treatment of oral and nonoral sources of halitosis in elderly patients

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DRUG THERAPY Drugs & Aging 6 (5) 397-408,1995 1170-229X/95/0005-0397/S06.00/0 © Adis International Limited. All rights reserved. Treatment of Oral and Nonoral Sources of Halitosis in Elderly Patients John D. McDowell and Denise K. Kassebaum Department of Diagnostic and Biological Sciences, Division of Oral Diagnosis/Medicine/Radiology, University of Colorado School of Dentistry, Denver, Colorado, USA Contents Summary , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , 1, Treatment Planning for the Reduction or Elimination of Oral Malodours 1 ,1 Patient History , , , , , , , , , , , , , , 1,2 Screening for Neurological Disorders, 1,3 Tobacco Products , , 1.4 Diet Assessment , , , , , , , , , , , , , 1 ,5 Physical Examination , , , , , , , , , , 1,5,1 Malodour in Nasally Expired Air 1 ,5.2 Malodour in Orally Expired Air , 1 ,5,3 Systemic Disease " 1 ,5,4 Candidosis , , , , , , 1,5,5 Ingested Substances 1 ,6 Oral Examination , , , , , , 1 ,6,1 Lips and Adjacent Skin 1 ,6.2 Oral Vestibules , , , , 1,6,3 Tongue , , , , , , , , , 1.6,4 Teeth and Prostheses , 1 ,6,5 Dental Pulpal Involvement , 1 ,6,6 Periodontal Tissues 1.6,7 Oropharynx " , , , , , , , 1 ,6,8 Xerostomia , , , , , , , , , , 2, Laboratory Tests or Additional Diagnostic Studies 2,1 Biopsy ,',""" 2,2 Culture and Sensitivity 2,3 Psychological Factors 3, Conclusion "',,'," 397 400 400 401 401 401 401 402 402 402 402 403 404 404 404 404 405 405 405 405 , 405 406 406 407 407 407 Summary The increasing number of older patients being seen in medical and dental offices in the industrialised world emphasises the need for a thorough under- standing of the normal aging process, Additionally, close attention must be paid to the disease processes that affect this special needs population. Although there are many positive psychosocial issues associated with the aging patient, many diseases and disabilities associated with the aging process place an increased

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Page 1: Treatment of Oral and Nonoral Sources of Halitosis in Elderly Patients

DRUG THERAPY Drugs & Aging 6 (5) 397-408,1995 1170-229X/95/0005-0397/S06.00/0

© Adis International Limited. All rights reserved.

Treatment of Oral and Nonoral Sources of Halitosis in Elderly Patients John D. McDowell and Denise K. Kassebaum Department of Diagnostic and Biological Sciences, Division of Oral Diagnosis/Medicine/Radiology, University of Colorado School of Dentistry, Denver, Colorado, USA

Contents Summary , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , 1, Treatment Planning for the Reduction or Elimination of Oral Malodours

1 ,1 Patient History , , , , , , , , , , , , , , 1,2 Screening for Neurological Disorders, 1,3 Tobacco Products , , 1.4 Diet Assessment , , , , , , , , , , , , , 1 ,5 Physical Examination , , , , , , , , , ,

1,5,1 Malodour in Nasally Expired Air 1 ,5.2 Malodour in Orally Expired Air , 1 ,5,3 Systemic Disease " 1 ,5,4 Candidosis , , , , , , 1,5,5 Ingested Substances

1 ,6 Oral Examination , , , , , , 1 ,6,1 Lips and Adjacent Skin 1 ,6.2 Oral Vestibules , , , , 1,6,3 Tongue , , , , , , , , , 1.6,4 Teeth and Prostheses , 1 ,6,5 Dental Pulpal Involvement , 1 ,6,6 Periodontal Tissues 1.6,7 Oropharynx " , , , , , , , 1 ,6,8 Xerostomia , , , , , , , , , ,

2, Laboratory Tests or Additional Diagnostic Studies 2,1 Biopsy ,',""" 2,2 Culture and Sensitivity 2,3 Psychological Factors

3, Conclusion "',,',"

397 400 400 401 401 401 401 402 402 402 402 403 404 404 404 404 405 405 405 405

, 405 406 406 407 407 407

Summary The increasing number of older patients being seen in medical and dental offices in the industrialised world emphasises the need for a thorough under­standing of the normal aging process, Additionally, close attention must be paid to the disease processes that affect this special needs population. Although there are many positive psychosocial issues associated with the aging patient, many diseases and disabilities associated with the aging process place an increased

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398 McDowell & Kassebaum

burden on the elderly patient. The relationship between general and oral health must be understood by the practitioner if therapies are to be effective.

Although it is not the objective of this article to provide a comprehensive review of oral healthcare, an attempt will be made to provide general information on the diagnosis and treatment planning for oral malodours often associated with poor oral and/or systemic health. Every healthcare provider treating the elderly patient for oral malodours must recognise that there is potentially a direct rela­tionship between the oral and systemic health of the patient. While most oral malodours have a simple cause, no single therapy is always effective. For best results, a team approach to diagnosing and treating oral malodours involves the dentist, physician, dietician and pharmacist. This multidisciplinary approach should be arranged before the onset of any complex therapy. When indicated, supportive, responsible family members should be additionally involved to assure patient compliance.

The mouth and teeth can be a source of great pride and pleasure. A beautiful smile is one of the most pleasant greetings a human can offer. Enjoying a meal of fine food and drink is truly gratifying. Unfortunately, the oral hard and soft tissues can also be a source of pain, social discomfort and disease. Additionally, the mouth can be a valuable diagnostic tool. In fact, the oral environment has long been recognised as a potential early indicator of systemic disease. Unfortunately, in the presence of systemic or oral disease, the mouth and surrounding structures can be a source of a significant social problem - disagreeable breath odours. In severe cases, oral malodours can lead to social isolation and ostracism.

Disagreeable personal odours are not a phenom­enon unique to the modern era. Unpleasant oral odours have long been a medical and social prob­lem. References have been made to oral malodours in classic medical literature. The early Greeks, Ro­mans and Chinese noticed a correlation between dirty mouths and bad breath. Anton van Leeuwen­hoek is credited with first identifying the oral or­ganisms that may cause oral disease and bad breath. However, comprehensive articles dealing with the terminology, documented causes and ef­fective treatments of oral malodours are relatively recent in the literature. Excellent overviews of the problem can be found beginning as early as 1939.[1,21

mouth and associated sinusesPI Although it has also been recommended that the term halitosis be reserved for odours which have a systemic origin, most commonly the term halitosis is used to de­scribe any disagreeable odour in the expired air. It has been suggested that another term, oral malodour, be used to describe the mouth's contribution to un­pleasant breath. [41 Some physicians suggest that the terms halitosis and bad breath can be used inter­changeably and that bad breath or other oral malodours be recognised as a symptom (sign) and not an actual disease.l51 More recently, the profes­sionalliterature has not placed emphasis on termi­nology but has stressed the importance of the diag­nosis and treatment of bad breath.

Halitosis, fetor ex ore, fetor oris and bad breath are terms that have been used to describe unpleas­ant or disagreeable oral odours emitted with the expired air. Historically, it has been recommended that the term fetor ex ore be used to describe mal odours arising from conditions within the

© Adis Intemationallimited. All rights reserved.

In most societies, bad breath is considered so­cially unacceptable. A person who is socially iso­lated - either by personal choice or the choice of others - may not be aware that there is a problem with oral malodours. Testimonials and other anec­dotes from family members support the premise

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Treatment of Halitosis in the Elderly

that even patients with extremely bad breath may not personally be aware of the problem.

Even in the young and healthy, the sensations of taste and olfaction are both subject to the sensory phenomenon known as adaptation. Reduced abil­ity to smell unpleasant odours can be related to the specialised olfactory bipolar neurons (peripheral receptors) being constantly occupied with the offensive substance making the person insensitive to the odour.

Although sensory complaints and irritations are common in the elderly population, the senses of smell and taste significantly decline with age. The loss of these 2 senses can have a significant impact on the elderly person's quality of life.

The diminution of the sense of smell can con­tribute to a patient's inability to detect offensive personal odours. While in some cases the patient might be aware of personal oral malodours, the problem of bad breath is usually related to the pa­tient by those around them.

Patients may also present for treatment of bad breath because of their own sense of malodour re­sulting from an altered or disagreeable taste pres­ent in the mouth. Alterations in the chemical senses are affected by multiple factors including normal changes associated with aging, xerostomia, arti­ficial dentition, poor oral hygiene, craniofacial abnormalities, psychiatric disorders and neo­plasms)6l

For whatever reason the patient presents, it is essential to identify the pathophysiology leading to the malodour prior to developing and initiating an effective treatment plan.

Unpleasant oral odours are mainly the result of sulphur-containing proteins and peptides being hydrolysed by Gram-negative bacteria in an alka­line environment.14,7,8l During putrefaction of amino acids, unpleasant-smelling, volatile sul­phur-containing end products, predominantly hy­drogen sulphide and methylmercaptan, are created. Other breakdown products such as ammonia, in­dole, skatole, putrescine and cadaverine - com­pounds normally causing odours during putrefac­tion in biological systems - have been found not to

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399

be major contributors to oral malodours)4,9, lOl Pro­duction and release of the volatile compounds, and subsequent detection of these oral malodorous sub­stances, appears to depend on multiple local factors which include salivary pH, reduced ambient oxy­gen concentration, bacterial population and the substrate available for bacterial metabolism)4,7,Jll

Production of putrid odours is associated with oral conditions contributing to a shift from Gram­positive to Gram-negative bacteria)4,7,lll Factors contributing to this bacterial shift are reduced sali­vary flow, stagnation of saliva, reduced carbohy­drates available as bacterial substrates and a rise in the oral pH)4l

Reduced salivary flow leading to a dry mouth (xerostomia) is a frequent complaint among the el­derly population. Unfortunately, xerostomia is also a common cause of oral malodour. Reduced sali­vary flow can be caused by many factors: dehydra­tion, anaemia, avitaminosis, diabetes, emotional stress, metabolic disease, inflammatory or autoim­mune disease of the salivary glands, mechanical blockage, malignancy, multiple sclerosis, AIDS, head and neck irradiation, and medications)12,13l Although aging was previously thought to be a sig­nificant contributor to reduced salivary flow, no clinical studies absolutely support this premise.

It is especially important to take a complete drug history, as many medications commonly taken by the aged population are known to induce xerostomia. Drugs which decrease salivary flow include antidepressants, tranquillisers, antihista­mines, decongestants, antihypertensive and car­diovascular agents. I12,13l

Not all reductions in salivary flow are caused by pathological or drug-induced conditions. As sali­vary flow is normally decreased during the sleep­ing hours, xerostomia and increased oral alkalinity occurring during sleep also contribute to oral malodours. Patients and their companions can be especially aware of bad breath in the morning be­cause of reduced salivary flow and the absence of chewing activity occurring during sleep.

Mouth breathing caused by exercise, nasal ob­struction, abnormal skeletal and/or dental anat-

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omy, or habit can also cause oral drying, contribut­ing to oral malodours.

Oral malodour production may be directly re­lated to the patient's periodontal condition. Sali­vary putrefaction and the production of disagree­able oral odours occurs more rapidly in patients with periodontal disease.[2,4,7] Generally, the con­ditions that provide a favourable environment for a shift from Gram-positive to Gram-negative bac­teria also contribute to the production of bad breath.

In the presence of periodontal disease, increased growth factors and substrates are available from the inflammatory process which stimulate the growth of bacterial populations on the oral soft and hard tissues.l4,7,ll,14] Meticulous oral hygiene com­bined with a professional hygiene programme is essential to the maintenance of periodontal health. Elimination of periodontal disease and maintaining periodontal health are essential to reducing oral malodours.

1. Treatment Planning for the Reduction or Elimination of Oral Malodours

The development of an accurate differential di­agnosis and effective treatment plan requires the collection of a comprehensive patient history (in some cases requiring an interview of family mem­bers), a thorough physical examination, and the ac­curate interpretation of any indicated tests.

1.1 Patient History

It is essential that the interviewer listen closely to the information provided so an effective treat­ment plan be developed. An accurate diagnosis de­pends on the analysis of pertinent data collected from the patient's history. Whenever possible, the patient interview must be performed in a support­ive' quiet, private environment and should be free from interruptions.

The patient's chief complaint (usually a single cause for the patient to present for care) must be investigated and related to the history of present illness. The patient should be encouraged to speak openly about the chief complaint and why it is of

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McDowell & Kassebaum

concern. Emphasis must be placed on when the pa­tient (or others) first detected the oral malodours and on any potential initiating factors. The clini­cian should try to determine whether the malodours are constantly present or intermittent in their pre­sentation. Precipitating, aggravating or relieving factors should be recorded and thoroughly investi­gated.

A thorough historical evaluation requires that significant aspects of the patient's family and so­cial history be reviewed. The patient's dental, med­icaVsurgical and drug histories must be compre­hensively reviewed and thoroughly examined. Special emphasis must be placed on the patient's drug history, as drug pharmacodynamics play an important role in developing oral malodours. The patient history must include a complete review of the patient's past illnesses, hospitalisations and sur­geries (table I).

Although there are no conclusive data indicat­ing gender differences in chemosensory acuity,

Table I. Developing a treatment plan for halitosis

Developing a diagnosis Patient history:

review the patient's chief complaint and history of present iIIness(es)

review the patient's past history of malodour review the patient's current history (investigate diet and

medications)

Physical examination: extra-oral examination

intra·oral examination Analysis of tests or special studies:

radiographs microbiologic cultures and sensitivity studies findings and diagnoses of consultants

A final or working diagnosis is often derived from detected abnormalities of structure, function or mentation.

Developing a treatment plan The therapy selected must be appropriate to the diagnosis. For

instance, odour-masking agents should not be used as the sole therapeutic agent to cover the signs and symptoms associated with an inflammatory, infectious or neoplastic disease of the oral structures

Evaluate the patient's response to trial therapy. If there is no response to therapy in a compliant patient, re-evaluate the working diagnosis

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Treatment of Halitosis in the Elderly

some studies indicate lower sensory thresholds for women.l6] The temporal relationship of odour changes should be investigated in women as olfac­tory and taste sensations have been reported to change over the menstrual cycle.l 16] If aware of the malodour problem, the patient is often able to pro­vide an accurate history as to the progression of symptoms/signs. Questions dealing with whether the mal odours are getting worse, staying the same or diminishing can be helpful in determining po­tential disease course.

1 .2 Screening for Neurological Disorder

A neurological assessment with special empha­sis on cranial nerve evaluation is an essential part of the physical examination. If sensory dysfunc­tion is suspected while developing the history, the patient's ability to perceive the malodours should be investigated. A simple check of olfactory nerve (CNl) function can be quickly performed in the office using common aromatic substances like soaps, tobacco and aromatic oils (orange, winter­green, cloves, etc.). Ammonia should not be used to test olfaction as it stimulates the pain receptors of the trigeminal nerve (CN5) rather than the olfac­tory nerve (CNl))17]

The patient should also be questioned regarding associated symptoms, including taste disorders. Central lesions and potential dysfunctions of the facial (CN7), glossopharyngeal (CN9) and vagus (CNlO) nerves should be investigated if taste dis­orders are suspected. Disease or dysfunction can exist at any point of reception, transmission or in­terpretation as gustatory information is received by the receptor cells, and then projects to the medulla, pons, thalamus and cortical taste area.[6]

1.3 Tobacco Products

In the presence of a positive history of tobacco use, the patient should be questioned regarding the type, technique and frequency of use. In particular, patients should be asked if a change in tobacco usage has been associated with the oral malo dour detection by the patient or others. Although studies are equivocal, a history of smoking has been im-

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401

plicated in bitter tastes and a deterioration in olfac­tory sensitivity.[6]

At some point during the interview, the patient must be informed about the dangers associated with the use of cigarettes, cigars, pipes and smoke­less tobacco. Tobacco cessation counselling should become a routine part of the patient interview.

1 .4 Diet Assessment

The examiner should carefully consider the pa­tient's dietary habits as related to the chief com­plaint. Bogdasarian[20] has reported that the hunger state contributes to the creation of objectionable breath odours resulting from pulmonary excretion of metabolic breakdown products of fats and pro­teins. While certain foods have been implicated in imparting an offensive odour to the breath, the act of eating has been reported to actually reduce oral malodours)20] Increased salivary flow and oral cleansing from mastication reduce - at least tem­porarily - oral malodours.

To assist with good nutrition and to help reduce oral malodours, the examiner should consider sug­gesting that the elderly patient eat nutritionally bal­anced, noncariogenic snacks during the waking hours PO] A careful patient record of diet and malodour production should be kept if the exam­iner or patient believes that the oral mal odours are related to the patient's food or fluid intake. Con­sultation with a physician or dietitian may be nec­essary to assist in developing alternative diet plans should certain foods be identified as contributing to oral mal odours.

1 .5 Physical Examination

A systematic, thorough examination of the head and neck area must be performed as bad breath can originate from several regions in the upper aer­odigestive tract. In some cases it is possible to dis­tinguish between oral and nasal sources of malodours by separating the expired air (see table 11))5]

Instruct the patient to pinch the nose closed and exhale through the mouth, then to close the mouth and exhale through the nose. The patient's expired

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Table II. Subjective assessment 01 expired air

Possible nasal source 01 malodour detected by:

instructing the patient to close the mouth and exhale through the nose

Possible oral source 01 malodour detected by:

instructing the patient to pinch the nose closed and exhale through the mouth

The relative intensity 01 the malodour should give a reasonably reliable indicator 01 odour source. II redirecting the expired air does not significantly alter the malodour, a systemic or respiratory tract source should be investigated

air can be wafted across the nose of the examiner with the palm of the hand or a card. If the malodour changes when altering the course of expired air, further investigation of the suspected site should be undertaken.

1.5. 1 Malodour in Nasally Expired Air

A stronger smell from the nasally expired air can indicate lesions or disease of the nasopharynx, nose or sinuses. The nasopharynx is a common site of bacterial overgrowth contributing to bad breath. Conditions altering the mucous blanket of the nose, including atrophic rhinitis or rhinitis medica­mentosa, can contribute to bacterial overgrowth and malodour.l51 Chronic sinusitis, unilateral cho­anal atresia and nasal foreign bodies have been re­ported to cause halitosis.l5,181 Tumours of the nasal cavity can have malodour as an early symptom.l51 Referral to a otolaryngologist is indicated if an in­fection, foreign body or neoplasm is suspected.

1.5.2 Malodour in Orally Expired Air

A more noxious odour found in the orally ex­pired air can indicate an oral, oropharyngeal, hypopharyngeal or, rarely, a gastric source. Pha­ryngeal ulcers, tonsillitis, nasopharyngeal dis­charge or post-tonsillectomy necrotic eschar can harbour anaerobic bacteria contributing to bad breathJ51 Nearly every physician or dentist is aware of the noxious odours associated with tonsillitis, pharyngitis, mononucleosis, and other viral or bac­terial infections of the oropharynx. Retaining in­gested or regurgitated food in the hypopharyngeal diverticulum can lead to stagnation and putrefac­tion, producing malodorous volatile substances in

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McDowell & Kassebaum

the expired air. [51 Lucente and coworkers[51 have also reported that patients with hiatus hernia can have gastroesophageal reflux giving rise to a sense of bad taste in the mouth. A patient with an oesoph­ageal stricture or cardiospasm can on rare occasion request medical and/or dental evaluation with bad breath as a presenting symptom. [201

In the healthy elderly individual, gases from the upper gastrointestinal tract do not normally mix with the expired air. Vomiting or eructation (belch­ing) can result in bad breath. Patients with a posi­tive history of bad breath in the presence of dys­pepsia, or constipation or other bowel disturbance should be referred to an internist/gastroenterolo­gist for further evaluation.l201

1.5.3 SystemiC Disease If the expired air is equally offensive, whether

expired through the nose or mouth, a systemic source should be investigated. Bad breath has been reported to rise from systemic disease such as he­patic failure (lending a sulphur odour), uraemia (ammonia odour) and diabetic ketoacidosis (ace­tone odour). Other oral and systemic malodours have been suggested to have diagnostic value to practitioners.l61 Schiffman has stated that specific emitted odours detected on physical examination can be associated with infectious, nutritional and mental diseases.l6]

Expired air with an unpleasant odour can be an indicator of disease of the upper respiratory tree. Neoplasms anywhere along the respiratory tract can cause bad breath. Bronchitis, pneumonia and bronchiectasis (a congenital or acquired disorder marked by chronic dilatation and destruction of the large bronchi) have been reported to cause foul odours in the expired airJ5,191 Signs and symptoms associated with bronchiectasis include a paroxys­mal cough productive of a malodorous mucopuru­lent exudate.

1.5.4 Candidosis Patients with bronchiectasis and other respira­

tory diseases are frequently treated with combina­tion therapy, including corticosteroids and anti­biotics. Such therapy can contribute to the development of oropharyngeal candidosis. Long

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Treatment of Halitosis in the Elderly

tenn use of inhaled corticosteroids in asthma pa­tients can lead to a change in the respiratory tract flora,[5) contributing to the development of oropha­ryngeal candidosis.

Oropharyngeal candido sis caused by local and/or systemic factors can frequently be associ­ated with foul breath in the elderly patient. Al­though the growth of the candidal organisms does not directly cause the malodour, the associated oral conditions can contribute to the production of nox­ious aromas.

Healthcare providers must be aware that whereas candidosis can be seen in patients receiv­ing chronic steroid therapy or broad spectrum an­tibiotics, candido sis can also be found in patients with cancer, diabetes or xerostomia. Immuno­compromised or immunosuppressed patients or any patient with a debilitating systemic disease can also develop candidal infections. Poor oral hygiene and prosthetic appliances are local factors poten­tially contributing to the development oral can­didosis.

Identifying and treating the cause of oropharyn­geal candidosis utilising the appropriate antifungal agent should relieve the problem. A topical antifun­gal agent which is commonly used is nystatin pas­tilles 200 000 units. The patient should be in­structed to slowly dissolve 1 or 2 pastilles in the mouth 4 to 5 times per day for 14 days. Clo­trimazole 10mg troches can also be used as 1 troche slowly dissolved in the patient's mouth 5 times a day for 14 days. When prescribing clotrimazole in the presence of pre-existing liver disease, consider periodic evaluation of liver function, as elevated liver enzymes have been reported in a small num­ber of patients on clotrimazole therapy.

Close medical supervision is frequently re­quired for patients who have developed oropharyn­geal, oesophageal or pulmonary fungal infections. When oropharyngeal candidosis does not respond to topical therapies, the condition can be treated with a systemic antifungal agent. Systemic anti­fungal therapy is especially valuable in the im­munocompromised, extremely ill or severely de­bilitated elderly patient. [29) Two commonly

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prescribed systemic antifungal agents are ketocon­azole and fluconazole. In most cases, treatment of oropharyngeal or oesophageal candidosis with fluconazole consists of two 100mg tablets on the first day followed by one 100mg tablet per day for a total of 14 days' therapy. Ketoconazole 200mg tablets should be taken once daily for 2 weeks. Itra­conazole is a newer, less commonly prescribed sys­temic antifungal drug with varying activity against a wide range of fungal organisms. Itraconazole is available as 100mg capsules with the usual dosage of 200mg once daily for a minimum of 3 months.

Clinicians must be aware that many systemic antifungals have been associated with hepatotoxi­city, and that appropriate monitoring is indicated when prescribing these drugs. Ketoconazole and itraconazole are contraindicated in patients receiv­ing concomitant therapy with terfenadine and astemizole because of the risk of adverse cardio­vascular events.

When any new or additional medication is pre­scribed for a patient on combination therapy, the patient's drug history must be thoroughly re­viewed. Many elderly patients are being seen by several different healthcare providers. Combined therapies require that all healthcare providers be familiar with their patient's current medications and potential drug interactions prior to prescribing any new medications.

1.5.5 Ingested Substances Food, drink and medications can be absorbed

from the mouth, stomach or intestines, then ab­sorbed into the bloodstream and later transferred to the pulmonary alveoli. Pulmonary excretion of malodorous substances dissolved in the blood­stream can contribute to noxious aromas in the ex­pired air. Certain foods including garlic, onions and other spices are absorbed from the intestine, metabolised in the liver, released into the blood­stream and excreted via the lungs and other routes.[20] Drug-specific halitosis has been associ­ated with iodine-based medications, amyl nitrate and chloral hydrate.l20]

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1 .6 Oral Examination

While the nonoral physical examination is im­portant to some diagnoses of oral mal odours, the vast majority of cases of bad breath have their ori­gin in the oral cavity. During oral examination, careful attention must be paid to each area of the hard and soft tissues. As with the nonoral examina­tion, an organised, systematic approach to the oral examination is essential to developing a definitive diagnosis. Without a clear diagnosis, an effective treatment plan cannot be developed. While this ar­ticle cannot provide a comprehensive description of the diagnostic process, the more common oral conditions and diseases that can contribute to malodours are described.

The oral examination must be made recognising that some patients are skilled at masking the oral malodours with candies, chewing gums, sprays or drops to freshen the breath, or various mouth rinses. In order to decrease the possibility of totally masking the malodour, patients should be coun­selled to discontinue the breath fresheners shortly prior to the physical examination.

1.6.1 Ups and Adjacent Skin The patient's lips should be examined and any

deviations from normal should be recorded in the patient chart. Because of the close anatomic rela­tionship between the lips and nose, inflammatory or degenerative processes of the lip tissues can cause the patient to become aware of malodours.

Lip ulcerations can be caused by trauma, local infections or neoplasms. Of particular importance are any ulcerations or necrotic areas that harbour Gram-negative bacteria and other opportunistic in­fective agents such as those often seen in HIV­positive patients. Rarely, a foul-smelling odour may be detected from neoplasms or large ulcers of the skin or lip. Patients with large herpes labialis lesions or major aphthous ulcers can complain of noxious odours associated with the ulceration. Any lip or skin ulceration or erosion suspected of being a neoplasm should be biopsied and appropriately treated.

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McDowell & Kassebaum

If the lip ulcers are found to be aphthous ulcers, topical steroids are useful in treatment. Triamcino­lone, fluocinonide and clobetasol are commonly used therapeutic agents. A steroid/oral paste com­bination can be sparingly applied to the ulcer 4 to 5 times per day and at bedtime. Antibiotics, when indicated, can also be used to treat major aphthous ulcers. In HIV-positive patients, large, atypical, nonhealing ulcers should be biopsied to rule out opportunistic infections or neoplasms.

1.6.2 Oral Vestibules The vestibules should be examined for evidence

of infection or neoplasms. When indicated, pa­tients with ulceration affecting bone or fistulae that emanate from bone should be examined radio­graphically. Other advanced imaging techniques [computerised tomography (CT) or magnetic reso­nance imaging (MRI)] may be necessary if the le­sions are suspected of being malignant.

Oral-antral fistulae can be created after extrac­tion of maxillary teeth that are in close approxima­tion to the maxillary sinuses. Although rare, pe­ripheral manifestations of sinus cancer can present as destructive oral lesions. Fistulae from the max­illary sinus or an abscessed tooth can be the cause of oral malodours.

1.6.3 Tongue The tongue, especially the dorsal surface, is a

common source of bad breath. The filiform papil­lae, appearing as pinkish-white, hairlike projec­tions, cover most of the tongue's dorsal surface. The surface anatomy of the tongue provides an ideal environment for collection of desquamated cells, food debris and anaerobic bacterial growth capable of malodour productionp,1l,17) A normal anatomic structure, the midline depression, can be of varying depths predisposing to the collection of food debris. A fissured tongue (sometimes called scrotal tongue) can also contribute to food collec­tion and putrefaction.

Tonzetich and Ng[8) reported that combining tooth and tongue brushing was the most effective technique for reducing oral malodour emanating from the tongue. Bosy and colleagues[21) have re­ported that there is a discrete subpopulation of

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patients complaining of oral malodours who do not have periodontal disease. In the population studied by Bosy, the mucosal surface of the tongue was the major source of oral malodour production. Various mixtures of toothpaste, mouth rinses (chlorhexid­ine 0.12%) and pumice, applied to the toothbrush to gently but thoroughly clean the tongue, have been suggested to have value in reducing the tongue's bacterial load. The patient should be counselled not to overbrush the tongue as traumatic ulcers might develop in the overzealous patient.

1.6.4 Teeth and Prostheses During every oral examination, the teeth should

be examined for evidence of decay and food im­paction. Sulser and colleagues[2] reported that car­ious lesions provided sites for food retention and putrefaction. A dental referral is indicated when carious lesions are suspected or detected during the oral examination. The lesions should be removed and the tooth restored to functional, cleansable anatomy. When possible, all conditions leading to food impaction should be corrected. Poorly con­toured restorations should be replaced or recon­toured. Crowns, appliances, and fixed and remov­able prostheses should be examined and replaced or repaired if defective.

Proper cleaning of removable prostheses (full dentures or partial dentures) is essential to main­taining nonoffensive breath. Patients should be counselled to thoroughly clean dental prostheses at least once per day. Whenever possible, patients should refrain from wearing removable prostheses during sleep. Patients who wear their dentures for prolonged periods without removal are at risk of tissue hyperplasia and candidal infections. Anti­fungal therapy (clotrimazole 1% ointment or gel, or nystatin powder) applied to the denture base can be effective in reducing candida colonisation. When used conscientiously, commercially avail­able denture cleansers offer an effective method of reducing the bacterial and fungal population on dental prostheses.

1.6.5 Dental Pulpal Involvement Advanced, untreated dental caries or trauma can

lead to exposure of the dental pulp. Diseases of the

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dental pulp can provide an environment favourable to noxious gas production. Any teeth with exposed pulpal tissues, irreversible pulpitis, necrotic pulps, apical periodontitis or periapical abscesses should be treated endodontically. Alternatively, tooth ex­traction is indicated. Draining abscesses of odonto­genic origin should be immediately treated. When indicated, endodontic treatment with antibiotic therapy should allow for the retention of the natural dentition. Teeth should only be extracted when ef­fective alternative care is not in the patient's best interest.

1.6.6 Periodontal Tissues Periodontal disease is another common cause of

oral malodours. A complete periodontal examina­tion is essential for every dental patient. In the pre­sence of periodontal disease, there are elevated concentrations of volatile sulphur compounds in the mouth airp·11.14.20] Effective periodontal treat­ment, including patient-performed oral hygiene procedures, should reduce the level of noxious oral gases detectable in the expired air.l24-26.28] Plaque removal is essential to reducing the dental bacterial load. Retained food, salivary proteins, large molec­ular weight products, blood elements, inflamma­tory exudates and epithelial cells all provide nutri­ents rich in sulphur-containing substrate.

1.6.7 Oropharynx Along with the other oral structures, the oro­

pharynx should be examined for potential causes of bad breath. Food and other particles trapped in the enlarged foliate papillae and/or the lingual ton­sils at the base of the tongue can contribute to bad breath. Cryptic tonsils can also retain food par­ticles, thus contributing to bad breath.l5] Bacterial, fungal or viral infections of the oropharynx can contribute to oral malodours. Any infections, ul­cerations, swellings or suspected neoplasms of the oropharynx require immediate referral to the ap­propriate dental/medical specialist trained in the diagnosis and treatment of these disorders.

1.6.8 Xerostomia Approximately one-third of patients over the

age of 50 complain of a dry mouth. Because of this

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high symptom rate, patients should be routinely questioned about xerostomia (dry mouth) as part of the patient history. The oral tissues should be ex­amined for signs of xerostomia. Signs and symp­toms of xerostomia include diminution of taste, in­ability to swallow food, and loss of the salivary electrolytes and immunoproteins that protect against microbial infections. [6) Ahigh rate of dental decay, especially the decay that encircles the tooth at the cervical margin, is highly suggestive of re­duced salivary flow. Additional oral changes can include painful, parched, inflamed and erythema­tous oral mucosa. The filiform papillae may be re­duced or lost from the dorsal surface of the tongue causing the tongue to appear shiny and erythema­tous. Decreased salivary flow can contribute to a reduced cleansing action and a change in the oral flora toward the Gram-negative organisms respon­sible for oral malodours. Many pathological oral conditions can be caused at least in part by a re­duced salivary flow.

Whenever possible, the causes for xerostomia should be identified and treated. In cases where the xerostomia is drug-related, a medical or pharmaco­logical consultation can identify alternative medi­cations that cause less reduction in salivary flow. Increased fluid intake, salivary stimulation with sugarless candies, artificial salivary substitutes (usually compounds based on carboxymethyl cel­lulose), reduction of caffeine intake, and the use of sialogogues can reduce the effects of a dry mouth. A cholinergic agonist, pilocarpine, has been shown to increase salivary flow at dosages of 5 to 10 mg/day. Higher dosages can be considered for pa­tients not responding adequately and who can tol­erate the lower dosages. As with all medications, the prescriber should have a thorough knowledge of the drug's actions, potential adverse effects and drug-drug interactions before prescribing this med­ication.

Advanced age is risk factor for cancer. Oral can­cers can be associated with mal odours either from debris collecting on an ulcer or from tissue necro­sis. Oral and perioral cancers represent less than 10% of all human cancers, yet the morbidity and

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McDowell & Kassebaum

mortality associated with these cancers is high. Head and neck (including oral) cancers often re­quire surgery, chemotherapy and radiation therapy. Any of these therapies, individually or collectively, can cause or exacerbate previously existing xerostomia.

Red, crusted or fissured oral commissures (cor­ners of the mouth) can indicate skin and mucosal candidal infection. Topical nystatin-triamcinolone acetonide ointment used in conjunction with intra­oral antifungal therapy can quickly eliminate can­didal infections of the commissures. Because an­gular cheilitis is not frequently seen in the absence of oral candidosis, effective therapy should include treatment of the oral fungal infection.

2. Laboratory Tests and Additional Diagnostic Studies

As described above, the taking of the patient's history and physical examination are critical com­ponents of the data-gathering process, yet the final diagnosis often depends on the results of specific tests. Additional information leading to a final di­agnosis can be acquired through ordering and an­alysing appropriate laboratory tests or diagnostic studies. Radiographs and other imaging modalities can be essential for the diagnosis of diseases of the teeth, jaws or adjacent structures.

2.1 Biopsy

Although some diagnoses can be made on the clinical and/or radiographic appearance of a lesion, there is no substitute for a properly performed bi­opsy and microscopic examination of the submit­ted tissue. With the biopsy specimen, the patholo­gist should be provided with an adequate history including symptoms and signs associated with the lesion and any photographs or radiographs made of the area in question. Biopsy is indicated if ves­iculo-bullous or ulcerative disease is included in the differential diagnosis of the source of malod­our. Except in rare instances where the patient's medical status dictates otherwise, biopsy is essen­tial when neoplasia is suspected.

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Treatment of Halitosis in the Elderly

2.2 Culture and Sensitivity

If an infection of the oral cavity is suspected as the cause of oral malodours, cultures and sensitiv­ity studies should be considered. Maximum infor­mation regarding the infective organism(s) and ap­propriate antibiotic therapy can be gained from the microbiology laboratory. The healthcare provider should be prepared to collect specimens repre­sentative of the micro-organisms at the site of sus­pected infection. Sensitivity testing can be essen­tial to effectively treating severe infections. Culture and sensitivity studies should also be per­formed for those infections that have not re­sponded to initial antimicrobial therapy in compli­ant patients when such studies were not performed prior to initiating treatment.

2.3 Psychological Factors

If at the completion of the physical examination and diagnostic process there are no clinical find­ings supporting the history of oral malodours, con­sider the potential for a psychological component to the patient's chief complaint. Referral is indi­cated when a nonphysical cause for perceived oral malodour is suspected. Although uncommon, self­perception of bad breath might be a delusion asso­ciated with a monosymptomatic hypochondriacal psychosis.

Bishop[23] has reported that patients can present with monosymptomatic (single fixation) hypo­chondriasis manifesting as a delusion of offensive personal odours. Malasi and colleagues[22] have re­ported convictions of malodours that have been as­sociated with overvalued ideas, depression, schizophrenia and organic brain syndrome. It has also been reported that the olfactory hallucination may be a rationalisation for difficulties in interper­sonal relationships or a manifestation of low self­esteem,l22] Bogdasarian counsels otolaryngolo­gists to recognise neuroses as a condition causing patients to compulsively use mints, mouthwashes and oral spray deodorants PO] Without supportive physical findings, request a psychiatric consult­ation when personal malodours are reported.[22]

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3. Conclusion

Although foul odours in the expired air can come from several sources, the oral cavity is the most common source of volatile compounds caus­ing bad breath. Eliminating oral disease and metic­ulous oral hygiene are critical to maintaining non­offensive breath. The practitioner should be prepared to provide specific information to the pa­tient regarding oral hygiene and the use of mouth rinses and other agents that reduce the oral bacte­rial load. Recognising that the expired air may be a source of great social anxiety, the healthcare pro­vider should be able to perform the examination of the patient complaining of halitosis without adding to patient embarrassment. Every health profes­sional should be keenly perceptive to the psycho­social issues associated with personal malodours and avoid complicating an already sensitive pro­cessPO]

Once the source(s) of oral malo dour is identi­fied, a diagnosis can be made. Subsequently, an appropriate treatment plan can be developed and, with the patient's informed consent, that treatment plan should be implemented. Subjective com­plaints can be reduced and the patient's quality of life increased through appropriate therapy.

References 1. Brening RH, Sulser GF, Fosdick LS. The determination of hal­

itosis by the use of the osmoscope and the cryoscopic method. J Dent Res 1939; 18: 127-32

2. Sulser GF, Brening RH, Fosdick LS. Some conditions that ef­fect the odour concentration of breath. J Dent Res 1939; 18: 355-9

3. Crohn BB, Drosd R. Halitosis. JAMA 1941; 117: 2242-5 4. Kleinberg I, Westbay G. Oral ma1odour. Crit Rev Oral BioI Med

1990; 1 (4): 247-59 5. Lucente FE, Werber n, Guffin TN. Bad breath. In: Lucente,

Sobol. Essentials of Otolaryngology. 3rd ed. New York: Ra­ven, 1993: 275-7

6. Langlais RP, Miller CS. Color atlas of common oral diseases. Philadelphia: Lea and Febiger, 1992: 46

7. Schiffman SS. Taste and smell in disease (two parts). N Engl J Med 1983; 308 (22): 1275-9, 1337-43

8. Colman BH. Diseases of the nose, throat and ear, and head and neck. 14h ed. New York: Churchill Livingstone, 1992: 85

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10. McNamara TF, Alexander JF, Lee M. The role of micro-organ­isms in the production of oral malodour. Oral Med Oral Pathol 1972; 34: 41-8

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II. Solis-Gaffar MC, Fischer TJ, Gaffar A. Instrumental evaluation of odour produced by specific microorganisms. J Soc Cosmet Chern 1979; 12: 241

12. Tonzetich J, Ng SK. Reduction of malodour by oral cleansing procedures. Oral Med Oral Pathol 1976; 42: 172-81

13. Crohn BB. Halitosis in relation to oral diagnosis. Am J Orthod Oral Surg 1942; 28: 109-10

14. Tonzetich 1, McBride Be. Characterization of volatile sulphur production by pathogenic and non-pathogenic strains of oral bacteroides. Arch Oral BioI 1981; 26: 963-9

15. Causes of dry mouth: symposium. Practitioner 1990; 234: 610-5 16. Loesche WI. Importance of nutrition in gingival crevice micro­

bial ecology. Periodontology 1968; 6: 245-9 17. Goldberg S. The four-minute neurologic exam. Miami:

MedMaster 1992: 27 18. Baker RB. Does this patient have sinusitis? [letter; comment].

lAMA 1994 Feb 16; 271 (7): 502-3 19. Doty RL. A review of olfactory dysfunctions in man. Am 1

Otolaryngol1979; I: 57-9 20. Bogdasarian RS. Halitosis. Otolaryngol Clin North Am 1986;

19 (1): 111-7 21. Bosy A, Kulkarni GV, Rosenberg M, et al. Relationship of oral

malodor to periodontitis: evidence of independence in dis­crete subpopulations. 1 Periodontol 1994 Ian: 65 (I): 37-46

22. Barker AF, Bardana lr El. Bronchiectasis: update of an orphan disease. Am Rev Respir Dis 1988; 137: 969-78

23. Halitosis: symposium. Practitioner 1990; 234: 616-9

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24. Malasi TH, EI-Hilu SR, Mirza lA, et al. Olfactory delusional syndrome with various aetiologies. Br 1 Psychol 1990; 146: 256-60

25. Bishop ER. Monosymptomatic hypochondriasis. Psychosomat­ics 1980; 21: 731-47

26. MassIer M, Emslie R, Bolden TE. Fetor ex ore. Oral Surg Oral Med Oral Patho11951; 4: 110-23

27. Morris PP, Read RR. Halitosis: variations in mouth and total breath odour intensity resulting from prophylaxis and antisep­sis. 1 Dent Res 1949; 28: 324-33

28. Pianotti R, Pitts G. Effects of an antiseptic mouthwash on odorigenic microbes in the human gingival crevice. J Dent Res 1978; 57 (2): 175-9

29. Greenspan 0, Greenspan JS. Management of the oral lesions of HIV infection. J Am Dent Assoc 1991; 122: 26-32

30. McDowell 10, Kassebaum OK. Diagnosing and treating halito­sis. 1 Am Dent Assoc 1993; 124: 55-64

Correspondence and reprints: Professor John D. McDowell, Department of Diagnostic and Biological Sciences, Division of Oral Diagnosis/Medicine/Radiology, University of Col­orado School of Dentistry, 4200 East Ninth Avenue, Denver, CO 80262, USA.

Drugs & Aging 6 (5) 1995