THE SCIENCE OF BAD BREATH
The age-old
condition of bad breath is coming under new scientific scrutiny,
leading to insights into diagnostic approaches and possible solutions
Consider the case of Dr. John Floss. A
dedicated dentist, Dr. Floss works long hours, often so focused on his
patients that he neglects to eat or drink. His own teeth and gums are,
of course, exemplary. Nevertheless, Dr. Floss is unaware of a problem
emanating from his mouth. His patients know, as does his hygienist. But
they are too embarrassed to inform Dr. Floss: he has exceedingly bad
breath.
In this bad-breath scenario, as in many, the
foul odor is the result of the metabolic activity of oral bacteria that
are happily feeding on a small pool of postnasal drip that regularly
collects on the back of the dentist's tongue. The bacteria leave behind
a collection of rank compounds. Gargling with an effective mouthwash
and cleaning the tongue would most likely alleviate the problem. Even
chewing a few bites of food would help. For now, though, the dentist's
patients are protected only by his surgical mask.
Obviously, people have always been aware of
the phenomenon of bad breath, or halitosis (from the Latin halitus,
breath, and the Greek -osis, meaning abnormal condition). But halitosis
is now emerging as a fascinating scientific subject, involving an
intimate human condition of widespread concern and traversing a wide
range of scientific fields, including bacteriology, chemistry,
physiology and psychology.
Millions have bad breath and, like Dr. Floss,
probably don't know it, which makes it difficult to generate accurate
statistics about the frequency of halitosis. One recent study, a survey
of Brazilian college students by Paulo Nadanovsky of the Institute of
Social Medicine at the University of the State of Rio de Janeiro,
revealed that 31 percent of the students had at least one family member
with habitual bad breath, with serious implications: 24 percent
reported that they had trouble enjoying the company of the family
member with halitosis, and 62 percent said that they were affected in
some way by their relative's breath problem.
My own interest in this area began almost 20
years ago, when my group embarked on the development of a two-phase
mouthwash designed to trap oral bacteria and debris on the surface of
small oil droplets. At that time, only a handful of academic
researchers, led by the late Joseph Tonzetich of the University of
British Columbia, were investigating halitosis. Now hundreds of
scientists in universities and industry study the problem. Last July
the fledgling International Society for Breath Odor Research (ISBOR)
drew about 350 attendees to its fifth international meeting in Tokyo.
The growth in the science reflects a general
public concern (or in some cases obsession) with sweet-smelling breath.
According to a market research firm's findings, Americans spent $1.8
billion on toothpaste in 2000, around $715 million on oral-care gum,
almost $740 million on mouthwash and other dental rinses, and almost
$950 million on toothbrushes and dental floss. Although many of those
products are primarily for maintenance of oral health, people are
certainly buying them to ensure that their breath is pleasant as well.
And the $625 million spent on breath fresheners other than gum and
mouthwash--for example, breath mints--is directly for that purpose.
The Source of the Smell
THE BASIC CAUSES of most cases of halitosis
are now fairly well understood. According to research conducted by
ISBOR co-founder Daniel van Steenberghe and his co-workers at Catholic
University-Leuven in Belgium and our group at Tel Aviv University in
Israel, about 85 to 90 percent of cases originate in the mouth. As with
other odors emanating from the moist microbial jungles of the
body--such as underarms and shod feet-bad breath is primarily the
result of microbial metabolism.
The mouth is home to hundreds of bacterial
species with various nutritional preferences. These tiny organisms
particularly enjoy proteins, and the chemical compounds that result
from the digestion of these proteins include some truly fetid
substances. At any given time, oral bacteria, usually anaerobic, may be
producing hydrogen sulfide, with its distinctive rotten-egg smell;
methyl mercaptan and skatole, also present in feces; indole, used in
small amounts in perfume but foul in large quantities; cadaverine,
associated with rotting corpses; putrescine, found in decaying meat;
and isovaleric acid, which smells like sweaty feet. No wonder human
breath can at times be so offensive.
The University of Michigan's Walter J.
Loesche, a past president of ISBOR, recently discovered that the
microbiota on the tongue differ from those species living in plaque on
teeth. Loesche, who received a grant from the National Institutes of
Health to study halitosis, has uncovered previously undescribed
bacterial species making their home in our mouths. He is currently
cataloguing the microbiota in people with and without halitosis, work
that should be completed this summer.
In otherwise healthy people, the very back of
the tongue, rather than teeth or gums, is the main source of bad
breath. This region is poorly cleansed by saliva and contains numerous
tiny invaginations in which bacteria can hide. These bacteria have a
field day putrefying postnasal drip--common in perhaps one quarter of
the urbanites studied--and other oral debris that can collect there.
Additional oral sources of bad breath include
poor oral hygiene (especially if it leaves proteinaceous particles
between teeth), gum inflammation, faulty dental work, unclean dentures,
and abscesses. Because a steady flow of saliva washes away bacteria and
their smelly chemical products, anything that promotes dryness--mouth
breathing, fasting, prolonged talking, stress and hundreds of
medications--can exacerbate the situation. Tobacco smoking is a notable
enemy of fresh breath. Although smoke may reduce bacterial activity,
this potentially positive effect is drowned out by negatives: smoke
dries out the mouth, worsens gum conditions and postnasal drip, and
leaves a residue whose aroma mixes with the preexisting oral bouquet.
Some bad breath seems to be associated with
actual periodontal disease, the destruction of the gums, and is
therefore useful as a clue to physicians and dentists. Hydrogen sulfide
and methyl mercaptan are toxic as well as malodorous; they can damage
cells and thus may be a factor in gum disease. In addition, some
bacterial species implicated in gum disease work up quite a stink when
grown anaerobically on amino acids in the laboratory, according to
research by Israel Kleinberg of the State University of New York at
Stony Brook. The presence of several of these key bacteria--such as
Treponema denticola, Porphyromonas gingivalis and Bacteroides
forsythus--in plaque or the tongue coating can be determined in minutes
in the dental clinic using a color assay, the BANA test (for
benzoyl-DL-arginine-naphthylamide), devised by Loesche. These bacteria
produce an enzyme that degrades BANA, forming a new, colored compound.
Not surprisingly, positive BANA tests are statistically associated with
halitosis.
The various oral bacteria that prefer feeding
on sugars instead of on proteins have traditionally been considered
irrelevant to bad breath. Research by Nir Sterer in my laboratory,
however, suggests otherwise. Much of the available protein in the mouth
is actually in the form of glycoproteins, in which sugar residues are
linked to the protein core. The sugar-feeding organisms can clip the
residues from the glycoproteins, leaving naked proteins to be digested
by bacteria that favor them. Sterer and his co-workers have recently
shown, using a simple color test, that the amount of enzymatic sugar
cleavage in saliva correlates with bad breath levels. In the future,
scientists may be able to attack bad breath by preventing the initial
sugar cleavage.
One might be tempted to conclude that the
eradication of all microorganisms on the tongue would be a potential
treatment for halitosis. These bacteria, however, also play a
protective role. Ordinarily our tongues harbor the yeastlike Candida
fungus in small numbers, the population kept in check by the presence
of bacteria. When tongue bacteria are wiped out by antibiotics, Candida
can run rampant. And candidal diseases are more severe and difficult to
control than halitosis. The idea, then, is to keep bacterial
populations present but under control.
More Halitosis Diagnosis
THE MOST COMMON SOURCE of bad breath, after
the mouth, is the nose and nasal passages. In these 5 to 10 percent of
cases, the odor comes mainly out of the nose, not the mouth, and has a
very different quality, which once again can be a diagnostic tool to
the physician or dentist. Nasal odor may result from sinusitis or
conditions that impede or block mucus flow. In one odd case, an
uncharacteristic breath odor in a 2g-year-old woman led us to discover
an embedded bead that she had apparently stuck up her nostril as a
young child. Indeed, children are notorious for sticking objects up
their nose, sometimes generating a foul nasal discharge that they may
smear all over themselves; a foreign body in a nasal passage is
something to check for when a child suddenly develops an overall
offensive odor.
Putrid tonsils may cause about 3 percent of
halitosis cases. Hundreds of other diseases and conditions together
cause less than 1 percent of the halitosis generally encountered. One
interesting but rare instance is so-called fish-odor syndrome. Subjects
with this condition sense that their saliva and sweat sometimes have a
fishy quality, although others may have trouble verifying the smell. A
physician unaware of this condition may even refer these patients for
psychotherapy. In fact, fish-odor syndrome, or trimethylaminuria,
results from an insufficiency of an enzyme that normally breaks down
trimethylamine, a fishy-smelling molecule.
Many people believe--and some businesses
through advertising have attempted to foster that belief-that bad
breath comes from the stomach rather than from the mouth. The
infrequency of the stomach's being such a source was central to a
recent court case in which I participated as an expert witness [see box
on page 79]. Bad breath originating outside the mouth or nasal passages
is, in fact, quite uncommon. The esophagus is a closed tube, and
continuous flow (as opposed to a simple burp) of gas or putrid matter
from the stomach indicates a health problem, such as a fistula between
the stomach and intestine or reflux serious enough to be bringing up
stomach contents. Even after garlic is eaten, it is the mouth that
retains a substantial part of the sharp odor.
A lingering mystery is why people tend to be
exquisitely sensitive to the breath quality of their fellows and
notoriously bad at smelling their own. One previous theory, that we
become somehow inured to our own bad breath, seems lacking. Research
conducted with Ilana Eli, Ronit Bar-Ness Greenstein and others in our
laboratory revealed that people such as the blithely unaware Dr. Floss
are able to assess samples of their own oral malodors more objectively
when the source is removed from the mouth--for example, when they smell
debris sampled from between their teeth with a toothpick.
The answer may be simply that because we
expel air from our mouths horizontally and only subsequently breathe in
vertically through our nose, the chance of getting a representative
whiff is low. Whatever the reason, it is difficult for someone to know
if he or she has bad breath without being told. And given the
embarrassment involved, being told is unlikely. Ironically, the
billions of dollars that buy breath-freshening products annually may be
spent in large part by individuals who do not in fact have a problem
but merely fear they do. An extreme version of this common belief is
the phenomenon of halitophobia--a conviction, usually unsupported by
objective analysis, that one has bad breath [see box on page 76].
A Fresh Approach
THOUGH BY NO MEANS the only factors in
halitosis, the volatile sulfur compounds produced by bacterial
metabolism are a prime suspect. In the late 1980s, with Jacob H. Gabbay
of the Israeli Ministry of the Environment and later with Christopher
A. G. McCulloch of the University of Toronto, our research group
determined that the sulfides that contribute to bad breath could be
assessed using a portable sulfide monitor. The monitor's manufacturer,
Manny Shaw of Interscan in Chatsworth, Calif., was initially skeptical
that there would be a market for Halimeters, but he has since sold his
device to thousands of dentists and researchers. In 1999 Alfredo
SanzMe&l, a chemist at the University of Oviedo in Spain, reported
a different technique, one that indirectly quantifies sulfide
concentration by optically measuring the fluorescence induced by the
reaction of sulfides with a mercury compound.
Such technologies might someday lead to the
development of an effective, pocket-size sulfide meter. Existing
Halimeter scores do correlate statistically with more complex
chromatographic analyses and with the gradings of human odor judges,
who personally smell the breath of study subjects and rate it for
research purposes.
Once the presence of halitosis is
established, the affected individual ordinarily wishes to be rid of the
condition. Of course, basic oral hygiene--regular flossing and
brushing--cannot be underestimated as a preventive. The gingivitis
medication chlorhexidine, an antimicrobial agent sold by prescription
in the U.S., is quite effective against halitosis. Unfortunately, it
can also discolor teeth, impair taste and generate oral ulcerations.
These effects, though reversible, preclude the use of chlorhexidine for
more than a few days at a time.
Other cures date back thousands of years.
Tongue cleaning is an ancient oral hygiene practice from the Far East
that is still popular there and that is catching on in the West. One
early antidote mentioned in the Babylonian Talmud is gum mastic, which
may be the same ladanum referred to in Genesis. Gum mastic is the resin
of the Pistacia lentiscus shrub, which is still cultivated for this
purpose on the Mediterranean island of Chios, although modern synthetic
chewing gums have largely supplanted mastic. Interestingly, this resin
was once used extensively for treating wounds and is now known to have
potent antibacterial properties. Chewing the gum, therefore, might both
increase saliva flow and kill some bad-breath microbes.
Other natural products chewed around the
world for breath freshening include guava peels (Thailand), anise seeds
(Far East), parsley (Italy), clove (Iraq) and cinnamon (Brazil). Some
of the molecules responsible for the flavor in these plants have
antibacterial properties that give scientific credibility to these folk
practices. Many popular mouthwashes contain flavor oils, including
menthol, eucalyptol and methyl salicylate (wintergreen oil).
The American Dental Association currently has
guidelines whereby a product can get ADA approval as being efficacious
against plaque, gingivitis or cavities. The ADA is now reviewing
guidelines that would allow products to receive similar approval for
their breath-freshening powers. Seemingly paradoxically, some companies
that manufacture breath fresheners are against the ADA effort. A closer
look reveals that the approval would require the companies to create
better products: most available breath products work only briefly, on
the order of 20 to 120 minutes, and the ADA will most likely demand a
significantly longer effect for official recognition. For example, mint
is widely accepted as a primary example of a good ingredient in a
breath treatment. But mint is actually relatively weak and its effect
short-lived compared with other essential oils.
Over the past 15 years I have had the
opportunity to smell the mouths of thousands of individuals in clinics
and in research studies, not to mention the hundreds I have smelled
surreptitiously in supermarkets, in airplanes and in synagogue during
the fast day of Yom Kippur. Just as Camembert cheese smells quite
different than Edam does, bad breath is not one odor but a
constellation of them, depending on the microorganisms involved, where
they come from and what they have been up to. Whereas researchers
continue to argue about the best ways to quantify offensive breath,
future electronic noses [see "Plenty to Sniff At," by Mia
Schmiedeskamp; News and Analysis, SCIENTIFIC AMERICAN, March 2001] may
provide not only halitosis levels but also an indication of the types
of odors detected, which would give clues about their origins.
The ability to identify the probable origin
is of considerable importance in halitosis research and in counseling
individuals, and it requires extensive "nose-on" experience. There
remains much that we do not know. For example, we must match individual
bacterial species to the odors with which they are associated. The
details of the contributions of the nasal passages and the tonsils to
bad breath are still incompletely understood. And few psychologists
actively study halitophobics. Although the recognition and treatment of
halitosis may seem insignificant in the pantheon of medical conditions,
it can have a profound effect on a person's life and relationships.
Tips for Good Breath
Gently clean the very back of your tongue
with a plastic tongue cleaner. Take care not to damage your tongue;
just sweep the mucus layer away. Practice helps to overcome the gag
reflex.
Eat a good breakfast; it cleanses the mouth and gets the saliva flowing.
Prevent your mouth from drying out. Chewing
gum for just a few minutes can reduce bad breath. Drink sufficient
quantities of liquids.
Use a mouthwash. The most effective method is
to rinse and gargle just before sleep. This prevents the buildup of
microorganisms and odor during the night.
Clean your mouth after eating odorous foods
or drinks such as garlic, onions, curry and coffee. Make sure to clean
between your teeth, especially after eating food or beverages rich in
proteins.
Brush and floss [or otherwise clean between your teeth] according to your dentist's instructions.
Ask an adult family member or close friend
about your breath. This is the most reliable [and cheapest] way to find
out if you have halitosis.
Most Unwanted List
Compounds commonly produced by mouth bacteria and their odors
Hydrogen sulfide Rotten eggs
Methyl mercaptan Feces
Skatole Feces
Cadaverine Corpses
Putrescine Decaying meat
Isovaleric acid Sweaty feet
Overview/Halitosis
Halitosis, or bad breath, is a common
condition that affects personal relationships. In addition to cases of
actual halitosis, a pervasive fear of bad breath, known as
halitophobia, severly interferes with some people's quality of life.
Researchers have recently begun to analyze
halitosis qualitatively and quantitatively, leading to new insights
concerning the causes and possible treatments of the condition. Entire
new species of oral bacteria have been discovered in the process, and
the fact that the vast majority of halitosis cases originate in the
mouth has been confirmed.
Breath freshening and oral hygeine are big
business, with billions of dollars spent annually in the U.S. on
toothpaste, toothbrushes, floss, mouthwashes, mints and other breath
freshners.
More To Explore
Production and Origin of Oral Malodor: A
Review of Mechanisms and Methods of Analgsis. J. Tonzetich in Journal
of Periodontology, Vol. 48, No. 1, pages 13-20; January 1977.
What to Do about Halitosis. C. Scully, S. P.
Porter and J. Greenman in British Medical Journal, Vol. 305, pages
217-218; January 22, 1994.
Clinical Assessment of Bad Breath: Current
Concepts. M. Rosenberg in Journal of the American Dental Association,
Vol. 127, pages 475-482; April 1996.
Bad Breath: Research Perspectives. Second edition. Edited by M. Rosenberg. Ramot Publishing, Tel Aviv University, 1997.
Tel Aviv University's Web site on bad breath: www.tau.ac.il/~melros/
Possible causes of halitosis: www.tau.ac.il/~melros/bda/index.html
Bacterial species that inhabit the mouth:www.tau.ac.il/~melros/faq/S.html
PHOTO (COLOR): SMALL STONES called
tonsilloliths grow in the crypts of the tonsils and consist of
partially calcified bacteria and debris. Tonsilloliths smell foul
themselves but don't always cause bad breath. They are relatively
uncommon [perhaps 2 to 3 percent of the adolescent and adult population
have or have had them]. Because they do not usually cause any medical
problems, many physicians and dentists have never heard of them. The
samples at the left were collected from a single individual.
PHOTO (COLOR)
PHOTO (COLOR)
PHOTO (COLOR)
~~~~~~~~
By Mel Rosenberg
Illustrations by Joseph Daniel Fiedler
Mel Rosenberg grew up in Canada and moved
to Israel in 1969. He is professor of microbiology at the Maurice and
Gabriela Goldschleger School of Dental Medicine at Tel Aviv University.
He has received several awards for his research as well as honorary
academic appointments in the U.S., the U.K., and Canada. In 1996,
together with Karl Laden and university support, he founded InnoScent,
a company that develops products for fighting body odors. He has
published a children's book on bacteria and enjoys expelling air
through his saxophone.
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