CLINICAL REVIEWS Halitosis, or the Meaning of Bad Breath BRUCE E. JOHNSON, MD
HALITOSIShas been popularized by the media, typically in the commercial pitches of high-priced remedies. Similar to "the heartbreak of psoriasis," this incessant repetition of a medical bogeyman threatens to c h e a p e n what can be a true sign of significant disease. A recent case demonstrates h o w the recognition of the meaning of bad breath can lead to expeditious treatment. A 35-year-old woman presented with fever, fatigue, and cough productive of discolored but not malodorous sputum. Her illness had begun shortly after a party one month before admission when she "may have drunk too much." She had continued to work in an office job until the day before presentation. Physical examination revealed dullness on chest percussion. The chest x-ray showed a huge (15-cm diameter), circumscribed postcardiac mass. She was admitted to the hospital with the consideration of a lung abscess or pulmonary tumor. Six hours after admission, she developed extreme shortness of breath with agitation. Upon entering the room, medical and nursing staff were met with an extremely foul, fetid odor. The patient was immediately intubated, with endotracheal suction of copious quantities of foulsmelling, dark grey sputum. Portable chest x-ray showed the new presence of an air/fluid level within the mass and the spread of a pneumonic process throughout much of the rest of the lung. The sputum eventually grew the anaerobes Fusobactertum nucleatum, Bacteroides melaninogenicus, and a Peptostreptococcus species. The woman survived only after a prolonged intensive care unit and a hospital stay. The onset of bad breath represented rupture of the abscess, and rapid recognition of the significance of this sign saved precious time in initiating therapy. Halitosis is important for at least three reasons. It is a social handicap: for p e o p l e w h o deal with the public, bad breath causes discomfort in others, with the person's usefulness b e c o m i n g diminished. Those w h o are aware of their o w n m o u t h odor may be obsessed with clean breath, to the point of impairing their o w n effectiveness. And finally, medically, halitosis is usually a sign that an abnormal condition exists, awaiting diagnosis and treatment.
Received from the Division of General and Geriatric Medicine, Department of Medicine, University of Kansas Medical Center, 3901 Rainbow Boulevard, Kansas City, Kansas 66160. Address correspondence and reprint requests to Dr. Johnson.
DEFINITION At one time, clinicians attempted to draw a distinction b e t w e e n " t r u e fetor ex o r e " or "fetor otis" and " t h e internal malady k n o w n familiarly as halitosis."~. 2 The former was felt to a p p l y to an odor emanating from local conditions of the m o u t h and h o l l o w cavities (sinuses, nose, pharynx), while the latter referred to odors having a systemic origin that were exhaled from the lungs. This difference is largely disregarded today. Halitosis is foul, offensive, or bad-smelling breath arising from a person's oral - nasal cavity, regardless o f the source. It is usually noticed by a nearby observer though, curiously, not always by the patient him- or herself. Halitosis is not dysgeusia (altered p e r c e p t i o n o f taste) and is not anosmia (absent or altered sense of smell). These disorders of senses represent distinct symptoms themselves, t h o u g h the evaluation of halitosis may overlap their evaluation.
CAUSES/DIFFERENTIAL DIAGNOSIS When c o n f r o n t e d with a patient complaining of, or presenting with, halitosis, it is useful to consider three separate diagnostic groups: n o n p a t h o l o g i c causes, pathologic causes, and psychiatric conditions (Table 1). A simple test identifies the first two groups. If an observer smells bad breath, there may be a pathophysiologic cause; if not, the complaint may reflect a psychiatric condition and necessitate a different approach. The o d o r itself arises from one or a combination of several processes. Body tissue and desquamated epithelium d e c o m p o s e and release odors; if located near the nose and m o u t h these odors are recognized as halitosis. Gram-negative and anaerobic bacteria in the oral cavity can overgrow, releasing o b n o x i o u s gases. There are foods, drugs, or other materials that, w h e n ingested, are processed by the b o d y and travel to the lungs, w h e r e they vaporize and are exhaled. Systemic illnesses sometimes have an associated breath odor. The delineation of these sources constitutes the differential diagnosis of halitosis.
Nonpathologic Causes Changes with age.
As far back as Pliny the 649
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Causes of Halitosis Nonpathologic Age Morning breath, hunger breath, menstrual breath Food and drugs Tobacco Pathologic Mouth--dental work. periodontitis, dehydration, stomatitis, glossitis, parotid disease, tumors Nose/sinuses--foreign bodies, infections, destructive lesions, tumors, chronic sinusitis Tonsils/pharynx--tonsillitis, concretions, pharyngitis, epiglottitis, foreign bodies, tumors, diverticula Digestive organs--achalasia, reflux, outlet obstruction, bezoars Pulmonary-- necrotizing pneumonia, anaerobicabscessand empyema Systemic illness--diabetic ketoacidosis, liver failure, renal failure Psychiatric Schizophrenia, olfactory reference syndrome
Younger (AD 6 1 - 1 1 3 ) , there have b e e n r e p u t e d changes in breath o d o r attributed to aging. 3, 4 Infants and children are described as having " s w e e t " breath, w h i l e adolescents have breath that is " n o t u n p l e a s a n t . " Adults' m o u t h o d o r can be described as " s t r o n g , " w h i l e that of the aged is n o t e d to be "heavy, pungent. ''4,s A general increase in bacteria in the m o u t h occurs w i t h advancing age 6; additionally, after middle age, m e n are found to have m o r e bacteria in the m o u t h than are w o m e n of the same age, p e r h a p s accounting for m o r e disagreeable breath in older men.
Morning breath. O f all the causes of halitosis, this is the most c o m m o n (and p r o b a b l y the one most successfully e x p l o i t e d c o m m e r c i a l l y ) . The m o u t h is b a t h e d t h r o u g h o u t the day b y saliva, w h i c h flows around the teeth, tongue, and gums, collecting particles of food and organic matter. Saliva is s w e p t b a c k to the pharynx and swallowed, carrying the material w i t h it. Saliva has a basal p H o f 6.5 and is mildly bacteriostatic to gram-negative and anaerobic bacteria. With sleep, saliva flow decreases and any p o o l e d saliva slowly changes. The pH rises above 7.0, and enzymatic breakd o w n occurs, making the saliva itself odoriferous. 4 The tidal m o v e m e n t of saliva is arrested, and a c c u m u l a t e d food and e p i t h e l i u m b e c o m e substrates to m o u t h flora. Bacterial o v e r g r o w t h and b r e a k d o w n of this organic matter cause m o r n i n g breath. ~ Arousal w i t h eating, drinking, and speaking all stimulate saliva flow, washing the material away. 8 In this way, morning breath n o r m a l l y ceases w i t h o u t intervention. Hunger breath. A disagreeable odor may b e detected on the breath of persons w h o have missed meals.3.8 It is postulated that " h u n g e r b r e a t h " represents the p u l m o n a r y exhalation o f volatile m e t a b o l i c b r e a k d o w n p r o d u c t s of b o d y fats and proteins. What-
ever the cause of hunger, w h e t h e r dieting or frank starvation, the decreased saliva flow and m o u t h dryness that c o m e from not masticating exacerbate the problem. Regular snacks or meals p r o v i d e a nutritional load and a stimulus to salivary production, thus correcting the malodor.
Menstrual breath. There are references to an oral malodor afflicting menstruating w o m e n ~, ~ ( t h o u g h it should be p o i n t e d out that these sources reference G e r m a n articles of the late 1800s). Described as the odor of decayed, clotted blood, this was s u p p o s e d l y present on the day p r e c e d i n g menstruation. Menstrual breath was described as especially likely to o c c u r in w o m e n with dysmenorrhea. Food and drugs. The most recognized food causing halitosis is garlic. Garlic has b e e n used in a n u m b e r of e x p e r i m e n t s that sought to d e t e r m i n e the causes of halitosis.i, 9, 10 In one series of observations involving patients with natural or postsurgical intestinal abnormalities, garlic was instilled directly into gastrointestinal ostomies or fistulae. The characteristic odor was n o t e d on the breath w i t h o u t the garlic's having b e e n swallowed. Garlic c o u l d even be detected on the breath after being r u b b e d on the feet. 9 A garlic-like o d o r has b e e n attributed to several inorganic materials, including arsenic, selenium, vanadium, and inorganic phosphorus, t 1 O t h e r foods p r o d u c e a distinct m o u t h odor. Onion, fish, and m a n y alcoholic drinks are readily recognized. People in cultures that do not use c o w ' s milk (e.g., the Chinese) allegedly find the breath of milk drinkers objectionable1, 12; years ago Occidental physicians c o u l d even detect those patients w h o w e r e prescribed a milk-based (Sippy's) diet for the treatment of u l c e r disease. 1 Certain medicines cause halitosis. Most notorious for this in recent years was dimethyl sulfoxide (DMSO), w h e t h e r used for interstitial cystitis or as a l i n i m e n t ) 3 O t h e r drugs i m p l i c a t e d in halitosis include amyl nitrate, chloral hydrate, disulfiram ( w h e n given with warfarin), paraldehyde, and metronidazole. ~4"t6 Tobacco breath. The odor of tobacco smoking lingers long after the last cigarette, cigar, or pipe. Dentists are frequently a d m o n i s h e d b y their peers to r e m e m b e r this manifestation of the smoking habit.4, s, 12
Pathologic Causes Mouth. The mouth, tongue, and teeth are implicated in the majority of cases of halitosis. This is no surprise to dentists, oral surgeons, and otolaryngologists, w h o are often consulted regarding this complaint. Retained food, especially meats and fish, w h i c h are
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high in sulfur-containing amino acids, is simple to detect and easy to remedy. 7, 17 Dental p r o b l e m s that result in t r a p p e d food particles include p o o r l y finished restorations with overhanging margins and lack of contact points b e t w e e n restorations. O r t h o d o n t i c braces are notorious for collecting food particles. Plaque, the g u m m y mass of microorganisms that a c c u m u l a t e s along the crowns and roots of teeth, may cause halitosis, 7, ~8 particularly if associated w i t h periodontitis. Periodontitis (inflammation of the p e r i o s t e u m , alveolar bone, and s u p p o r t i n g structures) and gingivitis (inflammation of the gums) are the teeth-related conditions p r o d u c i n g the most disagreeable m o u t h odor.19, 2o Desquamated, necrotic tissue, m i n o r bleeding, and microbial infestation c o m b i n e to p r o d u c e foul odor. Periodontitis and gingivitis exist in a confined, anaerobic e n v i r o n m e n t c o n d u c i v e to bacterial g r o w t h and p r o t e c t e d from the cleansing action of saliva. Pericoronitis (inflammation of the tooth c r o w n ) and dental caries are m u c h m o r e e x p o s e d to the cleansing activity of saliva and mastication. 19 In fact, dental caries contribute little to m o u t h breath unless there is a necrotic pulp.6, 2o Gas c h r o m a t o g r a p h i c analysis of m a l o d o r o u s m o u t h air reveals two basic gases. 7, 21 The substance most frequently present is hydrogen sulfide. The n e x t c o m m o n e s t , but the gas most objectionable at low concentrations, is m e t h y l m e r c a p t a n . Together, these two gases account for over 90% of m o u t h gas p r o d u c t i o n , w i t h the remainder b e i n g small levels of dimethyl sulfide and dimethyl disulfide. Typically found in gingiv a l / p e r i o d o n t a l disease, food trapping, and p o o r oral hygiene, these w e r e the gases also f o u n d in dental students with m o r n i n g breath. 8 Similarly, m e n t a l l y retarded, handicapped, or seriously ill persons w h o cannot carry out their o w n oral hygiene regimens are likely to have halitosis. 2~ Decreased saliva flow (xerostomia) c o m p r o m i s e s normal cleansing m e c h a n i s m s of the mouth, allowing the d e v e l o p m e n t of halitosis. 3, ~4, 22 This is the p r o b a b l e m e c h a n i s m for m o u t h o d o r in the sicca s y n d r o m e (including Sj/Sgren's syndrome, r h e u m a t o i d arthritis, syst e m i c lupus erythematosus, scleroderma, chronic hepatitis, or p r i m a r y biliary cirrhosis). Xerostomia also occurs following radiation therapy to the head and neck, due to decreased w a t e r intake itself (as often seen in the elderly); f r o m medications, including diuretics, antihypertensives, anticholinergics, and tricyclic antidepressants; and in m o u t h breathing. Stomatitis and glossitis occasionally cause halitosis w h e n o p e n ulcers, fissures, or enlarged papillae trap food particles and d e s q u a m a t e d t i s s u e ) 9, 22 Deficiencies of vitamins or minerals such as vitamin A, vitamin B~2, iron, or zinc m a y dry the m o u t h w i t h fissuring. 23 Liquid or soft diets coat the tongue w i t h p r o t e i n a c e o u s matter but might not stimulate normal mastication. 8 Infections involving the tongue and m u c o u s m e m branes, such as Vincent's stomatitis (necrotizing ulcer-
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ative gingivostomatitis), measles, diphtheria, thrush, and herpangina involve significant tissue breakdown, altered ~aliva flow, and putrefaction. 3, 16 Ironically, despite the gross appearance, m a n y p r i m a r y or secondary conditions of the tongue (e.g., black hairy tongue, geographic tongue, midline r h o m b o i d glossitis) only occasionally cause halitosis. 23 Certain diseases of the parotid gland, such as m u m p s , ascending parotitis, u v e o p a r o t i d fever, or parotid abscess, decrease saliva p r o d u c t i o n , c o n t r i b u t i n g to dry m o u t h and halitosis. 22, 24 C a n c r u m oris ( n o m a ) , occurring in severely m a l n o u r i s h e d children, and occasionally in acute leukemia, is a w i d e s p r e a d destructive infection of the cheeks, maxilla, and mandible2S: this anaerobic infection is described as especially foulsmelling. Oral bleeding, especially in debilitated patients w h o cannot cleanse the mouth, provides a rich substrate for protein b r e a k d o w n and release of gases; this is not u n c o m m o n in gingivitis, h e m o p h i l i a , or leukemia, or in cancer c h e m o t h e r a p y . Primary malignant or benign tumors of the m o u t h , including t u m o r s of the tongue, gums, cheeks, or palate, may cause halitosis. 26, 27 Necrotic material, oozing of blood, and food trapping c o m b i n e in putrefaction. These t u m o r s are not infrequently f o u n d in persons w i t h p o o r oral hygiene, giving dual sources for gas production. In the past, dentures w e r e m a d e of a p o r o u s vulcanite material, w h i c h bacteria w e r e able to penetrate.3, 4 These c o u l d p r o d u c e malodor, even w h e n rem o v e d from the mouth. Current acrylic dentures do not have this p r o b l e m , but persons w h o do not r e m o v e and clean their dentures, o r w h o a l l o w food to be t r a p p e d in prosthetic devices, d e v e l o p halitosis. N o s e a n d s i n u s e s . Normal rhinorrhea has no disagreeable odor. Even thick, p u r u l e n t nasal discharge found in typical u p p e r respiratory infections is rarely odoriferous. Some observers attribute a disagreeable odor to atrophic rhinitis as might b e seen in the elderly.16, 24 Malodor f r o m the nose and sinuses otherwise involves destructive nasal/palatine processes, nasal foreign bodies, or c h r o n i c infection of the sinuses. An assortment of objects m a y be inserted into the nose and n e g l e c t e d for long periods of time. Children and m e n t a l l y retarded persons have p l a c e d pellets of paper, seeds, peanuts, beads, or parts of toys in the nose.21, 2a. 29 A foreign b o d y present in the nose induces an inflammatory response that b e c o m e s secondarily infected, p r o d u c i n g o b n o x i o u s gases. Destructive lesions of the nose create an inflammatory response and necrotic tissue, which, w h e n putrefied, cause halitosis. Simple nasal septal perforation, w h e t h e r from chronic nose picking, from cocaine use, or as a c o m p l i c a t i o n of nasal surgery, typically exists w i t h o u t an odor. 3° Ozena is a severe, c h r o n i c rhinitis characterized b y a thick, greenish, m a l o d o r o u s dis-
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charge, mucosal crusting, and turbinate b o n e atrophy. If not m a n a g e d aggressively w i t h antibiotics, local cleansing, or even surgery, ozena m a y destroy nasal turbinates and cause anosmia. 31 O t h e r invasive infectious conditions such as leprosy, yaws, or a syphilitic g u m m a have an offensive odor. 31 Equally serious is the nasal/palatine presentation of lethal midline granuloma and W e g e n e r ' s granulomatosis. 32, 33 T r e a t m e n t of patients w h o have these destructive diseases m a y be successful, b u t the o d o r can be quite offensive until c u r e is achieved. Tumors of the nasal cavities are u n c o m m o n . W h e n t h e y occur, though, they are f r e q u e n t l y e x o p h y t i c and bloody, p r o d u c i n g malodor. 34 The person w i t h chronic sinusitis may have a disagreeable odor. 3, 16, 24 Halitosis f r o m sinusitis c o n n o t e s infection w i t h anaerobic bacteria, 19 including organisms that are present in a b o u t half of the cases of chronic sinusitis necessitating surgery. Acute sinusitis is typically not caused b y an anaerobic infection31; halitosis presenting in acute disease suggests spread from an anaerobic tooth abscess.
Tonsilsandpharynx. Repeated infections of the tonsils and adenoids lead to c h r o n i c follicular tonsillitis.2, 16, 2~ D e e p crypts form, w h i c h collect food, saliva, and necrotic matter. If natural m e c h a n i s m s do not cleanse the crypts, such collections form tonsilloliths. These are concretions lying on an inflammatory base and c a p a b l e of causing halitosis.3S It is unclear w h e t h e r tonsilloliths are also causative in peritonsillar abscess, an acute, purulent, m a l o d o r o u s infection. 36 Tonsillect o m y leaves a raw, surgical w o u n d with bleeding, necrotic tissue that is foul for several days postoperatively. 24 Pharyngitis f r o m virtually any organism can cause halitosis.3. 19 Most dramatic, perhaps, is that due to diphtheria, b u t severe pharyngitis from infectious mononucleosis, streptococcal infection, infection w i t h Candida (thrush), herpangina, or infection w i t h o t h e r microorganisms can all generate bad breath. The key factors include d e s q u a m a t e d e p i t h e l i u m , inadequate hygiene, and " n o r m a l " m o u t h flora, w h i c h p r o d u c e putrefaction. Acute epiglottitis, w h i l e typically due to Hemophilus influenzae infection in children, m a y result from infection w i t h H. influenzae, Streptococcus pyogenes, or S. pneumoniae in adults. 37 While halitosis is admittedly u n c o m m o n in acute epiglottitis, the rapid e n l a r g e m e n t o f the epiglottis makes swallowing difficult and results in p o o l i n g of saliva and inflammatory material. The p h a r y n x also is a site for tumors, w i t h uncleared, necrotic material causing halitosis. 16
A mentally impaired woman developed halitosis and weight loss. Multiple efforts to determine the cause were unsuccessful, and panendoscopy was scheduled. Intuba-
tion could not be accomplished. On investigation, the anesthetist discovered the wheel from a toy lodged in her pharynx. Air and some fluid, but no food, had been able to pass through the axle hole of the wheel. 38 Zenker's d i v e r t i c u l u m is an o u t p o u c h i n g that occurs at the junction of the posterior h y p o p h a r y n x and the esophagus, a site of natural weakness. 39 W h e n small, the d i v e r t i c u l u m is asymptomatic, but as it enlarges food and saliva lodge within it. D e c o m p o s i t i o n releases o b n o x i o u s gases but often o n l y intermittently, d e p e n d i n g on esophageal peristaltic activity.
Digestive organs--the esophagus, stomach, small intestines. Diverticula similar to Zenker's div e r t i c u l u m may f o r m virtually anywhere in the esophagus and be a source of halitosis. Achalasia is a p r i m a r y m o t o r disorder that results in altered or absent peristalsis of the esophagus, partial or i n c o m p l e t e relaxation of the l o w e r esophageal sphincter (LES), and increased resting LES pressure.4° Dysphagia is the typical presenting complaint, t h r o u g h the condition can be asymptomatic for long periods of time. Another hallmark of the disease is a lack of c o m p l e t e e m p t y i n g of the esophagus into the stomach. This results in retention of food, liquid, and saliva within a gradually e x p a n d i n g esophagus. Breakdown of this matter with eructation of the resultant gases is r e c o g n i z e d as halitosis. Tumors of the gastroesophageal junction, chronic idiopathic pseudoobstruction of the esophagus, and Chagas' disease may present w i t h achalasia-like symptoms, including food and liquid retention. Gastroesophageal reflux is an e x t r e m e l y c o m m o n disorder that may rarely have halitosis as one of multiple presentations. 41 The most f r e q u e n t s y m p t o m is heartburn, though atypical chest pain and p u l m o n a r y disorders (cough, wheezing, recurrent p n e u m o n i a ) o c c u r regularly. Since the esophagus collapses in its natural state, air does not pass easily to the outside. With eructation, though, swallowed gases do escape. The o d o r associated w i t h gastroesophageal reflux, like that of simple belching,21.39 is of stomach contents and resembles the o d o r of the most recently ingested meal. O t h e r mechanical disorders of the stomach have b e e n r e p o r t e d in association with halitosis. A trichobezoar caused bad breath in a y o u n g girl. 42 Adults with gastric outlet obstruction d e v e l o p e d halitosis, w h i c h cleared only briefly w i t h antibiotic treatment. 43 Two children w i t h peritoneal bands causing duodenal obstruction had resolution of halitosis with release of the bands. 44 At one time, odors w e r e described in association with intestinal maladies, most particularly obstruction or constipation. 5,9 Few hold this v i e w presently. 1, 4, 21, 45
Pulmonary.
Anaerobic lung abscess, necrotiz-
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ing p n e u m o n i a , and e m p y e m a all frequently have halitosis as an i m p o r t a n t presenting s y m p t o m . 16. 24, 46 Halitosis is present in as m a n y as 40 - 50% of patients w i t h anaerobic p u l m o n a r y infections .46 These infections are thought to originate from aspirated m o u t h flora 7, 46, 47 since the m o u t h s of persons w i t h periodontal disease and gingivitis have very high concentrations of anaerobic bacteria. Consequently, these lung infections o c c u r most c o m m o n l y in persons w i t h p o o r oral hygiene w h o are likely to aspirate (e.g., alcoholics).48 Even so, halitosis from an anaerobic lung abscess has b e e n described in an e d e n t u l o u s patient. 49 Bronchiectasis, w h e t h e r congenital or acquired, is also a source of malodor. Generally, though, w h e n o d o r is present the patient is having an exacerbation of the underlying disease. 46 Patients w i t h bronchitis or p n e u monia from aerobes, m y c o p l a s m a or viruses, even if productive of c o p i o u s quantities of s p u t u m , do not usually have bad breath.
Systemic illness. It has long b e e n r e c o g n i z e d that odor f r o m a patient's breath can b e a clue to diagnosis of a systemic illness. As m e n t i o n e d above, until recent times physicians defined "halitosis" as the m o u t h odor originating from a systemic cause. However, smell is a highly subjective sense, and precision in identification of various odors for medical usage is a skill little p r a c t i c e d and p o o r l y taught. Some odors are characteristic e n o u g h to be discriminating as diagnostic aids. l, 12, 14, 45 The sweetish, fruity, acetone smell of diabetic ketoacidosis is classic. Fetor hepaticus is variably described as fishy, mousy, metallic, or like decaying blood. Ammoniacal or urinous odors emanate from persons w i t h renal disease and uremia. Smells have b e e n ascribed to a n u m b e r of o t h e r diagnoses. A m u s t y smell m a y have b e e n noticed in p e o p l e w i t h scarlet fever or t y p h o i d fever ( t h o u g h this t e r m was also e m p l o y e d for liver disease). Patients w i t h "intestinal d y s f u n c t i o n " and " c h o l e m i a " m i g h t have had a heavy, sour breath. A decaying b l o o d smell was ascribed to intestinal h e m o r r h a g e and menstrual breath. A sweetish, sour breath has b e e n attributed to a high dairy intake, w h i l e c o n s u m p t i o n of fatty m e a t c o u l d have given a bitter, fecal, stinking breath. Eskimos w e r e alleged to smell like blubber. [Additional terms describing local, not systemic, conditions included: sweetish acid for thrush; rotting hay for Vincent's infection (necrotizing ulcerative stomatogingivitis); sweetish for lactation; intense, disagreeable, fetid, and foul for periodontal disease; alliaceous (garlic-like) for b i s m u t h or p h o s p h o r u s intake; and Limb u r g e r cheese-like for chronic follicular tonsillitis.] It is doubtful that precise a g r e e m e n t o c c u r r e d in the attribution of these various odors to specific diseases in the past; it is certain that other means of diagnosis are m o r e valuable today.
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Psychiatric Conditions If a patient presents w i t h a c o m p l a i n t of halitosis and no m a l o d o r is present, the physician should not i m m e d i a t e l y c o n c l u d e that no p a t h o l o g i c condition is present; an evaluation m a y still b e indicated. However, if no organic cause for halitosis is f o u n d and r e p e a t e d examinations do not reveal bad breath, then a psychiatric condition should be considered. The psychiatric causes fall into two classes largely distinguished b y w h e t h e r the p e r c e i v e d odor, the olfactory hallucination, is extrinsic or intrinsic to the patient's body. A t r u e olfactory hallucination has b e e n defined as the "subjective p e r c e p t i o n of an o d o r w i t h o u t an objective s t i m u l u s . " 5o
Olfactory hallucinations o f extrinsic sources. These patients r e p o r t odors that e m a n a t e f r o m an external source, s°. 51 The smells are described as chemicals or p e o p l e or animals. Unlike smells from an organic illness, w h i c h tends to fatigue w i t h t i m e (adaptation p h e n o m e n o n , discussed b e l o w in the Evaluation section), these extrinsic smells are c o n t i n u o u s l y perceived b y the patient. T w o clinical settings a c c o u n t for most olfactory hallucinations of extrinsic sources. T e m p o r a l lobe epilepsy (which, of course, is not a psychiatric disease) s o m e t i m e s begins w i t h a p e r c e i v e d smell, the aura. This hallucination is usually brief and only rarely mistaken for halitosis. 5° Schizophrenics have olfactory hallucinations, and such c o m p l a i n t s can be r e m a r k a b l y difficult to extinguish. Olfactory hallucinations o f intrinsic sources. The olfactory r e f e r e n c e s y n d r o m e (ORS) is the t e r m a p p l i e d to olfactory hallucinations of intrinsic sources.52, 53 This s y n d r o m e is a s u b t y p e of m o n o s y m p tomatic h y p o c h r o n d r i a c a l psychosis (DSM-III-R), the classification that includes other conditions in w h i c h there is a p r e o c c u p a t i o n w i t h imagined b o d y defects. The patient w h o has ORS believes that the offending smell has an intrinsic source B either sweat, intestinal gas, or the breath (halitosis). The patient m a y r e s p o n d in three ways: 1) minimally, w i t h f e w efforts to guard others f r o m the odor; 2) s o m e w h a t reasonably, w i t h efforts to hide the odor; or 3) contritely, w i t h self-abasement and embarrassment, believing that he or she stinks and offends others. 5° People w i t h ORS suffer the delusion that others readily detect the odor, and so they have h e i g h t e n e d distress around o t h e r p e o p l e . T h e y do not believe that o t h e r p e o p l e cannot smell them; small m o v e m e n t s , grimaces, or responses in acquaintances and strangers are i n t e r p r e t e d as efforts to distance themselves from the patient. Unlike p e o p l e w h o truly have halitosis, the o d o r to patients w i t h ORS remains constant, does not fatigue, and is always present. This results in obsessive
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behavior consisting of frequent washing, clothes changing, and use of deodorant or mouthwash, and social withdrawal. Further psychiatric evaluation m a y disclose the fact that a person is quietly paranoid, isolating him- or herself to p r e v e n t embarrassment. These persons have b e e n described as sensitive, obsessive, and insecure. Typically there are s y m p t o m s of depressive illness. The s y n d r o m e may originate after an episode of rhinorrhea, sinusitis, or an allergic reaction. Occasionally, ORS h a p p e n s after a friend or family m e m b e r has c o m p l a i n t s of halitosis. 53 The patient w i t h ORS is rarely satisfied that an organic cause cannot b e f o u n d and so f r e q u e n t l y has had m u l t i p l e consultations w i t h different doctors, complaining of the same symptom. There are concerns that p e o p l e w i t h this disorder w h o remain untreated are at risk for suicide. 52
EVALUATION The evaluation of halitosis begins w i t h recognition of the p r o b l e m . The adaptation p h e n o m e n o n describes the physiologic condition in w h i c h the threshold of sensitivity for a particular o d o r rises w i t h c o n t i n u e d e x p o s u r e to the scent. 5 Consequently, a foul smell is often u n n o t i c e a b l e to the patient; this explains w h y so m a n y w i t h halitosis are oblivious to their malodor. A typical scenario has the condition identified by a family m e m b e r or friend, at w h i c h time the patient b e c o m e s aware (and often upset).5~ If the odor is not immediately obvious to the doctor, there are several means by w h i c h awareness can be heightened. O n e suggestion has the doctor standing to the patient's side and, using a card, stirring the m o u t h air towards him- or herself. 3, 17 If a potential source is clearly identified; a p i e c e of gauze or a c o t t o n - t i p p e d applicator is used to sample the debris; asking a family m e m b e r to identify the o d o r as the offending smell confirms the source. 17 If important, a systemic or nasal source can be differentiated f r o m a m o u t h source by closing the m o u t h and exhaling t h r o u g h the nose, f o l l o w e d b y p i n c h i n g the nose and exhaling through the mouth. 1, is Because the esophagus is generally collapsed, certain disorders of the esophagus and s t o m a c h do not c o n t i n u o u s l y p r o d u c e an odor but rather d e p e n d on eructation. 43 Absolute confirmation f r o m family m e m b e r s or r e p e a t e d examinations m a y be n e e d e d to detect halitosis from these sources. Several instruments w e r e d e v e l o p e d in efforts to qualitate or quantitate m o u t h odor. The "olfactom e t e r , " " o s m o s c o p e , " and " c r y o s m o s c o p e " w e r e emp l o y e d to deliver c o n c e n t r a t e d boluses of air, w h i c h c o u l d be identified directly b y the investigator or analyzed in a mass s p e c t r o m e t e r or gas c h r o m a t o g r a p h . 7, is While of s o m e historical interest, these instruments s e e m to b e of little practical use to the clinician today.
Having d e t e r m i n e d that an odor is present, a careful history focuses attention to the a p p r o p r i a t e organ system, be it the oral cavities, the gastrointestinal system, or the lungs. A dietary and smoking history and a review of medications m a y b e helpful. The thorough history and physical e x a m i n a t i o n o u g h t to detect syst e m i c causes of halitosis s u c h as diabetic ketoacidosis, liver failure, and renal disease. A m e t i c u l o u s examination of the mouth, teeth, nose, and pharynx is indicated, because these are the sites w h e r e most causes of halitosis are identified. The pathologic condition is generally not subtle and should be easily detected, though rhinoscopic or laryngoscopic devices may need to be e m p l o y e d . Special attention is paid to periodontal tissues, p o o r l y m a n u f a c t u r e d or fitting dental restorations, tonsillar crypts, h y p e r t r o p h i e d tongue papillae, foreign bodies in the nose, and ulcerated mucosal or pharyngeal l e s i o n s - - eventually considering the w h o l e of the differential diagnosis for halitosis arising in the oral/nasal/pharyngeal cavities. Findings consistent with x e r o s t o m i a or m o u t h breathing may be intermittent and m o r e likely to be present early in the day. Physical findings of p n e u m o n i a , lung abscess, or emp y e m a should be apparent. Radiographic studies have limited usage: paranasal sinus x-rays are indicated w h e n sinusitis is suspected, and a chest x-ray is done w h e n the physician is looking for lung abscess or e m p y e m a . U p p e r gastrointestinal investigation, either radiographic or endoscopic, finds diverticula, achalasia, bezoars, or other disorders. Laboratory b l o o d and urine studies h e l p confirm a susp e c t e d systemic illness. If no organic disorder is obvious, ORS should be considered. Inherent in this diagnosis is a c o m p l a i n t of constant halitosis and the admission of c o m p u l s i v e cleansing contrasting w i t h an inability of observers to detect an odor. Efforts to identify underlying depression are often fruitful.
TREATMENT In most pathologic and altered physiologic conditions, identification of the underlying abnormality and a p p r o p r i a t e therapy eliminate the offending odor. Meticulous attention to p r o p e r oral hygiene excludes the c o m m o n e s t benign causes of halitosis. 6' 8 Simple toothbrushing, especially c o m b i n e d w i t h tongue brushing, suffices for m o r n i n g breathl8; vigorous tongue brushing the night before helps r e d u c e halitosis the next morning. 12 Dental flossing is an important adjunct. In one e x p e r i m e n t , students flossed one side of the m o u t h and not the other for a week. Selected judges c o u l d detect an offensive o d o r f r o m dental floss subsequently used on the nonflossed sides. 55 Poorly constructed or fitting dental appliances trap food particles, w h i c h then serve as the nidus for putrefaction. ~7 Proper m a n a g e m e n t of periodontitis, gingivitis,
JOURNALOF GENERALINTERNALMEDICINE,Volume 7 (November/December), 1992
p e r i c o r o n i t i s , n e c r o t i c cavities, a n d o t h e r d e n t a l causes o f halitosis is c l e a r l y i n d i c a t e d . M o u t h o d o r after t o o t h e x t r a c t i o n is t h o u g h t to b e d u e to a c o m b i n a t i o n o f a n e s t h e t i c agents a n d d e c a y i n g b l o o d i n the socketlS; it u s u a l l y clears o v e r a f e w days w i t h o u t s p e c i a l treatment. H u n g e r b r e a t h c a n b e c o u n t e r a c t e d b y e a t i n g , mast i c a t i n g (e.g., g u m c h e w i n g ) , o r e v e n r i n s i n g t h e m o u t h w i t h water, s Halitosis a r i s i n g f r o m m o u t h dryness, w h e t h e r d u e to a s y s t e m i c i l l n e s s s u c h as t h e sicca synd r o m e or s i m p l e m o u t h b r e a t h i n g , is i m p r o v e d b y prov i d i n g m o i s t u r e to t h e m o u t h . M a n y sufferers have a r e a d y glass o f l i q u i d n e a r b y . Hard c a n d i e s a n d g u m c h e w i n g s t i m u l a t e saliva flow. Swabs w i t h g l y c e r i n a n d l e m o n p r o v i d e relief. Specific l e s i o n s of t h e m o u t h , nose, s i n u s e s , phary n x , e s o p h a g u s , s t o m a c h , or l u n g s s h o u l d b e i d e n t i f i e d a n d m a n a g e d directly. Systemic i l l n e s s e s for w h i c h a m a l o d o r is o n e sign m u s t b e i d e n t i f i e d a n d t h e r a p y started. M i s g u i d e d a t t e m p t s to a v o i d e v a l u a t i o n a n d d i s g u i s e disease w i t h m o u t h w a s h o n l y d e l a y t h e diagnosis. O n e s h o u l d r e m e m b e r that m o s t causes o f halitosis c a n b e m a n a g e d w i t h g o o d c h a n c e s for r e s o l u t i o n . T h e r e a p p a r e n t l y are p e r s o n s w h o b e l i e v e that constipation (in one source, euphemistically called " m e c h a n i c a l d i s t e n s i o n o f t h e c o l o n ''5) is a c a u s e o f halitosis. Most a u t h o r s d o n o t a c c e p t this a n d m a k e t h e e x p l i c i t p o i n t that cathartics or c o l o n i c i r r i g a t i o n is o f n o h e l p . ~, 4, 2~, 45 H o w e v e r , o d o r s o r i g i n a t i n g f r o m the s m a l l i n t e s t i n e s are p u r p o r t e d to c a u s e m a l o d o r , a n d s u g g e s t i o n s to c o n t r o l this r a n g e f r o m s a l i n e laxatives 1 to strict v e g e t a r i a n i s m ) 2 ORS m a y r e s o l v e w i t h c o u n s e l i n g a l o n e . E v i d e n c e o f d e p r e s s i o n , h o w e v e r , is f r e q u e n t l y p r e s e n t . Pharmac o l o g i c t r e a t m e n t w i t h a n t i d e p r e s s a n t s is helpfulS2; t h e n e u r o l e p t i c p i m o z i d e is also r e p o r t e d to b e effective. 53 Finally, t h e r e are p e r s o n s w i t h halitosis for w h i c h a c a u s e c a n n o t b e f o u n d . W h i l e m o u t h w a s h e s have l i t t l e r e p o r t e d effect o n microflora,12these p r o d u c t s d o h i d e t h e o d o r t e m p o r a r i l y a n d are b e t t e r t h a n aerosols. Oils o f p e p p e r m i n t , s p e a r m i n t , a n d w i n t e r g r e e n are m e n t i o n e d as h a v i n g v a l u e L 4; c h l o r o p h y l l - b a s e d p r o d u c t s are t h o u g h t n o t to h e l p . 4s P r e p a r a t i o n s c o n t a i n i n g z i n c a n d / o r a s c o r b i c a c i d c a n d e c r e a s e m o u t h odors, ~7 t h o u g h these p r o d u c t s are n o t c o m m e r c i a l l y a v a i l a b l e . W h i l e n o t a c o m m o n c o m p l a i n t , halitosis c a n b e a n i m p o r t a n t sign of u n d e r l y i n g disease. A m e t i c u l o u s hist o r y a n d p h y s i c a l e x a m i n a t i o n are r e q u i r e d , b u t t h e l i k e l i h o o d o f f i n d i n g a m a n a g e a b l e c o n d i t i o n is r a t h e r high. Both p a t i e n t satisfaction a n d p h y s i c i a n satisfact i o n f r o m t h e i d e n t i f i c a t i o n o f t h e p r o b l e m are gratifying.
REFERENCES 1. Crohn BB, Drosd R. Halitosis. JAMA. 1941:117:2242-5. 2. Castellani A. Foetor oris of tonsillar origin and certain bacilli causing it. Lancet. 1930; 1:623-4.
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3. Bogdasarian RS. Halitosis. Otolaryngol Clin North Am. 1986; 19:111-7. 4. Massler M, Emslie RD, Bolden TE. Fetor ex ore. Oral Surg. 1951;4:110-25. 5. MarcuA. Let's talkabout bad breath. NYJDent. 1979;49:231-3. 6. Wantland WW, Lauer D. Correlation of some oral hygiene variables with age, sex and incidence of oral protozoa. J Dent Res. 1970;49:293-7. 7. Tonzetich J. Production and origin of oral malodor: a review of mechanisms and methods of analysis. J Periodontol. 1977; 48:13-20. 8. TonzetichJ, Ng SK. Reduction of malodor by oral cleansing procedures. Oral Surg. 1976;42:172-81. 9. Blankenhorn MH, Richards CE. Garlic and breath odor. JAMA. 1936; 107:409-13. 10. Goodman L, Bearg P. That garlic odor. JAMA. 1937; 108:136. 11. Goldfrank LR, Howland MA, Kirstein RH. Arsenic. In: Goldfrank LR, Weissman RS, Flomenbaum NE, Howland MA, Lewin NA, Kulberg AG (eds). Goldfrank's toxocologic emergencies, 3rd ed. East Norwalk, CT: Appleton-Century-Crofts, 1986;609-15. 12. WikesjOU. Halitosis-- foeter ex ore. Swed DentJ. 1978;2:55-9. 13. Anonymous. Dimethyl sulphoxide. In: Reynolds JEF, Parfitt K, Parsons AV, Sweetman SC (eds). Martindale: the extra pharmacopoeia, 29th ed. London: The Pharmaceutical Press, 1989; 1426-7. 14. Nally F. Halitosis. Practitioner. 1990;234:616-7. 15. O'Reilly RA, Motley CH. Breath odor after disulfiram. JAMA. 1977;238:2600. 16. FIether SM, Blair PA. Chronic halitosis from tonsilloliths. J La State Med Soc. 1988;140:7-9. 17. Van Eck C. Some thoughts on halitosis. J N Z Soc Periodontol. 1988;66:19-21. 18. Ceravolo FJ, Baumhammers A. Halitosis. Periodontol Abstr. 1973;21:151-4. 19. Chow AW, Roser SM, Brady FA. Orofacial odontogenic infections. Ann Intern Med. 1978;88:392-402. 20. Sulser G, Brening R, Foskick L. Some conditions that affect the odor concentration of breath. J Dent Res. 1939;18:355-9. 21. Hawkins C. Real and imaginary halitosis. Br Med J. 1987; 294:200-1. 22. Nally F. Causes of dry mouth. Practitioner. 1990;234:610-5. 23. Archard HO. Common stomatologic disorders. In: Fitzpatrick TB, Arndt KA, Clark WH, Eisen AZ, Van Scott EJ, Vaughan JH (eds): Dermatology in general medicine, 7th ed. New York: McGraw Hill, 1971;795-911. 24. Bailey BJ. Foul bi'eath. JAMA. 1988;259:3051. 25. Pelletier LLJr. Infections due to mixed anaerobic organisms. In: Petersdorf RG, Adams RD, Braunwald E, Isselbacher KJ, Martin JB, Wilson JD (eds). Harrison's principles of internal medicine, 10th ed. New York: McGraw Hill, 1983; 1013-8. 26. Jabaley ME, Clement RL, Bryant WM. Recognizing oral lesions. Am Fam Physician. 1976;13:60-4. 27. Block PL, Houston GD. Speech impediment and halitosis due to an extensive palatal fibroma. Ann Dent. 1987;46:20-2. 28. Bennett JD. Unexpected cause of halitosis. J R Army Med Corps. 1988;134:151-2. 29. Lovewell R. An unexpected cause of halitosis. Br Dent J. 1984;157:384. 30. Kuriloft DB. Nasalseptal perforations and nasal obstruction. Otolaryngol Clin North Am. 1989;22:333-50. 31. Weinstein L. Diseases of the upper respiratory tract. In: Petersdoff RG, AdamsRD, Braunwald E, Isselbacher KJ, MartinJB, Wilson JD (eds). Harrison's principles of internal medicine, 10th ed. New York: McGraw Hill, 1983; 1567-72. 32. Kassel SH, Echevarria RA, Guzzo FP. Midline malignant reticulosis: so-called midline lethal granuloma. Cancer. 1969; 23:920-35. 33. Fauci AS, Wolff SM. Wegener's granulomatosis: studies in eighteen patients and a review of the literature. Medicine. 1973;52:535-61. 34. Komisar A. Nasal obstruction due to benign and malignant neoplasms. Otolaryngol Clin North Am. 1989;22:351-65. 35. Pruet CW, Duplan DA. Tonsil concretions andtonsilloliths. Otolaryngol Clin North Am. 1987;20:305-9. 36. Hardingham M. Periotonsillar infections. Otolaryngol Clin North Am. 1987;20:273-8. 37. Ossoff RH, Wolff AP. Acute epiglottitis in adults. JAMA.
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1980;244:2639-40. 38. Sharma NK. An unexpected cause of halitosis. Br Dent J. 1984;157:281-2. 39. Greenberger NJ. Gastrointestinal disorders: a pathophysiologic approach. Chicago: Year Book, 1981; 14-5. 40. Cohen S. Motor disorders of the esophagus. N Engl J Med. 1979;301:184-92. 41. Richter JE, Castell DO. Gastroesophageal reflux. Ann Intern Med. 1982;97:93-103. 42. Thomas DF. Bad breath. JAMA. 1988;260:2665. 43. Tydd TF, Dyer NH. Pyloric stenosis presenting with halitosis. Br MedJ. 1974;3:321. 44. Stephenson BM, Rees BI. Extrinsic duodenal obstruction and halitosis. Postgrad Med J. 1990;66:568-7045. Hine MK. Halitosis. J Am Dent Assoc. 1957;55:37-46. 46. Bartlett JG, Finegold SM. Anaerobic pleuropulmonary infections. Medicine. 1972;51:413-50. 47. Lorber B. "Bad breath" and pulmonary infection. Ann Rev Respir
Dis. 1975;112:875-7. 48. Gudiol F, Manresa F, Pallares R, et al. Clindamycin vs penicillin for anaerobic lung infections. Arch Intern Med. 1990;150: 2525-9. 49. Turck M. Foul breath and a productive cough. Hosp Pract [Off]. 1985;20(5a):50. 50. Pryse-PhillipsWEM. Disturbance in the sense ofsmell in psychiattic patients. Proc R Soc Med. 1975;68:472-4. 51. Hirsch AR. Bad breath. JAMA. 1988;260:2665. 52. Pryse-Phillips WEM. An olfactory reference syndrome. Acta Psychiatr Scand. 1971;47:484-509. 53. Goldberg RL, Buongiorno PA, Henkin RI. Delusions of halitosis. Psychosomatics. 1985;26:325-7,331. 54. Berkman S. Those embarrassing ailments: here's help! Good Housekeeping. 1986;203:318-9. 55. Ceravolo FJ, Baumhammers A, Robin G. The odor emitted from dental floss used on flossed teeth and non-flossed teeth for a one week time period. Periodontol Abstr. 1973;21 : 155-8.
REFLECTIONS Old Voices On hospital rounds one morning I f o u n d an o l d m a n d y i n g f r o m pneumonia Saying
Young man, gain knowledge. I t u r n e d , w r o t e a n o t e in his chart. Around the corner I f o u n d an o l d m a n s p i t t i n g b l o o d Saying
Young man, learn to love. I t u r n e d , w r o t e a n o t e in his chart. U p t h e stairs I f o u n d an o l d m a n c o n s u m e d w i t h TB Saying
Young man, tell m e the truth. I t u r n e d , w r o t e a n o t e in his chart. D o w n t h e hall I f o u n d an o l d m a n c h o k i n g w i t h cancer Saying
Young man, enjoy yourself. I t u r n e d , w r o t e a n o t e in his chart. W h e n I finished r o u n d s a c h o r u s Of old voices spoke to me from nowhere Saying
Young man, we are k n o w n by m a n y names. Quit scribbling, j u s t listen to us. ERIC L. DYER, MD
Nashville, TN
HALITOSIShas been popularized by the media, typically in the commercial pitches of high-priced remedies. Similar to "the heartbreak of psoriasis," this incessant repetition of a medical bogeyman threatens to c h e a p e n what can be a true sign of significant disease. A recent case demonstrates h o w the recognition of the meaning of bad breath can lead to expeditious treatment. A 35-year-old woman presented with fever, fatigue, and cough productive of discolored but not malodorous sputum. Her illness had begun shortly after a party one month before admission when she "may have drunk too much." She had continued to work in an office job until the day before presentation. Physical examination revealed dullness on chest percussion. The chest x-ray showed a huge (15-cm diameter), circumscribed postcardiac mass. She was admitted to the hospital with the consideration of a lung abscess or pulmonary tumor. Six hours after admission, she developed extreme shortness of breath with agitation. Upon entering the room, medical and nursing staff were met with an extremely foul, fetid odor. The patient was immediately intubated, with endotracheal suction of copious quantities of foulsmelling, dark grey sputum. Portable chest x-ray showed the new presence of an air/fluid level within the mass and the spread of a pneumonic process throughout much of the rest of the lung. The sputum eventually grew the anaerobes Fusobactertum nucleatum, Bacteroides melaninogenicus, and a Peptostreptococcus species. The woman survived only after a prolonged intensive care unit and a hospital stay. The onset of bad breath represented rupture of the abscess, and rapid recognition of the significance of this sign saved precious time in initiating therapy. Halitosis is important for at least three reasons. It is a social handicap: for p e o p l e w h o deal with the public, bad breath causes discomfort in others, with the person's usefulness b e c o m i n g diminished. Those w h o are aware of their o w n m o u t h odor may be obsessed with clean breath, to the point of impairing their o w n effectiveness. And finally, medically, halitosis is usually a sign that an abnormal condition exists, awaiting diagnosis and treatment.
Received from the Division of General and Geriatric Medicine, Department of Medicine, University of Kansas Medical Center, 3901 Rainbow Boulevard, Kansas City, Kansas 66160. Address correspondence and reprint requests to Dr. Johnson.
DEFINITION At one time, clinicians attempted to draw a distinction b e t w e e n " t r u e fetor ex o r e " or "fetor otis" and " t h e internal malady k n o w n familiarly as halitosis."~. 2 The former was felt to a p p l y to an odor emanating from local conditions of the m o u t h and h o l l o w cavities (sinuses, nose, pharynx), while the latter referred to odors having a systemic origin that were exhaled from the lungs. This difference is largely disregarded today. Halitosis is foul, offensive, or bad-smelling breath arising from a person's oral - nasal cavity, regardless o f the source. It is usually noticed by a nearby observer though, curiously, not always by the patient him- or herself. Halitosis is not dysgeusia (altered p e r c e p t i o n o f taste) and is not anosmia (absent or altered sense of smell). These disorders of senses represent distinct symptoms themselves, t h o u g h the evaluation of halitosis may overlap their evaluation.
CAUSES/DIFFERENTIAL DIAGNOSIS When c o n f r o n t e d with a patient complaining of, or presenting with, halitosis, it is useful to consider three separate diagnostic groups: n o n p a t h o l o g i c causes, pathologic causes, and psychiatric conditions (Table 1). A simple test identifies the first two groups. If an observer smells bad breath, there may be a pathophysiologic cause; if not, the complaint may reflect a psychiatric condition and necessitate a different approach. The o d o r itself arises from one or a combination of several processes. Body tissue and desquamated epithelium d e c o m p o s e and release odors; if located near the nose and m o u t h these odors are recognized as halitosis. Gram-negative and anaerobic bacteria in the oral cavity can overgrow, releasing o b n o x i o u s gases. There are foods, drugs, or other materials that, w h e n ingested, are processed by the b o d y and travel to the lungs, w h e r e they vaporize and are exhaled. Systemic illnesses sometimes have an associated breath odor. The delineation of these sources constitutes the differential diagnosis of halitosis.
Nonpathologic Causes Changes with age.
As far back as Pliny the 649
Johnson, HALITOSIS
650 TABLE 1
Causes of Halitosis Nonpathologic Age Morning breath, hunger breath, menstrual breath Food and drugs Tobacco Pathologic Mouth--dental work. periodontitis, dehydration, stomatitis, glossitis, parotid disease, tumors Nose/sinuses--foreign bodies, infections, destructive lesions, tumors, chronic sinusitis Tonsils/pharynx--tonsillitis, concretions, pharyngitis, epiglottitis, foreign bodies, tumors, diverticula Digestive organs--achalasia, reflux, outlet obstruction, bezoars Pulmonary-- necrotizing pneumonia, anaerobicabscessand empyema Systemic illness--diabetic ketoacidosis, liver failure, renal failure Psychiatric Schizophrenia, olfactory reference syndrome
Younger (AD 6 1 - 1 1 3 ) , there have b e e n r e p u t e d changes in breath o d o r attributed to aging. 3, 4 Infants and children are described as having " s w e e t " breath, w h i l e adolescents have breath that is " n o t u n p l e a s a n t . " Adults' m o u t h o d o r can be described as " s t r o n g , " w h i l e that of the aged is n o t e d to be "heavy, pungent. ''4,s A general increase in bacteria in the m o u t h occurs w i t h advancing age 6; additionally, after middle age, m e n are found to have m o r e bacteria in the m o u t h than are w o m e n of the same age, p e r h a p s accounting for m o r e disagreeable breath in older men.
Morning breath. O f all the causes of halitosis, this is the most c o m m o n (and p r o b a b l y the one most successfully e x p l o i t e d c o m m e r c i a l l y ) . The m o u t h is b a t h e d t h r o u g h o u t the day b y saliva, w h i c h flows around the teeth, tongue, and gums, collecting particles of food and organic matter. Saliva is s w e p t b a c k to the pharynx and swallowed, carrying the material w i t h it. Saliva has a basal p H o f 6.5 and is mildly bacteriostatic to gram-negative and anaerobic bacteria. With sleep, saliva flow decreases and any p o o l e d saliva slowly changes. The pH rises above 7.0, and enzymatic breakd o w n occurs, making the saliva itself odoriferous. 4 The tidal m o v e m e n t of saliva is arrested, and a c c u m u l a t e d food and e p i t h e l i u m b e c o m e substrates to m o u t h flora. Bacterial o v e r g r o w t h and b r e a k d o w n of this organic matter cause m o r n i n g breath. ~ Arousal w i t h eating, drinking, and speaking all stimulate saliva flow, washing the material away. 8 In this way, morning breath n o r m a l l y ceases w i t h o u t intervention. Hunger breath. A disagreeable odor may b e detected on the breath of persons w h o have missed meals.3.8 It is postulated that " h u n g e r b r e a t h " represents the p u l m o n a r y exhalation o f volatile m e t a b o l i c b r e a k d o w n p r o d u c t s of b o d y fats and proteins. What-
ever the cause of hunger, w h e t h e r dieting or frank starvation, the decreased saliva flow and m o u t h dryness that c o m e from not masticating exacerbate the problem. Regular snacks or meals p r o v i d e a nutritional load and a stimulus to salivary production, thus correcting the malodor.
Menstrual breath. There are references to an oral malodor afflicting menstruating w o m e n ~, ~ ( t h o u g h it should be p o i n t e d out that these sources reference G e r m a n articles of the late 1800s). Described as the odor of decayed, clotted blood, this was s u p p o s e d l y present on the day p r e c e d i n g menstruation. Menstrual breath was described as especially likely to o c c u r in w o m e n with dysmenorrhea. Food and drugs. The most recognized food causing halitosis is garlic. Garlic has b e e n used in a n u m b e r of e x p e r i m e n t s that sought to d e t e r m i n e the causes of halitosis.i, 9, 10 In one series of observations involving patients with natural or postsurgical intestinal abnormalities, garlic was instilled directly into gastrointestinal ostomies or fistulae. The characteristic odor was n o t e d on the breath w i t h o u t the garlic's having b e e n swallowed. Garlic c o u l d even be detected on the breath after being r u b b e d on the feet. 9 A garlic-like o d o r has b e e n attributed to several inorganic materials, including arsenic, selenium, vanadium, and inorganic phosphorus, t 1 O t h e r foods p r o d u c e a distinct m o u t h odor. Onion, fish, and m a n y alcoholic drinks are readily recognized. People in cultures that do not use c o w ' s milk (e.g., the Chinese) allegedly find the breath of milk drinkers objectionable1, 12; years ago Occidental physicians c o u l d even detect those patients w h o w e r e prescribed a milk-based (Sippy's) diet for the treatment of u l c e r disease. 1 Certain medicines cause halitosis. Most notorious for this in recent years was dimethyl sulfoxide (DMSO), w h e t h e r used for interstitial cystitis or as a l i n i m e n t ) 3 O t h e r drugs i m p l i c a t e d in halitosis include amyl nitrate, chloral hydrate, disulfiram ( w h e n given with warfarin), paraldehyde, and metronidazole. ~4"t6 Tobacco breath. The odor of tobacco smoking lingers long after the last cigarette, cigar, or pipe. Dentists are frequently a d m o n i s h e d b y their peers to r e m e m b e r this manifestation of the smoking habit.4, s, 12
Pathologic Causes Mouth. The mouth, tongue, and teeth are implicated in the majority of cases of halitosis. This is no surprise to dentists, oral surgeons, and otolaryngologists, w h o are often consulted regarding this complaint. Retained food, especially meats and fish, w h i c h are
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high in sulfur-containing amino acids, is simple to detect and easy to remedy. 7, 17 Dental p r o b l e m s that result in t r a p p e d food particles include p o o r l y finished restorations with overhanging margins and lack of contact points b e t w e e n restorations. O r t h o d o n t i c braces are notorious for collecting food particles. Plaque, the g u m m y mass of microorganisms that a c c u m u l a t e s along the crowns and roots of teeth, may cause halitosis, 7, ~8 particularly if associated w i t h periodontitis. Periodontitis (inflammation of the p e r i o s t e u m , alveolar bone, and s u p p o r t i n g structures) and gingivitis (inflammation of the gums) are the teeth-related conditions p r o d u c i n g the most disagreeable m o u t h odor.19, 2o Desquamated, necrotic tissue, m i n o r bleeding, and microbial infestation c o m b i n e to p r o d u c e foul odor. Periodontitis and gingivitis exist in a confined, anaerobic e n v i r o n m e n t c o n d u c i v e to bacterial g r o w t h and p r o t e c t e d from the cleansing action of saliva. Pericoronitis (inflammation of the tooth c r o w n ) and dental caries are m u c h m o r e e x p o s e d to the cleansing activity of saliva and mastication. 19 In fact, dental caries contribute little to m o u t h breath unless there is a necrotic pulp.6, 2o Gas c h r o m a t o g r a p h i c analysis of m a l o d o r o u s m o u t h air reveals two basic gases. 7, 21 The substance most frequently present is hydrogen sulfide. The n e x t c o m m o n e s t , but the gas most objectionable at low concentrations, is m e t h y l m e r c a p t a n . Together, these two gases account for over 90% of m o u t h gas p r o d u c t i o n , w i t h the remainder b e i n g small levels of dimethyl sulfide and dimethyl disulfide. Typically found in gingiv a l / p e r i o d o n t a l disease, food trapping, and p o o r oral hygiene, these w e r e the gases also f o u n d in dental students with m o r n i n g breath. 8 Similarly, m e n t a l l y retarded, handicapped, or seriously ill persons w h o cannot carry out their o w n oral hygiene regimens are likely to have halitosis. 2~ Decreased saliva flow (xerostomia) c o m p r o m i s e s normal cleansing m e c h a n i s m s of the mouth, allowing the d e v e l o p m e n t of halitosis. 3, ~4, 22 This is the p r o b a b l e m e c h a n i s m for m o u t h o d o r in the sicca s y n d r o m e (including Sj/Sgren's syndrome, r h e u m a t o i d arthritis, syst e m i c lupus erythematosus, scleroderma, chronic hepatitis, or p r i m a r y biliary cirrhosis). Xerostomia also occurs following radiation therapy to the head and neck, due to decreased w a t e r intake itself (as often seen in the elderly); f r o m medications, including diuretics, antihypertensives, anticholinergics, and tricyclic antidepressants; and in m o u t h breathing. Stomatitis and glossitis occasionally cause halitosis w h e n o p e n ulcers, fissures, or enlarged papillae trap food particles and d e s q u a m a t e d t i s s u e ) 9, 22 Deficiencies of vitamins or minerals such as vitamin A, vitamin B~2, iron, or zinc m a y dry the m o u t h w i t h fissuring. 23 Liquid or soft diets coat the tongue w i t h p r o t e i n a c e o u s matter but might not stimulate normal mastication. 8 Infections involving the tongue and m u c o u s m e m branes, such as Vincent's stomatitis (necrotizing ulcer-
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ative gingivostomatitis), measles, diphtheria, thrush, and herpangina involve significant tissue breakdown, altered ~aliva flow, and putrefaction. 3, 16 Ironically, despite the gross appearance, m a n y p r i m a r y or secondary conditions of the tongue (e.g., black hairy tongue, geographic tongue, midline r h o m b o i d glossitis) only occasionally cause halitosis. 23 Certain diseases of the parotid gland, such as m u m p s , ascending parotitis, u v e o p a r o t i d fever, or parotid abscess, decrease saliva p r o d u c t i o n , c o n t r i b u t i n g to dry m o u t h and halitosis. 22, 24 C a n c r u m oris ( n o m a ) , occurring in severely m a l n o u r i s h e d children, and occasionally in acute leukemia, is a w i d e s p r e a d destructive infection of the cheeks, maxilla, and mandible2S: this anaerobic infection is described as especially foulsmelling. Oral bleeding, especially in debilitated patients w h o cannot cleanse the mouth, provides a rich substrate for protein b r e a k d o w n and release of gases; this is not u n c o m m o n in gingivitis, h e m o p h i l i a , or leukemia, or in cancer c h e m o t h e r a p y . Primary malignant or benign tumors of the m o u t h , including t u m o r s of the tongue, gums, cheeks, or palate, may cause halitosis. 26, 27 Necrotic material, oozing of blood, and food trapping c o m b i n e in putrefaction. These t u m o r s are not infrequently f o u n d in persons w i t h p o o r oral hygiene, giving dual sources for gas production. In the past, dentures w e r e m a d e of a p o r o u s vulcanite material, w h i c h bacteria w e r e able to penetrate.3, 4 These c o u l d p r o d u c e malodor, even w h e n rem o v e d from the mouth. Current acrylic dentures do not have this p r o b l e m , but persons w h o do not r e m o v e and clean their dentures, o r w h o a l l o w food to be t r a p p e d in prosthetic devices, d e v e l o p halitosis. N o s e a n d s i n u s e s . Normal rhinorrhea has no disagreeable odor. Even thick, p u r u l e n t nasal discharge found in typical u p p e r respiratory infections is rarely odoriferous. Some observers attribute a disagreeable odor to atrophic rhinitis as might b e seen in the elderly.16, 24 Malodor f r o m the nose and sinuses otherwise involves destructive nasal/palatine processes, nasal foreign bodies, or c h r o n i c infection of the sinuses. An assortment of objects m a y be inserted into the nose and n e g l e c t e d for long periods of time. Children and m e n t a l l y retarded persons have p l a c e d pellets of paper, seeds, peanuts, beads, or parts of toys in the nose.21, 2a. 29 A foreign b o d y present in the nose induces an inflammatory response that b e c o m e s secondarily infected, p r o d u c i n g o b n o x i o u s gases. Destructive lesions of the nose create an inflammatory response and necrotic tissue, which, w h e n putrefied, cause halitosis. Simple nasal septal perforation, w h e t h e r from chronic nose picking, from cocaine use, or as a c o m p l i c a t i o n of nasal surgery, typically exists w i t h o u t an odor. 3° Ozena is a severe, c h r o n i c rhinitis characterized b y a thick, greenish, m a l o d o r o u s dis-
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charge, mucosal crusting, and turbinate b o n e atrophy. If not m a n a g e d aggressively w i t h antibiotics, local cleansing, or even surgery, ozena m a y destroy nasal turbinates and cause anosmia. 31 O t h e r invasive infectious conditions such as leprosy, yaws, or a syphilitic g u m m a have an offensive odor. 31 Equally serious is the nasal/palatine presentation of lethal midline granuloma and W e g e n e r ' s granulomatosis. 32, 33 T r e a t m e n t of patients w h o have these destructive diseases m a y be successful, b u t the o d o r can be quite offensive until c u r e is achieved. Tumors of the nasal cavities are u n c o m m o n . W h e n t h e y occur, though, they are f r e q u e n t l y e x o p h y t i c and bloody, p r o d u c i n g malodor. 34 The person w i t h chronic sinusitis may have a disagreeable odor. 3, 16, 24 Halitosis f r o m sinusitis c o n n o t e s infection w i t h anaerobic bacteria, 19 including organisms that are present in a b o u t half of the cases of chronic sinusitis necessitating surgery. Acute sinusitis is typically not caused b y an anaerobic infection31; halitosis presenting in acute disease suggests spread from an anaerobic tooth abscess.
Tonsilsandpharynx. Repeated infections of the tonsils and adenoids lead to c h r o n i c follicular tonsillitis.2, 16, 2~ D e e p crypts form, w h i c h collect food, saliva, and necrotic matter. If natural m e c h a n i s m s do not cleanse the crypts, such collections form tonsilloliths. These are concretions lying on an inflammatory base and c a p a b l e of causing halitosis.3S It is unclear w h e t h e r tonsilloliths are also causative in peritonsillar abscess, an acute, purulent, m a l o d o r o u s infection. 36 Tonsillect o m y leaves a raw, surgical w o u n d with bleeding, necrotic tissue that is foul for several days postoperatively. 24 Pharyngitis f r o m virtually any organism can cause halitosis.3. 19 Most dramatic, perhaps, is that due to diphtheria, b u t severe pharyngitis from infectious mononucleosis, streptococcal infection, infection w i t h Candida (thrush), herpangina, or infection w i t h o t h e r microorganisms can all generate bad breath. The key factors include d e s q u a m a t e d e p i t h e l i u m , inadequate hygiene, and " n o r m a l " m o u t h flora, w h i c h p r o d u c e putrefaction. Acute epiglottitis, w h i l e typically due to Hemophilus influenzae infection in children, m a y result from infection w i t h H. influenzae, Streptococcus pyogenes, or S. pneumoniae in adults. 37 While halitosis is admittedly u n c o m m o n in acute epiglottitis, the rapid e n l a r g e m e n t o f the epiglottis makes swallowing difficult and results in p o o l i n g of saliva and inflammatory material. The p h a r y n x also is a site for tumors, w i t h uncleared, necrotic material causing halitosis. 16
A mentally impaired woman developed halitosis and weight loss. Multiple efforts to determine the cause were unsuccessful, and panendoscopy was scheduled. Intuba-
tion could not be accomplished. On investigation, the anesthetist discovered the wheel from a toy lodged in her pharynx. Air and some fluid, but no food, had been able to pass through the axle hole of the wheel. 38 Zenker's d i v e r t i c u l u m is an o u t p o u c h i n g that occurs at the junction of the posterior h y p o p h a r y n x and the esophagus, a site of natural weakness. 39 W h e n small, the d i v e r t i c u l u m is asymptomatic, but as it enlarges food and saliva lodge within it. D e c o m p o s i t i o n releases o b n o x i o u s gases but often o n l y intermittently, d e p e n d i n g on esophageal peristaltic activity.
Digestive organs--the esophagus, stomach, small intestines. Diverticula similar to Zenker's div e r t i c u l u m may f o r m virtually anywhere in the esophagus and be a source of halitosis. Achalasia is a p r i m a r y m o t o r disorder that results in altered or absent peristalsis of the esophagus, partial or i n c o m p l e t e relaxation of the l o w e r esophageal sphincter (LES), and increased resting LES pressure.4° Dysphagia is the typical presenting complaint, t h r o u g h the condition can be asymptomatic for long periods of time. Another hallmark of the disease is a lack of c o m p l e t e e m p t y i n g of the esophagus into the stomach. This results in retention of food, liquid, and saliva within a gradually e x p a n d i n g esophagus. Breakdown of this matter with eructation of the resultant gases is r e c o g n i z e d as halitosis. Tumors of the gastroesophageal junction, chronic idiopathic pseudoobstruction of the esophagus, and Chagas' disease may present w i t h achalasia-like symptoms, including food and liquid retention. Gastroesophageal reflux is an e x t r e m e l y c o m m o n disorder that may rarely have halitosis as one of multiple presentations. 41 The most f r e q u e n t s y m p t o m is heartburn, though atypical chest pain and p u l m o n a r y disorders (cough, wheezing, recurrent p n e u m o n i a ) o c c u r regularly. Since the esophagus collapses in its natural state, air does not pass easily to the outside. With eructation, though, swallowed gases do escape. The o d o r associated w i t h gastroesophageal reflux, like that of simple belching,21.39 is of stomach contents and resembles the o d o r of the most recently ingested meal. O t h e r mechanical disorders of the stomach have b e e n r e p o r t e d in association with halitosis. A trichobezoar caused bad breath in a y o u n g girl. 42 Adults with gastric outlet obstruction d e v e l o p e d halitosis, w h i c h cleared only briefly w i t h antibiotic treatment. 43 Two children w i t h peritoneal bands causing duodenal obstruction had resolution of halitosis with release of the bands. 44 At one time, odors w e r e described in association with intestinal maladies, most particularly obstruction or constipation. 5,9 Few hold this v i e w presently. 1, 4, 21, 45
Pulmonary.
Anaerobic lung abscess, necrotiz-
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ing p n e u m o n i a , and e m p y e m a all frequently have halitosis as an i m p o r t a n t presenting s y m p t o m . 16. 24, 46 Halitosis is present in as m a n y as 40 - 50% of patients w i t h anaerobic p u l m o n a r y infections .46 These infections are thought to originate from aspirated m o u t h flora 7, 46, 47 since the m o u t h s of persons w i t h periodontal disease and gingivitis have very high concentrations of anaerobic bacteria. Consequently, these lung infections o c c u r most c o m m o n l y in persons w i t h p o o r oral hygiene w h o are likely to aspirate (e.g., alcoholics).48 Even so, halitosis from an anaerobic lung abscess has b e e n described in an e d e n t u l o u s patient. 49 Bronchiectasis, w h e t h e r congenital or acquired, is also a source of malodor. Generally, though, w h e n o d o r is present the patient is having an exacerbation of the underlying disease. 46 Patients w i t h bronchitis or p n e u monia from aerobes, m y c o p l a s m a or viruses, even if productive of c o p i o u s quantities of s p u t u m , do not usually have bad breath.
Systemic illness. It has long b e e n r e c o g n i z e d that odor f r o m a patient's breath can b e a clue to diagnosis of a systemic illness. As m e n t i o n e d above, until recent times physicians defined "halitosis" as the m o u t h odor originating from a systemic cause. However, smell is a highly subjective sense, and precision in identification of various odors for medical usage is a skill little p r a c t i c e d and p o o r l y taught. Some odors are characteristic e n o u g h to be discriminating as diagnostic aids. l, 12, 14, 45 The sweetish, fruity, acetone smell of diabetic ketoacidosis is classic. Fetor hepaticus is variably described as fishy, mousy, metallic, or like decaying blood. Ammoniacal or urinous odors emanate from persons w i t h renal disease and uremia. Smells have b e e n ascribed to a n u m b e r of o t h e r diagnoses. A m u s t y smell m a y have b e e n noticed in p e o p l e w i t h scarlet fever or t y p h o i d fever ( t h o u g h this t e r m was also e m p l o y e d for liver disease). Patients w i t h "intestinal d y s f u n c t i o n " and " c h o l e m i a " m i g h t have had a heavy, sour breath. A decaying b l o o d smell was ascribed to intestinal h e m o r r h a g e and menstrual breath. A sweetish, sour breath has b e e n attributed to a high dairy intake, w h i l e c o n s u m p t i o n of fatty m e a t c o u l d have given a bitter, fecal, stinking breath. Eskimos w e r e alleged to smell like blubber. [Additional terms describing local, not systemic, conditions included: sweetish acid for thrush; rotting hay for Vincent's infection (necrotizing ulcerative stomatogingivitis); sweetish for lactation; intense, disagreeable, fetid, and foul for periodontal disease; alliaceous (garlic-like) for b i s m u t h or p h o s p h o r u s intake; and Limb u r g e r cheese-like for chronic follicular tonsillitis.] It is doubtful that precise a g r e e m e n t o c c u r r e d in the attribution of these various odors to specific diseases in the past; it is certain that other means of diagnosis are m o r e valuable today.
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Psychiatric Conditions If a patient presents w i t h a c o m p l a i n t of halitosis and no m a l o d o r is present, the physician should not i m m e d i a t e l y c o n c l u d e that no p a t h o l o g i c condition is present; an evaluation m a y still b e indicated. However, if no organic cause for halitosis is f o u n d and r e p e a t e d examinations do not reveal bad breath, then a psychiatric condition should be considered. The psychiatric causes fall into two classes largely distinguished b y w h e t h e r the p e r c e i v e d odor, the olfactory hallucination, is extrinsic or intrinsic to the patient's body. A t r u e olfactory hallucination has b e e n defined as the "subjective p e r c e p t i o n of an o d o r w i t h o u t an objective s t i m u l u s . " 5o
Olfactory hallucinations o f extrinsic sources. These patients r e p o r t odors that e m a n a t e f r o m an external source, s°. 51 The smells are described as chemicals or p e o p l e or animals. Unlike smells from an organic illness, w h i c h tends to fatigue w i t h t i m e (adaptation p h e n o m e n o n , discussed b e l o w in the Evaluation section), these extrinsic smells are c o n t i n u o u s l y perceived b y the patient. T w o clinical settings a c c o u n t for most olfactory hallucinations of extrinsic sources. T e m p o r a l lobe epilepsy (which, of course, is not a psychiatric disease) s o m e t i m e s begins w i t h a p e r c e i v e d smell, the aura. This hallucination is usually brief and only rarely mistaken for halitosis. 5° Schizophrenics have olfactory hallucinations, and such c o m p l a i n t s can be r e m a r k a b l y difficult to extinguish. Olfactory hallucinations o f intrinsic sources. The olfactory r e f e r e n c e s y n d r o m e (ORS) is the t e r m a p p l i e d to olfactory hallucinations of intrinsic sources.52, 53 This s y n d r o m e is a s u b t y p e of m o n o s y m p tomatic h y p o c h r o n d r i a c a l psychosis (DSM-III-R), the classification that includes other conditions in w h i c h there is a p r e o c c u p a t i o n w i t h imagined b o d y defects. The patient w h o has ORS believes that the offending smell has an intrinsic source B either sweat, intestinal gas, or the breath (halitosis). The patient m a y r e s p o n d in three ways: 1) minimally, w i t h f e w efforts to guard others f r o m the odor; 2) s o m e w h a t reasonably, w i t h efforts to hide the odor; or 3) contritely, w i t h self-abasement and embarrassment, believing that he or she stinks and offends others. 5° People w i t h ORS suffer the delusion that others readily detect the odor, and so they have h e i g h t e n e d distress around o t h e r p e o p l e . T h e y do not believe that o t h e r p e o p l e cannot smell them; small m o v e m e n t s , grimaces, or responses in acquaintances and strangers are i n t e r p r e t e d as efforts to distance themselves from the patient. Unlike p e o p l e w h o truly have halitosis, the o d o r to patients w i t h ORS remains constant, does not fatigue, and is always present. This results in obsessive
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behavior consisting of frequent washing, clothes changing, and use of deodorant or mouthwash, and social withdrawal. Further psychiatric evaluation m a y disclose the fact that a person is quietly paranoid, isolating him- or herself to p r e v e n t embarrassment. These persons have b e e n described as sensitive, obsessive, and insecure. Typically there are s y m p t o m s of depressive illness. The s y n d r o m e may originate after an episode of rhinorrhea, sinusitis, or an allergic reaction. Occasionally, ORS h a p p e n s after a friend or family m e m b e r has c o m p l a i n t s of halitosis. 53 The patient w i t h ORS is rarely satisfied that an organic cause cannot b e f o u n d and so f r e q u e n t l y has had m u l t i p l e consultations w i t h different doctors, complaining of the same symptom. There are concerns that p e o p l e w i t h this disorder w h o remain untreated are at risk for suicide. 52
EVALUATION The evaluation of halitosis begins w i t h recognition of the p r o b l e m . The adaptation p h e n o m e n o n describes the physiologic condition in w h i c h the threshold of sensitivity for a particular o d o r rises w i t h c o n t i n u e d e x p o s u r e to the scent. 5 Consequently, a foul smell is often u n n o t i c e a b l e to the patient; this explains w h y so m a n y w i t h halitosis are oblivious to their malodor. A typical scenario has the condition identified by a family m e m b e r or friend, at w h i c h time the patient b e c o m e s aware (and often upset).5~ If the odor is not immediately obvious to the doctor, there are several means by w h i c h awareness can be heightened. O n e suggestion has the doctor standing to the patient's side and, using a card, stirring the m o u t h air towards him- or herself. 3, 17 If a potential source is clearly identified; a p i e c e of gauze or a c o t t o n - t i p p e d applicator is used to sample the debris; asking a family m e m b e r to identify the o d o r as the offending smell confirms the source. 17 If important, a systemic or nasal source can be differentiated f r o m a m o u t h source by closing the m o u t h and exhaling t h r o u g h the nose, f o l l o w e d b y p i n c h i n g the nose and exhaling through the mouth. 1, is Because the esophagus is generally collapsed, certain disorders of the esophagus and s t o m a c h do not c o n t i n u o u s l y p r o d u c e an odor but rather d e p e n d on eructation. 43 Absolute confirmation f r o m family m e m b e r s or r e p e a t e d examinations m a y be n e e d e d to detect halitosis from these sources. Several instruments w e r e d e v e l o p e d in efforts to qualitate or quantitate m o u t h odor. The "olfactom e t e r , " " o s m o s c o p e , " and " c r y o s m o s c o p e " w e r e emp l o y e d to deliver c o n c e n t r a t e d boluses of air, w h i c h c o u l d be identified directly b y the investigator or analyzed in a mass s p e c t r o m e t e r or gas c h r o m a t o g r a p h . 7, is While of s o m e historical interest, these instruments s e e m to b e of little practical use to the clinician today.
Having d e t e r m i n e d that an odor is present, a careful history focuses attention to the a p p r o p r i a t e organ system, be it the oral cavities, the gastrointestinal system, or the lungs. A dietary and smoking history and a review of medications m a y b e helpful. The thorough history and physical e x a m i n a t i o n o u g h t to detect syst e m i c causes of halitosis s u c h as diabetic ketoacidosis, liver failure, and renal disease. A m e t i c u l o u s examination of the mouth, teeth, nose, and pharynx is indicated, because these are the sites w h e r e most causes of halitosis are identified. The pathologic condition is generally not subtle and should be easily detected, though rhinoscopic or laryngoscopic devices may need to be e m p l o y e d . Special attention is paid to periodontal tissues, p o o r l y m a n u f a c t u r e d or fitting dental restorations, tonsillar crypts, h y p e r t r o p h i e d tongue papillae, foreign bodies in the nose, and ulcerated mucosal or pharyngeal l e s i o n s - - eventually considering the w h o l e of the differential diagnosis for halitosis arising in the oral/nasal/pharyngeal cavities. Findings consistent with x e r o s t o m i a or m o u t h breathing may be intermittent and m o r e likely to be present early in the day. Physical findings of p n e u m o n i a , lung abscess, or emp y e m a should be apparent. Radiographic studies have limited usage: paranasal sinus x-rays are indicated w h e n sinusitis is suspected, and a chest x-ray is done w h e n the physician is looking for lung abscess or e m p y e m a . U p p e r gastrointestinal investigation, either radiographic or endoscopic, finds diverticula, achalasia, bezoars, or other disorders. Laboratory b l o o d and urine studies h e l p confirm a susp e c t e d systemic illness. If no organic disorder is obvious, ORS should be considered. Inherent in this diagnosis is a c o m p l a i n t of constant halitosis and the admission of c o m p u l s i v e cleansing contrasting w i t h an inability of observers to detect an odor. Efforts to identify underlying depression are often fruitful.
TREATMENT In most pathologic and altered physiologic conditions, identification of the underlying abnormality and a p p r o p r i a t e therapy eliminate the offending odor. Meticulous attention to p r o p e r oral hygiene excludes the c o m m o n e s t benign causes of halitosis. 6' 8 Simple toothbrushing, especially c o m b i n e d w i t h tongue brushing, suffices for m o r n i n g breathl8; vigorous tongue brushing the night before helps r e d u c e halitosis the next morning. 12 Dental flossing is an important adjunct. In one e x p e r i m e n t , students flossed one side of the m o u t h and not the other for a week. Selected judges c o u l d detect an offensive o d o r f r o m dental floss subsequently used on the nonflossed sides. 55 Poorly constructed or fitting dental appliances trap food particles, w h i c h then serve as the nidus for putrefaction. ~7 Proper m a n a g e m e n t of periodontitis, gingivitis,
JOURNALOF GENERALINTERNALMEDICINE,Volume 7 (November/December), 1992
p e r i c o r o n i t i s , n e c r o t i c cavities, a n d o t h e r d e n t a l causes o f halitosis is c l e a r l y i n d i c a t e d . M o u t h o d o r after t o o t h e x t r a c t i o n is t h o u g h t to b e d u e to a c o m b i n a t i o n o f a n e s t h e t i c agents a n d d e c a y i n g b l o o d i n the socketlS; it u s u a l l y clears o v e r a f e w days w i t h o u t s p e c i a l treatment. H u n g e r b r e a t h c a n b e c o u n t e r a c t e d b y e a t i n g , mast i c a t i n g (e.g., g u m c h e w i n g ) , o r e v e n r i n s i n g t h e m o u t h w i t h water, s Halitosis a r i s i n g f r o m m o u t h dryness, w h e t h e r d u e to a s y s t e m i c i l l n e s s s u c h as t h e sicca synd r o m e or s i m p l e m o u t h b r e a t h i n g , is i m p r o v e d b y prov i d i n g m o i s t u r e to t h e m o u t h . M a n y sufferers have a r e a d y glass o f l i q u i d n e a r b y . Hard c a n d i e s a n d g u m c h e w i n g s t i m u l a t e saliva flow. Swabs w i t h g l y c e r i n a n d l e m o n p r o v i d e relief. Specific l e s i o n s of t h e m o u t h , nose, s i n u s e s , phary n x , e s o p h a g u s , s t o m a c h , or l u n g s s h o u l d b e i d e n t i f i e d a n d m a n a g e d directly. Systemic i l l n e s s e s for w h i c h a m a l o d o r is o n e sign m u s t b e i d e n t i f i e d a n d t h e r a p y started. M i s g u i d e d a t t e m p t s to a v o i d e v a l u a t i o n a n d d i s g u i s e disease w i t h m o u t h w a s h o n l y d e l a y t h e diagnosis. O n e s h o u l d r e m e m b e r that m o s t causes o f halitosis c a n b e m a n a g e d w i t h g o o d c h a n c e s for r e s o l u t i o n . T h e r e a p p a r e n t l y are p e r s o n s w h o b e l i e v e that constipation (in one source, euphemistically called " m e c h a n i c a l d i s t e n s i o n o f t h e c o l o n ''5) is a c a u s e o f halitosis. Most a u t h o r s d o n o t a c c e p t this a n d m a k e t h e e x p l i c i t p o i n t that cathartics or c o l o n i c i r r i g a t i o n is o f n o h e l p . ~, 4, 2~, 45 H o w e v e r , o d o r s o r i g i n a t i n g f r o m the s m a l l i n t e s t i n e s are p u r p o r t e d to c a u s e m a l o d o r , a n d s u g g e s t i o n s to c o n t r o l this r a n g e f r o m s a l i n e laxatives 1 to strict v e g e t a r i a n i s m ) 2 ORS m a y r e s o l v e w i t h c o u n s e l i n g a l o n e . E v i d e n c e o f d e p r e s s i o n , h o w e v e r , is f r e q u e n t l y p r e s e n t . Pharmac o l o g i c t r e a t m e n t w i t h a n t i d e p r e s s a n t s is helpfulS2; t h e n e u r o l e p t i c p i m o z i d e is also r e p o r t e d to b e effective. 53 Finally, t h e r e are p e r s o n s w i t h halitosis for w h i c h a c a u s e c a n n o t b e f o u n d . W h i l e m o u t h w a s h e s have l i t t l e r e p o r t e d effect o n microflora,12these p r o d u c t s d o h i d e t h e o d o r t e m p o r a r i l y a n d are b e t t e r t h a n aerosols. Oils o f p e p p e r m i n t , s p e a r m i n t , a n d w i n t e r g r e e n are m e n t i o n e d as h a v i n g v a l u e L 4; c h l o r o p h y l l - b a s e d p r o d u c t s are t h o u g h t n o t to h e l p . 4s P r e p a r a t i o n s c o n t a i n i n g z i n c a n d / o r a s c o r b i c a c i d c a n d e c r e a s e m o u t h odors, ~7 t h o u g h these p r o d u c t s are n o t c o m m e r c i a l l y a v a i l a b l e . W h i l e n o t a c o m m o n c o m p l a i n t , halitosis c a n b e a n i m p o r t a n t sign of u n d e r l y i n g disease. A m e t i c u l o u s hist o r y a n d p h y s i c a l e x a m i n a t i o n are r e q u i r e d , b u t t h e l i k e l i h o o d o f f i n d i n g a m a n a g e a b l e c o n d i t i o n is r a t h e r high. Both p a t i e n t satisfaction a n d p h y s i c i a n satisfact i o n f r o m t h e i d e n t i f i c a t i o n o f t h e p r o b l e m are gratifying.
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REFLECTIONS Old Voices On hospital rounds one morning I f o u n d an o l d m a n d y i n g f r o m pneumonia Saying
Young man, gain knowledge. I t u r n e d , w r o t e a n o t e in his chart. Around the corner I f o u n d an o l d m a n s p i t t i n g b l o o d Saying
Young man, learn to love. I t u r n e d , w r o t e a n o t e in his chart. U p t h e stairs I f o u n d an o l d m a n c o n s u m e d w i t h TB Saying
Young man, tell m e the truth. I t u r n e d , w r o t e a n o t e in his chart. D o w n t h e hall I f o u n d an o l d m a n c h o k i n g w i t h cancer Saying
Young man, enjoy yourself. I t u r n e d , w r o t e a n o t e in his chart. W h e n I finished r o u n d s a c h o r u s Of old voices spoke to me from nowhere Saying
Young man, we are k n o w n by m a n y names. Quit scribbling, j u s t listen to us. ERIC L. DYER, MD
Nashville, TN
