The Journal of Laryngology & Otology (2006), 120, 650–654.

Main Article
# 2006 JLO (1984) Limited
doi:10.1017/S0022215106001149
Printed in the United Kingdom
First published online 31 March 2006

Influence of diabetes mellitus on deep neck infection

H-T LIN, C-S S TSAI*, Y-L CHEN†, J-G LIANG

Abstract
Objective: To investigate the influence of hyperglycaemia on deep neck infection (DNI) and the
differences between the diabetic and non-diabetic form of DNI.
Study design and setting: Retrospective review of 131 patients with DNI treated between 1993 and 2002
at Shin Kong Memorial Hospital, Taipei, Taiwan.
Results: Deep neck infection was significantly more prevalent in patients with diabetes mellitus (DM)
over 60 years of age than in non-DM subjects of a similar age ( p ¼ 0.004). In the DM group, Klebsiella
pneumoniae was the most common aerobic pathogen and tended to involve more than two anatomical
spaces ( p , 0.0001). Seventeen out of 18 patients (94.4 per cent) displayed an elevated (
7 per cent)
glycosylated haemoglobin level. The DM group had a significantly higher complication rate, longer
hospital stay and tracheotomy rate than the non-DM group.
Conclusions: Diabetic DNI differs from non-diabetic DNI in several aspects and is associated with a
higher morbidity. A greater than normal haemoglobin A1c level was commonly observed.
Key words: Neck, Abscess; Diabetes Mellitus

Introduction linking this condition with diabetes.6 – 9 However,

It is a commonly held premise that patients with dia-
betes mellitus (DM) are susceptible to frequent
infections. Studies in vivo and in vitro have impli-
cated a number of defective host immune defence
responses in the occurrence and progression of
DM.1 – 3 These responses include impaired polymor-
phonuclear neutrophil functions (e.g. chemotaxis,
bacterial killing, phagocytosis and impaired adhe-
rence), a decrease in cytokine response during leuko-
triene release in humoral immunity, impaired
myeloperoxidase activity and impairment of the anti-
oxidant system.
Diabetes mellitus has been a significant cause of
death in the Taiwanese population since 1983. In
the last 10 years, the number of deaths from diabetes
has increased sharply, by 47.4 per cent compared
with that in 1994 and by 120.3 per cent compared
with that in 1989; this represents the largest increase
in any of the main causes of death.4 Nearly 1 000 000
Taiwanese (5 per cent of the total population) have
DM. In comparison, the prevalence of diabetes in
the United States rose from 4.9 per cent in 1990 to
6.5 per cent in 1998, an increase of 33 per cent.5
Deep neck infection (DNI) has been the topic of
several scholarly research papers. There is evidence
several questions regarding the influence of hyper-
glycaemia on DNI have not been fully explored.
The present study was prompted in part by the lack
of data concerning the association of glycosylated
haemoglobin (HbA1c) and DNI with DM.
Methods and materials
This retrospective study included all the consecutive
patients with DNI admitted to Shin Kong Wu Ho-Su
Memorial Hospital during the nine-year period from
1993 to 2002. A number of demographic, clinical and
surgical variables were collected by studying the
patients’ hospital records and radiology files.
Patients’ records also indicated their DM status,
allowing patients to be categorized into two groups:
DM and non-DM. The criteria used for new DM
diagnoses were a fasting blood glucose level of

126 mg/dl or a post-prandial blood glucose level
of
200 mg/dl, accompanied by the classical symp-
toms of diabetes.6 The remainder of the DM patients
had been previously diagnosed by an endocrinolo-
gist. The duration of patients’ DM and their blood
HbA1c levels were obtained from their records.
In our hospital, every patient with DNI was
initially given an empirical dose of antibiotic. The

From the Departments of Otolaryngology-Head & Neck Surgery and †Internal Medicine (Division of Endocrinology), Shin Kong
Wu Ho-Su Memorial Hospital, Taipei, and the *Department of Otolaryngology, Tungs’ Taichung MetroHarbor Hospital, Wuchi,
Taichung, Taiwan.
Presented at the Annual Meeting of the Taiwan Society for Head and Neck Surgery Combined Otorhinolaryngologic Meeting,
9 November 2002, Taipei, Taiwan.
Accepted for publication: 3 December 2005.

650
INFLUENCE OF DIABETES MELLITUS ON DEEP NECK INFECTION
dosage was then adjusted according to the bacterio-
logical results of the pus culture. Diabetes mellitus
patients were treated with a DM diet and subcu-
taneous insulin injections. If there was no clinical
improvement within 24– 48 hours or if a patient’s
condition worsened after several days of antibiotic
administration, surgical drainage was carried out
under general anaesthesia.
Statistical analyses were performed to assess the risk
factors for DNI. The analyses included the Student
t-test, Chi-square and Fisher exact tests, Mann–
Whitney U test, and multiple logistic regression.
Significance was judged to be present at p , 0.05.
Results
Of the 131 patients in the retrospective study, 73 were
male and 58 were female. Of these 131 patients, 40
(31 per cent) were diabetic, 20 males and 20
females (male to female ratio, 1:1). The remaining
91 patients (69 per cent of the total) were non-
diabetics, 53 males and 38 females (male to female
ratio, 1.4:1). The age distribution of the DM and
non-DM groups is illustrated in Figure 1. The
median age in the DM group was 60.5 years. The
median age in the non-DM group was 45 years
(ranging from one to 88 years).
Deep neck infections were significantly more
prevalent in DM subjects over 60 years of age than
in non-DM subjects of a similar age (x2 test,
p ¼ 0.004; odds ratio ¼ 3.14). The duration of the
DM and the level of HbA1c found are shown in
Table I. Haemoglobin A1c was checked in 18
patients, either on the day of admission or within
three months prior to admission. Of these 18
patients, five were newly diagnosed with diabetes,
two had been diagnosed within the previous two
years, while 10 had been diagnosed at least five
years previously. One patient did not have their dura-
tion of diabetes recorded. Eleven out of 18 patients
(61.1 per cent) had an HbA1c level that was elevated
by .10 per cent. Seventeen out of the 18 patients
(94.4 per cent) had an HbA1c level that was elevated
by
7 per cent.
FIG. 1
Age of deep neck infection (DNI) patients with diabetes mel-
litus (DM) and without DM included in the study. (Note that
DNI was more prevalent in DM subjects over 60 years of age
than in non-DM subjects of a similar age ( p ¼ 0.004)).
651
The average hospital stay in the DM group was
24.3 days (ranging from two to 210 days). The
average hospital stay in the non-DM group was 12.9
days (ranging from two to 107 days). The longer
hospital stay of DM individuals was statistically
significant ( p , 0.04).
A swollen neck was evident as a symptom of DNI
in 70 per cent of the DM patients as compared with
only 46.1 per cent of the non-DM patients. Odyno-
phagia was evident in 22.5 per cent of DM patients
but in only 8.7 per cent of non-DM patients. Sore
throat was a symptom in both populations (20 per
cent of DM patients and 24.1 per cent of non-DM
patients). Leukocyte counts were also obtained in
both groups of patients; a WBC count greater than
15 000/mm was found in 22 per cent of the DM
group, compared with 18.6 per cent of the non-DM
group ( p . 0.05).
The DNI was of unknown aetiology in 40 per cent
of the DM group and 40.6 per cent of the non-DM
group. Of those cases of DNI of identifiable aetio-
logy, odontogenic origin and acute pharyngotonsilli-
tis predominated in both groups. There were 11
odontogenic DNIs (27.5 per cent) in the DM group,
involving five males and six females. Pharyngotonsil-
litis as the origin of DNI was diagnosed in 25 per cent
of the DM patients, 19.7 per cent of the non-DM
patients and 21.3 per cent of all patients. Less
common aetiologies were aerodigestive trauma, laryn-
geal foreign body and pharyngo-laryngeal cancer.
Thirty-three pus samples were taken for culture
analysis from DM patients, 32 from surgical drainage
and the remainder from needle aspiration. Positive
cultures were obtained in 28 of these 33 samples
(84.8 per cent). In all, 28 positive cultures grew 13
genera, with Klebsiella pneumoniae as the most
common aerobic pathogen, being found in 18 of the
cultures (54.4 per cent) (and representing the sole
bacterial species in 72.2 per cent of those 18 cultures).
Streptococcus groups A, D and E were the next most
abundant, these three groups being found in 18.2 per
cent of cultures. Cultures from five patients (15.1 per
cent) yielded anaerobic bacteria. Three of these
patients had necrotizing fasciitis, which caused
sepsis and death in one patient. Aerobic bacteria
also dominated in the pus samples obtained from
non-DM patients (28 of 55 samples; 50.9 per cent).
Streptococcus species were the second most
common isolates (25 per cent of samples), followed
by K. pneumoniae.
The submandibular and parapharyngeal spaces
were the two most commonly involved spaces in
both groups (Table II). Deep neck infection in the
DM group tended to involve more than two anato-
mical locations (72.5 per cent) ( p , 0.0001).
As shown in Table III, complications occurred in
19 patients in the DM group (47.5 per cent) and 12
in the non-DM group (13.0 per cent); this difference
was significant ( p , 0.0001). However, the rest of the
indicators were not significant after Bonferroni
correction.
The 19 DM patients with complications were cate-
gorized into four groups with respect to the length of
time their DM had been diagnosed (Table I). There
652 H-T LIN, C-S S TSAI, Y-L CHEN et al.

TABLE I
DM DURATION, CORRESPONDING HBA1C LEVEL AND DNI COMPLICATIONS

DM duration Patients Patients’ recorded HbA1c Mean HbA1c Patients with DNI
n (%) (%) complications
Individual levels (%) Patients (n) n (%)
‡ ‡ ‡ ‡ †
.5 years 16 (43) 7.0 , 9.2 , 9.4, 9.9 ,10.1 , 10.3 , 10 10.28 12 (63.2)
11, 11.4, 11.5†, 13‡
,5 years 6 (14) 7.2, 12.1§ 2 9.65 0
New DM diagnosis 8 (19) 4.8, 8.2, 10.6‡, 11‡, 14.7‡ 5 9.86 3 (15.8)
No record of DM 10 (24) 12.3 1 12.3 4 (21)
Total 40 18 10.2 19
‡
¼ patients with complications; † ¼ died; § ¼ second episode of deep neck infection; DM ¼ diabetes mellitus; HbA1c ¼
haemoglobin A1c; DNI ¼ deep neck infection

was no statistically significant difference between the a different mechanism of DNI onset in diabetics
complication rates of the four groups ( p ¼ 0.013). compared with non-diabetics.
Ten of the 19 patients had elevated HbA1c levels The control of hyperglycaemia is one topic of
recorded (average, 10.73 per cent). The average concern for the diabetic group. Two clinical para-
HbA1c level for those patients without compli- meters should be emphasized, the daily blood sugar
cations was 9.55 per cent. There was no statistically and the HbA1c.
significant difference between these two groups The optimal daily blood glucose control during
( p ¼ 0.56 by Mann – Whitney U test). admission was between 140–200 mg/dl.13 To avoid
Logistic regression equations for the four variables complications following surgery, blood sugar should
of age, sex, identity of pathogen and DM duration be controlled to ,220 mg/dl.14 Such studies have
were calculated. None of the variables appeared to not been carried out in hyperglycaemic DNI patients
be predictors of DNI. undergoing surgical drainage. In our hospital, we aim
The treatment results are shown in Table IV. The to control blood sugar to ,200 mg/dl. More stringent
non-DM group had a statistically significantly blood sugar control, using intensive insulin therapy,
higher rate of recovery with antibiotic alone should be performed in the intensive care unit.
( p ¼ 0.001). In the DM group, tracheostomy was It is well known that HbA1c represents glycaemic
performed significantly more often than in the control status within the recent past (i.e. two to three
non-DM group ( p ¼ 0.007). months). Previous research has demonstrated that a
raised HbA1c level is associated with increased mor-
tality and that for every one per cent increase in
Discussion HbA1c level, the possibility of heart failure increases
The results of the present study are consistent with by 8 per cent.15,16 Our results demonstrate that, in
those of previous studies, in that the clinical course our patients with DM, 61.1 per cent of the HbA1c
of DNI comorbid with DM was more severe and levels recorded were elevated by more than 10 per
had a poorer prognosis.7 – 11 In our series, all DM cent. The mean HbA1C level was especially high in
was of the type II (adult onset) variety. There was those patients in whom diabetes had been diagnosed
an increased tendency toward DNI in DM subjects more than five years previously. Thus, the high
compared with non-DM subjects, especially above
the age of 60 years ( p , 0.05). Our observations of
an increased prevalence of DNI in diabetic indivi- TABLE III
duals aged 60 years and older could reflect the preva- COMPLICATIONS OF DEEP NECK INFECTION
lence of diabetes in the general population aged 50 to
70 years.5 Additionally, the documented decline in Complication DM patients Non-DM patients
immune system efficiency with age may play a n (%) n (%)
role.12 However, it remains unclear whether there is Sepsis 10 (25) 9 (9.8)
Necrotizing fasciitis 5 (12.5) 3 (3.3)
Airway obstruction 9 (22.5) 8 (8.7)
TABLE II Mediastinitis/abscess 4 (10) 2 (2.1)
ANATOMICAL LOCATIONS OF DEEP NECK INFECTION Pleural effusion 3 (7.5) 2 (2.1)
EAC fistula 1 (2.5) 0
Location DM patients Non-DM patients O-R fistula 1 (2.5) 0
n (%) n (%) Acute renal failure 1 (2.5) 0
IJV thrombosis 0 1 (1)
Submandibular 20 (50) 36 (39.5) Pulmonary embolism 0 1 (1)
Parapharyngeal 17 (42.5) 54 (59.3) Encephalitis 0 1 (1)
Retropharyngeal 3 (7.5) 7 (7.6) Empyema 0 1 (1)
Ludwig 3 (7.5) 3 (4.9) Death 3/40 (7.5) 4/91 (4.3)
Parotid 1 (2.5) 6 (9.8) Total 19/40 (47.5) 12/91 (13.1)
Posterior triangle 3 (7.5) 2 (3.2)


2 locations 29 (72.5) 18 (19.7) ¼ significant; EAC ¼ external acoustic canal; O-R ¼
oesophageal – retropharyngeal; IJV ¼ internal jugular vein;

¼ significant; DM ¼ diabetes mellitus DM ¼ diabetes mellitus
INFLUENCE OF DIABETES MELLITUS ON DEEP NECK INFECTION
TABLE IV
TREATMENT FOR DEEP NECK INFECTION
Treatment DM patients Non-DM patients
n (%) n (%)
Antibiotic only 8 (19) 45 (49.4)
Antibiotic þ I&D 32 (80) 46 (50.5)
Tracheostomy 6/40 (15) 3/91 (3.2)

¼ significant; I&D ¼ incision and drainage; DM ¼ diabetes
mellitus
HbA1c level recorded for most of these patients was
indicative of poor hyperglycaemia control for at least
three months before DNI onset.
To our knowledge, this is the first study to report
that most diabetics suffering DNI had a high
HbA1c level before DNI onset. Although the
higher mean HbA1c level in DM patients with com-
plications, as compared with those without compli-
cations, was not statistically significant (perhaps
reflecting the small sample size), the role of HbA1c
in diabetics with DNIs remains to be more rigorously
assessed. It may be prudent to monitor HbA1c levels
in all DNI patients who also have DM. However,
such vigilance is not currently observed in hospitals
in Taiwan or in the United States.17 Further study
of daily blood sugar control and HbA1c levels may
represent another approach to the investigation of
DNI with DM.
In agreement with published observations, DNI
infections caused by K. pneumoniae in our study
were clustered in the DM group. The reason for the
association of K. pneumoniae infection with diabetes
mellitus is still unknown. The documented increase of
pharyngeal colonization with Gram-negative bacteria
may play a role.18 A second reason may be the failure
of macrophages to recognize this bacteria.19
Therefore, the choice of antibiotic is an important
issue in the treatment of DNI. At our hospital, anti-
biotics are given empirically and then adjusted
according to the bacteriological results of pus
sample cultures. Given the variability of dominant
bacteria in DNI, the initial combined use of penicil-
lin, an aminoglycoside and clindamycin for DNI
patients with DM is prudent. However, the delivery
of antibiotic seems to be influenced by the diabetic
microangiopathic and macroangiopathic compli-
cations present. There is a considerable weight of evi-
dence that supports the view that exercising better
control of blood glucose level leads to a decreased
rate of chronic complications and also of microangio-
pathic and macroangiopathic complications.20,21 This
fact may be reflected in our study, in which the dia-
betic group, with mostly poorly controlled previous
blood glucose levels, had a longer hospital stay and
a lower rate of recovery when antibiotic therapy
alone was used.
The overall surgical drainage rate observed in the
present study (59.5 per cent) was less than that
noted by Parhiscar and Har-El (88 per cent)7 and
Har-El et al. (87.3 per cent).8 Our lower rate is pro-
bably due to the early intravenous administration
of antibiotics. This antibiotic regime is common
653
practice in Taiwan, where an under-developed
medical referral system leads to a lack of medial con-
sultation prior to patients’ presentation at a medical
centre. As expected, the surgical drainage rate and
tracheotomy rate in the DM group were significantly
higher than those in the non-DM group. Thus, anti-
biotic administration alone was not sufficient for
recovery. Early surgical intervention and airway
support should be planned during the initial clinical
preparation of DNI patients with DM.
Conclusions
Diabetic DNI differs in several respects from that
occurring in non-diabetics. Clinicians need to be
alert to the higher complication rate and abnormal
HbA1c levels associated with DM. More aggressive
treatment should be included in the initial treatment
plan.
. This is a retrospective study of 131 patients
treated for deep neck infection
. Diabetes mellitus was a significant risk factor
in the development of deep neck infection and
occurred in 18 patients. Klebsiella
pneumoniae was the commonest pathogen
. Diabetic patients with deep neck infection had
a higher rate of complications and
tracheotomies and a longer hospital stay
Acknowledgement
We would like to thank Dr Lu Long-Sheng for his
advice regarding this paper.
References
1 Delamaire M, Maugendre D, Moreno M, Le Goff MC,
Allannic H, Genetet B. Impaired leukocyte functions in
diabetic patients. Diabet Med 1997;14:29 – 34
2 Uchimura K, Nagasaka A, Hayashi R, Makino M, Nagata
M, Kakizawa H et al. Changes in superoxide dismutase
activities and concentrations and myeloperoxidase activi-
ties in leukocytes from patients with diabetes mellitus. J
Diabetes Complications 1999;13:264– 70
3 Alexiewicz JM, Kumar D, Smogorzewski M, Klin M,
Massry SG. Polymorphonuclear leukocytes in
non-insulin-dependent diabetes mellitus: abnormalities in
metabolism and function. Ann Intern Med 1995;123:
919– 24
4 Department of Health, Executive Yuan, Taiwan, ROC.
Statistics & Analysis. Health Statistics: Health Trends,
II-19, 1999. http://www.doh.gov.tw/cht/index.aspx [10
November 2002]
5 Mokdad AH, Ford ES, Bowman BA, Nelson DE,
Engelgau MM, Vinicor F et al. Diabetes trends in the
US: 1990 –98. Diabetes Care 2000;23:1278–83
6 Gavin JR 3rd, Alberti KGMM, Mayer BD, DeFronzo RA,
Drash A, Gabbe SG, Genuth S, Maureen IH, Kahn R,
Keen H et al. Report of the expert committee on the diag-
nosis and classification of diabetes mellitus. Diabetes Care
1997;20:1183 –97
7 Parhiscar A, Har-El G. Deep neck abscess: a retrospective
review of 210 cases. Ann Otol Rhinol Laryngol 2001;110:
1051 –4
8 Har-El G, Aroesty JH, Shaha A, Lucente FE. Changing
trends in deep neck abscess. A retrospective study of 110
patients. Oral Surg Oral Med Oral Pathol Radiol Endod
1994;77:446 – 50
654
9 Lee KC, Tami TA, Echavez M, Wildes TO. Deep neck
infections in patients at risk for acquired immunodeficiency
syndrome. Laryngoscope 1990;100:915– 19
10 Chen MK, Wen YS, Chang CC, Huang MT, Hsiao HC.
Predisposing factors of life-threatening deep neck infec-
tion: logistic regression analysis of 214 cases. J Otolaryngol
1998;27:141 –4
11 Chen MK, Wen YS, Chang CC, Lee HS, Huang MT, Hsiao
HC. Deep neck infections in diabetic patients. Am J
Otolaryngol 2000;21:169– 73
12 Naliboff BD, Rosenthal M. Effects of age on complications
in adult onset diabetes. J Am Geriatr Soc 1989;37:838– 42
13 Levetan CS, Magee MF. Hospital management of diabetes.
Endocrinol Metab Clin North Am 2000;29:745– 70
14 Pomposelli JJ, Baxter JK 3rd, Babineau TJ, Pomfret EA,
Driscoll DF, Forse RA et al. Early postoperative glucose
control predicts nosocomial infection rate in diabetic
patients. JPEN 1998;22:77 – 81
15 Leibovici L, Yehezkelli Y, Porter A, Regev A, Krauze I,
Harell D. Influence of diabetes mellitus and glycaemic
control on the characteristics and outcome of common
infections. Diabet Med 1996;13:457 –63
16 Khaw KT, Wareham N, Luben R, Bingham S, Oakes S,
Welch A et al. Glycosylated hemoglobin, diabetes, and
mortality in men in Norfolk cohort of European prospec-
tive investigation of cancer and nutrition. BMJ 2001;322:
15– 18
17 Weiner JP, Parente ST, Garnick DW, Fowles J, Lawthers
AG, Palmer RH. Variation in office-based quality. A
claims-based profile of care provided to Medicare patients
with diabetes. JAMA 1995;273:1503– 8
18 Mackowiak PA, Martin RM, Smith JW. The role of
bacterial interference in the increased prevalence of
H-T LIN, C-S S TSAI, Y-L CHEN et al.
oropharyngeal gram-negative bacilli among alcoholics
and diabetics. Am Rev of Respir Dis 1979;120:589 –93
19 Chen KY, Hsueh PR, Liaw YS, Yang PC, Luh KT. A
10-year experience with bacteriology of acute thoracic
empyema: emphasis on Klebsiella pneumoniae in patients
with diabetes mellitus. Chest 2000;117:1685– 9
20 UK Prospective Diabetes Study (UKPDS) Group. Inten-
sive blood-glucose control with sulphonylureas or insulin
compared with conventional treatment and risk of compli-
cations in patients with type 2 diabetes (UKPDS 33).
Lancet 1998;352:837– 53
21 The Diabetes control and Complications Trial Research
Group. The effect of intensive treatment of diabetes on
the development and progression of long-term compli-
cations in insulin-dependent diabetes mellitus. N Engl J
Med 1993;329:977– 86
Address for correspondence:
Dr Jia-Guang Liang,
Departments of Otolaryngology-Head and Neck Surgery,
Shin Kong Wu Ho-Su Memorial Hospital,
95 Wen-Chang Road, Shihlin,
Taipei 111, Taiwan, Republic of China.
Fax: 886 2 2885 0686
E-mail: ht_lin6245@yahoo.com.tw
Dr J-G Liang takes responsibility for the integrity of the
content of the paper.
Competing interests: None declared
Reproduced with permission of the copyright owner. Further reproduction prohibited without permission.