Halitosis, colloquially called bad breath, is a symptom in which a noticeably unpleasant odor is present on the exhaled breath. Concern about halitosis is estimated to be the third most frequent reason for people to seek dental care, following tooth decay and gum disease; and about 20% of the general population are reported to suffer from it to some degree.
Not all who think they have halitosis have a genuine problem. Of those who feel they have halitosis, significant percentages (5‑72%) have been reported to have no genuine halitosis when professionally examined. Of those who have genuine halitosis, often the odor is caused by bacteria present below the gumline and on the back of the tongue. The remaining 10% is accounted for by many different conditions, including disorders in the nasal cavity, sinuses, throat, lungs, esophagus, stomach or elsewhere. See the related article on tonsilloliths for another possible cause of halitosis.
Very rarely, halitosis can be one of many symptoms of a serious underlying medical condition such as liver failure; but, in the vast majority of cases, the cause is minor and can often be reduced by adjustments to oral hygiene, including brushing or gently scraping the back of the tongue and improving the health of the gums by using dental floss. Occasionally, however, especially if the origin of the odor is not in the mouth, halitosis can be more difficult to diagnose and to manage successfully. Bad breath is a social taboo; and, as a result, perceived or genuine halitosis can sometimes trigger social anxiety and depression.
- 1 Classification
- 2 Differential diagnosis
- 3 Diagnostic approach
- 4 Management
- 5 Epidemiology
- 6 History, society and culture
- 7 Research
- 8 References
Two main classification schemes exist for halitosis, although none is universally accepted.
The Miyazaki et al. classification was originally described in 1999 in a Japanese scientific publication, and has since been adapted to reflect North American society, especially with regards halitophobia. The classification assumes three primary divisions of the halitosis symptom, namely genuine halitosis, pseudohalitosis and halitophobia. This classification has been suggested to be most widely used, but it has been criticized because it is overly simplistic and is largely of use only to dentists rather than other specialties.
- Genuine halitosis
- A. Physiologic halitosis
- B. Pathologic halitosis
- (i) Oral
- (ii) Extra-oral
The Tangerman and Winkel classification was suggested in Europe in 2002. This classification focuses only on those cases where there is genuine halitosis, and has therefore been criticized for being less clinically useful for dentistry when compared to the Miyazaki et al. classification.
- Intra-oral halitosis
- Extra-oral halitosis
- A. Blood borne halitosis
- (i) Systemic diseases
- (ii) Metabolic diseases
- (iii) Food
- (iv) Medication
- B. Non-blood borne halitosis
- (i) Upper respiratory tract
- (ii) Lower respiratory tract
- A. Blood borne halitosis
The same authors also suggested that halitosis can be divided according to the character of the odor into 3 groups:
- "Sulfurous or fecal" caused by volatile sulfur compounds (VSC), most notably methyl mercaptan, hydrogen sulfide and dimethyl sulfide.
- "Fruity" caused by acetone, present in diabetes.
- "Urine-like or ammoniacal" caused by ammonia, dimethyl amine and trimethylamine (TMA), present in trimethylaminuria and uremia.
Based on the strengths and weaknesses of previous attempts at classification of halitosis, an etiologic classification has now been proposed:
- Type 0 (physiologic)
- Type 1 (oral)
- Type 2 (airway)
- Type 3 (gastroesophageal)
- Type 4 (blood-borne)
- Type 5 (subjective)
Any halitosis symptom is potentially the sum of these types in any combination, superimposed on the physiologic odor present in all healthy individuals.
In about 90% of genuine halitosis cases, the origin of the odor is in the mouth itself. This is known as intra-oral halitosis, oral malodor or oral halitosis.
There is an extensive list of possible causes of halitosis in the mouth alone, however by far the most prevalent causes reported are halitogenic biofilm on the posterior dorsal tongue and within gingival crevices and periodontal pockets (i.e. bacteria living on the back of the tongue and below the gumline, and in the pockets created by gum disease between teeth and the gums). Both of these main causes share a common theme of proteolytic putrefaction of sulfur containing amino acids in dietary and salivary protein by mostly anaerobic, Gram negative bacterial species. There are over 600 types of bacteria found in the average mouth. Some of these can produce high levels of foul odors when incubated in the laboratory. The odors are produced mainly due to the breakdown of proteins into individual amino acids, followed by the further breakdown of certain amino acids to produce detectable foul gases. For example, the breakdown of cysteine and methionine produce hydrogen sulfide and methyl mercaptan, respectively. Volatile sulfur compounds have been shown to be statistically associated with oral malodor levels, and usually decrease following successful treatment. Other parts of the mouth may also contribute to the overall odor, but are not as common as the back of the tongue. These locations are, in order of descending prevalence: inter-dental and sub-gingival niches, faulty dental work, food-impaction areas in between the teeth, abscesses, and unclean dentures. Oral based lesions caused by viral infections like Herpes Simplex and HPV may also contribute to bad breath.
The intensity of bad breath may differ during the day, due to eating certain foods (such as garlic, onions, meat, fish, and cheese), smoking, and alcohol consumption. Since the mouth is exposed to less oxygen[medical citation needed] and is inactive during the night, the odor is usually worse upon awakening ("morning breath"). Bad breath may be transient, often disappearing following eating, drinking, tooth brushing, flossing, or rinsing with specialized mouthwash. Bad breath may also be persistent (chronic bad breath), which affects some 25% of the population in varying degrees.
The most common location for mouth related halitosis is the tongue. Tongue bacteria produce malodorous compounds and fatty acids, and account for 80 to 90% of all cases of mouth-related bad breath. Large quantities of naturally-occurring bacteria are often found on the posterior dorsum of the tongue, where they are relatively undisturbed by normal activity. This part of the tongue is relatively dry and poorly cleansed, and the convoluted microbial structure of the tongue dorsum provides an ideal habitat for anaerobic bacteria, which flourish under a continually-forming tongue coating of food debris, dead epithelial cells, postnasal drip and overlying bacteria, living and dead. When left on the tongue, the anaerobic respiration of such bacteria can yield either the putrescent smell of indole, skatole, polyamines, or the "rotten egg" smell of volatile sulfur compounds (VSCs) such as hydrogen sulfide, methyl mercaptan, Allyl methyl sulfide, and dimethyl sulfide. The presence of halitosis-producing bacteria on the back of the tongue is not to be confused with tongue coating. Bacteria are invisible to the naked eye, and degrees of white tongue coating are present in most people with and without halitosis. A visible white tongue coating does not always equal the back of the tongue as an origin of halitosis, however a "white tongue" is thought to be a sign of halitosis. In oral medicine generally, a white tongue is considered a sign of several medical conditions. Patients with periodontal disease were shown to have sixfold prevalence of tongue coating compared with normal subjects. Halitosis patients were also shown to have significantly higher bacterial loads in this region compared to individuals without halitosis.
The normal anatomy of the dorsal tongue surface consists of a posterior third and an anterior two thirds. The posterior third constitutes the lingual tonsil, with cryptolymphatic units roughening the surface of this area. Between the anterior and posterior portions of the dorsal tongue is the V shaped line of vallate papillae. Anteriorly, the surface is even more irregular, with filiform, fungiform and foliate papillae. This irregular surface is a perfect habitat for bacteria and it can also trap debris. The roughly 25 cm2 area carries the heaviest bacterial loads in the oral cavity. The posterior dorsum of the tongue is the site of greatest generation of VSC and hence usually the greatest contributor to oral malodor. Hence, this irregular surface usually forms a coating which can be easily removed. This coating consists of desquamated epilethia (shed skin cells from the tongue), food debris, bacteria and their extracellular matrix. Essentially, a layer of living and non living components referred to as a biofilm. Two conditions that may further predispose to halitogenic biofilm on the dorsal tongue are lingua plicata (fissured or scrotal tongue), a common condition where there are many grooves or fissures on the tongue, and lingua villosa (hairy tongue) where the normal hair-like projections of the specializeds oral mucosa on the dorsal tongue are longer than usual, and may even be discolored.
Gingival crevices are the small grooves between teeth and gums, and they are present in health, although they may become inflamed when gingivitis is present. The difference between a gingival crevice and periodontal pocket is that former is <3mm in depth and the latter is >3mm. Periodontal pockets usually accompany periodontal disease (gum disease). There is some controversy over the role of periodontal diseases in causing bad breath. However, advanced periodontal disease is a common cause of severe halitosis. Waste products from the anaerobic bacteria growing below the gumline (subgingival) have a foul smell and have been clinically demonstrated to produce a very intense bad breath. Removal of the subgingival calculus (i.e. tartar or hard plaque) and friable tissue has been shown to improve mouth odor considerably. This is accomplished by subgingival scaling and root planing and irrigation with an antibiotic mouth rinse. The bacteria that cause gingivitis and periodontal disease (periodontopathogens) are invariably gram negative and capable of producing VSC. Methyl mercaptan is known to be the greatest contributing VSC in halitosis that is caused by periodontal disease and gingivitis. The level of VSC on breath has been shown to positively correlate with the depth of periodontal pocketing, the number of pockets, and whether the pockets bleed when examined with a dental probe. Indeed, VSC may themselves have been shown to contribute to the inflammation and tissue damage that is characteristic of periodontal disease. However, not all patients with periodontal disease have halitosis, and not all patients with halitosis have periodontal disease. Although patients with periodontal disease are more likely to suffer from halitosis than the general population, the halitosis symptom was shown to be more strongly associated with degree of tongue coating than with the severity of periodontal disease. Another possible symptom of periodontal disease is a bad taste, which does not necessarily accompany a malodor that is detectable by others.
Other potential causes in the mouth
- Deep carious lesions (dental decay) – which cause localized food impaction and stagnation
- Recent dental extraction sockets – fill with blood clot, and provide an ideal habitat for bacterial proliferation
- Interdental food packing – (food getting pushed down between teeth) - this can be caused by missing teeth, tilted, spaced or crowded teeth, or poorly contoured approximal dental fillings. Food debris becomes trapped, undergoes slow bacterial putrefaction and release of malodorous volatiles. Food packing can also cause a localized periodontal reaction, characterized by dental pain that is relieved by cleaning the area of food packing with interdental brush or floss.
- Acrylic dentures (plastic false teeth) – inadequate denture hygiene practises such as failing to clean and remove the prosthesis each night, may cause a malodour from the plastic itself or from the mouth as microbiota responds to the altered environment. The plastic is actually porous, and the fitting surface is usually irregular, sculpted to fit the edentulous oral anatomy. These factors predispose to bacterial and yeast retention, which is accompanied by a typical smell.
- Oral infections
- Oral ulceration
- Menstrual cycle – at mid cycle and during menstruation, increased breath VSC were reported in women.
- Smoking – Smoking is linked with periodontal disease, which is the second most common cause of oral malodor. Smoking also has many other negative effects on the mouth, from increased rates of dental decay to premalignant lesions and even oral cancer.
- Volatile foodstuffs – e.g. onion, garlic, durian, cabbage, cauliflower and radish. Volatile foodstuffs may leave malodorous residues in the mouth, which are the subject to bacterial putrefaction and VSC release. However, volatile foodstuffs may also cause halitoisis via the blood borne halitosis mechanism.
- Medication – often medications can cause xerostomia (dry mouth) which results in increased microbial growth in the mouth.
Nose and sinuses
The second major source of bad breath is the nose. In this occurrence, the air exiting the nostrils has a pungent odor that differs from the oral odor. Nasal odor may be due to sinus infections or foreign bodies.
Halitosis is often stated to be a symptom of chronic rhinosinusitis, however gold standard breath analysis techniques have not been applied. Theoretically, there are several possible mechanisms of both objective and subjective halitosis that may be involved.
There is disagreement as to the proportion of halitosis cases which are caused by conditions of the tonsils. Some claim that the tonsils are the most significant cause of halitosis after the mouth. According to one report, approximately 3% of halitosis cases were related to the tonsils. Conditions of the tonsils which may be associated with halitosis include chronic caseous tonsillitis (cheese-like material can be exuded from the tonsillar crypt orifi), tonsillolithiasis (tonsil stones), and less commonly peritonsillar abscess, actinomycosis, fungating malignancies, chondroid choristoma and inflammatory myofibroblastic tumor.
The lower esophageal sphincter, which is the valve between the stomach and the esophagus, may not close properly due to a Hiatal Hernia or GERD, allowing acid to enter the esophagus and gases to escape to the mouth. A Zenker's diverticulum may also result in halitosis due to aging food retained in the esophagus.
The stomach is considered by most researchers as a very uncommon source of bad breath (except in belching). The esophagus is a closed and collapsed tube, and continuous flow (as opposed to a simple burp) of gas or putrid substances from the stomach indicates a health problem—such as reflux serious enough to be bringing up stomach contents or a fistula between the stomach and the esophagus—which will demonstrate more serious manifestations than just foul odor.
- Fetor hepaticus: an example of a rare type of bad breath caused by chronic liver failure.
- Lower respiratory tract infections (bronchial and lung infections).
- Renal infections and renal failure.
- Trimethylaminuria ("fish odor syndrome").
- Diabetes mellitus.
- Metabolic conditions, e.g. resulting in elevated blood dimethyl sulfide.
Individuals afflicted by the above conditions often show additional, more diagnostically conclusive symptoms than bad breath alone.
Halitophobia (delusional halitosis)
One quarter of the patients seeking professional advice on bad breath suffer from a highly exaggerated concern of having bad breath, known as halitophobia, delusional halitosis, or as a manifestation of Olfactory reference syndrome. These patients are sure that they have bad breath, although many have not asked anyone for an objective opinion. Halitophobia may severely affect the lives of some 0.5–1.0% of the adult population.
Scientists have long thought that smelling one's own breath odor is often difficult due to acclimatization, although many people with bad breath are able to detect it in others. Research has suggested that self-evaluation of halitosis is not easy because of preconceived notions of how bad we think it should be. Some people assume that they have bad breath because of bad taste (metallic, sour, fecal, etc.), however bad taste is considered a poor indicator.
Patients often self-diagnose by asking a close friend.
One popular home method to determine the presence of bad breath is to lick the back of the wrist, let the saliva dry for a minute or two, and smell the result. This test results in overestimation, as concluded from research, and should be avoided. A better way would be to lightly scrape the posterior back of the tongue with a plastic disposable spoon and to smell the drying residue. Home tests that use a chemical reaction to test for the presence of polyamines and sulfur compounds on tongue swabs are now available, but there are few studies showing how well they actually detect the odor. Furthermore, since breath odor changes in intensity throughout the day depending on many factors, multiple testing sessions may be necessary.
If bad breath is persistent, and all other medical and dental factors have been ruled out, specialized testing and treatment is required. Hundreds of dental offices and commercial breath clinics now claim to diagnose and treat bad breath. They often use some of several laboratory methods for diagnosis of bad breath:
- Halimeter: a portable sulfide monitor used to test for levels of sulfur emissions (to be specific, hydrogen sulfide) in the mouth air. When used properly, this device can be very effective at determining levels of certain VSC-producing bacteria. However, it has drawbacks in clinical applications. For example, other common sulfides (such as mercaptan) are not recorded as easily and can be misrepresented in test results. Certain foods such as garlic and onions produce sulfur in the breath for as long as 48 hours and can result in false readings. The Halimeter is also very sensitive to alcohol, so one should avoid drinking alcohol or using alcohol-containing mouthwashes for at least 12 hours prior to being tested. This analog machine loses sensitivity over time and requires periodic recalibration to remain accurate.
- Gas chromatography: portable machines, such as the OralChroma, are currently being introduced. This technology is specifically designed to digitally measure molecular levels of the three major VSCs in a sample of mouth air (hydrogen sulfide, methyl mercaptan, and dimethyl sulfide). It is accurate in measuring the sulfur components of the breath and produces visual results in graph form via computer interface.
- BANA test: this test is directed to find the salivary levels of an enzyme indicating the presence of certain halitosis-related bacteria.
- β-galactosidase test: salivary levels of this enzyme were found to be correlated with oral malodor.
Although such instrumentation and examinations are widely used in breath clinics, the most important measurement of bad breath (the gold standard) is the actual sniffing and scoring of the level and type of the odor carried out by trained experts ("organoleptic measurements"). The level of odor is usually assessed on a six-point intensity scale.
- Gently cleaning the tongue surface twice daily is the most effective way to keep bad breath in control; that can be achieved using a tooth brush, tongue cleaner or tongue brush/scraper to wipe off the bacterial biofilm, debris, and mucus. An inverted teaspoon may also do the job. Scraping or otherwise damaging the tongue should be avoided, and scraping of the V-shaped row of vallate papillae found at the extreme back of the tongue should also be avoided. Brushing a small amount of antibacterial mouth rinse or tongue gel onto the tongue surface will further inhibit bacterial action.
- Eating a healthy breakfast with rough foods helps clean the very back of the tongue.
- Chewing gum: Since dry-mouth can increase bacterial buildup and cause or worsen bad breath, chewing sugarless gum can help with the production of saliva, and thereby help to reduce bad breath. Chewing may help particularly when the mouth is dry, or when one cannot perform oral hygiene procedures after meals (especially those meals rich in protein). This aids in provision of saliva, which washes away oral bacteria, has antibacterial properties and promotes mechanical activity which helps cleanse the mouth. Some chewing gums contain special anti-odor ingredients. Chewing on fennel seeds, cinnamon sticks, mastic gum, or fresh parsley are common folk remedies.
- Gargling right before bedtime with an effective mouthwash (see below). Several types of commercial mouthwashes have been shown to reduce malodor for hours in peer-reviewed scientific studies. Mouthwashes may contain active ingredients that are inactivated by the soap present in most toothpastes. Thus it is recommended to refrain from using mouthwash directly after toothbrushing with paste (also see mouthwashes, below).
- Maintaining proper oral hygiene, including daily tongue cleaning, brushing, flossing, and periodic visits to dentists and hygienists. Flossing is particularly important in removing rotting food debris and bacterial plaque from between the teeth, especially at the gumline. Dentures should be properly cleaned and soaked overnight in antibacterial solution (unless otherwise advised by one's dentist).
- Probiotic treatments, specifically Streptococcus salivarius K12 has been claimed to suppress malodorous bacteria growth, however well designed randomised control clinical trails are needed to assess this. Certainly there is more evidence for mechanical tongue cleansing and to a lesser extent specific antimicrobial mouthwashes.
Cleaning the tongue
The most widely known reason to clean the tongue is for the control of bad breath. Methods used against bad breath, such as mints, mouth sprays, mouthwash or gum, may only temporarily mask the odors created by the bacteria on the tongue, but cannot cure bad breath because they do not remove the source of the bad breath. In order to prevent the production of the sulfur-containing compounds mentioned above, the bacteria on the tongue must be removed, as must the decaying food debris present on the rear areas of the tongue. Most people who clean their tongue use a tongue cleaner (tongue scraper), or a toothbrush.
There has not been a single documented medical case of successfully cured chronic halitosis using any of the currently available mouthwashes. However, a 2008 systematic review determined the efficacy of antibacterial mouthrinses for treating bad breath. Mouthwashes often contain antibacterial agents including cetylpyridinium chloride, chlorhexidine, zinc gluconate, essential oils, hydrogen peroxide, and chlorine dioxide. Cetylpyridinium chloride and chlorhexidine can temporarily stain teeth. Zinc and chlorhexidine provide strong synergistic effect. They may also contain alcohol, which is a drying agent.
Other solutions rely on odor eliminators, such as oxidizers, to eliminate existing bad breath on a short-term basis.
A new approach for home treatment of bad breath is the use of oil-containing mouthwashes and two-phase (oil:water) mouthwashes. Essential oils have been found effective in reducing halitosis, and are being used in several commercial mouthwashes.
It is difficult for researchers to make estimates of the prevalence of halitosis in the general population for several reasons. Firstly, halitosis is subject to societal taboo and stigma, which may impact individual's willingness to take part in such studies or to report accurately their experience of the condition. Secondly, there is no universal agreement about what diagnostic criteria and what detection methods should be used to define which individuals have halitosis and which do not. Some studies rely on self reported estimation of halitosis, and there is contention as to whether this is a reliable predictor of actual halitosis or not. In reflection of these problems, reported epidemiological data are widely variable.
History, society and culture
The word halitosis is derived from the Latin word halitus, meaning 'breath', and the Greek suffix -osis meaning 'diseased' or 'a condition of'. The earliest known mention of bad breath occurs in ancient Egypt, where detailed recipes for toothpaste are made before the Pyramids are built. The 1550 BC Ebers Papyrus describes tablets to cure bad breath based on incense, cinnamon, myrrh and honey. Hippocratic medicine advocated a mouthwash of red wine and spices to cure bad breath. Note that alcohol containing mouthwashes are now thought to exacerbate bad breath as they dry the mouth, leading to increased microbial growth. The Hippocratic Corpus also describes a recipe based on marble powder for female bad breath sufferers. The Ancient Roman Physician Pliny wrote about methods to sweeten the breath.
Ancient Chinese emperors required visitors to chew clove before an audience. The Talmud describes bad breath as a disability, which could be grounds for legal breaking of a marriage license. Early Islamic theology stressed that the teeth and tongue should be cleaned with a Siwak, a stick from the plant Salvadora persica tree. This traditional chewing stick is also called a Miswak, especially used in Saudi Arabia, an essentially is like a natural toothbrush made from twigs. During the Renaissance era, Laurent Joubert, doctor to King Henry III of France states bad breath is "caused by dangerous miasma that falls into the lungs and through the heart, causing severe damages".
In B. G. Jefferis and J. L. Nichols' "Searchlights on Health" (1919), the following recipe is offered: "[One] teaspoonful of the following mixture after each meal: One ounce chloride of soda, one ounce liquor of potassa, one and one-half ounces phosphate of soda, and three ounces of water."
With modern consumerism, there has been a complex interplay of advertising pressures and the existing evolutionary aversion to malodor. Contrary to the popular belief, also raised on QI, that Listerine coined the term halitosis, it actually dates from the 1870s, although it only became commonly used in the 1920s when a marketing campaign promoted Listerine as a solution for "chronic halitosis". The company was the first to manufacture mouth washes in the United States. According to Freakonomics:
"Listerine [...] was invented in the nineteenth century as powerful surgical antiseptic. It was later sold, in distilled form, as both a floor cleaner and a cure for gonorrhea. But it wasn't a runaway success until the 1920s, when it was pitched as a solution for "chronic halitosis"— a then obscure medical term for bad breath. Listerine's new ads featured forlorn young women and men, eager for marriage but turned off by their mate's rotten breath. "Can I be happy with him in spite of that?" one maiden asked herself. Until that time, bad breath was not conventionally considered such a catastrophe. But Listerine changed that. As the advertising scholar James B. Twitchell writes, "Listerine did not make mouthwash as much as it made halitosis." In just seven years, the company's revenues rose from $115,000 to more than $8 million."
In the present day, bad breath is one of the biggest societal taboos. The general population places great importance on the avoidance of bad breath, illustrated by the annual $1 billion that consumers in the United States spend on deodorant-type mouth (oral) rinses, mints, and related over-the counter products. Many of these practices are merely short term attempts at masking the odor. Some authors have suggested that there is an evolutionary basis to concern over bad breath. An instinctive aversion to unpleasant odors may function to detect spoiled food sources and other potentially invective or harmful substances. Body odors in general are thought to play an important role in mate selection in humans, and unpleasant odor may signal disease, and hence a potentially unwise choice of mate. Although reports of bad breath are found in the earliest medical writings known, the social stigma has likely changed over time, possibly partly due to sociocultural factors involving advertising pressures. As a result, the negative psychosocial aspects of halitosis may have worsened, and psychiatric conditions such as halitophobia are probably more common than historically. There have been rare reports of people committing suicide because of halitosis, whether there is genuine halitosis or not.
According to traditional Ayurvedic medicine, chewing areca nut and betel leaf is a remedy for bad breath. In South Asia, it was a custom to chew areca or betel nut and betel leaf among lovers because of the breath-freshening and stimulant drug properties of the mixture. Both the nut and the leaf are mild stimulants and can be addictive with repeated use. The betel nut will also cause dental decay and red or black staining of teeth when chewed. Both areca nut and betel leaf chewing, however, can cause premalignant lesions such as leukoplakia and submucous fibrosis, and are recognised risk factors for oral and oropharyngeal squamous cell carcinoma (oral cancer). Other traditional remedies for halitosis include Guava leaves in Thailand, eggshells in China, parsley in Italy, and urine-based mouth rinse in certain European cultures.
Practitioners and purveyors of alternative medicine sell a vast range of products that claim to beneficial in treating halitosis, including dietary supplements, vitamins, oral probiotics. Halitosis is often claimed to be a symptom of the so-called "candida hypersensitivity syndrome" or related fictitious diseases, and is claimed to be treatable with antifungal medications or alternative medications claimed to treat fungal infections.
In 1996, the International Society for Breath Odor Research (ISBOR) was formed to promote multidisciplinary research on all aspects of breath odors. The eighth international conference on breath odor took place in 2009 in Dortmund, Germany, while the ninth was held in 2011 in Salvador da Bahia, Brazil.
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