M i c ro o r g a n i s m s

o f t h e No s e an d
Paranasal Sinuses
Richard H. Haug, DDS

KEYWORDS
 Microorganism  Nose  Paranasal  Sinus

From a teleologic standpoint, the human nose NORMAL MICROFLORA OF THE NOSE AND
and paranasal sinuses developed from prehistoric PARANASAL SINUSES
ancestors with specific functions as the final Nomenclature
outcome. The pneumatization of the craniofacial
Consistent nomenclature is the key to com-
region by the nose and paranasal sinuses resulted
munication of the various microbes of the body
in a lighter weight of the skull, allowing humans to
from one health care professional to another.
begin standing upright, a departure from 4-legged
Taxonomy is the branch of biology that deals
mammalian relatives. The resonance provided by
with classification, and the taxonomic classifica-
this pneumatization permitted the development
tion system from the general to the most specific
of speech beyond simple barking and grunting
is kingdom, phylum, class, order, family, genus,
to eventually more culturally unique capabilities
and species.1,2 To create consistency and unifor-
such as chanting and ultimately singing. Although
mity during this review of microbes of the nose
the vibrissae of the nose create physical barriers to
and paranasal sinuses, the descriptions of the Pro-
foreign bodies ranging from insects to particulate
tista (bacteria, fungi, protozoa, and so forth), when
matter, the moist mucosal lining of the nose and
speaking in general terms, will include only the
paranasal sinuses traps finer substances and
genus. As an example, the genus Staphylococcus
microbes by mucostatic tension. The constant
contains many different species. When speaking in
fasciculation by the villi of the pseudostratified
more specific terms, both the genus and species
columnar epithelial lining helps to eliminate these
are included. Using the same example, the genus
potentially disease-threatening foreign bodies
and species might be Staphylococcus aureus or
and microbes. The moisture of this mucosa
Staphylococcus epidermidis. Although the viruses
humidifies and warms the air before it enters the
also follow the same classification scheme, they
lungs. The endogenous normal flora of the nose
are more frequently referred to by more common
and paranasal sinuses works to create an en-
names. For instance, the common name for one
vironment of homeostasis within the region. This
of the viruses of the herpes genera is herpes
homeostasis can be interrupted by eliminating
simplex virus type 1.
the anatomic barriers created by the skin, bone,
and mucosa, such as after trauma and/or surgery;
Factors Affecting Microbial Flora
by altering the atmosphere of the surroundings,
such as the creation of an anaerobic environment Most areas of the human body harbor an indige-
by obstruction of the sinus ostia or foramina; or by nous microbial flora that is specific to both that
a change in the normal flora of the region. To fully anatomic area and the individual human being.1,3–5
oralmaxsurgery.theclinics.com

understand the microbiological environment of As mentioned earlier, this specific ecosystem

this region, it is first important to understand the helps to play a role in protecting the individual
normal flora of the nose and paranasal sinuses. from invasion by pathogenic organisms. There

Carolinas Center for Oral Health, 1601 Abbey Place, Charlotte, NC 28209, USA
E-mail address: Richard.Haug@carolinashealthcare.org

Oral Maxillofacial Surg Clin N Am 24 (2012) 191–196

doi:10.1016/j.coms.2012.01.001
1042-3699/12/$ – see front matter Ó 2012 Elsevier Inc. All rights reserved.
192 Haug
are numerous factors that may alter the type,
frequency, and distribution of normally occurring
microbes of the body. These factors include such
entities as the individual host’s immune system,
the relative humidity of the specific anatomic
region, the presence or lack of oxygen, local
surface characteristics, the available nutrition,
any interaction between the microbes present,
and so forth.1,3,4 Although there is generally
a normal resident flora for any particular anatomic
region, a transient flora may also be found to colo-
nize for periods ranging from hours to weeks
without being retained permanently. The author’s
discussions are limited to indigenous flora (not
transient) and, for brevity, have been listed in box
form.
Nasal and Paranasal Sinus Microflora
Unlike the skin and mouth, the nasal passages and
paranasal sinuses are sterile at birth. Yet, within
days, the infant acquires a flora, mostly associated
with the mother, the nursing staff, and the specific
hospital that the newborn resides in.6–10 As the
human breathes air and its contents, it pass
through the nose. There the air is filtered, and
most of the microorganisms are trapped by
vibrissae and mucous secretions and are routinely
swallowed. These mucous secretions contain
enzymes and immunoglobulins that further kill or
inhibit the growth of microorganisms. Yet, with
time and altered host resistance, the adult human
acquires an indigenous microflora and occasion-
ally is subjected to colonization (Box 1).6–11 S
aureus and Haemophilus influenzae are the most
common inhabitants of the nose and paranasal
sinuses, although many others may inhabit this
region (see Box 1).
NASAL AND PARANASAL SINUS INFECTIONS
Acute Maxillary and Ethmoid Sinusitis
Sinusitis is a disease that results from an infection
of 1 or more of the paranasal sinuses.13,14 Acute
sinusitis is generally categorized by its etiology,
as nosocomial or community acquired, or as viral,
bacterial, or fungal.13,14 Combinations of these
etiologies are possible. Perhaps the most common
cause for acute maxillary sinusitis is an infection
secondary to a rhinovirus. The ability to accurately
culture viruses is a relatively recent development,
and thus changes and/or trends in viral pathoge-
nicity have not yet been established.
The etiology of acute community-acquired
bacterial sinusitis (ACABS) has been well substan-
tiated for the past 6 to 7 decades (Box 2).8,12–17 S
pneumoniae and H influenzae account for most
occurrences of this form of sinusitis. Yet other
Box 1
Some of the most common indigenous and
colonizing nasal and paranasal sinus flora
Aerobic and facultative isolates
Corynebacterium diphtheria
Corynebacterium species
H influenzae
Haemophilus parainfluenza
Neisseria species
Staphylococcus species
Streptococcus pneumoniae
Moraxella species
Micrococcus species
Neisseria meningitidis
S aureus
S epidermidis
Streptococcus viridans
Anaerobic isolates
Propionibacterium acnes
Data from Refs.6–9,12
Streptococcus species, S aureus, Moraxella catar-
rhalis, a-hemolytic Streptococci, and anaerobic
bacteria have also been associated with this
form of sinus infection. Complicating the diagnosis
and treatment of this problem has been the obser-
vation that both viruses and bacteria may be iden-
tified as simultaneously causing an ACABS. When
cultures fail to yield bacteria for an ACABS, which
occurs approximately 40% of the time, a viral
etiology should be suspected. Even fungi may be
responsible for an ACABS but are more associ-
ated with nosocomial sinusitis and sinus disease
developing in compromised hosts such as dia-
betic patients. S aureus, Pseudomonas aerugino-
sa, Serratia marcescens, Klebsiella pneumoniae,
Enterobacter species, Proteus mirabilis, and
Legionella pneumophila are also associated with
nosocomial sinusitis and the compromised host.13
The relative distribution of microorganisms res-
ponsible for ACABS has not changed in either
appearance or prevalence over the past 6
decades.12,13,17 What has changed is their antimi-
crobial susceptibility. Penicillin-resistant S aureus
has emerged as a difficult microbe to manage, along
with b-lactam–resistant strains of H influenza and
M catarrhalis. Worse yet has been the emergence
of multiple strains of resistant S pneumoniae.
The emergence of these forms of resistant
microbes is based on the acquisition of antibiotic
 Microorganisms of the Nose and Paranasal Sinuses 193

Box 2 Chronic Maxillary Sinusitis

Some common microorganisms responsible for
acute maxillary and ethmoid sinusitis
Aerobic and facultative isolates
Escherichia coli
H influenzae
M catarrhalis
Neisseria species
P aeruginosa
S aureus
S pneumoniae
Streptococcus pyogenes
Streptococcus
a-hemolytic
b-hemolytic
Anaerobic isolates
Bacteroides species
Fusobacterium species
Peptostreptococcus species
Viruses
Adenovirus
Influenza virus
Parainfluenza virus
Rhinovirus
Data from Refs.13,15–18
resistance mechanisms, either through mutation
or by transfer of genetic information from other
bacteria.19–21 Thus, there has been an increase
in the antibiotic resistance of important pathogenic
genera. The most dramatic example in the devel-
opment of resistance during the past 4 decades
in terms of cost, both economic and human, has
been the evolution of methicillin-resistant S aureus
(MRSA). It is estimated that methicillin resistance
in certain strains of Staphylococcus species has
arisen from 2.4% in the 1970s to 29% by the end
of the twentieth century and that the costs of
hospitalization for these types of nosocomial
infections could approach $3 billion annually in
the United States alone.13,22–36 Yet, it must be
remembered that money is not the real issue and
that the ultimate cost for humans is death. Post-
surgical patients who develop nosocomial infec-
tions such as MRSA are twice as likely to die as
those who do not.32,33
The specific etiology and pathogenicity of chronic
sinusitis disease (CSD) remains unanswered,
although its successful treatment modalities
continue to evade the clinician.16,17,37 Although
some cases of CSD exist as separate and distinct
entities, it has been assumed that most of these
infections arise from treatment failures of ACABS.
S pneumoniae, H influenzae, and other strepto-
coccal species have been isolated from patients
who have CSD (Box 3).8,9,15–17 Of particular
interest is that b-lactamase–producing strains of
S pneumoniae, H influenzae, and M catarrhalis
have been isolated in ACABS aspirates.37,38 It
would therefore seem likely that CSD is merely
the continued manifestation of an ACABS caused
by ineffective management.
Infectious Rhinitis
Infective rhinitis has been classified as acute, self-
limiting, or chronic and is the major component of
what many consider the common cold.39 Viruses
are the most frequent cause of infectious rhinitis,
and rhinoviruses are the most frequent causative
agent among viruses (Box 4).7,9,10,39 Bacteria are
an infrequent cause of isolated nasal infections but
are common as causes of combination nasal/para-
nasal sinus infections.39 Granulomatous nasal infec-
tions such as rhinoscleroma, tuberculosis, syphilis,
aspergillosis, and mucormycosis are rare and
caused by numerous microorganisms, including
fungi, protozoa, and mycobacterium.7,9,10,39
The herpes simplex virus is a common cause of
nasal/perinasal infection. This virus is usually intro-
duced into the body through mucosal exposure.
Although the initial infection may be subclinical,
recurrences are common. More than 90% of
Box 3
Some common microorganisms responsible for
chronic maxillary sinusitis
Aerobic and facultative isolates
Corynebacterium species
H influenzae
S pneumoniae
Anaerobic isolates
Bacteroides species
Peptostreptococcus species
Veillonella species
Data from Refs.8,12–17
194 Haug

Box 4 Frontal and Sphenoid Sinusitis

Some common microorganisms responsible for The microbial flora of infected frontal and sphenoid
rhinitis sinuses is separate and distinct from that of
Aerobic and facultative isolates maxillary and ethmoid sinuses. Acute sphenoid
and frontal sinusitis is uncommon, difficult to diag-
Klebsiella rhinoscleromatis
nose, carries with it a significant degree of
Mycobacteria morbidity, and yet accounts for less than 5% of
Mycobacterium tuberculosis paranasal sinus infections.18,40,41 Headache is the
most common consistent finding and may be
Spirochetes accentuated with activity or may become debili-
Treponema pallidum tating in the degree of pain associated with it.
Several organisms have been identified with this
Fungi disease (Box 5).15,18,40,41 S aureus, S pneumoniae,
Absidia species H influenza, and other streptococcal species are
Aspergillosis flavus the most frequent pathogens.18,40,41 Although
changes in the microbiology of the diseased frontal
Aspergillosis fumigatus
and sphenoid sinuses have not been identified by
Bipolaris species scientifically scrutinized investigations, changes
Cladosporium species in the clinical management point toward the use
Curvularia species of antibiotics that address b-lactamase–producing
strains of organisms. Especially problematic are
Exophiala species
b-lactamase–producing Staphylococci, Strepto-
Exserohilum species cocci, and H influenza.
Histoplasma capsulatum
Mucor species
Box 5
Rhinosporidium seeberi Some common microorganisms responsible for
Rhizopus species sphenoid and frontal sinusitis
Wangiella species Aerobic and facultative isolates
Protozoa b-hemolytic Streptococci
Leishmaniasis Citrobacter
Viruses Coliform bacilli
Adenovirus Enterococci
Enterovirus Escherichia coli
Influenza virus H influenzae
Parainfluenza virus K pneumoniae
Respiratory syncytial virus Pneumococci
Rhinovirus Proteus

Data from Refs.7,9,10,39 P aeruginosa

Serratia
S aureus
S epidermidis
adults have antibodies to herpes simplex virus.
The prevalence of this microorganism increases S pneumoniae
with decreasing socioeconomic status. It is more S viridans
prevalent in African Americans than other Ameri-
cans and more prevalent in Western Europe than Anaerobic isolates
the United States. Although relief and compla- Anaerobic streptococci
cency was initially perceived in medical and lay
Fungi
populations after the discovery of acyclovir,
consternation has again arisen with the isolation Aspergillus
of acyclovir-resistant strains of herpes simplex Data from Refs.15,18,40,41
virus with increasing frequency.
 Microorganisms of the Nose and Paranasal Sinuses
THE FUTURE
Although the taxonomic system described in the
introduction and used throughout the article
remains in clinical use, the development of a taxo-
nomic system based on DNA and RNA has
become of increasing importance in the potential
for identifying and/or classifying microbes.42–44
All living organisms of closely related individuals
share some basis of gene sequence similarity.
The use of sequence diversity in protein-coding
genes shows that there are sequence clusters
that correspond to unique ecological populations.
With this in mind, it is possible to identify related
and, conversely, unrelated individuals. The use of
polymerase chain reaction allows the use of
a single or very few strands of a DNA sequence
and then amplification of these strands thousands
or millions of times over, for the sequence to be
more readily identified. This technology permits
the identification and classification of living organ-
isms and, for the sake of this discussion, the iden-
tification of microbes in a more precise and
specific manner. Although an exciting concept
and useful in benchtop research and forensics,
this technology has not yet replaced the current
system of nomenclature.
THE PRESENT
S pneumoniae, H influenza, and S aureus are the
most common inhabitants of the healthy nose
and paranasal sinuses. When homeostasis is inter-
rupted by elective surgery, trauma, or a change in
the environment (altered humidity or oxygen
content), the normal flora will change. Although
acute sinusitis is most frequently attributed to
S pneumoniae and H influenza, acute rhinitis is
most commonly associated with viral infection.
From a microbial standpoint, chronic sinus infec-
tions seem to be mere failures of the treatment of
acute sinus infections. Of increasing concern is
the emergence of microbes that are resistant to
common antimicrobial agents. Whether by direct
mutation or transfer of genetic material from other
microbes, these bacteria have become a challenge
in antimicrobial management. At present, antibi-
otics that contain a b-lactamase inhibitor are
preferred.
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