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J Oral Maxillofac Surg

59:739-748, 2001

The Changing Face of Odontogenic


Infections
William Storoe, DDS,* Richard H. Haug, DDS,
and Thomas T. Lillich, PhD
Purpose:

The purpose of this investigation was to compare characteristics of patients hospitalized


with odontogenic infections during the 1980s to those of the 1990s.
Patients and Methods: This study was a retrospective record review that compared 2 cohorts of
patients admitted to the same institution during two 81-month periods, one decade apart. Admission
criteria were face or neck swelling suggesting abscess or cellulitis and one or more of the following:
temperature above 38C, white blood cell (WBC) count greater than 10.8 103/L, or concern about
airway compromise. Characteristics reviewed were age, gender, race, admission temperature, admission
WBC count, fascial space(s) involved, tooth of etiology, duration of hospitalization, and bacteria isolated.
Data were compared for statistical significance (P .05).
Results: No significant differences were found between the 2 cohorts for age, gender, race, admission
temperature, admission WBC count, space involvement, or length of stay (P .05). One tooth
(mandibular left first molar) of 52 was involved more frequently in the 1990 group (P .03).
Gram-positive cocci were isolated significantly more frequently from the 1990s patients than from the
1980s patients (P .03). There were also significant differences (P .02) between cohorts in the
isolation frequency of individual genera, such as alpha-hemolytic Streptococci, coagulase negative
staphylococci, Staphylococcus epidermidis, Bacteroides melanogenicus, beta-lactamase positive Bacteroides, Eikenella corrodens, and Neisseria species. Eighty-one percent of the bacteria cultured from the
1990s patients were resistant to one or more common antibiotics; 47% of these organisms were
Staphylococcus aureus.
Conclusion: No clinically significant differences existed in the characteristics of patients hospitalized
with odontogenic infections between the 1980s and the 1990s. Although there were differences in the
type and prevalence of bacteria isolated, this was probably a result of changes in nomenclature,
identification protocols, and isolation techniques.
2001 American Association of Oral and Maxillofacial Surgeons
discarded as no longer necessary because the new
drugs were so effective in treating common infections. Antibiotics were prescribed when symptoms
first appeared without first determining either the
cause of the disease or the chemotherapeutic susceptibility of the microbe. Many scientists and public
health professionals were ready to declare final victory over infectious diseases, being firmly convinced
that antibiotics and vaccines would solve existing and
future disease threats. Events of the last 20 years
suggest that such enthusiasm was premature.
Although there have been recent dramatic improvements in the morbidity and mortality associated with
infectious diseases, microorganisms have proved to
be quite adaptable, displaying an unsettling ability to
re-emerge in continuing cycles of disease.1 Neu2 observed that bacteria are more clever than men. They
have adapted to every environmental niche on the
planet and are now adjusting to a world laced with
antibiotics. This ability has been shown over the past
decade in the number and variety of so-called emerg-

The availability of penicillin and other wonder


drugs in the years immediately after World War II
ushered in an era of complacency in infectious disease treatment. Many traditional infectious disease
management approaches, such as isolation, quarantine, and scrupulous application of aseptic technique
in the office and operatory, were de-emphasized or

*Chief Resident, Division of Oral and Maxillofacial Surgery


MetroHealth Medical Center, Cleveland, OH.
Division Director and Professor of Oral and Maxillofacial Surgery, College of Dentistry, University of Kentucky, Lexington, KY.
Professor and Associate Dean, College of Dentistry, University
of Kentucky, Lexington, KY.
Address correspondence and reprint requests to Dr Haug: University of Kentucky, 800 Rose St, D-508 College of Dentistry,
Lexington, KY 40536-0084.
2001 American Association of Oral and Maxillofacial Surgeons

0278-2391/01/5907-0005$35.00/0
doi:10.1053/joms.2001.24285

739

740

CHANGING FACE

ing infections not previously recognized in humans


and also in the re-emergence of diseases, sometimes
in slightly different form, caused by well-known microorganisms such as Staphylococci, Streptococci,
Escherichia coli, and Mycobacterium tuberculosis.
Re-emergence is partly a result of acquisition of antibiotic resistance mechanisms either through mutation
or by transfer of genetic information from other bacteria.2,3 Consequently, there has been a significant rise
in the antibiotic resistance of important pathogenic
genera. Today, infectious diseases remain the leading
cause of death worldwide and are third in the United
States, where they also account for more than 25% of
physician office visits.1
Shifting infectious disease patterns and their manifestations have become a topic of discussion in the lay
press, often creating public alarm through hyperbole
and, occasionally, misinterpretation of events.4,5 According to Time magazine, for example, antibiotics
are so overused that the human body has become
saturated. This has depressed the immune system and
provided an environment for the creation of bacterial monsters.4 The media has also reported flesheating Streptococcus strains and killer bacteria that
are resistant to most common antibiotics.4,5 These
reports raise public concerns that the normal bacterial flora is mutating uncontrollably and that infections are much more severe than they used to be.
Although reports like these are dramatic, they are
based on assumption and empiricism rather than on
controlled investigations that identify demography,
epidemiology, and other characteristics of an infected
population. The question then arises: Is the face of
infection in the general population changing? More
specifically: Are the characteristics of patients with

odontogenic infections during this era different from


those in the past? The purpose of this investigation
was to review the characteristics of patients hospitalized with odontogenic infections within a specific
time frame (the 1980s) and then to compare them
with a similar population during an identical time
frame one decade later.

Patients and Methods


This investigation was conducted at the Cleveland
MetroHealth Medical Center, a large county teaching
hospital serving an urban population of 1.9 million
and a rural population of 2.0 million in northeastern
Ohio. Hospital charts and radiographs were reviewed
from 2 patient cohorts admitted to that institution;
the first during the 81 months between March 1983
and November 1989 (1980s patients)6 and the other
during the 81 months between July 1992 and March
1999 (1990s patients). There were eighty-six 1980s
patients; 79 of whom had complete records (91.9%)
(Table 1). There were seventy-three 1990s patients;
71 of whom (97.3%) had complete records (Table 1).
Admission criteria were swelling of the face or neck
suggesting abscess or cellulitis and 1 or more of the
following: temperature above 38.0C, white blood
cell (WBC) count greater than 10.8 103/L or
concern about airway compromise. Patient characteristics reviewed were gender, age, race, admission
temperature, admission WBC count, duration of hospitalization, fascial space(s) involved, tooth of etiology, and bacteria identified. Gender and race were
compared using a Pearson chi-square analysis. Age,
length of stay, admission temperature, and admission
WBC counts were compared with a 2-tailed t test.

Table 1. PATIENT CHARACTERISTICS

Total patients identified


Total patients with complete records
Gender
Male
Female
Race
White
African American
Hispanic
Asian
Age (yr)
Admission temperature (C)
Admission WBC count (WBC 103/l)
Length of stay (d)

No. of 1980s
Patients

No. of 1990s
Patients

Statistic*

86
79

73
71

0.063
0.006

.8
.9

45
34

40
31

0.006

.9

44
30
4
1

44
20
6
1

0.006

.6

0.989
0.960
1.040
0.567

.6
.4
.3
.6

31.40 17.97
37.76 0.76
14.40 5.36
6.66 6.20

Mean SD

32.58 10.90
37.62 0.92
13.93 4.837
8.27 11.59

*2 for total patients, gender, and race; t test for age, admission temperature, admission WBC, and length of stay.
Abbreviations: WBC, white blood cell.

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STOROE, HAUG, AND LILLICH

Tooth of etiology was compared using a chi- square


analysis. Fifty-two individual chi-square tests were required because 52 different teeth were identified as
being involved. For tests where 50% of the data cells
had expected counts less than 5, a Yates corrected
chi-square (continuity correction) was reported. Otherwise, a Pearson chi-square analysis was used to
determine the differences in tooth involvement between cohorts. No computations were performed for
frequency tables with zero tooth involvement. The
different anatomic spaces were compared with a
Mann-Whitney U test. Differences between cohorts in
frequency of bacteria identified by standard laboratory procedures were compared using a Pearson chisquare analysis. Thirty-five individual Pearson chisquare analyses were performed. A continuity
adjustment was made when more than 25% of the
cells had expected counts less than 6. Differences
between cohorts were considered significant for any
of the criteria if P .05.

Results
The 2 decades had equal proportions of patients
identified and patients with complete charts. There
was no significant difference between groups for gender, age, or ethnic distribution (Table 1). There was
also no difference for mean admission temperature,
mean admission WBC count, or mean length of stay
(Table 1).
There were 40 multispace infections (50.6%) in the
1980s patients and 37 (52.1%) in the 1990s patients
(Table 2). The submandibular space was most frequently involved in the patients with multispace infections in both groups; occurring 42 times (32.6%) in
the 1980s patients and 47 times (35.6%) in the 1990s
patients. It was also the most frequently involved
space in patients with single space infections; occuring 16 times in the 1980s patients (20.3%) and 17
times in the 1990s patients (23.9%). There was no
significant difference between groups with respect
to anatomic spaces involved (Mann-Whitney U
2505.5; (2-tailed) P .221).
Thirty different teeth were the source of infection
in the 1980s patients and 22 in the 1990s patients
(Table 3). Because this was a retrospective review of
records, it was not possible to identify the presence
or absence of any one tooth in all patients. Because
there were equal proportions between decades for
patients identified, patients with complete records,
and all other patient population characteristics such
as age, gender and race, it was assumed that there
would be equal proportions of individual teeth
present in individual patients from each decade. Because of these equal proportions, for our statistical
comparison, we assumed that all teeth were present

Table 2. FREQUENCY OF FASCIAL SPACE(S)


INVOLVED

Multiple space involvement


Total spaces
Multispace
Submandibular space
Lateral pharyngeal space
Buccal space
Submental space
Sublingual space
Retropharyngeal space
Canine space
Mediastinal space
Peritonsillar space
Pretracheal space
Medial pterygoid space
Masseteric space
Temporal space
Single space involvement
Total spaces
Submandibular space
Buccal space
Canine space
Submental space
Temporal space
Lateral pharyngeal space
Masseteric space

1980s
Patients

1990s
Patients

129
40(50.6%)
42(32.6%)
12(59.3%)
37(28.7%)
10(7.6%)
5(3.9%)
1(.8%)
13(10.1%)

5(3.9%)
4(3.1%)

132
37(52.1%)
47(35.6%)
23(17.4%)
15(11.4%)
12(9.1%)
5(3.8%)
4(3.0%)
3(2.3%)
2(1.5%)
1(.8%)
1(.8%)
1(.8%)

39
16(20.3%)
13(16.5%)
7(8.9%)
2(2.5%)
1(1.3%)

34
17(23.9%)
6(8.54%)
3(4.2%)
2(2.8%)
2(2.8%)
3(4.2%)
1(1.4%)

in all patients. The only tooth with a statistically


significant difference between decades was the mandibular left first molar (X2(1) 4.495, P .034),
being reported in the records with a frequency of
8.9% (7/79) for the 1980s and 20.1% (15/73) for the
1990s. Although a trend was observed that maxillary
molars were the etiology more frequently for the
1980s patients than for the 1990s patients (13 vs 8),
the mandibular molars as a group were the more
frequent etiology in the 1990s than the 1980s (91 vs
64). It must be noted that both single and multiple
mandibular molars were the etiology in individual
patients.
The manner in which we reported the bacteria
isolated was limited by our ability to retrieve data in a
retrospective review of records and by changes in
nomenclature and culture techniques from the 1980s
to the 1990s. Patients in both groups were cultured
according to prevailing clinical laboratory techniques
and protocols. All isolates from any one individual,
whether from a sterile abscess, multiple sites, or
multiple cultures, were recorded. At least one bacterium was isolated from 96% (76/79) of patients in the
1980s group and 90% (64/71) in the 1990s group.
Most patients from both groups (1980s: 65/79 and
1990s: 60/71) had multiple organisms isolated. There
were 180 bacteria isolated from seventy-nine 1980s
patients compared with 115 from seventy-one 1990s

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CHANGING FACE

Table 3. FREQUENCY OF TOOTH INVOLVEMENT

Tooth Number/Letter

1980s Patients

1990s Patients

Maxillary left third molar


Maxillary left second molar
Maxillary left first molar
Maxillary left second premolar
Maxillary left first premolar
Maxillary left canine
Maxillary left lateral incisor
Maxillary left central incisor
Maxillary right central incisor
Maxillary right lateral incisor
Maxillary right canine
Maxillary right first premolar
Maxillary right second premolar
Maxillary right fist molar
Maxillary right second molar
Maxillary right third molar
Mandibular right third molar
Mandibular right second molar
Mandibular right first molar
Mandibular right second premolar
Mandibular right first premolar
Mandibular right canine
Mandibular right lateral incisor
Mandibular right central incisor
Mandibular left central incisor
Mandibular left lateral incisor
Mandibular left canine
Mandibular left first premolar
Mandibular left second premolar
Mandibular left first molar
Mandibular left second molar
Mandibular left third molar
Maxillary deciduous left second molar
Maxillary deciduous left first molar
Maxillary deciduous left canine
Maxillary deciduous left lateral incisor
Maxillary deciduous left central incisor
Maxillary deciduous right central incisor
Maxillary deciduous right lateral incisor
Maxillary deciduous right canine
Maxillary deciduous right first molar
Maxillary deciduous right second molar
Mandibular deciduous right second molar
Mandibular deciduous right first molar
Mandibular deciduous right canine
Mandibular deciduous right lateral incisor
Mandibular deciduous right central incisor
Mandibular deciduous left central incisor
Mandibular deciduous left lateral incisor
Mandibular deciduous left canine
Mandibular deciduous left first molar
Mandibular deciduous left second molar

1
2
2
0
0
1
1
0
0
2
1
0
2
4
1
1
15
13
7
1
1
2
2
1
2
0
1
3
5
6
9
14
0
1
1
1
0
0
0
2
2
0
1
1
0
1
1
1
1
0
1
0

1
0
1
0
0
0
1
2
1
0
1
0
0
0
2
4
21
13
15
6
4
0
1
1
1
1
1
0
4
10
14
18
0
0
0
0
0
0
0
0
0
0
1
1
1
0
0
0
0
0
0
0

patients. For the initial analysis, isolates were grouped


into 4 categories: gram-positive cocci, other grampositive bacteria, gram-negative anaerobes and other
gram-negative bacteria (Table 4). Gram-positive cocci
(X2(1) 5.357, P .021) and gram-negative anaerobes (X2(1) 4.223, P .038) were isolated signif-

icantly less frequently from the 1990s patients than


from the 1980s patients.
Table 5 compares the frequency with which bacteria were isolated from the 2 groups. For instance,
alpha-hemolytic Streptococci were isolated from 47 of
79 patients during the 1980s and from 24 of 71 pa-

743

STOROE, HAUG, AND LILLICH

Table 4. BACTERIA ISOLATED

No. Isolated From


1980s Patients (% of total)

No. Isolated From


1990s Patients (% of total)

101(56)
9(5)
41(23)
29(16)
180(100)

80(70)
5(4)
15(13)
15(13)
115(100)

Gram-positive cocci
Other gram-positive bacteria
Gram-negative anaerobes
Other gram-negative bacteria
Total isolates

tients during the 1990s. Bacteria isolated from the


1980s patients belonged to 19 unique genera or species and those from the 1990s group to 24 unique
genera or species. Comparisons between the 2 patient groups revealed significant differences for alphahemolytic Streptococci, coagulase negative Staphylococci, Staphylococcus epidermidis, Bacteroides

5.357
0.066
4.323
0.520

.021
.8
.038
.5

melaninogenicus, beta-lactamase positive Bacteroides, Eikenella corrodens, and Neisseria species


(Table 5).
Culture and antibiotic sensitivity data were available from ten 1990s patients (14%) (Table 6). Data
from the 1980s patients were unavailable. Of the 32
bacterial isolates, 81% (26/32) were resistant to one

Table 5. COMPARISON OF BACTERIA IDENTIFIED FROM BOTH PATIENT GROUPS

Bacteria
Gram-positive cocci
Alpha-Hemolytic Streptococci
Beta-Hemolytic Streptococci
Staphylococcus aureus
Coagulase-negative Staphylococci
Staphylococcus epidermidis
Gamma-Hemolytic Streptococci
Peptostreptococcus sp
Enterococcus sp
Other gram-positive bacteria
Diphtheroids
Actinomyces sp
Lactobacillus sp
Corynebacterium sp
Gram-negative anaerobes
Bacteroides melaninogenicus
Bacteroides (-lactamase )
Bacteroides (-lactamase )
Bacteroides (not fragilis)
Fusobacterium necrophorum
Bacteroides fragilis
Other gram-negative bacteria
Eikenella corrodens
Haemophilus influenzae
Neisseria sp
Klebsiella sp
Enterobacter sp
Escherichia coli
Citrobacter sp
Hemophilus hemolyticus
Proteus mirabilis
Actinobacter calcoaceticus (Iwoffi)
Serratia marcescens
Pseudomonas aeruginosa
Pseudomonas sp
Stenotrophomonas maltophilia
Total Isolates

No. of
1980s Patients

No. of
1990s Patients

47
22
12

15
2
3

24
21
8
18

5
3
1

9.900
0.055
0.498
22.759
14.979
0.846*
0.000*
0.003*

0.002
0.815
0.480
0.001
0.001
0.358
1.000
0.957

6
2
1

0.023
0.406*
0.000*
0.003*

0.878
0.524
1.000
0.957

27

6
4
2
2
1

29.59
4.928
2.660*
0.622*
0.622*
0.000*

0.001
0.03
0.103
0.430
0.430
1.000

13
8
9
4
3
3
1
1

180

3
2

3
1

1
1
1
1
1
1
115

5.870
2.144*
6.704*
0.000*
0.159*
1.155*
0.000*
0.000*
0.003
0.003*
0.003*
0.003*
0.003*
0.003*

0.02
0.143
0.01
1.000
0.690
0.283
1.000
1.000
0.957
0.957
0.957
0.957
0.957
0.957

* Yates corrected chi-square is reported because more than 50% of the cells have expected counts less than 5.

744

CHANGING FACE

Table 6. ANTIBIOTIC RESISTANCE IN THE 1990s PATIENTS ISOLATES

Isolate
Gamma Streptococci (not Enterococcus)
Beta Streptococci (non A/B)
Coagulase-negative Staphylococci
Enterococcus
Staphylococcus aureus
Total gram positive
Actinobacter calcoaceticus (lwoffi)
Bacteroides sp
Eikenella sp
Enterobacter cloacae
Klebsiella pneumoniae
Pseudomonas aeruginosa
Pseudomonas-like
Stenothrophomonas maltophilia
Total gram negative
Totals

or more antibiotic. Sixty-two percent of the resistant


bacteria were gram positive (16/26) and 38% were
gram negative (10/26); Staphylococcus aureus and
coagulase negative staphylococci were the most common gram-positive antibiotic resistant bacteria isolated. Klebsiella pneumoniae was the most common
gram-negative antibiotic resistant isolate.

Discussion
There are several surveys in the surgical literature
concerning the epidemiology of odontogenic infections that are relevant to this investigation. Their
study designs will be summarized and then comparisons made with the present study in the context of
the patient populations investigated.
Kannangara et al7 studied the bacteriology and
treatment of dental infections in 61 patients treated
between 1976 and 1979. They reported limited population data, but did identify bacteria. Between January 1973 and January 1976, Hunt et al8 collected
epidemiologic and microbiologic data from patients
with odontogenic infections. However, data from this
study may be less relevant because the information
was from only 74 patients from among several hundred reviewed. Dodson et al9 retrospectively reviewed the demographics of 113 pediatric patients
with odontogenic infections admitted from January
1982 through December 1986. Heimdahl et al10 reported management and microbiologic data for 58
patients with odontogenic infections, but provided
only limited demographic data.
Sethi and Stanley11 reported gender, age, admission
temperature, and bacteria involved in their retrospective review of 61 patients with deep neck space
abscesses. However, not all their infections were

No. Resistant

No. Sensitive

Total

0
0
6
1
9
16
1
0
1
1
3
1
2
1
10
26

1
1
0
0
1
3
0
1
0
0
0
2
0
0
3
6

1
1
6
1
10
19
1
1
1
1
3
3
2
1
13
32

odontogenic. Bartlett and OKeefe12 reported demographic data for 20 patients; however, they concentrated on perimandibular space infections, not all of
which were odontogenic. Between 1978 and 1980,
Labriola et al13 treated 50 consecutive patients with
orofacial infections in whom they investigated anatomic space involvement and microbial etiology;
however, again the infections were not purely odontogenic. Between 1981 and 1990 Har-el et al14 conducted a retrospective survey of 110 patients with
deep neck abscesses in which microbe involvement,
space involvement, and selected patient characteristics were reported. This study also has limited applicability because not all infections were odontogenic.
Sakaguchi et al15 investigated 91 patients with deep
neck infections between 1985 and 1994. Although
they reported space involvement and some patient
characteristics, not all study participants had infections of odontogenic origin.
In their 1978 review, Chow et al16 concluded that
the clinical manifestations of odontogenic orofacial
infections were a result of both the microbial flora
causing the infection and the anatomic route(s) by
which it spread through the fascial planes. They also
discussed how different aspects of the human dentition are more apt to infect predetermined fascial
planes, and they identified the tooth of etiology corresponding to these infections. Moenning et al17 reported that the understanding of the complex microbial environment of odontogenic infections and the
perceived changes in etiology over time might be a
result of changes in the methods of collecting and
analyzing samples. It may reflect greater recognition
of bacterial species that have always been involved or
may merely reflect poor cutaneous skin preparation
and scrub techniques.

745

STOROE, HAUG, AND LILLICH

Haug et al6 previously observed that epidemiologic


survey groups vary with geographic region, population density, socioeconomic status, regional government, era in time, and facility in which the study was
conducted. The current study reduced or eliminated
most of the variables by comparing 2 matched patient
populations over 2 periods of 81 months each, 10
years apart, who were all treated at the same institution.
GENDER

There have been few reports describing the relationship between patient gender and the incidence of
odontogenic infection. Kannangara et al7 reported a
male predominance in his study, finding 40 (66%)
males and 21 females (34%). Dodson et al9 review of
113 pediatric patients with odontogenic infections
also identified a male predominance, with 67 males
(59%) and 46 females (41%). Hunt et als9 survey
noted a female predominance with 30 males (41%)
and 43 females (59%). Sethi and Stanley11 identified a
slight predilection for males, but did not list exact
numbers for each gender. Although the present investigation identified no significant gender differences
between the groups, both did have a slight predilection toward males.
AGE

A broad age range was found in both study groups.


The ages ranged from 3.0 years in both groups to 56.0
years in the 1980s patients and 83.3 years in the 1990s
patients. The mean age was 31.40 17.97 for the
1980s patients and was 32.58 10.90 for the 1990s
patients.
There was no significant difference in age between
the 2 groups. These findings correlate well with previous reports. Kannangara et als7 study was similar,
with a range of 6 to 79 years, and most patients being
between 20 and 29 years old. Sethi and Stanley11
reported a similar range of 3 to 87 years, with a mean
of 45.5. Sakaguchi et als15 study corresponds most
closely to this investigation, with a mean of 36 years
and a range of 1 to 81 years. However, as already
noted, not all of the deep neck space infections in
that investigation were odontogenic. Bartlett and
OKeefe12 reported an age range of 23 to 70 years,
with a mean of 43 years; however, their study only
involved 20 patients. Dodson et als9 study of 113
pediatric patients reported a mean age of 4.55 years.
RACE

This investigation was conducted in a region with


the following racial distribution: White (72%), African
American (24%), Hispanic (2%), Asian (1%), and other
(1%). The only previous study to consider the relationship between race and infection was by Haug et

al6 which showed a disproportionately high number


of infections in the racial minorities in the region. The
present study also found a disproportionately high
percentage of African Americans and Hispanics with
infection as compared with the general population of
the region (Table 1); although no significant differences were found between the 1989 and 1999 cohorts.6
ADMISSION TEMPERATURE

A temperature greater than 37.0C is considered to


be a fever, or pyrexia.18,19 It is a result of the hypothalamic-thermoregulation centers response to regulatory chemicals induced by bacterial cell components such as endotoxins or cell wall fragments.18-20
Temperature is both a good predictor of acute infection and a way to monitor a patients response to
treatment.20 Sethi and Stanley11 reported a mean admission temperature of 38.4C (range, 37.0C to
39.5C), but not all the infections were odontogenic.
Dodson et al9 reported a mean admission temperature
of 38.17C, but no range was reported. The mean oral
admission temperature for the 1980s patients in this
study was 37.76C (range, 36.0C to 39.2C). This
was similar to the mean for the 1990s patients oral
admission temperature of 37.62C (range, 36.0C to
39.8C). Both Sethi and Stanleys and Dodson et als
mean admission temperatures correlated well with
these findings.
ADMISSION WHITE BLOOD CELL COUNT

Acute bacterial infections trigger a neutrophil release from the bone marrow, and thus an increase in
these cells in peripheral blood is a useful indicator of
infection.18,19 Dodson et al9 reported an average admission WBC count of 13.29 103/L for a pediatric
population; however, no range was cited. Heimdahl
et al10 concluded that the WBC count is of minor
importance when judging the severity of an orofacial
infection. Perhaps the WBC count is most useful in
assessing improvement or regression of a patients response to therapy, rather than as a predictor of actual
patient status. There was no significant difference in
admission WBC counts between our 2 study groups.
LENGTH OF STAY

Patients generally remain hospitalized until the infection resolves or is controlled, until there is no
further airway compromise, and until the patient is
returning to a preinfection state of health. Har-el et
al14 reported an average hospital stay of 8.9 days for
110 patients with deep neck abscesses. Sakaguchi et
al8 reported an average stay of 8.2 days (range, 1 to 31
days) for patients with deep neck infections. Dodson
et al9 reported an average length of hospitalization of
3.5 days for a pediatric population. The present study

746
found an average stay of 6.66 days (range, 1 to 41
days) for the 1980s patients, and the 1990s patients
had an average stay of 8.27 days (range, 2 to 69 days).
The length of stay for both groups was similar to
those reported for other studies except Dodson et
als9 pediatric population. This indicates that the
length of hospitalization is similar in different regions
of the world when similar adult infections are compared. However, there is a difference between length
of hospitalization for adults and children. Also, although there has been a trend over the last decade
toward outpatient management of patients in the general medical community, this investigation identified
no such change in the treatment of patients with
odontogenic infections. Changes in health care reimbursement have shifted management of healthy patients or elective surgeries into the outpatient arena,
but acute emergencies and life-threatening problems
have remained as situations warranting admission and
inpatient management. Certainly airway compromise
and the potential for sepsis continue to warrant the
vigilance afforded by the inpatient setting. Moreover,
although not statistically significant, the mean length
of stay was longer in the 1990s, indicating that either
the patients were sicker or took longer to improve. A
contributing factor may be the increasing incidence
of antibiotic resistant bacteria.21,22
ANATOMIC SPACE

Odontogenic soft tissue infections usually spread


from the structures supporting the affected tooth
along the planes of least resistance to the fascial
spaces in the vicinity.16 Labriola et al13 found that the
most frequent single space infection was submandibular (26%), followed by buccal (21%), masticator
(15%), and canine (13%). They did not offer information about multispace infections. Our study identified
a similar order of frequency in both groups for both
single and multispace infections.
TOOTH INVOLVEMENT

Chow et al16 discussed potential pathways for


spread of infection and how odontogenic infections
most commonly involve the mandibular molar teeth.
Other authors have also reported the mandibular molars as the most frequently involved teeth in odontogenic infections.6,11,16 This report confirms these previous studies. The mandibular third molar was the
most frequently involved tooth in both groups; only
the mandibular left first molar was significantly different between the 2 groups. We have no explanation
for this observation.
BACTERIAL INVOLVEMENT

Until the mid-1970s, it was believed that odontogenic infections were caused by a single species of

CHANGING FACE

aerobic or facultative bacteria.18 Subsequently, it has


been well established that odontogenic infections are
polymicrobial.6,10,11,16-20,23-26 It has also been observed
that the bacteria identified from odontogenic infections have changed over the decades.17,18 Moenning
et al17 reported that the bacterial flora of odontogenic
infections is no longer predominately facultative or
microaerophilic, with Staphylococcus and Streptococcus as the primary genera, but rather is more often a
mixed flora with anaerobes outnumbering aerobes
2:1. Alpha-hemolytic streptococci are the most frequently isolated bacteria8,12,13; although Bacteroides
melaninogenicus has been reported as the most common in some studies.14,16 In this study, there were 19
bacterial genera or species isolated in the 1980s patients, with alpha-hemolytic Streptococci predominating almost 2:1 over B melaninogenicus and betahemolytic Streptococci 3:1 over S epidermidis, and
almost 4:1 over S aureus and E corrodens (Table 5).
There were 24 genera or species isolated in the 1990s
patients, with coagulase-negative Staphylococci, alpha-hemolytic Streptococci, and beta-hemolytic Streptococci having nearly a 1:1:1 ratio and predominating
equally over all other bacteria by more than a 2:1
ratio (Table 5). No isolates of B melaninogenicus
were reported in the 1990s patients; however 13
other Bacteroides isolates were identified. Significant differences between the groups were found
for alpha-hemolytic Streptococci, coagulase-negative
staphylococci, S epidermidis, B melaninogenicus,
beta-lactamase positive Bacteroides, E corrodens, and
Neisseria species suggesting that there has been a
shift in the microbiologic flora involved in odontogenic infections. Alpha-hemolytic Streptococci were
the most common isolates in both groups, thus confirming previous reports of the frequency with which
these bacteria are isolated from odontogenic infections.8,12,13 It is clear that these common Gram-positive cocci remain a threat to patients with odontogenic infections. The significance of the differences
for the other isolates is less clear because of changes
in bacterial nomenclature and laboratory protocols in
the past 10 years. For example, there was a statistically significant difference between groups for B
melaninogenicus mainly because there were no isolates identified from the 1990s patients. This is because B melaninogenicus was reclassified in 1990;
bacteria identified as B melaninogenicus in the 1980s
patients should have been reported as either Prevotella or Porphyromonas in the 1990s patients.25
Consequently, the difference between the 2 groups
for this obligate anaerobe is a statistical anomaly.
The statistically significant difference between
groups for S epidermidis and coagulase-negative
staphylococci can be explained by changes in laboratory protocol. S epidermidis is a coagulase-negative

747

STOROE, HAUG, AND LILLICH

staphylococcus. During the 1980s, it was common to


speciate isolates, although this provided little clinically useful information. Consequently, protocol
changes were made that resulted in all coagulasenegative staphylococci being reported as such without further identification. A more accurate picture
of the statistically significant differences between
groups emerges by analyzing S epidermidis and coagulase-negative staphylococci together. When this is
done, there is no significant difference between the
groups (X2(1) 0.883, 0.347). The significant decreases in Neisseria species and E corrodens from the
1980s patients to the 1990s patients are most probably a result of laboratory protocol changes and
changes in therapy, respectively. The complete absence of Neisseria identified in the 1990s patients
suggests a decision by the clinical laboratory not to
seek this species in clinical specimens from odontogenic infections. The decrease in E corrodens isolated
from the 1990s patients may be a result of improved
anaerobic infection treatment with antibiotics that
have been developed in the past 10 years. Unfortunately, no data about preadmission treatment were
available. The only other bacteria with a significant
difference between groups were beta-lactamase positive bacteroides, which were not reported at all in the
1980s patients. Although the reason for this change is
unclear, rather than reflecting some important shift in
odontogenic infection etiology, it is probably caused
by a nomenclature or protocol change. For example,
it is curious that there are no Prevotella or Porphyromonas species reported in the 1990s patients, despite their importance in periodontal and other odontogenic infections. It has been reported that more
than 50% of Prevotella species are beta- lactamase
producers.28 It is possible, therefore, that the significant difference seen between groups is another consequence of the nomenclature change in B melaninogenicus previously discussed. It can be concluded
that there has been little change in the kinds of bacteria isolated from odontogenic infections in the 2
groups of patients 10 years apart; alpha- hemolytic
streptococci remain the most frequently isolated bacteria.
From the limited antibiotic sensitivity data available
it was not possible to determine if there has been
changes between groups in the kind, number, and
frequency of resistant isolates. There were no data
available for the 1980s patients, and only 10% of the
1990s patients had a culture and antibiotic sensitivity
test done at least once during their hospitalization
(Table 6). Despite their limitations, the data confirm
some disturbing trends. Eighty-one percent (26/32) of
the isolates were resistant to one or more antibiotics.
Despite the relatively low overall occurrence (Table
5), S aureus was the most frequently identified anti-

biotic resistant isolate (9/32). In addition to its innate


virulence, S aureus is of increasing concern because
it, along with other Gram-positive cocci, is becoming
resistant to most common antibiotics. For example,
methicillin-resistant S aureus that also exhibits intermediate resistance (minimum inhibitory concentration 8 g/mL) to vancomycin, the antimicrobial
regarded as the antibiotic of last resort for these
bacteria, has recently been reported in Japan and the
United States.21 Another trend is the number of antibiotic-resistant coagulase-negative staphylococci isolated. These bacteria have long been regarded as apathogenic members of the normal flora; however,
they are increasingly becoming recognized as important causes of infections, especially those acquired in
hospitals.22 Because most of the infections they cause
are nosocomial, it should not be surprising to see increasing multiple antibiotic resistance. Against a background of the empiricism with which many clinicians
continue to treat these patients (eg, only 10% of the
patients in the 1990s had a culture and antibiotic
sensitivity test performed), it is predictable that there
will be more initial treatment failures and a consequent increase in patient morbidity and total cost of
care.
Moenning et al17 suggested that wounds or cavities
can become contaminated with normal skin microflora, including Staphylococcus species, through external drainage. Although it is possible that such contamination occurred during the harvest of culture
material in the cases included in this investigation, it
is unlikely because proper surgical technique and
rigorous preoperative antimicrobial skin preparation
were used. One would expect surgical technique and
skin preparation to improve with time, thereby reducing the incidence of sample contamination from cutaneous sources. However, this does not seem to be
the case in this comparison of odontogenic infections
from the 1980s and the 1990s, which showed no
change in the frequency of Staphylococcus species
isolated. Assuming that proper technique was followed
and that the sites were prepared properly, it is improbable that there has been a shift in the kinds of bacteria
causing odontogenic infections in the last 10 years.

Summary
This investigation of odontogenic infections and
the review of the literature indicate that patient characteristics and the clinical signs and symptoms patients exhibit have remained constant over the past 2
decades. There is a good deal of similarity between
the findings of this study and other investigations
performed at different institutions, under different
conditions, and at different times. What has changed
is the type and prevalence of bacteria isolated from

748
odontogenic infections; however, this is thought to
be due to changes in nomenclature, identification
protocols, and isolation techniques. Perhaps improvement in laboratory procedures to process, grow, and
identify bacteria from odontogenic infections has led
to this difference. A definitive explanation of this
change awaits prospective studies that use more rigorous microbial identification procedures than are
normally used in hospital settings. An especially important aspect of subsequent studies will be a determination of the antibiotic sensitivity patterns of the
bacteria isolated from odontogenic infections.

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