foundation) using scikit, SciPy, and NumPy arrays. Data were analyzed
from October 16, 2018, to September 4, 2019.

Table 1. Oakland Score Variables

Variable Score component value


Age group, y
≤39 0
40-69 1
≥70 2
Sex
Female 0
Male 1
Previous hospital admission with LGIB
No 0
Yes 1
DRE results
No blood 0
Blood 1
Heart rate, beats/min
≤69 0
70-89 1
90-109 2
≥110 3
Systolic blood pressure, mm Hg
50-89 5
90-119 4
120-129 3
130-159 2
≥160 0
Hemoglobin concentration, g/dL
3.6-6.9 22
7.0-8.9 17
9.0-10.9 13
11.0-12.9 8
13.0-15.9 4
≥16.0 0

Abbreviations: DRE, digital rectal examination; LGIB, lower gastrointestinal


bleeding.
SI conversion factor: To convert hemoglobin to grams per liter, multiply by 10.

JAMA Network Open. 2020;3(7):e209630. doi:10.1001/jamanetworkopen.2020.9630 (Reprinted) July 7, 2020 4/11

Downloaded From: https://jamanetwork.com/ by a Non-Human Traffic (NHT) User on 12/05/2021


JAMA Network Open | Gastroenterology and Hepatology Validation of a Score to Assess Patients With Lower Gastrointestinal Bleeding

Results
A total of 46 179 patients admitted to the hospital with a primary diagnosis of LGIB were initially
identified. Of those, 51 patients received endoscopic hemostasis at esophagogastoduodenoscopy
and were excluded because they were more likely to have UGIB, leaving a study population of 46 128
patients (mean [SD] age, 70.1 [16.5] years; 23 091 women [50.1%]) (eFigure in the Supplement). Of
those, 3251 patients (7.0%) were receiving oral anticoagulant medications at the time of hospital
admission (Table 2). Overall, 17 896 patients (38.8%) received inpatient colonoscopy, 21 629
patients (68.1%; missing data in 14 387 patients) received RBC transfusion, 3097 patients (6.7%)
experienced rebleeding during admission, 79 patients (0.2%) received endoscopic hemostasis
during colonoscopy, 15 patients (0.03%) received mesenteric embolization, and 1 patient underwent
laparotomy for refractory bleeding. The median length of stay was 3 days (range, 1-175 days), 2048
patients (4.4%) died during hospitalization, and 1166 patients (2.5%) were readmitted with
subsequent LGIB. Across the study population, the most common diagnoses were diverticular
bleeding (10 657 patients [23.1%]), hemorrhoids (5339 patients [11.6%]), and angiodysplasia (2227
patients [4.8%]). An additional 17 957 patients (38.9%) were classified as having an unspecified
gastrointestinal hemorrhage, and 3933 patients (8.5%) were classified as having a hemorrhage of the
anus and rectum.
Overall, 22 074 (47.9%; 95% CI, 47.4%-48.3%) experienced none of the adverse outcomes
specified and could be classified as meeting the criteria for safe discharge. A total of 11 056 patients
(50.1%) in this group were female. Compared with patients who did not meet the safe discharge
criteria, patients who met the criteria were younger (mean [SD] age, 72.2 [14.7] years vs 67.9 [18.1]
years, respectively) with fewer comorbidities (26 229 comorbidities vs 15 857 comorbidities) and

Table 2. Demographic Characteristics and Presenting Features of Patients Admitted to Hospital


With Acute LGIB

Validation data, No. (%) (N = 46 128)


Did not meet criteria for safe discharge Met criteria for safe discharge
(n = 24 054)a (n = 22 074)a
Proportion of Proportion of
Variable used in development data set Summary data missing data Summary data missing data
Age, mean (SD) 72.2 (14.7) 0 67.9 (18.1) 0
Sex
Male 12 019 (50.0) 0 11 018 (49.9) 0
Female 12 035 (50.0) 0 11 056 (50.1) 0
Previous hospital admission with LGIB 880 (3.7) NA 282 (1.3) NA
Comorbidity
Cardiovascular disease 10 826 (45.0) NA 6834 (31.0) NA
Cancer 6056 (25.2) NA 4046 (18.3) NA
Liver disease 2487 (10.3) NA 1636 (7.4) NA
Renal disease 6860 (28.5) NA 3341 (15.1) NA
Test result
Abbreviations: INR, international normalized ratio;
Heart rate, mean (SD), beats/min 84 (17.0) 293 (1.2) 81 (16.2) 363 (1.6) IQR, interquartile range; LGIB, lower gastrointestinal
Systolic blood pressure, 128 (25.0) 221 (0.9) 140 (24.8) 357 (1.6) bleeding; WBC, white blood cell.
mean (SD), mm Hg
SI conversion factors: To convert hemoglobin to grams
Hemoglobin concentration, 85 (2.5) 4550 (18.9) 122 (2.1) 3023 (13.7)
mean (SD), g/dL per liter, multiply by 10; platelet count to ×109/L,
multiply by 1.0; WBC count to ×109/L, multiply by
Platelet count, mean (SD), 103/μL 248.5 (111.7) 5143 (21.4) 239.0 (90.2) 3404 (15.4)
0.001; urea nitrogen to millimoles per liter, multiply by
WBC count, mean (SD), /μL 9.2 (4.5) 4929 (20.5) 8.8 (3.8) 3152 (14.3)
0.357; creatinine to millimoles per liter, multiply
Urea nitrogen level, mean (SD), mg/dL 34.5 (25.0) 6187 (25.7) 22.4 (15.1) 5564 (25.2) by 76.25.
Creatinine level, mean (SD), mg/dL 1.7 (1.8) 5935 (24.7) 1.3 (1.3) 5312 (24.1) a
Safe discharge was defined as the absence of all of
Medication the following: in-hospital rebleeding, red blood cell
Oral antiplatelet 3005 (12.5) NA 2058 (9.3) NA transfusion; therapeutic intervention to control
Oral anticoagulant 1995 (8.3) NA 1256 (5.7) NA bleeding, in-hospital death (all causes); and
readmission with subsequent lower gastrointestinal
INR, median (IQR) 1.6 (1.5) 9496 (39.5) 1.2 (0.7) 9243 (41.2)
bleeding within 28 days.

JAMA Network Open. 2020;3(7):e209630. doi:10.1001/jamanetworkopen.2020.9630 (Reprinted) July 7, 2020 5/11

Downloaded From: https://jamanetwork.com/ by a Non-Human Traffic (NHT) User on 12/05/2021


JAMA Network Open | Gastroenterology and Hepatology Validation of a Score to Assess Patients With Lower Gastrointestinal Bleeding

fewer patients had previous hospital admissions with LGIB (880 admissions vs 282 admissions), and
fewer patients were receiving oral anticoagulant or antiplatelet medications (5000 patients vs 3314
patients) at hospital admission.
In total, 38 067 patients (82.5%) had complete data on all components of the Oakland Score
and clinical outcomes. The AUROC of the composite outcome of safe discharge was 0.87 (95% CI,
0.87-0.87), suggesting good discriminative performance (Figure 1). In the models predicting adverse
outcomes, the AUROCs were as follows: for RBC transfusion, 0.90 (95% CI, 0.90-0.90); for
in-hospital rebleeding, 0.46 (95% CI, 0.45-0.47); for death, 0.63 (95% CI, 0.62-0.64); and for
hospital readmission with subsequent bleeding, 0.60 (95% CI, 0.59-0.62). Because only 190
patients or fewer (ⱕ0.5%) received therapeutic interventions to control bleeding, AUROCs were not
calculated for these outcomes. The median Oakland Score was 18 points (range, 2-33 points)
(Figure 2). In total, 3305 of 38 067 patients (8.7%) scored 8 points or lower, with a sensitivity of
98.4% and a specificity of 16.0% for safe discharge (Table 3). A sensitivity of 96.0% for safe
discharge was maintained to a score threshold of 10 points or lower, with a specificity of 31.9%. A
total of 4888 patients (12.8%) had a score of 9 points or lower, and 6770 patients (17.8%) had a score
of 10 points or lower.
The most common adverse outcomes in patients with Oakland Scores of 10 points or lower
were RBC transfusion and in-hospital rebleeding. No patients received mesenteric embolization or
surgery, and the percentage of patients who received endoscopic hemostasis was constant between
those scoring 8 points or lower (11 of 3305 patients [0.3%]), 9 points or lower (16 of 4888 patients
[0.3%]), and 10 points or lower (21 of 6770 patients [0.3%]). Death occurred in 37 of 3305 patients

Figure 1. Receiver Operating Characteristic Curve for Safe Discharge

1.0

0.8
True-positive rate

0.6

0.4
Score, 10
Score, 9
Score, 8
0.2

ROC curve (area under the curve = 0.87)


0
0 0.2 0.4 0.6 0.8 1.0
False-positive rate ROC indicates receiver operating characteristic.

Figure 2. Proportion of Patients Meeting Criteria for Safe Discharge by Total Oakland Score

1800

1600 Safe discharge


Not safe discharge
1400

1200
Patients, No.

1000

800

600

400

200

0
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29 31 33
Oakland Score

JAMA Network Open. 2020;3(7):e209630. doi:10.1001/jamanetworkopen.2020.9630 (Reprinted) July 7, 2020 6/11

Downloaded From: https://jamanetwork.com/ by a Non-Human Traffic (NHT) User on 12/05/2021


JAMA Network Open | Gastroenterology and Hepatology Validation of a Score to Assess Patients With Lower Gastrointestinal Bleeding

(1.1%) with a score of 8 points or lower, 60 of 4888 patients (1.2%) with a score of 9 points or lower,
and 96 of 6770 patients (1.4%) with a score of 10 points or lower (Table 3).

Discussion
This study of 140 US hospitals in the HCA network found that the Oakland Score could identify
patients at low risk of experiencing adverse outcomes who may be safe for hospital discharge. The
Oakland Score was able to discriminate patients at low risk of adverse outcomes despite having data
on only 6 of the 7 previously validated variables, suggesting that a modification of the total score
that does not include the variable of digital rectal examination could be safely used. We also found
that the previously recommended threshold of 8 points or lower7 to identify low-risk patients could
be extended to 10 points or lower while maintaining a sensitivity of 96% for safe discharge.
Consistent with other large observational studies, the most common intervention observed in
the present study was RBC transfusion, which was identified in 68.1% of patients. The percentage of
deaths (4.4%) is similar to those reported elsewhere (3.4% and 8.8%).1,13 Studies from the United
States and the United Kingdom indicated that endoscopic hemostasis is performed in only 2.1% to
4.6% of patients with LGIB,1,14 but the frequency of less than 1% of patients who received endoscopic
hemostasis in the present study is comparatively low. Only 1 CPT code is specific for endoscopic
hemostasis, but other codes corresponding with nonspecific band ligation or submucosal injection
exist. These CPT codes may have been used in place of the bleeding-specific code, which could have
produced underestimation of the frequency of endoscopic hemostasis in our study. The proportion
of patients receiving inpatient colonoscopy was also low, at only 38.8%. Reports on the rates of
colonoscopy in a US population of patients with LGIB are rare, as most observational studies use
colonoscopy to identify patients. The largest study, performed by Navaneethan et al,15 identified
hospitalizations of patients with LGIB using ICD-9-CM codes. Of the 58 296 patients discharged from
the hospital who were identified in that study, only 2270 patients (38.9%) received an inpatient
colonoscopy. This percentage is similar to those reported in a smaller US study (34.7%)16 and in
studies from the United Kingdom1 and Australia.17
Other scores used to assess risk among patients with LGIB have been developed. The BLEED
(ongoing bleeding, low systolic blood pressure, elevated prothrombin time, erratic mental status, and
unstable comorbid disease) score18 was designed to assess the risk of in-hospital complications, the
NOBLADS (nonsteroidal anti-inflammatory drug use, no diarrhea or abdominal tenderness, blood
pressure ⱕ100 mm Hg, antiplatelet drug use, albumin level <3.0 g/dL, disease score ⱖ2 points, and
syncope) score19 and the Strate score10 were developed to assess the risk of severe bleeding, and the
Sengupta score20 was designed to assess the 30-day mortality risk.

Table 3. Adverse Outcomes Among Patients With Low-Risk Oakland Scores

Oakland Score, No. (%)


≤8 Points ≤9 Points ≤10 Points
Outcome (n = 3305) (n = 4888) (n = 6770)
RBC transfusion 132 (4.0) 236 (4.8) 383 (5.7)
Endoscopic hemostasis 11 (0.3) 16 (0.3) 21 (0.3)
Mesenteric embolization 0 0 0
Surgery 0 0 0
In-hospital rebleeding 153 (4.6) 223 (4.6) 344 (5.1)
In-hospital death 37 (1.1) 60 (1.2) 96 (1.4)
Readmission with subsequent bleeding within 28 d 7 (0.2) 19 (0.4) 39 (0.6)
Any adverse outcome 182 (5.5) 316 (6.5) 507 (7.5)
Safe discharge sensitivity, % 98.4 97.5 96.0
Safe discharge specificity, % 16.0 23.42 31.9
Abbreviation: RBC, red blood cell.

JAMA Network Open. 2020;3(7):e209630. doi:10.1001/jamanetworkopen.2020.9630 (Reprinted) July 7, 2020 7/11

Downloaded From: https://jamanetwork.com/ by a Non-Human Traffic (NHT) User on 12/05/2021


JAMA Network Open | Gastroenterology and Hepatology Validation of a Score to Assess Patients With Lower Gastrointestinal Bleeding

Risk scores developed for patients with UGIB, such as the AIMS-65 (albumin level <3.0 g/dL,
international normalized ratio >1.5, altered mental status, systolic blood pressure ⱕ90 mm Hg, and
age >65 years) score21 and the Glasgow-Blatchford score,3 have also been evaluated in patients with
LGIB. A study by Oakland et al5 reported that the AIMS-65 score was the best predictor of death
(AUROC, 0.78), the Oakland Score and Glasgow-Blatchford score were the best predictors of
rebleeding (AUROC, 0.74), and the Oakland Score was the best predictor of RBC transfusion (AUROC,
0.92). Tapaskar et al6 reported that the Oakland Score was the best predictor of severe bleeding
(AUROC, 0.74), the Strate score was the best predictor of rebleeding (AUROC, 0.66), and the
Glasgow-Blatchford score was the best predictor of RBC transfusion (AUROC, 0.87). Since
publication of the Oakland Score, other scores aimed at identifying low-risk patients have been
developed. The SHA2PE (systolic blood pressure ⱖ100 mm Hg, hemoglobin level >12 g/dL,
hemoglobin level 10.5-12.0 g/dL, no antiplatelet medication, no anticoagulant medication, pulse
ⱕ100 beats/min, and visible bleeding in the emergency department) score22 was derived from a
study of 580 patients but has not been externally validated.
To assess the generalizability of a prognostic model, the TRIPOD guidelines state that “it is
preferable to use a slightly different case-mix in external validation to judge model transportability.
Successful external validation studies in diverse settings (with different case-mix) indicate that it is
more likely that the model will be generalizable to plausibly related, but untested settings.”23(p214)
The Oakland Score was originally derived using prospective data from patients in the United
Kingdom; however, in the present study, we found that the Oakland Score also has prognostic value
in a US population. A strength of the Oakland Score is the simplicity of its components, which include
demographic factors, vital signs, and a single blood test, allowing the score to be fully calculated at
initial assessment without an observation period or endoscopic findings. A key criticism of the
Oakland Score is that because it was designed to be highly sensitive, some patients who might safely
be discharged may instead be identified as requiring hospitalization. This possibility is less important
than the potential of misclassifying high-risk patients as low risk. The specificities reported in the
present article are low (16.0% for an Oakland Score of ⱕ8 points and 31.9% for an Oakland Score of
ⱕ10 points). These low specificities are consistent with those reported for other risk scores; for
example, the specificity of the Glasgow-Blatchford score is 8% to 22% for a score of 0 points and
34% to 39% for a score of 1 point.11
Although most patients identified as low risk will not experience adverse outcomes, some
patients at each Oakland Score threshold experienced rebleeding, required hospital-based
intervention, or died. The same outcomes have been observed in studies of other risk scores that
have been adopted into clinical practice.12,24 Determining the safe threshold for identification of
patients who have a low risk of experiencing adverse outcomes and whose conditions can safely be
managed without hospitalization requires balancing the risk of misclassification with the need to
identify an adequate real-world population for the score to be clinically useful. In the Oakland Score
development study, a score of 8 points or lower was found to be the safe threshold for identifying
low-risk patients despite the threshold being applicable to only 8% of patients.5 In the present study,
an Oakland Score of 8 points or lower also identified only 8.7% of patients. When the score threshold
was extended to 10 points or lower, 17.8% of patients were identified as low risk, with a sensitivity
for safe discharge of 96%. Nonetheless, because the study population comprised patients admitted
to the hospital with LGIB, the proportion of patients scoring 8 points or lower or 10 points or lower
would likely be greater if patients who were discharged from the emergency department were
included. To determine this proportion, a prospective cohort study is needed, in which all patients
presenting to the emergency department are included, regardless of their admission status.
When comparing patient outcomes using a score threshold of 8 points or lower vs 10 points or
lower, the number of patients who received hospital-based interventions to treat bleeding remained
constant, the percentage of patients who received RBC transfusion increased, and the percentage
of patients who died increased. The percentage of deaths at these score thresholds (1.1% at ⱕ8
points and 1.4% at ⱕ10 points) is concerning and is similar to the percentage of deaths among

JAMA Network Open. 2020;3(7):e209630. doi:10.1001/jamanetworkopen.2020.9630 (Reprinted) July 7, 2020 8/11

Downloaded From: https://jamanetwork.com/ by a Non-Human Traffic (NHT) User on 12/05/2021


JAMA Network Open | Gastroenterology and Hepatology Validation of a Score to Assess Patients With Lower Gastrointestinal Bleeding

low-risk patients reported for the Glasgow-Blatchford score24 and other risk scores.11 The use of
clinician judgment in combination with risk scores is important. The need for RBC transfusion does
not necessarily require patient hospitalization because transfusions or iron can be administered in an
ambulatory setting. If patients have bled sufficiently to develop symptomatic anemia, they are
unlikely to meet the Oakland Score threshold for safe discharge, which allocates at least 13 points to
hemoglobin concentrations less than 110 g/L.5
Reducing the number of hospitalizations of patients with LGIB has important benefits. Few data
are available describing the economic burden of LGIB, but data from a national US database
suggested that costs are between $22 142 and $28 749 per hospitalization, or $4492 per bed-day.15
Although LGIB is likely to have a more benign course than UGIB, hospitalizations for patients with
LGIB are more expensive than those for patients with UGIB, primarily owing to the longer length of
stay and higher resource use.13 If an Oakland Score threshold of 8 points or lower was used to identify
low-risk patients, hospital admission could potentially be avoided in 8.7% of patients. Given that the
median length of stay in the present study was 3 days, this reduction in hospital admissions could
produce a savings of $44.5 million within the study population alone. If the score threshold was
extended to 10 points or lower, this savings could be $91.2 million. A retrospective analysis
performed in the United States found that 40% of costs associated with UGIB were incurred after
hospital discharge.25 Similar findings are likely to apply to LGIB. In addition, because patients with
LGIB are likely to be older than 65 years and to have a high comorbidity burden, other reasons for
hospital admission may be present.

Limitations
This study has several limitations. First, patient identification relied on the use of administrative
codes; however, previous large studies of patients with LGIB have successfully used ICD and CPT
codes for this purpose.26,27 Patients with hospital codes consistent with UGIB were excluded, as
were patients who received endotherapy during esophagogastoduodenoscopy. However, the
frequency of patients with the discharge code corresponding with an unspecified gastrointestinal
hemorrhage suggests that some patients may have had bleeding that originated in the upper rather
than the lower gastrointestinal tract, and some may have had small-bowel bleeding. This uncertainty
reflects that of clinicians during clinical assessment, in which it is often difficult to distinguish the site
of bleeding based on the patient’s medical history and examination alone.
Second, because only 38.8% of patients received inpatient colonoscopy, it is unclear how some
of the definitive diagnoses were made. Third, the digital rectal examination variable needed to
calculate the Oakland Score was missing; despite this limitation, the score performed well, which
provides the option of using this modification in patients who cannot tolerate digital rectal
examination, such as those with bleeding from an anal fissure. Fourth, the present study is limited to
patents who were hospitalized with LGIB. Fifth, data on RBC transfusion were frequently missing. It
is likely that these cases represent an absence of transfusion rather than missing data; however, the
missing data may have produced an overestimation of the proportion of patients who received
transfusions.

Conclusions
This large multicenter prognostic study found that the Oakland Score was externally valid for use in
assessing the risk of adverse outcomes in patients with LGIB. The Oakland Score threshold of 8
points or lower, which is currently used to identify patients at low risk of experiencing adverse
outcomes, could be extended to 10 points or lower to allow identification of a greater proportion of
low-risk patients while maintaining sensitivity; however, an increase in adverse events may occur
with use of the higher score threshold.

JAMA Network Open. 2020;3(7):e209630. doi:10.1001/jamanetworkopen.2020.9630 (Reprinted) July 7, 2020 9/11

Downloaded From: https://jamanetwork.com/ by a Non-Human Traffic (NHT) User on 12/05/2021


JAMA Network Open | Gastroenterology and Hepatology Validation of a Score to Assess Patients With Lower Gastrointestinal Bleeding

ARTICLE INFORMATION
Accepted for Publication: April 23, 2020.
Published: July 7, 2020. doi:10.1001/jamanetworkopen.2020.9630
Open Access: This is an open access article distributed under the terms of the CC-BY License. © 2020 Oakland K
et al. JAMA Network Open.
Corresponding Author: Kathryn Oakland, MD, Department of Digestive Diseases, HCA Healthcare UK, 242
Marylebone Rd, Marylebone, London, United Kingdom (kathryn.oakland@hcahealthcare.co.uk).
Author Affiliations: Department of Digestive Diseases, HCA Healthcare UK, London, United Kingdom (Oakland,
Bucknall); Faculty of Medicine, Imperial College London, London, United Kingdom (Oakland); Department of Data
Science, HCA Healthcare, Nashville, Tennessee (Kothiwale, Forehand, Jackson, Perlin); Division of
Gastroenterology, Western University, London, Ontario, Canada (Sey, Jairath); Division of Gastroenterology and
Biomedical Informatics, University of California, San Diego, San Diego (Singh).
Author Contributions: Drs Oakland and Kothiwale had full access to all of the data in the study and take
responsibility for the integrity of the data and the accuracy of the data analysis.
Concept and design: Oakland, Kothiwale, Perlin.
Acquisition, analysis, or interpretation of data: All authors.
Drafting of the manuscript: Oakland, Kothiwale, Bucknall, Jairath.
Critical revision of the manuscript for important intellectual content: Oakland, Kothiwale, Forehand, Jackson, Sey,
Singh, Jairath, Perlin.
Statistical analysis: Kothiwale, Sey.
Administrative, technical, or material support: Oakland, Forehand, Bucknall, Perlin.
Supervision: Oakland, Jackson, Jairath, Perlin.
Conflict of Interest Disclosures: Drs Oakland and Jairath developed the original Oakland Score. Dr Singh reported
receiving grants from AbbVie and Janssen Pharmaceuticals and personal fees from AbbVie, Pfizer, and Takeda
Pharmaceutical Company outside the submitted work. No other disclosures were reported.
Funding/Support: HCA Healthcare sponsored this study.
Role of the Funder/Sponsor: HCA Healthcare sponsored the design and conduct of the study; collection,
management, analysis, and interpretation of the data; preparation, review, and approval of the manuscript; and
decision to submit the manuscript for publication.
Meeting Presentation: An abstract of this paper was published on the Digestive Disease Week website as part of
the 2020 Digestive Disease Week; May 2, 2020; https://ddw.apprisor.org/epsAbstractDDW.cfm?id=1.

REFERENCES
1. Oakland K, Guy R, Uberoi R, et al. Acute lower GI bleeding in the UK: patient characteristics, interventions and
outcomes in the first nationwide audit. Gut. 2018;67(4):654-662.
2. Rockall TA, Logan RF, Devlin HB, Northfield TC. Risk assessment after acute upper gastrointestinal
haemorrhage. Gut. 1996;38(3):316-321. doi:10.1136/gut.38.3.316
3. Blatchford O, Murray WR, Blatchford M. A risk score to predict need for treatment for upper-gastrointestinal
haemorrhage. Lancet. 2000;356(9238):1318-1321. doi:10.1016/S0140-6736(00)02816-6
4. Strate LL, Gralnek IM. ACG clinical guideline: management of patients with acute lower gastrointestinal
bleeding. Am J Gastroenterol. 2016;111(5):755. doi:10.1038/ajg.2016.155
5. Oakland K, Jairath V, Uberoi R, et al. Derivation and validation of a novel risk score for safe discharge after acute
lower gastrointestinal bleeding: a modelling study. Lancet Gastroenterol Hepatol. 2017;2(9):635-643. doi:10.1016/
S2468-1253(17)30150-4
6. Tapaskar N, Jones B, Mei S, Sengupta N. Comparison of clinical prediction tools and identification of risk factors
for adverse outcomes in acute lower GI bleeding. Gastrointest Endosc. 2019;89(5):1005-1013. doi:10.1016/j.gie.
2018.12.011
7. Oakland K, Chadwick G, East JE, et al. Diagnosis and management of acute lower gastrointestinal bleeding:
guidelines from the British Society of Gastroenterology. Gut. 2019;68(5):776-789. doi:10.1136/gutjnl-2018-317807
8. Collins GS, Reitsma JB, Altman DG, Moons KGM. Transparent reporting of a multivariable prediction model for
individual prognosis or diagnosis (TRIPOD): the TRIPOD statement. Ann Intern Med. 2015;162(1):55-63. doi:10.
7326/M14-0697
9. World Health Organization. International Statistical Classification of Diseases and Related Health Problems,
Tenth Revision. World Health Organization; 1992.

JAMA Network Open. 2020;3(7):e209630. doi:10.1001/jamanetworkopen.2020.9630 (Reprinted) July 7, 2020 10/11

Downloaded From: https://jamanetwork.com/ by a Non-Human Traffic (NHT) User on 12/05/2021


JAMA Network Open | Gastroenterology and Hepatology Validation of a Score to Assess Patients With Lower Gastrointestinal Bleeding

10. Strate LL, Orav EJ, Syngal S. Early predictors of severity in acute lower intestinal tract bleeding. Arch Intern
Med. 2003;163(7):838-843. doi:10.1001/archinte.163.7.838
11. Barkun AN, Almadi M, Kuipers EJ, et al. Management of nonvariceal upper gastrointestinal bleeding: guideline
recommendations from the International Consensus Group. Ann Intern Med. 2019;171(11):805-822. doi:10.7326/
M19-1795
12. Stanley AJ, Laine L, Dalton HR, et al; International Gastrointestinal Bleeding Consortium. Comparison of risk
scoring systems for patients presenting with upper gastrointestinal bleeding: international multicentre
prospective study. BMJ. 2017;356:i6432. doi:10.1136/bmj.i6432
13. Lanas A, Garcia-Rodriguez LA, Polo-Tomas M, et al. Time trends and impact of upper and lower gastrointestinal
bleeding and perforation in clinical practice. Am J Gastroenterol. 2009;104(7):1633-1641. doi:10.1038/ajg.
2009.164
14. Ron-Tal Fisher O, Gralnek IM, Eisen GM, Williams JL, Holub JL. Endoscopic hemostasis is rarely used for
hematochezia: a population-based study from the Clinical Outcomes Research Initiative National Endoscopic
Database. Gastrointest Endosc. 2014;79(2):317-325. doi:10.1016/j.gie.2013.09.004
15. Navaneethan U, Njei B, Venkatesh PG, Sanaka MR. Timing of colonoscopy and outcomes in patients with lower
GI bleeding: a nationwide population-based study. Gastrointest Endosc. 2014;79(2):297-306. doi:10.1016/j.gie.
2013.08.001
16. Strate LL, Ayanian JZ, Kotler G, Syngal S. Risk factors for mortality in lower intestinal bleeding. Clin
Gastroenterol Hepatol. 2008;6(9):1004-1010. doi:10.1016/j.cgh.2008.03.021
17. Ng K-S, Nassar N, Soares D, Stewart P, Gladman MA. Acute lower gastrointestinal haemorrhage: outcomes and
risk factors for intervention in 949 emergency cases. Int J Colorectal Dis. 2017;32(9):1327-1335. doi:10.1007/
s00384-017-2844-2
18. Kollef MH, O’Brien JD, Zuckerman GR, Shannon W. BLEED: a classification tool to predict outcomes in patients
with acute upper and lower gastrointestinal hemorrhage. Crit Care Med. 1997;25(7):1125-1132. doi:10.1097/
00003246-199707000-00011
19. Aoki T, Nagata N, Shimbo T, et al. Development and validation of a risk scoring system for severe acute lower
gastrointestinal bleeding. Clin Gastroenterol Hepatol. 2016;14(11):1562-1570.e2. doi:10.1016/j.cgh.2016.05.042
20. Sengupta N, Tapper EB. Derivation and internal validation of a clinical prediction tool for 30-day mortality in
lower gastrointestinal bleeding. Am J Med. 2017;130(5):601.e1-601.e8. doi:10.1016/j.amjmed.2016.12.009
21. Saltzman JR, Tabak YP, Hyett BH, Sun X, Travis AC, Johannes RS. A simple risk score accurately predicts
in-hospital mortality, length of stay, and cost in acute upper GI bleeding. Gastrointest Endosc. 2011;74(6):
1215-1224. doi:10.1016/j.gie.2011.06.024
22. Hreinsson JP, Sigurdardottir R, Lund SH, Bjornsson ES. The SHA2PE score: a new score for lower
gastrointestinal bleeding that predicts low-risk of hospital-based intervention. Scand J Gastroenterol. 2018;53(12):
1484-1489. doi:10.1080/00365521.2018.1532019
23. Collins GS, Ogundimu EO, Altman DG. Sample size considerations for the external validation of a multivariable
prognostic model: a resampling study. Stat Med. 2016;35(2):214-226. doi:10.1002/sim.6787
24. Oakland K, Kahan BC, Guizzetti L, et al. Development, validation, and comparative assessment of an
international scoring system to determine risk of upper gastrointestinal bleeding. Clin Gastroenterol Hepatol.
2019;17(6):1121-1129.e2. doi:10.1016/j.cgh.2018.09.039
25. Cryer BL, Wilcox CM, Henk HJ, Zlateva G, Chen L, Zarotsky V. The economics of upper gastrointestinal bleeding
in a US managed-care setting: a retrospective, claims-based analysis. J Med Econ. 2010;13(1):70-77. doi:10.3111/
13696990903526676
26. Nigam N, Ham SA, Sengupta N. Early colonoscopy for diverticular bleeding does not reduce risk of
postdischarge recurrent bleeding: a propensity score-matching analysis. Clin Gastroenterol Hepatol. 2019;17(6):
1105-1111.e1. doi:10.1016/j.cgh.2018.09.050
27. Jun M, James MT, Manns BJ, et al; Alberta Kidney Disease Network. The association between kidney function
and major bleeding in older adults with atrial fibrillation starting warfarin treatment: population based
observational study. BMJ. 2015;350:h246. doi:10.1136/bmj.h246

SUPPLEMENT.
eMethods. Eligible ICD-9-CM and ICD-10-CM Codes, Laparotomy CPT Codes, and Development of the Oakland
Score
eFigure. Flow Chart of Participant Inclusion and Exclusion
eReferences

JAMA Network Open. 2020;3(7):e209630. doi:10.1001/jamanetworkopen.2020.9630 (Reprinted) July 7, 2020 11/11

Downloaded From: https://jamanetwork.com/ by a Non-Human Traffic (NHT) User on 12/05/2021

You might also like