Abst ract
Submitted: June 30, 2016 0RGL¿FDWLRQ6HSWHPEHU Accepted: October 12, 2016
Assessm ent of t he accuracy of
port able m onit ors for halit osis
evaluat ion in subj ect s wit hout
m alodor com plaint . Are t hey reliable
for clinical pract ice?
+DOLWRVLVLVGH¿QHGDVDIRXORGRUHPDQDWHGIURPWKHRUDOFDYLW\ZLWKJUHDW im pact in quality of life and social restraints. Recently, the use of Breath Alert™ LQUHVHDUFKLQFUHDVHGVLJQL¿FDQWO\+DOLPHWHUDQRWKHUSRUWDEOHGHYLFHLV RIWHQXVHGLQFOLQLFDOSUDFWLFH1HYHUWKHOHVVQRWPDQ\VWXGLHVKDYHYHUL¿HGWKH accuracy and com pared t he result s of bot h devices sim ult aneously. Obj ect ive: To verify t he accuracy of Breat h Alert ™ and Halim et er™ in pat ient s wit hout chief com plaint of halitosis, using the organoleptic test (OT) as “ gold standard.” The second aim was t o verify whet her t heir concom it ant use could enhance t he diagnost ic accuracy of halit osis. Mat erial and Met hods: A cross- sect ional analytical study was perform ed. The quality of expired air of 34 subjects without chief com plaint of halit osis was assessed. Two experienced exam iners carried out t he OT. Aft erward, a t hird blinded exam iner perform ed Halim et er™ ( HT) DQG%UHDWK$OHUW%$WHVWV5HVXOWV7KH27LGHQWL¿HGKDOLWRVLVLQVXEMHFWV 7KHDUHDXQGHUWKH52&FXUYHFRQ¿GHQFHLQWHUYDOZDV ±DQG±IRU+7DQG%$UHVSHFWLYHO\7KHDFFXUDF\ for HT and BA was 59% and 47% , respect ively. The com bined usage of HT and BA provided 11 posit ive result s, being 9 subj ect s ( 43% ) out of t he t ot al of 21 posit ive cases. Conclusions: Halim et er™ and Breat h Alert ™ were not able t o diagnose halit osis in non- com plainer subj ect s at t he sam e level as t he organolept ic exam inat ion, since t heir accuracy were low. Our result s suggest t hat such port able devices are not reliable t ools t o assess halit osis and m ay neglect or m isdiagnose a considerable num ber of pat ient s in clinical pract ice.
Ke yw or ds: Halit osis. Diagnosis. Denise Pinheiro FALCÃO1
Priscila Carvalho MIRANDA1 Tayana Filgueira Galdino ALMEIDA2 0RQLTXH*RPHVGD6LOYD6&$/&2 Felipe FREGNI3 Rivadávio Fernandes Batista de
AMORIM3
http://dx.doi.org/10.1590/1678-7757-2016-0305
1Universidade de Brasília, Faculdade de Medicina, Programa de Pós-Graduação em Ciências
Médicas, Brasília, DF, Brasil.
2Serviço Público de Saúde do Distrito Federal, Brasília, DF, Brasil.
3Harvard Medical School, Laboratory of Neuromodulation & Center for Clinical Research Learning,
Charlestown, Massachusetts, United States.
I nt roduct ion
Halitosis is a universally experienced condition that has a variet y of physiologic, pat hologic and adapt ive et iologic fact ors and affect s nearly 15 t o 30% of t he populat ion5,7,11,21. The gold st andard m et hod t o
evaluat e halit osis is t he organolept ic or “ sniff” t est ( OT) , which access all oral odorants collectively. I n this t est , t he exam iner uses t he sense of sm ell t o det ect m alodor and subj ect ively score pat ient s’ halit osis21.
I t has som e im por t ant draw backs, such as being dependent on som eone’s int erpret at ion about t he qualit y of t he odor and t he offensiveness score of t he sm ell. Subj ect ive m easures are an issue in research, since objective data are m ore likely to be standardized. I n addit ion, t he organolept ic t est requires calibrat ion and can be an em barrassing procedure1,15. Therefore, LW LV FULWLFDO WR DFFHVV WKH VHQVLWLYLW\ DQG VSHFL¿FLW\
of ot her m et hods in order t o decrease t he need of perform ing OT.
Many efforts have been m ade to create reliable and obj ect ive m et hods t o evaluat e halit osis. Halim et er™ ( I nt erscan Corporat ion, Chat swort h, CA, USA) is a port able m onit or t hat m easure t he am ount of sulphur com pounds r esponsible for bad br eat h. How ever, it st ill does not m eet all t he r equir em ent s t o be considered an “ ideal” device in t he assessm ent of halitosis25. Breath Alert™ is another device that (Tanita
Corporat ion, Tokyo, Kant õ, Japan) has been gaining special attention in clinical practice3,6,12,13,17. I t is a sm all
handheld breat h- checking equipm ent t hat m easures and calculat es t he volat ile sulphur com pounds and hydrocarbon gases in expired air. Nevert heless, not
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in clinical pract ice.
We believe not enough st udies have accessed t he breat h odor qualit y in pat ient s wit hout chief com plaint of halit osis. Since som e pat ient s wit h halit osis m ight be unaware of t heir condit ion, we aim ed t o st udy a populat ion m or e r epr esent at ive of daily clinical pract ice. Thus, t he m ain purpose of t his st udy was t o access sim ult aneously t he accuracy of Breat h Alert ™ and Halim et er™ in pat ient s wit hout chief com plaint of halit osis, using t he OT as “ gold st andard.” We also hypot hesized t hat t he concom it ant use of bot h m et hods could enhance t he diagnost ic accuracy of halit osis, and t hus could be helpful in decreasing t he use of OT in clinical pract ice.
Mat erial and m et hods
The st udy design has followed t he guidelines for quality of evidence for studies of diagnostic accuracy19. A cr oss- sect ional analy t ical st udy was per for m ed using a convenience and consecut ive sam ple. The hum an subj ect prot ocol was in accordance wit h t he principles laid down in t he Declarat ion of Helsinki and was approved by t he correspondent I nst it ut ional Boar d ( 033/ 04) . I nfor m ed consent w as obt ained from t hose who accept ed t he invit at ion. Part icipant s w er e ex am in ed in t w o m om en t s. A per iodon t ist per f or m ed in t r aor al ex am in at ion an d in st r u ct ed about t he following visit for halit osis assessm ent . I n t he second visit , t wo experienced exam iners who have been working wit h halit osis for m ore t han 15 years carried out t he OT. Considering t hat t he unit of m easurem ent is on a cat egorical scale, reliabilit y needed t o be properly assessed as a m easure of agr eem ent . The ex am iner s w er e calibrat ed unt il t he level of concordance reached 80% . Hence, t he kappa index was 0.8 ( great agreem ent level) . Bot h exam iners were blinded regarding the oral condition of t he pat ient . Aft erwards, anot her exam iner perform ed Halim et er™ ( HT) and Breat h Alert ™ ( BA) t est s in a blind fashion ( oral st at us and OT result s) .
Subj ect s
The sam ple was com posed of m en and wom en ZKRYLVLWHGWKHSULYDWHRI¿FHRIRQHRIWKHDXWKRUV FRQVHFXWLYHO\GXULQJRQHPRQWK6XEMHFWVZKRIXO¿OOHG t he following crit eria were eligible: not diagnosed wit h gingival and or chronic periodont al diseases based on WKH$PHULFDQ$FDGHP\RI3HULRGRQWDO&ODVVL¿FDWLRQ2 and wit hout com plaint of halit osis. I n addit ion, oral-SKDU\Q[ LQÀDPPDWRU\ SURFHVVHV FROG RU ÀX RUDO ¿VWXODDQGFXUUHQWXVHRIDQWLELRWLFVWUHDWPHQWZLWKLQ t he pr ev ious 3 w eek s) r epr esent ed t he exclusion crit eria.
t old t o have a m eal and t o perform t heir usual oral hygiene pract ices 2 hours before t he assessm ent . At the day of halitosis assessm ent, the use of any scented cosm et ic, such as perfum e and aft ershave, was not allow ed once it could int er fer e in t he ex am iner s’ olfact ory sense and wit h t he equipm ent sensors.
Organolept ic t est
Ex am in er s w er e in st r u ct ed t o p ost p on e t h e assessm ent in t he pr esence of any unpr edict able situations that could lead to olfactory disturbance, such as post nasal drip, rhinit is, sinusit is or cold. Volunt eers were required t o close t heir m out h and refrain from t alking for 3 m inut es before t he evaluat ion. Aim ing t o st andardize t he assessm ent dist ance, t he edge of a 15 cm lengt h rule was placed on t he m ent olabial sulcus of t he pat ient and t he ot her edge bellow t he nost rils of t he exam iner. Subj ect s were inst ruct ed t o slowly exhale t heir breat h by saying “ raaaaaaaaaus” unt il t hey could feel t heir lungs em pt y.
Volatile sulphur com pound (VSC) m easurem ent
Measurem ent s of t ot al VSC of expired air were t aken w it h a por t able indust r ial sulphide m onit or Halim eter™ ( I nterscan m odel 1170) . For this purpose, t he inst rum ent was zeroed on environm ent air and pat ient s were inst ruct ed t o keep t heir m out h closed, as previously required for t he OT. The breat h sam ple was assessed t hree t im es, as recom m ended by t he m anufact urer. A disposable st raw connect ed t o t he device sensor was insert ed int o t he pat ient ’s m out h in a st andardized dist ance of 4 cent im et ers. The pat ient was instructed to close his m outh with the straw inside by keeping t he lips on a leaked silicone cylinder. The
UHVXOWVSDUWVper- billion ( ppb) were considered posit ive for HT.
Breat h Alert ™ assessm ent
Befor e each m easur em ent , Br eat h Aler t ™ was
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or m oist ure left in t he device, as recom m ended by t he m anufact urer. Pat ient s received t he sam e inst ruct ions r egar din g k eepin g t h eir m ou t h closed f or t h r ee m inut es. Aft erwards, t he device was t urned on and t he pat ient s’ t hum b was posit ioned on t he front of t he unit t o help direct ing t he sensor t oward t he m out h. As soon as t he display showed t he word “ st art ,” pat ient s expired t he air, as recom m ended in t he OT. This st udy considered t he BA scores 1 and 2 as negat ive, and scores 3 and 4 as posit ive for halit osis.
St at ist ical analysis
Dat a analyses were carried out using St at ist ical Package for Social Sciences SPSS™ version 20.0 for Windows™ ( SPSS I nc./ I BM Group, Chicago, I L, USA) .
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t he difference am ong OT, HT and BA t est s. I n order t o access and com pare t he diagnost ic accuracy of t hese t hree t est s, receiver- operat ing charact erist ic ( ROC) was carried out , and t he OT was considered t he “ gold st andard.”
Result s
The sam ple was com posed of 34 adult pat ient s ( 44% m en and 56% wom en) , m ean age of 44.2± 14.6 years ( range: 25 t o 75) wit h m ean value part s-per
-billion of volat ile sulphur com pounds of 52 ( range: 1 t o 167) .
The OT was posit ive for 21 part icipant s ( 62% ) ( Figure 1) . The area under t he ROC curve was 0.67
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BA, respect ively. The sensit ivit y was 33% and 24% for HT and BA, respect ively ( Table 1) .
The com bined usage of HT and BA provided 11 posit ive result s, being 9 ( 43% ) out of t he t ot al of 21 posit ive cases. Using sim ult aneously all t he m et hods
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and eleven as negat ive in t he sam e way. ( Figure 2) . The ppb m ean value of VSC of t he t hree posit ive cases was 167, 156 and 110 ppb ( dat a not shown) .
Figure 1- Prevalence of halitosis positive diagnosis performed by the Organoleptic Test (OT), Halimeter™ (HT) and Breath Alert™
Discussion
This st udy aim ed t o access and com par e t he accuracy/ sensit ivit y of t wo port able devices and OT in non- halit osis com plainer subj ect s. Furt herm ore, it w as v er if ied w h et h er t h e com b in ed m et h od s used could enhance accuracy for clinical diagnosis of halit osis. The sam ple was com posed of halit osis’ non- com plainers since t hose w ho are unaware of t heir condit ion can have halit osis relat ed t o syst em ic diseases. I n addit ion, halit osis affect s individuals’
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of ut m ost im port ance requires special at t ent ion. Our result s dem onst rat ed t hat 62% out of t he 34 pat ient s present ed bad breat h wit h any com plaint or when inquired about odor breat h qualit y.
Body odor elicit s a great concern including oral odor. Hygiene and beaut y product s sales increased 12% bet ween 2002 and 2003 in Lat in Am erica. A
VLJQL¿FDQWLQFUHDVHLQWKH per capit a consum pt ion of WRRWKSDVWHWRRWKEUXVKPRXWKULQVHDQGGHQWDOÀRVV
has been est im at ed from 1992 t o 2002, respect ively at rat es of 38.3% , 138.3% , 618.8% and 177.2%10.
I n t his cont ext , t he general populat ion can easily pur chase som e inex pensive palm - sized m onit or s, such as Breat h Alert ™, t o quickly access odor breat h.
The levels of com pounds in exhaled m out h air
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m et abolic subst rat es in t he m out h. VSC has been considered t he m ain cont ribut or t o oral m alodor due t o t heir low odor det ect ion t hresholds and high odor power. However, m any other lower odor power organic com pounds are present in t he expired air, such as ket ones, fat t y acids, am ines, alcohols, aldehydes and hydrocarbons
I n som e cases, t he t hreshold levels are at t ained by only one of t he port able devices. I n such cases, m alodor can also be organolept ically det ect ed. Thus, t he sulphur m onit ors can indicat e t hat t here is no obj ect ionable m alodor in case of pseudo- halit osis or halit ophobia. I t is well est ablished t hat OT is t he “ golden m et hod,” but it m ust be m ent ioned t hat oganolept ic scores are oft en regarded as subj ect ive, especially by pat ient s wit h an uncert ain diagnosis.
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odor subgroup out of all odorant groups relat ed t o m alodor, it could be hypothesized that the assessm ent of m out h odor w it h bot h dev ices sim ult aneously could increase t he accuracy of port able m onit ors. Unfort unat ely, our result s were not able t o indicat e
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t he t est s was high ( 100% and 85% for HT and BA, respect ively) , and t he sensit ivit y was t oo low ( 33% and 24% for HT and BA, respect ively) for allowing an exam iner t o subst it ut e t he OT for eit her t he single or t he com bined use of HT and BA ( Table 1) , t hough HT
Halimeter™ Breath Alert™
Sensitivity (%) 33 24
6SHFL¿FLW\ 100 85
Accuracy 59 47
PPVa 100 71
NPVb 48 41
PLRc 0.33 1.44
AUC (95% CI)d 0.67 (0.48 to 0.85) 0.54 (0.34 to 0.74)
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Table 1- Diagnostic results of Breath Alert™ and Halimeter™ tests
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( Figure 2) .
Measurem ent validity is a critical factor of evidence-based pract ice t o assure t hat our assessm ent t ools provide us reliable inform at ion for decision- m aking. Diagnost ic t est should be execut ed only if it s result can change t reat m ent decisions22. I n t his st udy, t he
accuracy of HT and BA were bot h low ( Table 1) , which showed t hat none of t hem could be reliable for t he diagnosis of halit osis in t he st udied sam ple. When a diagnost ic t ool has high sensit ivit y, it s negat ive t est result will indicat e t he absence of t he abnorm al
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and t he t est result is posit ive, t he probabilit y of an abnorm al condit ion will be st rong.
The pr evalence of posit iv e halit osis diagnosis t hrough t he OT was m uch higher ( 62% ) t han HT or BA ( 21% ) ( Figure 1) . From t hose cases diagnosed
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out of 21 cases, while BA correct ly diagnosed 5 ( 24% ) posit ive cases ( Figure 2) . The m ean VSC value found for such seven cases wit h halit osis diagnosed t hrough HT alone were 137 ppb, being t he m inim um value 94 ppb and t he m axim um one 167 ppb ( dat a not shown) . From t he t ot al of HT posit ive result s, only t hree cases were in accordance wit h bot h OT and BA ( Figure 2) , and t he ppb value for t heir VSC were 167, 156 and 110 ppb ( dat a not shown) .
VSC have t he pot ent ial role of prom ot ing halit osis, though other volatile com pounds can also com prom ise t h e odor qu alit y of ex pir ed air, su ch as v olat ile sh o r t - ch a i n f a t t y a ci d s, p o l y a m i n es, a l co h o l s, phenyl com pounds, alkanes, ket ones and nit rogen com pounds20,21. However, little attention has been given
for the later above- m entioned volatile com pounds due t o t heir low volat ilit y. Thus, it is believed t hat t hose com pounds have lit t le influence in im pair ing t he qualit y of t he expired breat h. Alt hough in t his st udy pat ient s did not report any com plaint regarding t heir breat h odor, and t hat only seven pat ient s out of t he t ot al of 34 subj ect s ( 20.5% ) present ed VSC values great er t han t he cut off value ( 80 ppb) est ablished by t he m anufact urer, t he offensive sm ell was present in anot her m ore 14 pat ient s. Thus, 66% of t he halit osis diagnosed pat ient s in t his sam ple did not present VSC as t he m ain responsible for t he bad breat h. I n t his way, m ore at t ent ion should be paid in ot her volat ile com pounds as m ent ioned above.
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ERWK PHWKRGV +7 DQG %$ )LJXUH WKH ¿UVW RQH VKRZHGEHWWHUSHUIRUPDQFHDVUHÀHFWHGLQLWVDFFXUDF\
value ( 59% ) . However, not even t he HT was reliable enough t o be used alone. This device does not det ect several volat ile com pounds nor som e VSC found in halit osis, as previously discussed23, while t he OT is
able t o perceive all of t hem . Differences regarding t he presence of halit osis m easured by organolept ic t est , HT and BA have been also reported in recent studies13,
but usually t here is great posit ive correlat ion bet ween organolept ic scores and VSC values22.
OT is con sid er ed t h e g old st an d ar d f or t h e clinical diagnosis of halit osis5VLQFHLWUHÀHFWVKXPDQ
percept ion, and, t o dat e, only hum ans can j udge t he accept abilit y of t he m ixed odors em anat ing from t he m out h8. However, it has already been m ent ioned t hat
OT can t ransm it diseases t o t he operat or t hrough t he expelled air14. I n addition, the OT m ethod can constrain
both the patient and the judge once it requires sm elling ot hers’ exhaled breat h. Addit ionally, OT has been crit icized for it s subj ect ivit y level even aft er get t ing good result s in olfact ory capabilit y t est , and aft er a rigorous calibrat ion of exam iners6,24. I t also m ight be
affect ed by environm ent al condit ions. Besides t hose issues, t he exam iner m ust post pone t he exam inat ion in case of any sign t hat could prom ot e t heir olfact ory dist urbance, such as post- nasal drip, rhinit is, sinusit is or cold. Since t here is a preparat ion for halit osis assessm ent , t he need of post pone m ight cost and be tim e-consum ing for both patient and exam iner. Despite all the drawbacks, organoleptic m easurem ents are still t he gold st andard for assessing halit osis13.
Anot her pot ent ial use and developm ent of t hese t est s is t o det ect subclinical halit osis when offensive o d o r s ar e n o t d et ect ed b y ex am i n er o l f act i o n regardless of pat ient ’s com plaint . I n t hese cases, t here is already a low am ount of VSC or even ot her volat ile com pounds perceived by t he ret ronasal sense of sm ell of t he pat ient t hat addit ionally m ay lead t o clinical halit osis in t he fut ure. I n t his cont ext , new st udies should be conduct ed for t he est ablishm ent of t he am ount of VSC able t o cause what has been considered as subclinical halit osis. I n addit ion, t hese devices could also be used t o different iat e t ypes of halit osis relat ed t o great am ount of VSC ver sus ot her
volatile com pounds perceived in OT for clinical halitosis cases. These m ight help t o delineat e t reat m ent s in t he fut ure.
and result s were st raight forward and lim it ed, t hey do indicat e pot ent ial lim it at ions of bot h com m ercially available devices t est ed. During clinical pract ice, t he m ost useful t ool for int erpret ing diagnost ic t est s is t he likelihood rat ios, and values close t o 1 indicat e t hat t he t est does not provide m uch inform at ion9.
Thus, supposing HT w ould pr esent high posit iv e likelihood rat io, while BA would have high negat ive likelihood rat io or vice- ver sa, we could assum e t hat their associated usage would allow diagnosing halitosis effect ively. However, t his st udy showed t he com bined use of HT and BA was not a reliable t ool for halit osis diagnosis. Even t hough HT in conj unct ion wit h t he organolept ic t est has been considered an effect ive m et hod for diagnosing oral m alodor4, our result s did QRWVXSSRUWWKLV¿QGLQJ
Alt hough t he cost s of t hese devices are feasible in
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valid inform at ion t o be used in a diagnost ic cont ext . Thus, our dat a are in accordance wit h ot her st udies t hat have considered t he organolept ic t est t o be t he “ gold st andar d” clinical m et hod for det ect ing t he presence or absence of halit osis7,16,18,25. The need t o
develop a reliable clinical m et hod t hat can be used as a subst it ut e for t he organolept ic t est for halit osis det ect ion rem ains.
Conclusion
Consider ing t he design and draw back s of t his st udy, we conclude t hat t he m easurem ent of t he VSC levels det ect ed by port able devices can be used as an adj uvant t ool wit h OT in subj ect s wit hout m alodor com plaint . I n spit e of t he gr eat im pr ovem ent of such devices in t he last years, OT rem ains t he “ gold st andard” m et hod for t he diagnosis of bad breat h. I t is known t hat Halim et er™ and Breat h Alert ™ have
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yet . Hence, t hey are not reliable m et hods t o diagnose halit osis in non- com plainer pat ient s at t he sam e level as t he organolept ic exam inat ion. I n addit ion, t hey cannot be considered reliable even when t heir result s are gat hered and analyzed t oget her. Even t hough t he use of t he port able devices can lead t o a considerable num ber of negat ive r esult s, t heir value m ust be highlighted as an im portant tool for m alodor screening. Finally, t hese devices can be also very useful for
pat ient ’s follow- up and t o different iat e dist inct t ypes of halit osis, such as t hose caused by great am ount of sulphur com pounds from ot hers ( i.e. organic volat ile com pounds) .
Acknowledgem ent s
The aut hor s t hank t he Coor dinat ion of Higher
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scholarship received for the developm ent of this study.
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