|DENTAL SCIENCE - REVIEW ARTICLE
|Year : 2015 | Volume
| Issue : 6 | Page : 339-343
Halitosis - An overview: Part-I - Classification, etiology, and pathophysiology of halitosis
GS Madhushankari1, Andamuthu Yamunadevi2, M Selvamani3, KP Mohan Kumar1, Praveen S Basandi1
1 Department of Oral and Maxillofacial Pathology and Microbiology, College of Dental Sciences and Hospital, Davangere, Karnataka, India
2 Department of Oral Pathology, Vivekanandha Dental College for Women, Tiruchengode, Tamil Nadu, India
3 Department of Oral and Maxillofacial Pathology and Microbiology, Mahe Institute of Dental Science and Hospital, Mahe, U.T. of Puducherry, India
|Date of Submission||28-Apr-2015|
|Date of Decision||28-Apr-2015|
|Date of Acceptance||22-May-2015|
|Date of Web Publication||1-Sep-2015|
Dr. Andamuthu Yamunadevi
Department of Oral Pathology, Vivekanandha Dental College for Women, Tiruchengode, Tamil Nadu
Source of Support: None, Conflict of Interest: None
| Abstract|| |
Halitosis is a condition where the breath is altered in an unpleasant manner for the affected individuals and impairs them socially as well as psychologically. Halitosis can be clinically classified as real halitosis, pseudohalitosis, and halitophobia. Real halitosis has oral and extra-oral etiologies and the pathophysiology involves interaction of anaerobic microbes (mainly) with the proteins present in the oral cavity fluids and contents, resulting in production of volatile sulfur compounds (VSCs). These VSCs, beyond responsible for halitosis, can also initiate and accelerate periodontal disease progression. Thus, this review is about the pathophysiology and various etiologies of halitosis, the knowledge of which can help in the betterment of treatment options.
Keywords: Anaerobic microbes, halitosis, pseudohalitosis, volatile sulfur compounds
|How to cite this article:|
Madhushankari G S, Yamunadevi A, Selvamani M, Mohan Kumar K P, Basandi PS. Halitosis - An overview: Part-I - Classification, etiology, and pathophysiology of halitosis. J Pharm Bioall Sci 2015;7, Suppl S2:339-43
|How to cite this URL:|
Madhushankari G S, Yamunadevi A, Selvamani M, Mohan Kumar K P, Basandi PS. Halitosis - An overview: Part-I - Classification, etiology, and pathophysiology of halitosis. J Pharm Bioall Sci [serial online] 2015 [cited 2020 Jan 20];7, Suppl S2:339-43. Available from: http://www.jpbsonline.org/text.asp?2015/7/6/339/163441
Halitosis (Synonyms: Bad breath, fetid halitus, mouth odor, bad breath, bad mouth odor, malodor) "is a condition in which halitus/breath is altered in a manner unpleasant for the affected individual and affects both the individual and also those with whom he/she interacts."  It set backs an individual from his/her social interactions and also affects psychologically. Here, the responsibility comes to the dentist in assessing and treating this apparently common phenomenon, since oral cavity is the most common source of halitosis. At times, bad breath can also reflect the systemic pathologies and is of real concern to diagnose these pathologies at the earliest. References related to this common problem are rare and, this article gives an overview on the different aspects of halitosis.
| Epidemiology|| |
Flipping through the pages of ancient Greek and Roman  literature thousands of years back, bad breath is mentioned in their writings also, and Mediterranean countries have used ladaneey (a resion) for freshening the breath. Parsley (Italy), cloves (Iraq), guava peels (Thailand), and egg shells (China) are the folk cures for halitosis. Thus, it is revealed that oral halitosis is a problem of all centuries, occurring universally in both the genders. All age groups are affected and the incidence of halitosis increases with age, with varying prevalence rate (5-75%, , 60%,  14.6%  ) in children and (8-50%)  in general population. Moderate chronic halitosis is common in one-third of the population, and the rest are affected by halitosis at least during a part of the day (morning mouth/morning halitosis is widely prevalent). Severe halitosis affects less than 5% of the population  that requires immediate attention.
| Classification|| |
In general, halitosis can be either primary or secondary: 
- Primary halitosis: Refers to respiration exhaled by the lungs 
- Secondary halitosis: Originates either in the mouth or upper airways. 
Clinically, halitosis can be classified into three groups,  namely:
- Real/Genuine halitosis
- Physiologic halitosis: E.g.: Morning halitosis
- Pathologic halitosis:
- Oral pathologic halitosis
- Extra-oral pathologic halitosis
- Pseudohalitosis - Complains of halitosis without the actual existence and can be treated by the dental practitioner by counseling and simple oral hygiene procedures.
- Halitophobia - People with a fear of halitosis. Interestingly, this group of patients present with symptoms of halitosis in the absence of objective oral malodor. This symptom may be attributable to a form of delusion or monosymptomatic hypochondriasis (self-oral malodor, halitophobia, phantom bad breath).  This condition can be identified by questionnaire method and require psychological investigation or support rather than a dental treatment. 
| Etiology|| |
Bad breath can originate either from oral and related (ear, nose, throat) sources (87%) or extra-oral (systemic) in origin (13%).  Poor oral hygiene, gingivitis and periodontitis, tongue coating, ear, nose, and throat problems (e.g.: Tonsillitis, sinusitis, presence of foreign bodies and rhinitis), decrease in saliva, dry mouth, habits such as smoking, alcohol, tobacco, and betel nut chewing are the leading oral factors associated with halitosis,  with male gender being affected more commonly.  Caries experience, age, habits such as mouth breathing leading to dryness of mouth  are associated with malodor in children. Extraoral or systemic conditions leading to halitosis include gastrointestinal (GIT) problems , and even stress. 
Enumeration of possible etiological sources ,,,,,,,, is given in [Table 1].
| Pathophysiology|| |
Though the exact pathogenesis of oral malodor is not known, the most accepted one is that the microbial putrefaction of food debris, desquamated cells, saliva and blood causes oral malodor. The bacterial interactions are mainly due to several proteolytic and anaerobic, Gram-negative bacterial species and are not associated with any specific bacterial infection. The only Gram-positive bacteria so far proved to be associated with halitosis is Stomatococcus mucilaginous. 
Various agents such as volatile sulfur compounds (VSCs), diamines and short chain fatty acids are produced due to this microbial breakdown of amino acids by enzymes, resulting in oral malodor (For e.g.: Breakdown of cystine, cysteine, and methionine produces VSC  ) [Figure 1] and [Figure 2].
|Figure 2: Enzymatic breakdown of amino acids, resulting in production of VSCs|
Click here to view
The intensity of malodor corresponds to the level of odoriferous substances in the oral cavity  and gingival crevices, periodontal pockets, and posterior dorsum of the tongue are the most likely sites involved in the whole process.
| Factors in the Pathophysiology of Halitosis|| |
Saliva, performing numerous functions in the oral cavity, has protective and anti-bacterial properties as prime functions. Its protective function is mainly due to cleansing action causing constant removal of bacteria and food debris, and the anti-bacterial property is attributed to the presence of salivary Ig A, lysozyme, lactoferrin, and several glycoproteins. Furthermore, the normal salivary pH is slightly acidic in nature (pH - 6.5) and helps in suppressing the growth and proliferation of Gram-negative and anaerobic bacteria. Thus, the activation of enzymes necessary for the putrefaction of amino acids such as cystine, cysteine, and methionine is hindered, preventing the production of foul smelling sulfur-containing compounds. ,
Xerostomic conditions causing reduction in salivary flow causes a negative effect on the self-cleansing action of saliva and produces odoriferous volatile compounds. , Mucin precipitation and alkalization of the oral environment enhances proteolytic bacterial growth. Thus, dehydration, salivary gland diseases, certain drugs, mouth breathing remain as one of the causes for halitosis by causing xerostomia.
The people with morning breath (evening breath in night shift workers!!) will not experience halitosis during the day, but during sleep, the body produces less saliva, and unpleasant odor is experienced in the morning.
Gingivitis and periodontitis
About 10% of the population with severe periodontitis are accompanied by bad breath. The applied reasons are,
- The spaces between the teeth and the gums act as site of entrapment of food for the people with periodontitis and eventually bacteria acts on these entrapped food substances, producing odoriferous substances 
- Also, the bleeding tendency of gums in gingivitis and periodontitis, makes the condition worse.  Initially, it will impart an iron or metallic smell and later as the blood decomposes, a more foul smell is produced. 
Malodor can arise from the patients even with good oral hygiene and the source is from the posterior dorsal tongue,  as the large, papillary surface area of the dorsum of tongue can retain large amounts of desquamated cells, leukocytes, salivary constituents, and microorganisms and can facilitate putrefaction. Though, the microbial content of the tongue is greater, , it is not necessarily different for the people with and without periodontitis.  Tongue cleaning along with regular brushing improves the condition.
Mouth breathing accounts for 40%  in children with halitosis by causing surface drying of mucosa due to evaporation of water from saliva.  Notoriously, humming facilitates nasal breathing in these patients by increased nitric oxide production that causes smooth muscle relaxation and vasodilatation.  As a treatment option, mouth breathing children are suggested to hum with the tongue on the palate to ensure nose breathing.
Respiratory related illness and increased mucus production
In respiratory-related illness like postnasal drip, sinus related illness, and tonsillitis, excessive mucus and phlegm accumulation is seen, which attracts more bacteria. This cause of halitosis is more common in children, as the children are more susceptible to postnasal drip and tonsillitis.
Drinking and/or smoking (active and passive), beyond giving alcoholic and nicotinic smell on the intakers, adds to halitosis by increasing mucus and phlegm in the throat.  Eating dairy rich food also increases mucus production.  Eliminating the above-mentioned etiologies reduces halitosis.
Other than oral and related causes, halitosis due to GIT disorders is considered to be rare, as the esophagus is normally collapsed and closed.  Two important GIT pathologies where association with halitosis is proved are Helicobacter pylori infection and gastroesophageal reflux disease. , Furthermore, halitosis is significantly associated with heartburn, regurgitation, sour taste, belching, and borborygmus but not with functional dyspepsia, peptic ulcer disease, upper abdominal pain, bloating, early satiety or chest pain. 
The association of H. pylori infection with halitosis was initially suggested by Marshall et al. in 1985.  Controversies with their association are noted in different studies and the researchers speculate that the strain-specific production of VSCs is responsible for variation in the study results that is, the production of VSC are observed only in three strains of H. pylori namely, H. pylori ATCC 43504, H. pylori SS 1, H. pylori DSM 4867. The other species of H. pylori does not produce odoriferous substances and thus not associated with halitosis.  H. pylori infection increases with age and has a prevalence rate of 19.6-43.9%.  Crowded families promote cross infection and its carcinogenic potential alarms us for early detection and treatment. Urea breath test, serum antibody detection, saliva analysis, biopsies and molecular DNA analysis helps in H. pylori detection. Treatment with antibiotics and proton pump inhibitors eliminates the infection and can bring down halitosis. 
Different medical conditions, impart different odor on the patient's breath.
- Diabetes - Fruity or citrusy breath
- Asthma or cystic fibrosis - Acidic breath
- Kidney problem - Scent of ammonia
- Hepatic cirrhosis - Musty or mousey odor 
- Trimethylaminuria - Foul fishy odor
- Nasal malodor - Slightly cheesy character
- Bowel obstruction - Fecal odor. 
Ketoacidosis (uncontrolled diabetes can produce diabetic ketoacidosis) - Sweet fruity and/or acetone breath or rotten apple breath.
Excessive ketone production can also result from dieting. Low carbohydrate diet, burns body's fat content for energy production and produces excessive ketones. Stopping the dieting, changing the diet with high carbohydrate content and low-fat content, drinking extra water to flush out the body prevents ketone breath. 
Eating strongly odoriferous food substances
Food substances with strong odor like garlic and onion, after being absorbed into the bloodstream during digestion, are transferred to the lungs, and the exhaled air is characterized by the odor of that particular food substance. 
| Need for Early Detection of these Volatile Sulfur Compounds|| |
These VSCs released during microbial interactions are capable of initiating and accelerating periodontal pathology. Recently, it has been reported that hydrogen sulfide induce mitochondria-mediated apoptosis and DNA damage in human gingival fibroblasts by increasing the levels of reactive oxygen species.  Extracellular matrix degradation is facilitated by induction of immune responses, matrix metalloproteinase activity by these VSCs. VSCs inhibit osteoblastic activity,  activate osteoclastic activity, thus leading to pathogenic bone loss. Thus, the effects of VSCs are much more than simple halitosis, and early detection and removal saves from periodontal disease progression also.
| Conclusion|| |
The patients with halitosis initially approach the dentists for the betterment of the condition and here the responsibility lies on the dentists to treat the condition. Thus, a thorough understanding of the etiology and pathophysiology can upgrade us to a better treatment option. Researches on VSCs and their effect on oral tissues have given a real concern to the problem of halitosis and thus early remedy to this apparently normal phenomenon is essential.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Motta LJ, Bachiega JC, Guedes CC, Laranja LT, Bussadori SK. Association between halitosis and mouth breathing in children. Clinics (Sao Paulo) 2011;66:939-42.
Geist H. Halitosis in ancient literature. Dent Abstr 1957;2:417-8.
Kharbanda OP, Sidhu SS, Sundaram K, Shukla DK. Oral habits in school going children of Delhi: A prevalence study. J Indian Soc Pedod Prev Dent 2003;21:120-4.
Nalçaci R, Dülgergil T, Oba AA, Gelgör IE. Prevalence of breath malodour in 7- 11-year-old children living in Middle Anatolia, Turkey. Community Dent Health 2008;25:173-7.
Scully C, Felix DH. Oral medicine - update for the dental practitioner: Oral malodour. Br Dent J 2005;199:498-500.
Rösing CK, Loesche W. Halitosis: An overview of epidemiology, etiology and clinical management. Braz Oral Res 2011;25:466-71.
Yilmaz AE, Bilici M, Tonbul A, Karabel M, Dogan G, Tas T. Paediatric halitosis and Helicobacter pylori
infection. J Coll Physicians Surg Pak 2012;22:27-30.
Porter SR, Scully C. Oral malodour (halitosis). BMJ 2006;333:632-5.
Nadanovsky P, Carvalho LB, Ponce de Leon A. Oral malodour and its association with age and sex in a general population in Brazil. Oral Dis 2007;13:105-9.
Moshkowitz M, Horowitz N, Leshno M, Halpern Z. Halitosis and gastroesophageal reflux disease: A possible association. Oral Dis 2007;13:581-5.
Kinberg S, Stein M, Zion N, Shaoul R. The gastrointestinal aspects of halitosis. Can J Gastroenterol 2010;24:552-6.
Queiroz CS, Hayacibara MF, Tabchoury CP, Marcondes FK, Cury JA. Relationship between stressful situations, salivary flow rate and oral volatile sulfur-containing compounds. Eur J Oral Sci 2002;110:337-40.
Rosenberg M. Clinical assessment of bad breath: Current concepts. J Am Dent Assoc 1996;127:475-82.
Lin MI, Flaitz CM, Moretti AJ, Seybold SV, Chen JW. Evaluation of halitosis in children and mothers. Pediatr Dent 2003;25:553-8.
Bornstein MM, Kislig K, Hoti BB, Seemann R, Lussi A. Prevalence of halitosis in the population of the city of Bern, Switzerland: A study comparing self-reported and clinical data. Eur J Oral Sci 2009;117:261-7.
Haumann TJ, Kneepkens CM. Halitosis in two children caused by a foreign body in the nose. Ned Tijdschr Geneeskd 2000;144:1129-30.
Amir E, Shimonov R, Rosenberg M. Halitosis in children. J Pediatr 1999;134:338-43.
Ermis B, Aslan T, Beder L, Unalacak M. A randomized placebo-controlled trial of mebendazole for halitosis. Arch Pediatr Adolesc Med 2002;156:995-8.
Alamoudi N, Farsi N, Faris J, Masoud I, Merdad K, Meisha D. Salivary characteristics of children and its relation to oral microorganism and lip mucosa dryness. J Clin Pediatr Dent 2004;28:239-48.
Kleinberg I, Wolff MS, Codipilly DM. Role of saliva in oral dryness, oral feel and oral malodour. Int Dent J 2002;52 Suppl 3:236-40.
Yaegaki K, Sanada K. Volatile sulfur compounds in mouth air from clinically healthy subjects and patients with periodontal disease. J Periodontal Res 1992;27:233-8.
Yaegaki K, Sanada K. Biochemical and clinical factors influencing oral malodor in periodontal patients. J Periodontol 1992;63:783-9.
Weitzberg E, Lundberg JO. Humming greatly increases nasal nitric oxide. Am J Respir Crit Care Med 2002;166:144-5.
Ierardi E, Amoruso A, La Notte T, Francavilla R, Castellaneta S, Marrazza E, et al.
Halitosis and Helicobacter pylori
: A possible relationship. Dig Dis Sci 1998;43:2733-7.
Fedorowicz Z, Aljufairi H, Nasser M, Outhouse TL, Pedrazzi V. Mouthrinses for the treatment of halitosis. Cochrane Database Syst Rev 2008;4:CD006701.
Marshall BJ, Armstrong JA, McGechie DB, Glancy RJ. Attempt to fulfil Koch′s postulates for pyloric Campylobacter.
Med J Aust 1985;142:436-9.
Ongole R, Shenoy N. Halitosis: Much beyond oral malodor. Kathmandu Univ Med J (KUMJ) 2010;8:269-75.
Fujimura M, Calenic B, Yaegaki K, Murata T, Ii H, Imai T, et al.
Oral malodorous compound activates mitochondrial pathway inducing apoptosis in human gingival fibroblasts. Clin Oral Investig 2010;14:367-73.
Imai T, Ii H, Yaegaki K, Murata T, Sato T, Kamoda T. Oral malodorous compound inhibits osteoblast proliferation. J Periodontol. 2009;80:2028-34.
[Figure 1], [Figure 2]
|This article has been cited by|
||Comparison of oral malodors before and after nonsurgical periodontal therapy in chronic periodontitis patients
| ||Sao-Shen Liu,Earl Fu,Hsiao-Pei Tu,Min-Wen Fu,Chia-Te Lin,E-Chin Shen |
| ||Journal of Dental Sciences. 2017; 12(2): 156 |
|[Pubmed] | [DOI]|
||Recombinant Sox Enzymes from Paracoccus pantotrophus Degrade Hydrogen Sulfide, a Major Component of Oral Malodor
| ||Atik Ramadhani,Miki Kawada-Matsuo,Hitoshi Komatsuzawa,Takahiko Oho |
| ||Microbes and environments. 2017; 32(1): 54 |
|[Pubmed] | [DOI]|
||Detection of halitosis in breath: Between the past, present, and future
| ||MK Nakhleh,M Quatredeniers,H Haick |
| ||Oral Diseases. 2017; |
|[Pubmed] | [DOI]|
||Association between Purpose in Life/(<i>Ikigai</i>), Prefrontal Cortex Function, and the Prevention of Halitosis Caused by Mental Stress, Pseudo-Halitosis, and Halitophobia
| ||Riichiro Ishida |
| ||Psychology. 2016; 07(03): 271 |
|[Pubmed] | [DOI]|