Although the term “Halitosis” (bad breath) was first coined in 1874, people have become more aware of the problem as recently as the COVID-19 pandemic due to the widespread wearing of protective masks. In fact, after caries and periodontal disease, bad breath is the third most common reason patients visit a dentist. Due to the multifactorial etiology, the diagnosis of halitosis requires a thorough medical/dental/social history, clinical examination, and additional examination methods. Treatments for the disease range from the use of dentifrices, mouth rinses, tongue scrapings, and concealers, and more recently, also include the use of photodynamic therapy, probiotics, and ozone. The aim of this descriptive review was to review the published literature on halitosis over the past 30 years and to discuss the diagnosis, etiology, and treatment of this disease.
The term “halitosis” was first used in 1874 by Dr. Joseph William Howe in his book The Breath and the Diseases That Give it a Foul Smell. “Halitosis” comes from the Latin word “halitus” (“breath”) and the Greek suffix “-osis”, which means a painful condition. The Oxford English Dictionary defines halitosis as “A condition in which the breath smells bad.”
Although the disease was identified about 150 years ago, interest in halitosis has increased recently due to the need or even the requirement in some places for people to wear a mask due to the COVID-19 virus. Basically, whenever you were indoors, whether it was in supermarkets, buses or subways, or in offices (with the exception of some cases where people around were vaccinated), people wore masks. A TV news broadcast in May 2020 featured a snippet titled “Bad Breath Behind a Coronavirus Mask? 10 Causes and Remedies for Halitosis.” A 2021 review article identified halitosis as one of the oral manifestations of COVID-19.
Most people have experienced bad breath at some point in their lives. According to the National Institute of Dental Research, approximately 65 million Americans suffer from halitosis at some point in their lives. What's more, at least 50% of the population has persistent bad breath, and half of those people suffer from a chronic problem. Bad breath is considered the third most common reason for dental office visits, after cavities and periodontal disease.
The prevalence of halitosis worldwide ranges from 22% to 50%, with the highest percentage being self-reported. This large discrepancy has to do with perceptions, self-perceptions, and diagnostic tools that are influenced by racial and cultural differences. There is an increase in the prevalence of age-related halitosis; however, there is no relationship between severity of halitosis and gender. In addition to the lack of disease prevalence studies, available data on the prevalence of halitosis may be inaccurate due to differences in research methodologies and the large number of self-reported cases that were not considered a true manifestation of halitosis.
Recent interest in the manifestations of halitosis caused by wearing masks during the pandemic has led the authors to study the problem over the past 30 years, focusing on its diagnosis, etiology and treatment, and whether any or all of these three aspects have changed over time. The purpose of the following descriptive review was to review the published literature on halitosis over the past three decades and discuss the diagnosis, etiology, and treatment of this condition.
Materials and methods
An electronic search was performed on the PubMed, MedLine and Google Scholar databases for the following keywords: “halitosis” AND/OR “bad breath” AND “etiology”, “diagnosis” AND “treatment”. A total of 2083 articles were found. However, search results were limited to articles published between 1990 and 2021 in English only with full text access. In addition, search results were limited to systematic reviews, reviews, meta-analyses, randomized controlled trials, controlled clinical trials, clinical trials, case series, and human-only case reports. The inclusion criteria resulted in 136 articles being included in this literature review according to their relevance, which was determined by the agreement of the authors.
The review was divided into four parts: diagnosis, measurement methods, etiology and treatment.
Diagnosis
Diagnosis of halitosis should begin with recognition of the problem by the patient or a close confidant of the patient. Determining the cause of bad breath requires a thorough history and physical examination, as well as knowledge of the possible etiology. In 1992, three distinct diagnostic groups were considered in diagnosing bad breath: non-pathological causes, pathological causes, and finally psychiatric conditions and psychosomatic bad breath. However, a systematic classification for distinguishing and diagnosing halitosis was only established in 2000 by Yaegaki and Coil.
This classification of halitosis includes the categories of genuine halitosis, pseudo-halitosis and halitophobia. Genuine halitosis is identified as a distinct malodor that exceeds socially acceptable levels. This can be perceived by patients and quantified using measurement methods. Genuine bad breath is classified into physiological bad breath and pathological bad breath. Physiological halitosis is described as an unpleasant odor that occurs as a result of putrefactive processes in the oral cavity without any associated pathological condition. The source of physiological bad breath is mainly the dorsal-posterior region of the tongue. Temporary halitosis caused by dietary factors is excluded from the definition of physiological halitosis, even if no pathological condition is observed. Pathological halitosis is subdivided into pathological intraoral halitosis and pathological extraoral halitosis. The true pathological etiology is found in this type of disease. Pseudo-bad breath is a condition in which patients persistently complain of bad breath, but this is not perceived by others.
So, halitosis is any unpleasant odor in the air exhaled by a person.
Halitophobia is a condition in which patients continue to insist that they have bad breath, even after being treated for genuine or pseudo-halitosis, without having any physical or social evidence of bad breath. from mouth. The condition of halitophobia was confirmed in a study that showed that individuals with a main complaint of bad breath had a lower percentage of true bad breath than those whose complaints did not include this condition. This classification not only clearly demonstrates the different etiologies and origins for each type of halitosis, but also allows the doctor to assess the psychological state of the patient. This classification is generally recognized and the most cited.
Different methods for measuring breath odor
Due to the presence of a classification of pseudo-halitosis and halitophobia, a method for measuring bad breath is important for accurate diagnosis and effective treatment. To date, six main measurement methods have been used: self-assessment, sensory assessment, gas chromatography, sulfide monitoring, microbial quantification, and coated tongue condition. Each of these methods has its own advantages and disadvantages.
So, the patient can independently measure the level of unpleasant odor by exhaling air into the palm of his hand, or ask his relatives to evaluate the smell from his mouth by exhaling it close to the person. The disadvantage of this method is the difficulty in processing the results of the experiment and the difference in their interpretation.
Organoleptic examination is the gold standard in the examination of patients with suspected halitosis. In this study, the doctor is located at a distance of 10 centimeters. The patient can either leave a trace of saliva on his hand, or the saliva on the spoon used by the patient can be examined, or a metal spatula or dental floss used by the patient can be used to assess the presence of an unpleasant odor on these objects. It is also possible to evaluate the smell from prosthetic structures in the patient's mouth by comparing it with the air exhaled by him. The advantages of this method are the acceptable cost of its implementation, the absence of the need for any expensive equipment, as well as a wide range of detectable odors, the ability to determine the strength and quality of the exhaled odor. The disadvantages of the method include a large variability of the results of the study and the fact that the accuracy of the results directly depends on the experience of the researcher.
Gas chromatography – analysis of the concentration of volatile sulfur compounds in the air (hydrogen sulfide and methyl mercaptan). The advantages of the method are highly accurate results with a high percentage of certainty, especially for amines and non-volatile gases. The disadvantages are the high cost of the method and the required extensive experience of the researcher.
Sulfide monitoring, a method in which volatile sulfur compounds are measured in the air exhaled by the patient, for this a special device is used – Halimeter. The values obtained are compared with the norm – 70-110 parts per billion (ppb). The advantages of the method are its low cost, the ability to quantitatively measure the volume of particles in the air, fast results and no need for special training. But still, in the absence of proper experience, the researcher conducting the measurements may misinterpret the results.
Microbiological examination of a saliva sample can be carried out in two ways: a portion of milk from the patient's mouth is placed in a container with a solution of methylene blue, the higher the level of bacterial contamination of the sample, the faster the color of the liquid will change from blue to white. You can also take a scraping from the back of the tongue with a cotton swab, if after 30 minutes the tip of the swab turns yellow-brown, this indicates the presence of chronic halitosis in the patient.
The advantage of this method lies in the fact that its result can be qualitatively assessed (color change correlates with the number of anaerobic bacteria in the sample). The disadvantage is the required presence of a certain experience of the researcher for a reliable assessment of the results obtained and the inability to obtain the result instantly.
Estimation of the degree of coating of the tongue, the amount (thickness) of the coating of the tongue with plaque is measured: invisible to the eye, thin layer, very thick layer of plaque (does not allow taste buds to be distinguished). The degree of imposition of the tongue is also assessed: less than 2/3 of the tongue, or more than 2/3 of the tongue. The advantages of this method can be considered that the coating of the tongue indicates a large number of anaerobic bacteria in the oral cavity, which correlates with the amount of volatile sulfur compounds in the air exhaled by the patient. The disadvantage of the method is its subjectivity, since the lining of the tongue itself can be caused by various other factors, in addition to the presence of anaerobic bacteria in the mouth, for example, such factors include xerostomia, features of the anatomy of the tongue itself (deep grooves).
Since 2000, a method for measuring malodor with a chemical sensor called “electronic nose” has also been used, this method is used both in the clinical practice of dentists and for research purposes. The sensor is built into the probe and can take measurements in periodontal pockets and on the back of the tongue. The 0.25″ x 0.75″ probe is applied to the test areas with light pressure. Electrochemical voltage from the sulphate sensor. generated depending on the amount of sulfide ions. The method showed results very similar to those obtained by sensory examination and gas chromatography indices and measurements. Currently, the use of this chemical sensor is the most promising alternative method for both research and clinical purposes. In early 2000, a different testing method, cysteine testing, was used in numerous studies to test the effectiveness of ongoing manipulations to reduce malodor. Subjects were instructed to rinse their mouths with cysteine to create bad breath, after which various methods were tried to eliminate this bad breath in order to determine the most effective of all. In 2017, another measurement method using copper oxide or molybdenum oxide sensors, which have a high affinity and sensitivity to hydrogen sulfide, began to gain popularity, it gained great acceptance among specialists and began to be used as a tool for diagnosing bad breath.
Additional indirect methods for measuring halitosis have also been proposed and described in the literature, such as the BANA test, which detects the presence of proteolytic obligate Gram-negative anaerobes, primarily those that form a red complex. The test strip shows a blue color after 5 minutes if the results are positive. It is convenient to use and can show a strong positive correlation with periodontal disease activity. Other tests include β-galactosidase activity quantification, lead acetate determination, breath ammonia monitoring, ninhydrin method, polymerase chain reaction, and more. It was found that the readings of these tests are highly correlated with those obtained by measuring the content of volatile sulfur compounds in exhaled air (VSC) and indicators of sensory examination, which allows them to be considered an alternative to the described methods.
Etiology
Halitosis has a multifactorial etiology. Understanding the etiology of bad breath is important not only for diagnosis, but also for the development of multidisciplinary treatment. Another classification of halitosis reveals the complex etiology of this disease, the causes of which can be divided into non-pathological/physiological causes, pathological causes and psychiatric causes.
So, the physiological causes of halitosis include: age, bad breath after waking up, bad breath when a person is hungry, human consumption of specific foods or medicines.
Pathological odor from the mouth can occur for a number of reasons, so directly in the mouth the cause of the odor can be various prosthetic structures, periodontitis, dehydration, stomatitis, glossitis, inflammation of the parotid or other salivary glands, the presence of tumors or chronic odontogenic sinusitis. Sinusitis of non-odontogenic origin can be caused by the presence of a foreign body in the nasal passage or sinus, the penetration of infection by destructive pathological changes, as well as tumors in the nose or chronic sinusitis provoked by colds of the nose. From the side of the tonsils and pharynx, tonsillitis, plugs in the tonsils, pharyngitis, inflammation of the epiglottis, the presence of foreign bodies, tumors, diverticula in the pharynx can become the cause of halitosis. On the part of the gastrointestinal tract, halitosis can be caused by diseases such as achalasia, reflux, esophageal obstruction, bezoar stones. On the part of the lungs, bad breath can be caused by necrotizing pneumonia, anaerobic abscess, lung empyema. Systemic diseases such as diabetic ketoacidosis, liver and kidney failure can cause halitosis. Mental disorders can also be the cause of halitosis, among them schizophrenia and a disorder of smell are distinguished.
Genuine bad breath can occur both directly inside the oral cavity and without affecting the oral cavity; however, approximately 80% to 90% of cases of bad breath still come from the mouth. Halitosis, due to the smell inside the mouth, can be explained by three main factors: host (saliva, topography of the tongue, external factors such as stress), bacteria and substrate. The substrate can be exogenous (food) or endogenous (saliva). Saliva plays an important role in the formation of bad breath. Depending on the oxygen supply, substrate used, flow rate, and pH level, saliva can either suppress or promote bad breath. The main cause of bad breath, however, is the accumulation of Gram-negative anaerobic bacteria in plaque on the tongue and below the gingival margin, which in turn produce volatile sulfur dioxide gases as microbial degradation products. The relationship between anaerobic bacteria that produce sulfur gases and bad breath has been well documented since the 1990s. In the 1990s, the etiology of bad breath was thought to be mainly the release of three sulfur dioxide compounds—hydrogen sulfide, methyl mercaptan, and dimethyl sulfide—with the former two gases accounting for 90% of the volatile sulfur compounds in human exhaled air. Since 2000, more odor-related compounds have been found. These include five groups: volatile aromatic compounds, short chain fatty acids, alcohols, volatile aliphatic compounds, and aldehydes and ketones. However, hydrogen sulfide has a low threshold and a high odor strength, so it is this gas that needs to be eliminated.
Physiological halitosis, as a subclass of true halitosis, is what is known as halitosis in the morning, affecting about half of adults. This is a transient condition and occurs regardless of the state of oral health, usually this type of halitosis is less pronounced and its occurrence can fluctuate at different times of the day. Its source is mainly the dorso-pastoral region of the tongue, where there is a greater accumulation of microbes and food debris, also in this area there is the highest level of keratinized cells of the tongue, saliva and blood elements, which is aggravated during sleep and a decrease in salivation at night. The rough surface of the tongue with a complex papillary structure is a reservoir for anaerobic gram-negative bacteria that produce hydrogen sulfide well from food debris from epithelial cells. Clinically, higher levels of plaque on the tongue are closely related to the intensity of halitosis. Other physiological causes of bad breath are hormonal changes, especially in women, consumption of certain types of foods such as garlic, onions, choline, foods containing animal fats, curry, durian, spices, etc., or habits such as smoking and drinking alcohol.
Pathological halitosis, as a subclass of true halitosis, can have both intraoral and extraoral etiologies and is more intense than physiological halitosis. With halitosis, it is inside the mouth that the smell spreads only from the mouth, while with an extraoral cause of halitosis, the smell comes from both the mouth and the nose.
Intraoral sources of bad breath
Periodontal diseases such as gingivitis, periodontitis, as well as necrotizing ulcerative form of these diseases, periodontal abscess and peri-implantitis usually contribute to the occurrence.
Odontogenic causes of halitosis can be carious lesions of the teeth, exposed pulp necrosis, accumulation of food debris around old fillings or restorations. Various types of devices (orthodontic equipment, dentures).
When healing wounds, bad breath can also occur, for example, when the tooth socket becomes inflamed, infection enters the wound (during bone regeneration) and manifestations of bone necrosis. Also, a number of diseases of the mucous membranes can provoke halitosis, especially syphilis, tuberculosis, intraoral neoplasia and malignancy of tumors.
Many studies have shown that periodontal health is directly related to bad breath. Patients with periodontitis are three times more likely to have bad breath and have eight times more hydrogen sulfide compounds in their exhaled breath, as well as four times more plaque on the tongue. The frequency of bad breath in the elderly may be due to the higher prevalence and severity of periodontal disease. Patients with chronic periodontitis and deep periodontal pockets develop bad breath due to an increased number of gram-negative anaerobic bacteria, the accumulation of food debris and their increased decay. The microbiological link between bad breath and periodontal disease is that the main microbiological flora (anaerobic gram-negative bacteria) producing hydrogen sulfide gases are present in the inflamed gum tissue. In addition, the lining of the sublingual surface of the tongue with bacteria from pockets in the gums and the mixing of saliva with gum fluid contributes to the release of volatile sulfur compounds. Other factors of the state of the oral cavity that cause the development of halitosis are associated with poor removal of food debris from the tooth gaps, the presence of deep carious cavities, overhanging edges of fillings, the presence of non-removable orthodontic equipment in the patient's mouth, and leaving removable lamellar dentures in the mouth at night.
Extraoral sources of bad breath are listed.
So, to the previously listed factors on the part of the respiratory, digestive and metabolic systems, such specific conditions as trimethylaminuria and an increased content of methionine in the blood are added. Also consecrated are conditions induced by the use of drugs, such as amphetamines, hydrochlorides, cytotoxic agents, dimethyl sulfoxides, nitrates, solvent use.
Although only approximately 10% of cases of bad breath are of extraoral origin, it is still important to understand the potential sources for a proper diagnosis and treatment plan. As most authors assumed in the 1990s, the main sources are the ear/nose/throat region, with the tonsils, pharynx, and sinuses being the most common source due to the presence of streptococci. The lower respiratory tract is the source of the problem due to inflammation or infection, trapped foreign bodies are a less common cause, and metabolic or gastric dysfunction is a rare cause. However, since 2000, a growing body of research has shown an association between gastrointestinal disease and bad breath, especially gastroesophageal reflux disease (GERD) and the presence of Helicobacter pylori, both of which are common diseases. Although they are much less common, certain metabolic disorders can also cause bad breath. In these systemic diseases, odorous substances circulating in the bloodstream can be exhaled through alveolar gas exchange and cause bad breath. This is also known as bloodborne bad breath. Dimethyl sulfide of three highly volatile sulfur compounds is a major cause of extraoral or blood-borne bad breath. Systemic diseases that cause bad breath include uncontrolled diabetes, pancreatic, liver, and kidney dysfunction, and the genetic metabolic disorder trimethylaminuria (fishy odor syndrome). Less commonly, bad breath can occur as a side effect of medications containing the dimethyl sulfide structure, which can appear in the breath. In 2020, drugs that cause bad breath were divided into 10 groups: acid-reducing agents, aminothiols, anticholinergics, antidepressants, antifungals, antihistamines and steroids, antispasmodics, chemotherapeutic agents, dietary supplements, and organosulfur agents. Bad breath varies depending on the systemic condition: diabetic ketoacidosis is characterized by a fruity odor, bowel obstruction causes a fecal odor, chronic kidney failure causes an ammonia or urine odor, and liver cirrhosis causes a musty odor.
Delusional/hallucinatory/imaginary halitosis is caused by mental disorders; it is also known as pseudo-bad breath or halitophobia. These patients complain of bad breath, however, after careful clinical examination, history taking, and treatment of bad breath, the symptoms persist but are not detected by other people. These types of halitosis can be mineral and vitamin deficiencies that alter a person's taste buds and sense of taste, structural anatomical damage and anomalies that cause taste disorders, neurodegenerative diseases, or exposure to certain types of chemicals. Patients experiencing imaginary bad breath may exhibit specific behaviors such as covering their mouths and keeping their distance from others. However, these patients find it difficult to accept the connection between bad breath and their psychological state. Therefore, the clinician should try to convince the patient, without resorting to argumentation, to contact a specialist psychologist or psychiatrist.
Treatment
The first step in the treatment of bad breath is to determine the etiology, and then prescribe the appropriate treatment. A thorough medical, dental, and dietary history will help establish an accurate diagnosis and formulate an effective treatment plan. Treatment may be prescribed depending on the nature of the extraoral or intraoral cause of the disease. However, bad breath can also have a detrimental effect on the psychological state of the patient. Therefore, it is important, if necessary, to connect a specialist to check the mental state of the patient.
Since the 1990s, treatments have included dental treatment, mouth rinses, various dentifrices, tongue scrapers, odor masking agents, eating behavior modification, and herbal treatments, as described in Table 6. However, a combination of mechanical and chemical methods is the most effective and efficient treatment for bad breath.
In the late 2000s, the concepts of vaccine therapy and photodynamic therapy (laser) were introduced. However, laser treatment has been found to be inferior to regular preventive treatments such as plaque and calculus removal to reduce malodor in patients with periodontal disease. In 2009, a program was launched to maintain the functions of the oral cavity, which included exercises for the muscles of the face and tongue, massage of the salivary glands and education in the anatomy of the oral cavity and adherence to the rules of this program proved to effectively reduce halitosis, improve saliva flow and articulation of the patient as a whole. After 2010, new treatments for bad breath included the use of lactoferrin and lactoperoxidase tablets. A review reviewed by Scully and Greenman also described the use of metronidazole in the treatment of persistent cases of halitosis.
In a more recent review published in 2016, the authors developed a treatment strategy based on the type of halitosis.
So, if the main complaint of the patient is bad breath, the authors suggest taking a thorough history, find out how the patient eats, whether halitosis has been noticed before, whether he undergoes regular oral hygiene procedures. Further, the authors suggest that the patient undergo an organoleptic examination of breathing, if it confirms the presence of halitosis, then a thorough examination of the oral cavity is carried out. Especially, you need to pay attention to the presence of specific foci of inflammation in the mouth, or signs of syphilis. The patient should also be referred for examination of the gastrointestinal tract. And a complete blood count and blood biochemistry to detect hidden conditions, either diabetes or other systemic diseases of the liver or kidneys. If the organoleptic examination did not reveal halitosis, other specific studies, such as the BANA test, can be performed, if halitosis is not confirmed after it, then imaginary halitosis should be suspected.
Alternatively, odor pulling with oil particles has been found to be a relatively effective way to combat halitosis in many randomized controlled trials. The mechanism of odor extraction by oil particles is that microbes with a hydrophobic shell adhere to oil droplets and are expectorated along with the oil. Rice bran oil and sesame oil showed a comparable effect to chlorhexidine in reducing bad breath.
Treatment for bad breath has been consistent over the past three decades; only in the last decade have probiotics been promoted as an effective treatment. A recent study found that taking probiotic tablets daily can help control bad breath. Although probiotics do not cause permanent colonization, the long-term effect of probiotics can be anywhere from 3 days to 2 weeks. In 2019, the concept of prebiotics, carbohydrates in the form of fibers, was used alongside probiotics in the treatment of bad breath and was shown to be successful in reducing bad breath parameters tested in ongoing research on the topic. In another study, researchers used E. coli to successfully treat non-oral halitosis caused by bowel disease. Although probiotics lead to a decrease in the intensity of bad breath in a number of parameters described in many studies, but since the authors used different strains of probiotics in each case and the bacterial flora varied, there is a need for more standardized studies on this topic. for proper interpretation of the results. In 2018, a case of a decrease in the level of halitosis in a patient undergoing orthodontic treatment using a device for rapid palatal expansion of the upper jaw was described. In 2019, it was proposed to use ozone in the form of gas, water, or oil form to destroy bacterial pathogens that contribute to the development of halitosis.
Another new trend that has emerged since 2010 is photodynamic or laser treatment. Laser therapy for the treatment of bad breath involves the use of a light-sensitive dye (photosensitizer), a high power light source and oxygen. This combination leads to the formation of reactive oxygen species and promotes the death of bacterial cells. Laser treatment has been found to result in short-term elimination of bad breath after a single session. A systematic review reported that laser therapy may be an effective adjunct to mechanical treatment, but its effectiveness requires further study.
A Cochrane review reviewing the numerous studies on this topic referred to in this review concluded that most of the studies have a low level of evidence, and therefore it is not possible to understand which treatment of halitosis is most effective .
Conclusion
Due to the multifactorial origin of halitosis, correct diagnosis, identification of the etiology, and timely referral to related specialists are important for effective treatment. An interdisciplinary approach to the management of bad breath is critical to avoid the risk of misdiagnosis and/or unnecessary treatment. If the etiology is related to the teeth (eg, caries, periodontal disease, poor oral hygiene), elimination of bad breath can be achieved by correcting these factors, which may be within the power of the patient and the dentist. However, if systemic factors contribute to the problem, a multidisciplinary approach is required. Despite this, more controlled studies are needed to determine the most effective treatment for various types of bad breath.
Author:
Stuart J. Frome, DDS
Ye Shi, DDS; Natacha Reis, DDS
Tanatorn Asvaplungprohm, DDS