Gary Robinson

 By Mel Rosenberg, PhD, Gary Robinson, MBChB, and Erica Amir, DMD 

 Bad breath is no laughing matter for the child or adolescent   who has it. Most cases can be alleviated by relatively simple measures, but   not before the cause is pinpointed by a targeted history and physical exam. 

A 3-year-old brought in for an office visit has a terrible odor emanating   from all over his body. Where do you begin your examination?

A 17-year-old complains of very bad breath, but neither you nor her   parents can smell anything. What's wrong?

A 14-year-old tells you that he coughs up whitish "stones" that smell   awful. What are they? 

 Although bad breath is rarely the primary presenting complaint in pediatric   practice, it's not unusual for it to be mentioned during the consultation. Bad   breath is a symptom of any number of conditions, from poor dental hygiene to   sinusitis, and it can have serious social consequences for the affected child.   Kids pull no punches, and a child with bad breath is often ridiculed by peers. 

 Sometimes referred to as halitosis, fetor oris, fetor ex ore, or oral malodor,   bad breath is any detectable, offensive smell carried on the breath. One of   the most frustrating aspects of this condition is not being able to tell whether   or not one actually has it.

 Children and adults who do have halitosis   are usually unaware of the problem unless alerted by others. At the other extreme,   some teenagers (and adults) develop halitophobiaan exaggerated fear that   they have bad breath when, in fact, they have only mild malodor or none at all.   This fear may be accompanied by social withdrawal, depression, and even thoughts   of suicide.

Because halitophobics do not always voice their worries   in this regard, this phobia can be particularly insidious. 

 There are many types of bad breath, including the rare fishy odor that accompanies   trimethylaminuria.

The large majority of cases encountered by   the pediatrician, however, involve odor that comes from the teeth, gums, tongue,   nose, or tonsils.

 Children of almost any age can have halitosiswe have detected bad breath   in patients as young as 2 years. The prevalence of bad breath increases with   age and may be as high as 65% among adults.

 The prevalence of severe   halitophobia in the general population is reported to be 0.5% to 1% (Stein M:   Personal communication, May 1999). 

 This article aims to throw light on the subject of bad breath. The information   presented is based on available studies (most of them performed on adults) and   our clinical and research experience. 

 Almost 70 years ago, Grapp showed that bad breath in adults often comes from   the far back region of the dorsum of the tongue.

 We postulated several   years ago that this is largely due to the accumulation of postnasal drip on   the back of the tongue.

That is probably also true in most cases   of bad breath in otherwise healthy children. Unless there is frank nasal infection,   postnasal drip does not smell immediately upon reaching the tongue; it becomes   putrid upon degradation of the mucus by copious bacteria on the far back reaches   of the dorsum.

 As a child gets older, more dental plaque accumulates on the teeth, and the   likelihood of bad breath coming primarily from subgingival and interdental sites   increases.

 As with bad breath caused by postnasal drip, bad breath   from dental sites involves bacterial activity. 

 Bacteria in the mouth degrade proteins there, yielding amino acids that are   further degraded and produce odorous volatile gases. The breakdown of methionine   and cysteine yields, respectively, hydrogen sulfide and methylmercaptangases   both implicated in bad breath.

 Other products of amino acid breakdown,   such as indole and skatole (products of the breakdown of tryptophan) and cadaverine   (a product of the breakdown of lysine), may contribute to oral malodor.

   Because the various kinds of bad breath are quite different in character (nasal   odor differs from interdental odor, for example), dozens of types of molecules   are likely involved. 

 Gram-negative anaerobic proteolytic bacteria (such as 

, and spirochetes)   have been implicated as a cause of oral malodor.

 These microorganisms   are thought to cause periodontal disease in adults, and studies have shown a   correlation between bad breath and periodontal disease.

 A child   may harbor these microorganisms interdentally, on the dorsum of the tongue,   and in the throat. 

The most common causes of halitosis involve the mouth, nose, and throat.

 that contribute to malodor include not only   dental plaque but also impacted food, advanced dental decay (food can get trapped   and putrefy), and inflamed gingivae. The most common of these is dental plaque,   which can accumulate on both the readily visible buccal (Figure 1) and lingual   surfaces and between the teeth. 

The connection between dental health and breath underscores how important it is for children to receive regular, professional dental care and to faithfully follow a rigorous oral hygiene regimen at homeone that includes brushing the teeth at least twice daily. More detailed recommendations for dental-related bad breath are discussed in the section on treatment. 

 whether transient or chronic, is common in children, and, as noted, is probably the leading cause of bad breath. In a study of 52 children with chronic sinusitis,

 90% were considered to suffer from purulent nasal discharge and 63% from postnasal drip. Sixty-seven percent of the children were judged to have bad breath. Postnasal drip may also help account for the oral malodor that accompanies chronic rhinitis in young children. In the case of allergic rhinitis, "allergic salute" (nose rubbing) and "allergic shiners" (swollen, inflamed, ecchymotic eyelids) may be present.

 The odor of postnasal drip is detected most strongly from a child's mouth,   and can often be reproduced by taking a sample (with, say, a small spoon) from   the very posterior region of the dorsum (Figure 2). Wait a few seconds, and   then smell the contents of the spoon. 

 About one in three healthy children harbors the nasal microorganism 

 And, a recent study of bad breath in   healthy children found that odor from the back of the tongue (judged by sampling   material taken from the lingual dorsum with a plastic spoon) was indeed associated   with both oral and nasal odor.

 These data, taken together, suggest   that the mouth-nose bad breath association may be even more pronounced in children   than in adults, possibly because of the close anatomic connection between the   nose and oral cavity (Figure 3). 

Breathing through the mouth rather than the noseas when the nose is congestedis a risk factor for bad breath in people of all ages (see the discussion of saliva, below). Adenoidal hypertrophy, a common problem in childhood that may lead to mouth breathing, may present with chronic intermittent purulent or watery rhi- nitis, snoring, dry mouth, and bad breath. 

 are the second most common source of bad breath after the mouth, accounting for about 5% to 10% of cases of bad breath in adults.

 Typical nasal malodor has a slightly cheesy character and differs appreciably from other types of bad breath. It is easy to distinguish from oral malodor because most of the odor exits the nose rather than the mouth.

Odor from the nose may indicate a frank nasal infection, such as sinusitis, or a problem affecting airflow or mucous secretions, such as polyps. In some cases, a craniofacial anomaly, such as cleft palate, may be involved.

Nasal odor often comes and goes for no apparent reason. In a study of 24 healthy children examined over three appointments,

 nine had nasal odor at one appointment, eight at two appointments, and one at all three appointments. Only six children had no nasal odor at any of the appointments!

 Very young children tend to stick things   in their nose.

 These objects can be almost anything that fits in   the nostrils: food (corn, peas, sunflower seeds, beans), pieces of tissue, tacks,   small toys, buttons, and outdoor objects (parts of plants and even small animals   such as snails) (Figure 4). If the foreign body is absorbent, it putrefies relatively   quickly, and the child often smears the ensuing purulent exudate over his skin   and hair. This can give the physician the mistaken impression that the odor   is coming from all over the child's body (as is likely the case with the 3-year-old   in the opening scenario). 

If the foreign body is hard and impervious to moisture, it does not readily putrefy and can remain undetected for a long time. We once traced a case of mild nasal odor to a calcified plastic bead embedded in the nose of a 28-year-old woman who had apparently placed it there some 25 years earlier!

On rare occasions, children may ingest a foreign body that then gets caught in the upper gastrointestinal tract, resulting in halitosis. In addition, any obstruction of the nasal passages that leads to mouth breathing will likely increase oral malodor. 

The role of tonsils in chronic malodor in children is unclear. In adults, tonsils have been estimated to cause about 3% of cases of bad breath, although some ear, nose, and throat specialists believe tonsils play an even greater role than this figure indicates. Parents commonly report a transient oral malodor with the onset of sore throat in their children, an odor that can be sensed by the attending physician as well.

Transient bad breath following tonsillectomy has also been reported. Clearly, further investigation is necessary to assess the role of tonsils in pediatric oral malodor. 

 Some patients complain of small, foul-smelling   stones on their tongue or tonsils when they cough. These stones are "tonsilloliths"partially   calcified deposits of bacteria and debris that originate in crypts of the tonsils   (Figure 5). 

Based on our experience, we estimate that about 3% of the adult population have, or have had, tonsilloliths. Despite their foul odor, tonsilloliths do not necessarily cause bad breath. But because people often squeeze the stones between their fingers and become horrified by the smell, tonsilloliths may lead to halitophobia. 

The formation of these deposits can be prevented by laser cryptolysis, which seals the crypts. This is not a common clinical procedure, however.

 contains antibacterial agents and continually washes away bacteria from oral surfaces. When the mouth dries out, odor increases, not only because of increased proliferation of bacteria but also because gases escape into the air when the liquid dries. Bad breath gets worse during the day when saliva flow is lowestseveral hours following a meal, for exampleand at night, when the flow of saliva is negligible. Factors that dry out the mouth, such as mouth breathing, certain medications, prolonged talking, lack of sufficient fluid intake, and stress, increase the likelihood of bad breath.

   The breakdown of proteins in the oral cavity that leads to malodor usually takes place under neutral or alkaline conditions. Therefore, acidity in the mouth probably reduces oral malodor; on the down side, it promotes dental caries.

 Surprisingly little is known about the relationship between diet and breath, particularly in children. Since most cases of malodor involve proteolysis, one might surmise that proteinaceous foods can cause bad breath, particularly if they remain in the mouth a long time after eating (as with impacted meat between teeth). Investigators have suggested that milk products and coffee can lead to bad breath, although this hypothesis has not been clinically investigated. Foods containing garlic and onion can, of course, cause bad breath following ingestion. Although some of this odor enters the bloodstream and percolates out through the lungs, most of the odor is related to the oral cavity. In a recent experiment at Tel Aviv University, students were instructed to either chew and swallow a sandwich containing garlic or chew the sandwich and spit it out. No difference in odor level was found between the two regimens. Furthermore, odor exiting the mouth was consistently stronger than odor exiting the nose (Hoffman D, Greenstein R: Unpublished data, June 2000). 

Since oral malodor is generally worst in the morning, eating a good breakfast can help reduce bad breath. The increased saliva flow, together with the mechanical action of chewing and swallowing, helps lower oral microbial levels and, in turn, decrease odor. 

Interestingly, researchers have found elevated levels of bad breath in hyperactive children, who also had other possible predisposing factors such as allergy and stuffy nose.

 24 children who had attention deficit hyperactivity disorder were fed a special diet (Alberta Children's Hospital Diet; "ACH") that eliminated food dyes, food flavors, preservatives, monosodium glutamate, chocolate, and caffeine; reduced the amount of simple sugars; and provided multivitamin supplements. The diet resulted in a significant reduction in bad breath (

<.01) and a less significant reduction in rhinitis (

People who diet or fast often complain of bad breath. It is unclear whether their bad breath is caused by ensuing changes in the oral cavity (the mouth drying out or lack of mastication) or by altered body metabolism.

Among those who have the rare genetic condition trimethylaminuria ("fish odor syndrome"), diets high in choline can result in self-perceived fishlike breath and body odor caused by buildup of trimethylamine in sweat, saliva, and urine.

 People have long smoked cigarettes to mask their bad breath, a practice that results in its own unpleasant odor. Cigarette odor can linger for more than a day. In some cases, the odor of cigarette smoke can be detected on the breath of people who don't smoke but who are continually exposed to the smoke of others.

In the United States, the use of smokeless tobacco has been cited as an important cause of bad breath in adolescents.

 Indeed, tobacco-use prevention programs should emphasize the risk of bad breath as a deterrent to smoking.  

 In postpubertal girls, bad breath may occur during the menstrual cycle. This may be caused by transient gingivitis.

 Many illnesses have been reported to cause bad breath, including untreated diabetes, bronchial and lung infections, kidney or liver failure, various carcinomas, metabolic dysfunction, and biochemical disorders. These are rare causes in the ambulatory population, however, and are usually accompanied by more obvious symptoms.

In the case of diabetes, older literature on bad breath often cites ketone (acetone) odor as a sign of the disease. In modern societies, ketone odor is rare among diabetics whose disease is well managed (Hollenberg C: Personal communication, May 1990). In less developed countries, in indigent populations, and among diabetic teenagers away from home (who might binge on pizzas and other taboo foods then), ketone odor may still be a telltale sign of diabetes.

 Contrary to popular belief, bad breath almost never arises from the esophagus, stomach, or intestines. The esophagus is normally collapsed and closed; an occasional belch may carry odor up from the stomach, but the possibility of air escaping continuously is remote. Nevertheless, several gastroenterologists have proposed a relationship between 

 and bad breath, a hypothesis that requires further study. In general, performing gastroscopy solely because of bad breath should be strongly discouraged.

 Reports in the literature of cases of bad breath related to gastric conditions, such as congenital hypertrophic pyloric stenosis, are rare.

When evaluating bad breath, the input of a confidantsomeone close to the patient who is aware of the problemis invaluable. The confidantusually a parent, older sibling, close friend, or relative is often the person who has complained about the patient's bad breath. He (or she) should be present at the consultation for several reasons:

 Bad breath is often a subjective complaint. People who complain they have     bad breath are notoriously incompetent at judging their own malodor. Similarly,     parents who complain about their child's bad breath may be exaggerating the     problem. At the office appointment, the physician should verify the objective     nature of the problem and the complaint. 

 The confidant can attest to whether the odor present at consultation represents,     in both intensity and character, the odor of the breath at other times. Bad     breath varies with the time of day (saliva flow), day of month (menstruation),     weather (allergies), and so on. 

 Patients are usually unaware of changes in their breath. The confidant     can help monitor the situation, report any changes, and build confidence that     the situation is improving (which it hopefully is). 

Patients should refrain from any oral activity, including eating, drinking, chewing, smoking, or brushing, for at least three hours before the appointment. Reschedule patients who are either on antibiotics or who have taken them during the past month; because malodor is often bacterial in origin, it usually decreases transiently during and directly after antibiotic therapy. 

Begin the evaluation with a medical history. Concentrate on finding out whether the patient maintains good oral hygiene, is a mouth breather, and has any history of allergy or nasal problems. Ask the confidant where he thinks the odor is coming from and why. Two scenarios that may be encountered during history taking are:

 "Our daughter Judy (5 years old) has bad breath, especially when she wakes     up in the morning and sometimes in the late afternoon. Her older brother and     sister never had this problem." 

 "Nobody has actually told me I have bad breath, but I know I do because     people cover their mouths when they talk to me." (Or: people open windows     in my presence; people touch their nose when talking to me; I have a bad taste     in my mouth; my father had bad breath.) 

That second group of answers is typical of halitophobics, who are often well groomed and commonly break into tears during the patient history. They frequently need psychological intervention but tend to resist it, convinced that their problem is organic.

Although several manufacturers are developing   "electronic noses" to analyze bad breath, no instrument is as yet able to replace   the human nose. So clinicians must still rely upon their sense of smell to distinguish   the main types of oral odors, summarized in Table 1. With practice and experience,   these odors become distinct and recognizable, even when found in various combinations. 

Ask the patient to breathe out through the mouth. Smell the odor from about 5 to 10 cm away and make a quantitative judgment (for example, on a scale of 0 to 5, where 0 is no odor, 1 is barely detectable odor, 2 is slight odor, 3 is moderate odor, 4 is foul odor, and 5 is is unbearably foul odor). Also make qualitative judgments (for example, typical/atypical, periodontal/ lingual).  When simple breathing through the mouth is inadequate to make an assessment, ask the patient to count out loud to 20 while you evaluate his breath; sometimes the odor is more obvious when speaking. In children younger than 4 years or so, simply lean toward them and smell the expirate.

After evaluating mouth odor, ask the patient to breathe out through the nose with the mouth closed. We often ask young children to pretend they are an elephant and to breathe out through their "trunk." Assess as above.

 Suspect an oral or pharyngeal origin to the bad breath when the odor is     largely confined to the mouth. 

 Suspect nasal involvement when the odor is largely confined to the nose     or has a different character than the oral odor. 

 Suspect a systemic origin in those rare cases when odor emanates both from     the mouth and nose and has the same quality. 

Evaluate the tongue by asking the patient to stick it out as far as possible while holding his breath. Use the spoon to scoop up some of the mucus at the very back of the dorsum of the tongue, toward the throat. In older children, you can hold the tip of the tongue with a piece of gauze in one hand and collect the sample with the spoon in the other hand. Wait a few seconds before smelling the spoon and scoring the odor. Ask the confidant to smell the spoon and tell you whether this is the odor the patient suffers from. (If it is, gentle tongue cleaning and gargling should resolve the problem.)

The level of intraoral volatile sulfur compounds   (VSC) produced by oral bacteria can be estimated using a portable sulfide monitor   (Figure 6). Readings are obtained by inserting a plastic straw attached to the   monitor into the patient's partially closed mouth and asking the patient to   breath normally through the nose while the instrument sucks the air through   the sensor. 

The association between sulfide monitor results and odor judgment scores is significant (coefficient correlations in studies range from about 0.45 to 0.65, 

 Sulfide monitor readings are sensitive to a reduction in mouth odor level following use of a rinse. Nevertheless, although these measurements can be helpful (such as to apprise the patient of any improvements in breath odor), they do not obviate the need for the clinician to smell the breath emanating from the patient's mouth, nose, and tongue.

Additional clinical and laboratory tests for measuring VSC and other bad breath-associated parameters are under development. For example, oral isolates can be plated onto selective agar that indicates by color those colonies that produce VSC. Our laboratory is working on a rapid color test to identify the presence of high levels of bacterial activity associated with the production of malodor.

 Most cases of bad breath can be alleviated by relatively simple measures (Table   2), such as maintaining proper dental care and oral hygiene. Encourage older   children to floss their teeth, to smell the floss between each passage, and   to clean the malodorous sites carefully. The ability to manipulate the floss   depends largely on eye-hand coordination and age; children younger than about   8 or 9 years are usually not able to floss on their own. Time and supervision   are needed to ensure that flossing is done properly.

Articles

Bad breath is no laughing matter for the child or adolescent who has it. Most cases can be alleviated by relatively simple measures, but not before the cause is pinpointed by a targeted history and physical exam.

Gary Robinson

Articles

Beating bad breath