559024

research-article2014

DVR0010.1177/1479164114559024Diabetes & Vascular Disease ResearchHelfand et al.

Original Article

Elevated serum glucose levels and survival

after acute heart failure: A populationbased perspective

Diabetes & Vascular Disease Research

2015, Vol. 12(2) 119125
The Author(s) 2014
Reprints and permissions:
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DOI: 10.1177/1479164114559024
dvr.sagepub.com

Benjamin KI Helfand1, Nicholas J Maselli2, Darleen M Lessard1,

Jorge Yarzebski1, Joel M Gore2, David D McManus2, Jane S
Saczynski1,2 and Robert J Goldberg1

Abstract
Background: Limited data are available about the characteristics, treatment and survival in patients without diabetes
mellitus (DM), previously diagnosed DM and patients with hyperglycaemia who present with acute decompensated heart
failure (ADHF). Our objectives were to examine differences in these endpoints in patients hospitalized with ADHF.
Methods: Patients hospitalized with ADHF during 1995, 2000, 2002 and 2004 comprised the study population.
Results: A total of 5428 non-diabetic patients were hospitalized with ADHF, 3807 with diagnosed DM and 513 with
admission hyperglycaemia. Patients with admission hyperglycaemia experienced the highest in-hospital death rates (9.9%)
compared to those with diagnosed DM (6.5%) and non-diabetics (7.5%). Patients with diagnosed DM had the greatest
risk of dying after hospital discharge.
Conclusions: Patients with elevated blood glucose levels at hospital admission are more likely to die acutely. After
resolution of the acute illness, patients with previously diagnosed DM need careful monitoring and enhanced treatment.
Keywords
Epidemiology, diabetes, heart failure, hyperglycaemia, cardiology, chronic diseases

Introduction
Heart failure is an increasingly common chronic medical
condition that is associated with significant morbidity,
mortality and health-care burden.1 Given the advanced age
of patients with heart failure, patients hospitalized for this
clinical syndrome typically have a substantial number of
additional comorbidities present, one of the most prevalent
of which is diabetes mellitus (DM).13 DM has also been
linked to the development of increased vascular stiffness
and impaired diastolic function.4,5
The prevalence of DM in American men and women
has been rising steadily over time, with approximately 1 in
14 adults affected by this metabolic disorder.68 Recent
estimates project a continuing increase in the prevalence of
diagnosed DM over the next several decades.9,10 A limited
number of studies have shown that upwards of 40% of
patients with heart failure have co-occurring DM, nearly
four times greater than the prevalence of DM in the general population.11,12 Among patients with heart failure, DM
is associated with increased mortality.13,14 Reduced survival among patients with heart failure and DM is, in part,
attributable to the presence of hyperglycaemia, which has
been associated with an increased risk of cardiovascular

events, heart failure-related hospitalizations and total mortality.10,1315 Despite an increased risk of dying among
heart failure patients with DM,16,17 the health-care practices in those with and without DM may be similar.3,1012
Furthermore, long-term mortality has been shown to be
similar among both diagnosed and undiagnosed diabetics
with hyperglycaemia.14,15 Limited data also exist to suggest that elevated serum glucose level at the time of hospital presentation, in the absence of a history of DM, may be
an important prognostic factor in patients with an acute
exacerbation of heart failure.

1Department

of Quantitative Health Sciences, University of

Massachusetts Medical School, Worcester, MA, USA
2Department of Medicine, University of Massachusetts Medical School,
Worcester, MA, USA
Corresponding author:
Robert J Goldberg, Department of Quantitative Health Sciences,
University of Massachusetts Medical School, 368 Plantation Street,
Worcester, MA 01605, USA.
Email: robert.goldberg@umassmed.edu

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Diabetes & Vascular Disease Research 12(2)

The objectives of this observational study were to

describe the epidemiology of DM and hyperglycaemia in a
large population-based cohort of patients hospitalized with
acute decompensated heart failure (ADHF) at all 11 medical centres in central Massachusetts. Our primary study
aims were to examine differences in patient characteristics, hospital treatment practices, in-hospital survival and
post-discharge mortality in non-diabetics, previously diagnosed diabetics, and in patients with elevated blood glucose levels at the time of hospital admission for ADHF
using data from the Worcester Heart Failure Study
(WHFS).1820

Methods
The WHFS is a population-based surveillance study of
adult male and female residents of the Worcester, MA,
metropolitan area (2000 census estimate=478,000) admitted to all 11 central MA medical centres for possible ADHF
during the years 1995, 2000, 2002 and 2004.1820 These
study years were selected due to the availability of federal
funding support and to correspond with population census
estimates.
The medical records of residents of central Massachusetts
admitted to all greater Worcester medical centres during the
years under study were reviewed in a standardized manner
for primary and/or secondary International Classification of
Diseases9 (ICD-9) discharge diagnoses consistent with
possible ADHF.1820 Patients with a discharge diagnosis of
ADHF (ICD-9 code 428) comprised the primary diagnostic
category reviewed for the identification of possible cases of
ADHF. In addition, trained study physicians and nurses
reviewed the medical records of patients with discharge
diagnoses of rheumatic heart failure, hypertensive heart and
renal failure, acute cor pulmonale, cardiomyopathy, pulmonary heart disease and congestion, acute lung oedema,
oedema, dyspnoea and respiratory abnormalities for purposes of identifying patients who may have experienced
new-onset heart failure. The diagnosis of heart failure was
confirmed using the Framingham criteria.21

Data collection
Information about patient demographics, medical history,
clinical characteristics and laboratory test results was collected through the review of information contained in hospital medical records. This information included patients
age, sex, race, prior comorbidities (e.g. history of DM,
hypertension), laboratory findings (e.g. admission serum
glucose and creatinine findings), clinical characteristics
(e.g. presenting heart rate, blood pressure) and hospital
survival status. Due to our methods of data collection, we
did not collect information about the specific cause of
death in patients who died either in the hospital or after
hospital discharge.

Information about the diagnosis of DM was obtained

from hospital medical records. Three diabetes groupings
were created: non-diabetics (absence of a history of DM
and a random admission serum glucose <200mg/dL measured at the time of hospitalization for ADHF); diagnosed
diabetics (prior history of DM or receipt of diabetic medications on admission as documented in hospital medical
records) and admission hyperglycaemic patients (absence
of a history of DM but serum glucose findings at the time
of hospital admission for ADHF200mg/dL based on
current American Diabetes Association guidelines).22 In
addition, because some patients with DM might have been
misclassified as being non-diabetic based on the extent of
information contained in hospital medical records, a sensitivity analysis was performed to examine the impact of a
different working definition of DM on our principal study
findings. For this analysis, patients without a history of
DM were re-classified as being diabetic if their serum glucose level was 140mg/dL at the time of hospital admission for ADHF. This additional cut point was chosen
because the American Diabetes Association considers
patients to be prediabetic with an oral glucose tolerance
test 140mg/dL.
Physicians progress notes and daily medication logs
were reviewed for information related to the prescribing of
selected cardiac medications. The cardiac medications
examined included those shown to be of benefit in improving the prognosis of patients with ADHF [angiotensin-converting enzyme (ACE) inhibitors, angiotensin receptor
blockers (ARBs) and beta-blockers], those shown to be
effective at improving the symptomatic status of patients
with acute heart failure,23 as well as other effective cardiac
medications (e.g. aspirin, lipid lowering agents). Survival
status after hospital discharge through the end of 2011 was
ascertained through a review of subsequent hospital medical records and a statewide and national search of death
certificates for residents of the Worcester metropolitan
area.

Data analysis
We examined differences between our three primary comparison groups with regard to their demographic characteristics, medical history, presenting symptoms, clinical
admission data and receipt of hospital therapies using chisquare tests and analysis of variance (ANOVA) for discrete and continuous variables, respectively.
Differences in hospital case-fatality rates (CFRs)
according to DM status were examined using unadjusted
and multivariate logistic regression modelling. Differences
in 3-month, 1-year and 2-year post-discharge survival estimates were examined using Cox proportional hazards
models, which adjusted for patients age, sex, presenting
symptoms, medical history and clinical admission data in
addition to duration of long-term follow-up.

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Helfand et al.
Table 1. Characteristics of patients with acute decompensated heart failure.
Nondiabetics
(n=5428)

Diagnosed
diabetics
(n=3807)

Admission
hyperglycaemics
(n=513)

p value

N or mean
(% or SD)

N or mean
(% or SD)

N or mean
(% or SD)

77.6 (12.6)
2370 (44)
272 (5)
6.4 (8)

74.0 (11.1)
1735 (46)
302 (8)
6.0 (7)

77.7 (12.2)
179 (35)
24 (5)
7.4 (9)

<0.001
<0.001
<0.001
0.008

1238 (23)
2721 (50)
1936 (36)
3489 (64)
1123 (21)
622 (12)

1061 (28)
2468 (65)
1370 (36)
2859 (75)
1310 (34)
618 (16)

100 (20)
267 (52)
194 (38)
345 (67)
97 (19)
58 (11)

0.001
0.001
0.62
<0.001
<0.001
<0.001

1639 (30)
5047 (93)
3691 (68)
819 (15)
1881 (35)
1399 (26)
373 (7)

1260 (33)
3562 (94)
2842 (75)
661 (17)
1420 (37)
942 (25)
386 (10.1)

143 (28)
495 (97)
319 (62)
80 (16)
154 (30)
102 (20)
25 (5)

0.003
0.008
<0.001
0.013
0.001
0.011
<0.001

Mean (SD)

Mean (SD)

Mean (SD)

Clinical admission dataa

BMI index (kg/m2)
Systolic BP (mmHg)
Diastolic BP (mmHg)
Heart rate (bpm)
Estimated GFR (mL/min)
Glucose (mg/dL)

26.3 (7)
139.9 (31)
74.4 (19)
89 (22)
53.4 (24)
124.8 (28)

30 (8)
145.2 (33)
74.3 (19)
87.7 (21)
47.3 (23)
193 (96)

26.6 (8)
153 (36)
81.4 (22)
101.9 (25)
51.1 (21)
260.5 (65)

<0.001
0.001
0.001
<0.001
<0.001
<0.001

Demographics
Age
Male
Non-white race
Length of stay (days)
Medical history (%)
Anaemia
Coronary heart disease
Chronic lung disease
Hypertension
Renal failure
Stroke
Presenting symptoms (%)
Angina
Dyspnoea
Oedema
Nausea/vomiting
Orthopnoea
Weakness
Recent weight gain

BMI: body mass index; BP: blood pressure; GFR: glomerular filtration rate; SD: standard deviation.
aBMI values missing in 20%; all other variables missing in <3%.

Results
Patient characteristics
The study sample consisted of 9748 residents of the Worcester
metropolitan area hospitalized at all 11 medical centres in
central Massachusetts with independently confirmed ADHF
in whom information about a history of DM and admission
serum glucose levels was available. Our study population
comprised 5428 (56%) non-diabetics, 3807 (39%) diagnosed
diabetics and 513 (5%) patients with hyperglycaemia at the
time of hospital admission for ADHF. The average age of the
study sample was 76years, 56% were women, and 29% were
diagnosed with an initial episode of ADHF.
Patients with diagnosed DM tended to be younger than
the other comparison groups, whereas patients with admission hyperglycaemia included a greater proportion of
women. There were a greater proportion of patients with
diagnosed DM who had additional comorbid conditions

previously diagnosed. Diabetic patients were more likely to

present with symptoms of angina/chest pain, oedema/recent
weight gain, nausea/vomiting and orthopnoea; admission
hyperglycaemic patients were more likely to have presented
with dyspnoea and non-diabetics with weakness (Table 1).
Among the three groups of patients, diabetics had the highest body mass index (BMI) and lowest estimated glomerular
filtration rate (eGFR), and admission hyperglycaemic
patients had the highest systolic and diastolic blood pressures, heart rate, and presented with higher mean serum glucose levels (260mg/dL) at the time of hospital admission for
ADHF as compared with the two other groups.

Hospital treatment practices

In examining between-group differences with regard to
hospital treatment practices, diagnosed diabetics were the
most likely to have been treated with effective cardiac

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Diabetes & Vascular Disease Research 12(2)

Table 2. Hospital treatment practices in patients with acute decompensated heart failure.

Medications (%)
ACEI/ARBs
Aspirin
Beta-blockers
Calcium channel blockers
Lipid lowering
Digoxin
Diuretics
Nitrates
Procedures (%)
Cardiac catheterization
Coronary angioplasty
Coronary artery bypass surgery

Non-diabetics
(n=5428)

Diagnosed
diabetics
(n=3807)

Admission
hyperglycaemics
(n=513)

p value

N (%)

N (%)

N (%)

2539 (47)
2864 (53)
2883 (53)
1640 (30)
1194 (22)
2343 (43)
5261 (97)
2799 (52)

1449 (38)
2325 (61)
2208 (58)
1384 (36)
1364 (36)
1668 (44)
3703 (97)
2422 (64)

224 (44)
297 (58)
295 (58)
164 (32)
105 (21)
231 (45)
501 (98)
336 (66)

<0.001
<0.001
<0.001
<0.001
<0.001
0.64
0.46
<0.001

320 (6)
270 (5)
31 (1)

244 (6)
227 (6)
23 (1)

42 (8)
43 (8)
9 (2)

0.10
0.002
0.006

ACEI: angiotensin-converting enzyme inhibitor; ARB: angiotensin II receptor blocker.

Table 3. Odds of dying during hospitalization for acute decompensated heart failure.
Group

Unadjusted

Multivariable adjusteda

Multivariable adjustedb

Diagnosed diabetics
Admission hyperglycaemics

0.85c (0.72,1.00)*
1.36 (1.00,1.85)

0.94 (0.79,1.12)
1.38 (1.01,1.88)

1.03 (0.86,1.24)
1.49 (1.07,2.06)

aAdjusted

for age, sex, presenting symptoms and prior medical history.

for variables in model 1 and systolic blood pressure, heart rate and estimated glomerular filtration rate.
cOdds ratio.
*95% confidence intervals.
Referent group=non-diabetics.
bAdjusted

medications including ACE inhibitors/ARBs, aspirin,

beta-blockers and lipid lowering agents. Admission hyperglycaemic patients were the most likely to have undergone
coronary angioplasty (8% vs 5%6%) and coronary artery
bypass graft surgery (1.8% vs 0.6%) during their index
hospitalization, but the rates across all three study groups
were low (Table 2).

Hospital death rates

Patients with admission hyperglycaemia experienced the
highest hospital CFRs at nearly 10%, non-diabetics had
lower hospital CFRs (7.5%) and diagnosed diabetics (6.5%)
had the lowest in-hospital CFRs. In our fully adjusted
regression model, controlling for several demographic and
clinical factors of prognostic importance, admission hyperglycaemic patients were at a 49% higher risk of dying in the
hospital compared with non-diabetics (Table 3).
In a sensitivity analysis using an admission serum glucose cut-off of 140mg/dL, admission hyperglycaemic
patients experienced the highest short-term CFRs (8.6%),
followed by diagnosed diabetics (7.7%) and non-diabetics
(6.5%). In our fully adjusted regression model, patients

with admission hyperglycaemia were at a 26% higher risk

for dying in the hospital compared with non-diabetics.

Post-discharge mortality
Patients with previously diagnosed DM had a 14% higher
risk for dying at 3-months post-discharge [hazard ratio
(HR)=1.14, 95% confidence interval (CI)=1.09,1.20] and
an 18% higher risk of dying from all causes at 1 and 2years
post-discharge (HR=1.18, 95% CI=1.11,1.24; HR=1.18,
95% CI=1.11,1.26). On the other hand, although not statistically significant, admission hyperglycaemic patients had an
intermediate risk for dying from all causes at 3months,
1year, and 2years post-discharge between that of the nondiabetics and previously diagnosed diabetics (Table 4).
Similar findings were observed when we carried out a sensitivity analysis using a serum glucose cut-off of 140mg/dL.

Discussion
The results of our study among residents of a large central
New England metropolitan area hospitalized for ADHF
suggest that admission hyperglycaemic patients are more

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Helfand et al.
Table 4. Odds of dying after hospital.
Group

Discharge in patients with acute decompensated heart failure

3months

Crude

1year
Multivariable
adjusteda

Crude

2years
Multivariable
adjusted

Crude

Multivariable
adjusted

Diagnosed diabetics
1.14b (1.09,1.20)* 1.16 (1.10,1.22) 1.18 (1.11,1.24) 1.19 (1.13,1.27) 1.18 (1.11,1.26) 1.17 (1.09,1.26)
Admission hyperglycaemics 1.09 (0.98,1.21)
1.08 (0.97,1.20) 1.09 (0.97,1.23) 1.06 (0.94,1.21) 1.10 (0.96,1.27) 1.06 (0.92,1.22)
aAdjusted

for age, sex, presenting symptoms, prior medical history, systolic blood pressure, heart rate and estimated glomerular filtration rate.
ratio.
*95% confidence intervals.
Referent group = non-diabetics.
bOdds

likely to die during their acute hospitalization than nondiabetics and patients with previously diagnosed DM. We
hypothesize that the higher short-term death rates experienced by patients with transiently elevated levels of blood
glucose at the time of hospitalization for ADHF may serve
as a marker for an acute stress response to severe illness.
This hypothesis is supported by the high acute mortality
rates as well as the higher utilization of cardiac procedures
(coronary artery bypass surgery and coronary angioplasty)
in these patients. After hospital discharge and resolution of
the acute illness, the adverse impact of previously diagnosed DM on patients long-term survival emerges.24
Patients with previously diagnosed DM experienced the
highest post-discharge death rates at all time points examined compared with the other groups under study in this
population-based investigation.

Risk of hyperglycaemia in diabetics and nondiabetics

Hyperglycaemia is associated with increased mortality,
risk of re-hospitalization and other adverse outcomes,
including dementia,25 in patients with and without DM.26,27
In a study of 1886 critically ill patients who were hospitalized at a community teaching hospital in Atlanta, Georgia,
26% had a history of DM and 12% had hyperglycaemia.27
Patients with hyperglycaemia, as measured by an admission or in-hospital fasting blood glucose level of 126mg/
dL or a random blood glucose level of 200mg/dL on two
or more determinations had a higher risk for intensive care
unit (ICU) admission, longer hospital stay, higher risk of
discharge to extended care and higher in-hospital death
rates than persons with either DM or normal serum glucose levels. In a study of 1122 non-diabetics with ADHF,
in-hospital mortality in patients with the highest admission
blood glucose levels was twice as high compared to
patients with lower blood glucose levels.28 However, there
were no between-group differences in mortality rates at the
time of the 1-year follow-up.28,29 Among a large multinational cohort of more than 6000 patients with ADHF, elevated levels of blood glucose at the time for hospitalization
for ADHF were associated with an increased risk of dying

at 30days, irrespective of a history of DM and other important covariates of prognostic importance.30 Our study
extends previous findings by comparing three distinct
groups of admission hyperglycaemic patients, non-diabetics and patients with previously diagnosed DM who were
derived from a large population-based study of patients
with independently confirmed ADHF.

Hospital treatment practices

In our study, patients with previously diagnosed DM were
more likely to have been treated with effective cardiac
medications than admission hyperglycaemic patients or
those without a history of DM. Our findings suggest that
these patients may have been receiving closer monitoring
and more aggressive treatment by their physicians.
However, patients with elevated blood glucose levels at
the time of hospital admission were most likely to have
undergone an interventional cardiac procedure, supporting
our hypothesis of an acute stress response to ADHF and
potentially more severe cardiac disease.

Long-term prognosis
In patients with heart failure, the presence of comorbid DM
is associated with an increased risk of long-term mortality.13,29 Among more than 600 patients with heart failure
and DM in Olmsted County, Minnesota, the 5-year survival
rate was 37% among patients with DM and 46% among
patients without DM.17 In addition, among a cohort of 528
individuals hospitalized for a first episode of heart failure
in Leicestershire, UK, elevated admission plasma glucose
levels (~180mg/dL) were associated with increased allcause mortality during follow-up, even among patients
without a clinical diagnosis of DM.31 It is clear that DM is
associated with a greater risk of dying in general, and more
so in the face of heart failure.
Non-diabetic patients who developed hyperglycaemia
during an acute illness have been shown to be at increased
risk for developing DM. In a study of 511 individuals
admitted to an ICU in a single University Hospital in
Croatia between 2000 and 2002, patients with modest

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Diabetes & Vascular Disease Research 12(2)

levels of hyperglycaemia (>140mg/dL) were at a more

than fourfold increased risk of developing Type II DM
over the ensuing 5years in comparison to persons with
normal serum glucose levels.32 These findings suggest the
need for careful long-term monitoring of patients with
transiently elevated blood glucose levels in the setting of
an acute illness, including ADHF.

hospitalized with acute decompensated heart failure. This work is

dedicated to the memory of Joshua Bryan Inouye Helfand.

Declaration of conflicting interests

The authors declare that there is no conflict of interest.

Funding
Grant support for this project was provided by the National
Heart, Lung, and Blood Institute (R01 HL69874).

Study strengths and limitations

Strengths of this study include its large sample size, the
population-based design and its decade-long prospective
follow-up. Identification of patients with elevated serum
glucose levels in the setting of duress, such as ADHF, offers
a novel finding, and sensitivity analyses showed that multiple definitions for hyperglycaemia yielded similar results.
Our study has several limitations, however, that must be
kept in mind in interpreting the study results. Due to our
methods of data abstraction, we were only able to characterize patients with a history of diabetes if the medical
record indicated DM as a diagnosis, or if the patient was
being treated with insulin or diabetic medications at admission. Information about the use of diabetic medications and
insulin during hospitalization was not recorded as part of
our data collection procedures, so it is possible that some
patients with hyperglycaemia were identified as incident
cases of DM and treated as such during their hospitalization
for ADHF. Laboratory information about serum glycated
haemoglobin (HbA1c) levels was not available, nor were
data collected on additional follow-up glucose measurements during hospital admission; inasmuch, it is unknown
to what extent persistent hyperglycaemia played a role in
patients in-hospital or long-term survival. We were unable
to determine whether or not patients developed DM over
the course of our extended follow-up. Finally, our study
population consisted predominantly of older Caucasian
patients and our findings may not be generalizable to other
patient groups hospitalized with ADHF.

Conclusion
The results of this population-based study show that in
patients hospitalized with ADHF, elevated serum glucose
levels in non-diabetic patients at the time of hospital
admission may deserve special attention. Admission
hyperglycaemia serves to identify patients at high risk for
hospital mortality, but this risk decreases with resolution
of the acute illness. However, hyperglycaemic non-diabetic patients may be at increased risk of developing diabetes over the long term, justifying the careful monitoring
of these individuals after hospital discharge.
Acknowledgements
We are indebted to the nurses and physicians who were involved
in the abstraction of data from the medical records of patients

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