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Normal Microbial Flora
of the Human Body
The term “normal microbial flora” denotes the population of microorganisms that inhabit the skin and
mucous membranes of healthy normal persons. It is
doubtful whether a normal viral flora exists in humans.
The skin and mucous membranes always harbor a
variety of microorganisms that can be arranged into two
groups: (1) The resident flora consists of relatively fixed
types of microorganisms regularly found in a given area
at a given age; if disturbed, it promptly reestablishes
itself. (2) The transient flora consists of nonpathogenic
or potentially pathogenic microorganisms that inhabit
the skin or mucous membranes for hours, days, or
weeks; it is derived from the environment, does not produce disease, and does not establish itself permanently
on the surface. Members of the transient flora are generally of little significance so long as the normal resident
flora remains intact. However, if the resident flora is disturbed, transient microorganisms may colonize, proliferate, and produce disease.
Organisms frequently encountered in specimens
obtained from various areas of the human body—and
considered normal flora—are listed in Table 11–1. The
classification of anaerobic normal bacterial flora is discussed in Chapter 22.
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tition for receptors or binding sites on host cells, competition for nutrients, mutual inhibition by metabolic or
toxic products, mutual inhibition by antibiotic materials or bacteriocins, or other mechanisms. Suppression of
the normal flora clearly creates a partial local void that
tends to be filled by organisms from the environment or
from other parts of the body. Such organisms behave as
opportunists and may become pathogens.
On the other hand, members of the normal flora
may themselves produce disease under certain circumstances. These organisms are adapted to the noninvasive
mode of life defined by the limitations of the environment. If forcefully removed from the restrictions of that
environment and introduced into the bloodstream or
tissues, these organisms may become pathogenic. For
example, streptococci of the viridans group are the most
common resident organisms of the upper respiratory
tract. If large numbers of them are introduced into the
bloodstream (eg, following tooth extraction or tonsillectomy), they may settle on deformed or prosthetic heart
valves and produce infective endocarditis. Small numbers occur transiently in the bloodstream with minor
trauma (eg, dental scaling or vigorous brushing). Bacteroides species are the commonest resident bacteria of
the large intestine and are quite harmless in that location. If introduced into the free peritoneal cavity or into
pelvic tissues along with other bacteria as a result of
trauma, they cause suppuration and bacteremia. There
are many other examples, but the important point is
that microbes of the normal resident flora are harmless
and may be beneficial in their normal location in the
host and in the absence of coincident abnormalities.
They may produce disease if introduced into foreign
locations in large numbers and if predisposing factors
are present.
ROLE OF THE RESIDENT FLORA
The microorganisms that are constantly present on
body surfaces are commensals. Their flourishing in a
given area depends upon physiologic factors of temperature, moisture, and the presence of certain nutrients and
inhibitory substances. Their presence is not essential to
life, because “germ-free” animals can be reared in the
complete absence of a normal microbial flora. Yet the
resident flora of certain areas plays a definite role in
maintaining health and normal function. Members of
the resident flora in the intestinal tract synthesize vitamin K and aid in the absorption of nutrients. On
mucous membranes and skin, the resident flora may
prevent colonization by pathogens and possible disease
through “bacterial interference.” The mechanism of
bacterial interference is not clear. It may involve compe-
NORMAL FLORA OF THE SKIN
Because of its constant exposure to and contact with the
environment, the skin is particularly apt to contain transient microorganisms. Nevertheless, there is a constant
and well-defined resident flora, modified in different
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NORMAL MICROBIAL FLORA OF THE HUMAN BODY
Table 11–1. Normal bacterial flora.
Skin
Staphylococcus epidermidis
Staphylococcus aureus (in small numbers)
Micrococcus species
Nonpathogenic neisseria species
Alpha-hemolytic and nonhemolytic streptococci
Diphtheroids
Propionibacterium species
Peptostreptococcus species
Small numbers of other organisms (candida species, acinetobacter species, etc)
Nasopharynx
Any amount of the following: diphtheroids, nonpathogenic neisseria species, α-hemolytic streptococci;
S epidermidis, nonhemolytic streptococci, anaerobes
(too many species to list; varying amounts of prevotella
species, anaerobic cocci, fusobacterium species, etc)
Lesser amounts of the following when accompanied by
organisms listed above: yeasts, haemophilus species,
pneumococci, S aureus, gram-negative rods, Neisseria
meningitidis
Gastrointestinal tract and rectum
Various Enterobacteriaceae except salmonella, shigella,
yersinia, vibrio, and campylobacter species
Non-dextrose-fermenting gram-negative rods
Enterococci
Alpha-hemolytic and nonhemolytic streptococci
Diphtheroids
S aureus in small numbers
Yeasts in small numbers
Anaerobes in large numbers (too many species to list)
Genitalia
Any amount of the following: corynebacterium species,
lactobacillus species, α-hemolytic and nonhemolytic
streptococci, nonpathogenic neisseria species
The following when mixed and not predominant: enterococci, Enterobacteriaceae and other gram-negative
rods, S epidermidis, Candida albicans, and other yeasts
Anaerobes (too many to list); the following may be important when in pure growth or clearly predominant: prevotella, clostridium, and peptostreptococcus species
anatomic areas by secretions, habitual wearing of clothing, or proximity to mucous membranes (mouth, nose,
and perineal areas).
The predominant resident microorganisms of the
skin are aerobic and anaerobic diphtheroid bacilli (eg,
corynebacterium, propionibacterium); nonhemolytic
aerobic and anaerobic staphylococci (Staphylococcus epidermidis, occasionally S aureus, and peptostreptococcus
species); gram-positive, aerobic, spore-forming bacilli
that are ubiquitous in air, water, and soil; alphahemolytic streptococci (viridans streptococci) and enterococci (enterococcus species); and gram-negative col-
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iform bacilli and acinetobacter. Fungi and yeasts are
often present in skin folds; acid-fast, nonpathogenic
mycobacteria occur in areas rich in sebaceous secretions
(genitalia, external ear).
Among the factors that may be important in eliminating nonresident microorganisms from the skin are
the low pH, the fatty acids in sebaceous secretions, and
the presence of lysozyme. Neither profuse sweating nor
washing and bathing can eliminate or significantly modify the normal resident flora. The number of superficial
microorganisms may be diminished by vigorous daily
scrubbing with soap containing hexachlorophene or
other disinfectants, but the flora is rapidly replenished
from sebaceous and sweat glands even when contact
with other skin areas or with the environment is completely excluded. Placement of an occlusive dressing on
skin tends to result in a large increase in the total microbial population and may also produce qualitative alterations in the flora.
Anaerobes and aerobic bacteria often join to form
synergistic infections (gangrene, necrotizing fasciitis,
cellulitis) of skin and soft tissues. The bacteria are frequently part of the normal microbial flora. It is usually
difficult to pinpoint one specific organism as being
responsible for the progressive lesion, since mixtures of
organisms are usually involved.
NORMAL FLORA OF THE MOUTH
& UPPER RESPIRATORY TRACT
The flora of the nose consists of prominent corynebacteria, staphylococci (S epidermidis, S aureus), and streptococci.
The mucous membranes of the mouth and pharynx
are often sterile at birth but may be contaminated by
passage through the birth canal. Within 4–12 hours
after birth, viridans streptococci become established as
the most prominent members of the resident flora and
remain so for life. They probably originate in the respiratory tracts of the mother and attendants. Early in life,
aerobic and anaerobic staphylococci, gram-negative
diplococci (neisseriae, Moraxella catarrhalis), diphtheroids, and occasional lactobacilli are added. When
teeth begin to erupt, the anaerobic spirochetes, prevotella species (especially P melaninogenica), fusobacterium species, rothia species, and capnocytophaga
species (see below) establish themselves, along with
some anaerobic vibrios and lactobacilli. Actinomyces
species are normally present in tonsillar tissue and on
the gingivae in adults, and various protozoa may also be
present. Yeasts (candida species) occur in the mouth.
In the pharynx and trachea, a similar flora establishes
itself, whereas few bacteria are found in normal bronchi.
Small bronchi and alveoli are normally sterile. The predominant organisms in the upper respiratory tract, par-
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ticularly the pharynx, are nonhemolytic and alphahemolytic streptococci and neisseriae. Staphylococci,
diphtheroids, haemophili, pneumococci, mycoplasmas,
and prevotellae are also encountered.
Infections of the mouth and respiratory tract are usually caused by mixed oronasal flora, including anaerobes. Periodontal infections, perioral abscesses, sinusitis,
and mastoiditis may involve predominantly Prevotella
melaninogenica, fusobacteria, and peptostreptococci.
Aspiration of saliva (containing up to 102 of these
organisms and aerobes) may result in necrotizing pneumonia, lung abscess, and empyema.
The Role of the Normal Mouth Flora
in Dental Caries
Caries is a disintegration of the teeth beginning at the
surface and progressing inward. First the surface enamel,
which is entirely noncellular, is demineralized. This has
been attributed to the effect of acid products of bacterial
fermentation. Subsequent decomposition of the dentin
and cement involves bacterial digestion of the protein
matrix.
An essential first step in caries production appears to
be the formation of plaque on the hard, smooth enamel
surface. The plaque consists mainly of gelatinous
deposits of high-molecular-weight glucans in which
acid-producing bacteria adhere to the enamel. The carbohydrate polymers (glucans) are produced mainly by
streptococci (Streptococcus mutans, peptostreptococci),
perhaps in association with actinomycetes. There
appears to be a strong correlation between the presence
of S mutans and caries on specific enamel areas. The
essential second step in caries production appears to be
the formation of large amounts of acid (pH < 5.0) from
carbohydrates by streptococci and lactobacilli in the
plaque. High concentrations of acid demineralize the
adjoining enamel and initiate caries.
In experimental “germ-free” animals, cariogenic
streptococci can induce the formation of plaque and
caries. Adherence to smooth surfaces requires both the
synthesis of water-insoluble glucan polymers by glucosyltransferases and the participation of binding sites on the
surface of microbial cells. (Perhaps carbohydrate polymers also aid the attachment of some streptococci to
endocardial surfaces.) Other members of the oral
microflora, eg, veillonellae, may complex with glucosyltransferase of Streptococcus salivarius in saliva and then
synthesize water-insoluble carbohydrate polymers to
adhere to tooth surfaces. Adherence may be initiated by
salivary IgA antibody to S mutans. Certain diphtheroids
and streptococci that produce levans can induce specific
soft tissue damage and bone resorption typical of periodontal disease. Proteolytic organisms, including actinomycetes and bacilli, play a role in the microbial action on
dentin that follows damage to the enamel. The development of caries also depends on genetic, hormonal, nutritional, and many other factors. Control of caries involves
physical removal of plaque, limitation of sucrose intake,
good nutrition with adequate protein intake, and reduction of acid production in the mouth by limitation of
available carbohydrates and frequent cleansing. The
application of fluoride to teeth or its ingestion in water
results in enhancement of acid resistance of the enamel.
Control of periodontal disease requires removal of calculus (calcified deposit) and good mouth hygiene.
Periodontal pockets in the gingiva are particularly rich
sources of organisms, including anaerobes, that are rarely
encountered elsewhere. While they may participate in
periodontal disease and tissue destruction, attention is
drawn to them when they are implanted elsewhere, eg,
producing infective endocarditis or bacteremia in a granulopenic host. Examples are capnocytophaga species and
Rothia dentocariosa. Capnocytophaga species are
fusiform, gram-negative, gliding anaerobes; rothia species
are pleomorphic, aerobic, gram-positive rods. Both probably participate in the complex microbial flora of periodontal disease with prominent bone destruction. In
granulopenic immunodeficient patients, they can lead to
serious opportunistic lesions in other organs.
NORMAL FLORA OF THE INTESTINAL
TRACT
At birth the intestine is sterile, but organisms are soon
introduced with food. In breast-fed children, the intestine contains large numbers of lactic acid streptococci
and lactobacilli. These aerobic and anaerobic, grampositive, nonmotile organisms (eg, bifidobacterium
species) produce acid from carbohydrates and tolerate
pH 5.0. In bottle-fed children, a more mixed flora exists
in the bowel, and lactobacilli are less prominent. As
food habits develop toward the adult pattern, the bowel
flora changes. Diet has a marked influence on the relative composition of the intestinal and fecal flora. Bowels
of newborns in intensive care nurseries tend to be colonized by Enterobacteriaceae, eg, klebsiella, citrobacter,
and enterobacter.
In the normal adult, the esophagus contains microorganisms arriving with saliva and food. The stomach’s
acidity keeps the number of microorganisms at a minimum (103–105/g of contents) unless obstruction at the
pylorus favors the proliferation of gram-positive cocci
and bacilli. The normal acid pH of the stomach
markedly protects against infection with some enteric
pathogens, eg, cholera. Administration of cimetidine for
peptic ulcer leads to a great increase in microbial flora of
the stomach, including many organisms usually prevalent in feces. As the pH of intestinal contents becomes
alkaline, the resident flora gradually increases. In the
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NORMAL MICROBIAL FLORA OF THE HUMAN BODY
adult duodenum, there are 103–106 bacteria per gram of
contents; in the jejunum and ileum, 105–108 bacteria
per gram; and in the cecum and transverse colon,
108–1010 bacteria per gram. In the upper intestine, lactobacilli and enterococci predominate, but in the lower
ileum and cecum, the flora is fecal. In the sigmoid colon
and rectum, there are about 1011 bacteria per gram of
contents, constituting 10–30% of the fecal mass. Anaerobes outnumber facultative organisms by 1000-fold. In
diarrhea, the bacterial content may diminish greatly,
whereas in intestinal stasis the count rises.
In the normal adult colon, 96–99% of the resident
bacterial flora consists of anaerobes: bacteroides species,
especially B fragilis; fusobacterium species; anaerobic lactobacilli, eg, bifidobacteria; clostridia (C perfringens,
103–105/g); and anaerobic gram-positive cocci (peptostreptococcus species). Only 1–4% are facultative aerobes (gram-negative coliform bacteria, enterococci, and
small numbers of protei, pseudomonads, lactobacilli,
candidae, and other organisms). More than 100 distinct
types of organisms occur regularly in normal fecal flora.
Minor trauma (eg, sigmoidoscopy, barium enema) may
induce transient bacteremia in about 10% of procedures.
Intestinal bacteria are important in synthesis of vitamin K, conversion of bile pigments and bile acids,
absorption of nutrients and breakdown products, and
antagonism to microbial pathogens. The intestinal flora
produces ammonia and other breakdown products that
are absorbed and can contribute to hepatic coma.
Among aerobic coliform bacteria, only a few serotypes
persist in the colon for prolonged periods, and most
serotypes of Escherichia coli are present only over a
period of a few days.
Antimicrobial drugs taken orally can, in humans, temporarily suppress the drug-susceptible components of the
fecal flora. This is commonly done by the preoperative
oral administration of insoluble drugs. For example,
neomycin plus erythromycin can in 1–2 days suppress
part of the bowel flora, especially aerobes. Metronidazole
accomplishes that for anaerobes. If lower bowel surgery is
performed when the counts are at their lowest, some protection against infection by accidental spill can be
achieved. However, soon thereafter the counts of fecal
flora rise again to normal or higher than normal levels,
principally of organisms selected out because of relative
resistance to the drugs employed. The drug-susceptible
microorganisms are replaced by drug-resistant ones, particularly staphylococci, enterobacters, enterococci, protei,
pseudomonads, Clostridium difficile, and yeasts.
The feeding of large quantities of Lactobacillus acidophilus may result in the temporary establishment of
this organism in the gut and the concomitant partial
suppression of other gut microflora.
The anaerobic flora of the colon, including B fragilis,
clostridia, and peptostreptococci, plays a main role in
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abscess formation originating in perforation of the
bowel. Prevotella bivia and P disiens are important in
abscesses of the pelvis originating in the female genital
organs. Like B fragilis, these species are penicillin-resistant; therefore, another agent should be used.
NORMAL FLORA OF THE URETHRA
The anterior urethra of both sexes contains small numbers of the same types of organisms found on the skin
and perineum. These organisms regularly appear in normal voided urine in numbers of 102–104/mL.
NORMAL FLORA OF THE VAGINA
Soon after birth, aerobic lactobacilli appear in the
vagina and persist as long as the pH remains acid (several weeks). When the pH becomes neutral (remaining
so until puberty), a mixed flora of cocci and bacilli is
present. At puberty, aerobic and anaerobic lactobacilli
reappear in large numbers and contribute to the maintenance of acid pH through the production of acid from
carbohydrates, particularly glycogen. This appears to be
an important mechanism in preventing the establishment of other, possibly harmful microorganisms in the
vagina. If lactobacilli are suppressed by the administration of antimicrobial drugs, yeasts or various bacteria
increase in numbers and cause irritation and inflammation. After menopause, lactobacilli again diminish in
number and a mixed flora returns. The normal vaginal
flora includes group B streptococci in as many as 25%
of women of childbearing age. During the birth process,
a baby can acquire group B streptococci, which subsequently may cause neonatal sepsis and meningitis. The
normal vaginal flora often includes also alpha hemolytic
streptococci, anaerobic streptococci (peptostreptococci),
prevotella species, clostridia, Gardnerella vaginalis, Ureaplasma urealyticum, and sometimes listeria or mobiluncus species. The cervical mucus has antibacterial activity
and contains lysozyme. In some women, the vaginal
introitus contains a heavy flora resembling that of the
perineum and perianal area. This may be a predisposing
factor in recurrent urinary tract infections. Vaginal
organisms present at time of delivery may infect the
newborn (eg, group B streptococci).
NORMAL FLORA OF THE CONJUNCTIVA
The predominant organisms of the conjunctiva are
diphtheroids (Corynebacterium xerosis), S epidermidis,
and nonhemolytic streptococci. Neisseriae and gramnegative bacilli resembling haemophili (moraxella
species) are also frequently present. The conjunctival
flora is normally held in check by the flow of tears,
which contain antibacterial lysozyme.
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REVIEW QUESTIONS
1. A 26-year-old woman visits her physician
because of an unusual vaginal discharge. On
examination the physician observes a thin,
homogeneous, white-gray discharge that
adheres to the vaginal wall. The pH of the discharge is 5.5 (normal: < 4.3). On Gram stain,
many epithelial cells covered with gram-variable rods are seen. Bacterial vaginosis is diagnosed. Which one of the following normal genital flora microorganisms is present in greatly
decreased numbers in bacterial vaginosis?
(A) Corynebacterium species
(B) Staphylococcus epidermidis
(C) Prevotella species
(D) Candida albicans
(E) Lactobacillus species
2. Certain microorganisms are never considered to
be members of the normal flora.They are always
considered to be pathogens. Which one of the
following organisms fits into that category?
(A) Streptococcus pneumoniae
(B) Escherichia coli
(C) Mycobacterium tuberculosis
(D) Staphylococcus aureus
(E) Neisseria meningitidis
3. A 9-year-old girl develops fever and severe pain
on the right side of her throat. On examination,
redness and swelling in the right peritonsillar
area are seen. A peritonsillar abscess is diagnosed. The most likely organisms to be cultured
from this abscess are
(A) Staphylococcus aureus
(B) Streptococcus pneumoniae
(C) Corynebacterium species and Prevotella
melaninogenica
(D) Normal oral nasal flora
(E) Viridans streptococci and Candida albicans
4. A 70-year-old man with a history of diverticulosis
of the sigmoid colon experiences a sudden onset
of severe left lower quadrant abdominal pain.
Fever develops. The severe pain gradually subsides and is replaced by a constant aching pain
and marked abdominal tenderness.A diagnosis of
probable ruptured diverticulum is made and the
patient is taken to the operating room. The diagnosis of ruptured diverticulum is confirmed and
an abscess next to the sigmoid colon is found.The
most likely bacteria to be found in the abscess are
(A) Mixed normal gastrointestinal flora
(B) Bacteroides fragilis alone
(C) Escherichia coli alone
(D) Clostridium perfringens alone
(E) Enterococcus species alone
5. Antimicrobial therapy can decrease the amount
of susceptible bowel flora and allow proliferation of relatively resistant colonic bacteria.
Which one of the following species can proliferate and produce a toxin that causes diarrhea?
(A) Enterococcus species
(B) Staphylococcus epidermidis
(C) Pseudomonas aeruginosa
(D) Clostridium difficile
(E) Bacteroides fragilis
6. Which one of the following microorganisms can
be part of the normal vaginal flora and cause
meningitis in newborns?
(A) Candida albicans
(B) Corynebacterium species
(C) Staphylococcus epidermidis
(D) Ureaplasma urealyticum
(E) Group B streptococci
7. Most serotypes of Escherichia coli can be
expected to remain in the colon for what period
of time?
(A) A few days
(B) A few weeks
(C) 6 months
(D) 2 years
(E) A lifetime
8. Which one of the following microorganisms is
closely associated with dental caries?
(A) Candida albicans
(B) Streptococcus mutans
(C) Prevotella melaninogenica
(D) Neisseria subflava
(E) Staphylococcus epidermidis
9. Anaerobic bacteria such as Bacteroides fragilis occur
in the sigmoid colon in a concentration of about
1011/g of stool. At what concentration do facultative organisms such as Escherichia coli occur?
(A) 1011/g
(B) 1010/g
(C) 109/g
(D) 108/g
(E) 107/g
10. Streptococcus pneumoniae can be part of the
normal flora of 5–40% of people. At what
anatomic site can it be found?
(A) Conjunctiva
(B) Nasopharynx
(C) Colon
(D) Urethra
(E) Vagina
(continued)
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NORMAL MICROBIAL FLORA OF THE HUMAN BODY
Answers
1. E
2. C
3. D
4. A
5. D
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REFERENCES
6. E
7. A
8. D
9. B
10. D
Hentges DJ: The anaerobic microflora of the human body. Clin
Infect Dis 1993;16(Suppl 4):S175.
Macowiak PA: The normal microbial flora. N Engl J Med
1982;307:83.
The pathogenesis of periodontal diseases. J Periodontol
1999;70:457.
Redondo-Lopez V, Cook RL, Sobel JD: Emerging role of lactobacilli in the control and maintenance of the vaginal bacterial
microflora. Rev Infect Dis 1984;6(Suppl 1):S62.