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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- several questions regarding the influence of hyper-
betes mellitus (DM) are susceptible to frequent glycaemia on DNI have not been fully explored.
infections. Studies in vivo and in vitro have impli- The present study was prompted in part by the lack
cated a number of defective host immune defence of data concerning the association of glycosylated
responses in the occurrence and progression of haemoglobin (HbA1c) and DNI with DM.
DM.1 – 3 These responses include impaired polymor-
phonuclear neutrophil functions (e.g. chemotaxis, Methods and materials
bacterial killing, phagocytosis and impaired adhe- This retrospective study included all the consecutive
rence), a decrease in cytokine response during leuko- patients with DNI admitted to Shin Kong Wu Ho-Su
triene release in humoral immunity, impaired Memorial Hospital during the nine-year period from
myeloperoxidase activity and impairment of the anti- 1993 to 2002. A number of demographic, clinical and
oxidant system. surgical variables were collected by studying the
Diabetes mellitus has been a significant cause of patients’ hospital records and radiology files.
death in the Taiwanese population since 1983. In Patients’ records also indicated their DM status,
the last 10 years, the number of deaths from diabetes allowing patients to be categorized into two groups:
has increased sharply, by 47.4 per cent compared DM and non-DM. The criteria used for new DM
with that in 1994 and by 120.3 per cent compared diagnoses were a fasting blood glucose level of
with that in 1989; this represents the largest increase 126 mg/dl or a post-prandial blood glucose level
in any of the main causes of death.4 Nearly 1 000 000 of 200 mg/dl, accompanied by the classical symp-
Taiwanese (5 per cent of the total population) have toms of diabetes.6 The remainder of the DM patients
DM. In comparison, the prevalence of diabetes in had been previously diagnosed by an endocrinolo-
the United States rose from 4.9 per cent in 1990 to gist. The duration of patients’ DM and their blood
6.5 per cent in 1998, an increase of 33 per cent.5 HbA1c levels were obtained from their records.
Deep neck infection (DNI) has been the topic of In our hospital, every patient with DNI was
several scholarly research papers. There is evidence 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 651

dosage was then adjusted according to the bacterio- The average hospital stay in the DM group was
logical results of the pus culture. Diabetes mellitus 24.3 days (ranging from two to 210 days). The
patients were treated with a DM diet and subcu- average hospital stay in the non-DM group was 12.9
taneous insulin injections. If there was no clinical days (ranging from two to 107 days). The longer
improvement within 24– 48 hours or if a patient’s hospital stay of DM individuals was statistically
condition worsened after several days of antibiotic significant ( p , 0.04).
administration, surgical drainage was carried out A swollen neck was evident as a symptom of DNI
under general anaesthesia. in 70 per cent of the DM patients as compared with
Statistical analyses were performed to assess the risk only 46.1 per cent of the non-DM patients. Odyno-
factors for DNI. The analyses included the Student phagia was evident in 22.5 per cent of DM patients
t-test, Chi-square and Fisher exact tests, Mann– but in only 8.7 per cent of non-DM patients. Sore
Whitney U test, and multiple logistic regression. throat was a symptom in both populations (20 per
Significance was judged to be present at p , 0.05. 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
Results 15 000/mm was found in 22 per cent of the DM
Of the 131 patients in the retrospective study, 73 were group, compared with 18.6 per cent of the non-DM
male and 58 were female. Of these 131 patients, 40 group ( p . 0.05).
(31 per cent) were diabetic, 20 males and 20 The DNI was of unknown aetiology in 40 per cent
females (male to female ratio, 1:1). The remaining of the DM group and 40.6 per cent of the non-DM
91 patients (69 per cent of the total) were non- group. Of those cases of DNI of identifiable aetio-
diabetics, 53 males and 38 females (male to female logy, odontogenic origin and acute pharyngotonsilli-
ratio, 1.4:1). The age distribution of the DM and tis predominated in both groups. There were 11
non-DM groups is illustrated in Figure 1. The odontogenic DNIs (27.5 per cent) in the DM group,
median age in the DM group was 60.5 years. The involving five males and six females. Pharyngotonsil-
median age in the non-DM group was 45 years litis as the origin of DNI was diagnosed in 25 per cent
(ranging from one to 88 years). of the DM patients, 19.7 per cent of the non-DM
Deep neck infections were significantly more patients and 21.3 per cent of all patients. Less
prevalent in DM subjects over 60 years of age than common aetiologies were aerodigestive trauma, laryn-
in non-DM subjects of a similar age (x2 test, geal foreign body and pharyngo-laryngeal cancer.
p ¼ 0.004; odds ratio ¼ 3.14). The duration of the Thirty-three pus samples were taken for culture
DM and the level of HbA1c found are shown in analysis from DM patients, 32 from surgical drainage
Table I. Haemoglobin A1c was checked in 18 and the remainder from needle aspiration. Positive
patients, either on the day of admission or within cultures were obtained in 28 of these 33 samples
three months prior to admission. Of these 18 (84.8 per cent). In all, 28 positive cultures grew 13
patients, five were newly diagnosed with diabetes, genera, with Klebsiella pneumoniae as the most
two had been diagnosed within the previous two common aerobic pathogen, being found in 18 of the
years, while 10 had been diagnosed at least five cultures (54.4 per cent) (and representing the sole
years previously. One patient did not have their dura- bacterial species in 72.2 per cent of those 18 cultures).
tion of diabetes recorded. Eleven out of 18 patients Streptococcus groups A, D and E were the next most
(61.1 per cent) had an HbA1c level that was elevated abundant, these three groups being found in 18.2 per
by .10 per cent. Seventeen out of the 18 patients cent of cultures. Cultures from five patients (15.1 per
(94.4 per cent) had an HbA1c level that was elevated cent) yielded anaerobic bacteria. Three of these
by 7 per cent. 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
FIG. 1
indicators were not significant after Bonferroni
correction.
Age of deep neck infection (DNI) patients with diabetes mel-
litus (DM) and without DM included in the study. (Note that The 19 DM patients with complications were cate-
DNI was more prevalent in DM subjects over 60 years of age gorized into four groups with respect to the length of
than in non-DM subjects of a similar age ( p ¼ 0.004)). 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 653
TABLE IV practice in Taiwan, where an under-developed
TREATMENT FOR DEEP NECK INFECTION medical referral system leads to a lack of medial con-
sultation prior to patients’ presentation at a medical
Treatment DM patients Non-DM patients
n (%) n (%) centre. As expected, the surgical drainage rate and
tracheotomy rate in the DM group were significantly
Antibiotic only 8 (19) 45 (49.4) higher than those in the non-DM group. Thus, anti-
Antibiotic þ I&D 32 (80) 46 (50.5) biotic administration alone was not sufficient for
Tracheostomy 6/40 (15) 3/91 (3.2)
recovery. Early surgical intervention and airway

¼ significant; I&D ¼ incision and drainage; DM ¼ diabetes support should be planned during the initial clinical
mellitus preparation of DNI patients with DM.

Conclusions
HbA1c level recorded for most of these patients was
indicative of poor hyperglycaemia control for at least Diabetic DNI differs in several respects from that
three months before DNI onset. occurring in non-diabetics. Clinicians need to be
To our knowledge, this is the first study to report alert to the higher complication rate and abnormal
that most diabetics suffering DNI had a high HbA1c levels associated with DM. More aggressive
HbA1c level before DNI onset. Although the treatment should be included in the initial treatment
higher mean HbA1c level in DM patients with com- plan.
plications, as compared with those without compli-
cations, was not statistically significant (perhaps
reflecting the small sample size), the role of HbA1c . This is a retrospective study of 131 patients
in diabetics with DNIs remains to be more rigorously treated for deep neck infection
assessed. It may be prudent to monitor HbA1c levels . Diabetes mellitus was a significant risk factor
in all DNI patients who also have DM. However, in the development of deep neck infection and
such vigilance is not currently observed in hospitals occurred in 18 patients. Klebsiella
in Taiwan or in the United States.17 Further study pneumoniae was the commonest pathogen
of daily blood sugar control and HbA1c levels may . Diabetic patients with deep neck infection had
represent another approach to the investigation of a higher rate of complications and
DNI with DM. tracheotomies and a longer hospital stay
In agreement with published observations, DNI
infections caused by K. pneumoniae in our study
were clustered in the DM group. The reason for the Acknowledgement
association of K. pneumoniae infection with diabetes
mellitus is still unknown. The documented increase of We would like to thank Dr Lu Long-Sheng for his
pharyngeal colonization with Gram-negative bacteria advice regarding this paper.
may play a role.18 A second reason may be the failure
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