Brazilian Journal of Oral Sciences Piracicaba Dental School - UNICAMP EISSN: 1677-3225 Vol. 10, Num. 2, 2011, pp. 88-92

Comparison of halitosis parameters andsialometry between patients subjected to headand neck radiotherapy and patients withperiodontal disease

Danielle Frota de Albuquerque¹, Elen de Souza Tolentino², Flávio Monteiro Amado³, Cazuo Arakawa⁴, Luiz Eduardo Montenegro Chinellato⁵

¹MSc in Stomatology, Department of Stomatology, Bauru Dental School, University of São Paulo, Brazil
²PhD student, Bauru Dental School, Department of Stomatology, University of São Paulo, Brazil
³PhD in Stomatology, Bauru Dental School, Department of Stomatology, University of São Paulo, Brazil
⁴ MD, Radiotherapy specialist, Department of Radiotherapy, Manoel de Abreu Hospital, Bauru, SP, Brazil
⁵PhD, Professor, Bauru Dental School, Department of Stomatology, University of São Paulo, Brazil

Correspondence to: Elen de Souza Tolentino Faculdade de Odontologia de Bauru-USP Departamento de Estomatologia Alameda Dr. Octávio Pinheiro Brisola, 9 - 75 Vila Universitária - CEP 17012-901 Bauru - SP - Brasil Phone: (14) 3235-8000 / Fax: (14) 3223-4679 E-mail: elen_tolentino@hotmail.com

Received for publication: January 28, 2011 Accepted: May 20, 2011

Code Number: os11018

Aim: The aim of this study was to evaluate halitosis parameters and sialometry in patients subjected to head and neck radiotherapy compared to patients with periodontal disease, establishing a relationship between oral concentration of volatile sulfur compounds (VSCs) and tongue coating presence, salivary flow rate and BANA_TM test.
Methods: Thirty-eight patients were examined and divided into 2 groups: group I: patients with chronic generalized periodontal disease previously diagnosed and not treated; group II: patients subjected to head and neck radiotherapy. All volunteers were subjected to halitosis measurements through a sulphide monitor, evaluation of tongue coating weight, stimulated and non-stimulated sialometry and BANA_TM test.
Results: The results were analyzed by analysis of the variance, Pearson's correlation coefficient and Students t-test, showing that both groups presented halitosis. There was also a relationship between tongue coating presence and VSC levels in both groups and the irradiated patients showed lower salivary flow rates.
Conclusions: Under the tested conditions, it may be concluded that halitosis can be considered as an adverse effect of radiotherapy, associated with low salivary flow and poor oral health, which seems to be the main contribution to bad breath, since patients with periodontal disease also showed halitosis.

Keywords: halitosis, radiotherapy, head and neck neoplasms, periodontitis.

Radiotherapy, alone or associated with surgery or chemotherapy, is the therapeutic method indicated in cases of oral cancer and has produced a significant increase in cure rates for several malignancies of the head and neck¹. The adverse effects of head and neck radiotherapy are very important for the dental surgeon, who has a key role in preventing and/or minimizing their occurrence. Salivary glands are radiosensitive and the atrophic and acinar degeneration caused by radiotherapy commonly result inreduction of the saliva production^2-5.

Halitosis is highly associated with the amount of saliva⁶. It has been shown a relationship between hyposalivation  and radiotherapy, as well as between halitosis and periodontal disease. However, the association among these variables is not well known. There is only one study which establisheda correlation between halitosis and head and neck radiotherapy, through evaluation of halitosis and sialometry in patients who had undergone radiotherapy when comparedto healthy and non-irradiated individuals⁷. Howsoever, there are no studies comparing halitosis between irradiated patients and patients with periodontal disease.

The aim of this study was to establish a correlation between halitosis and head and neck radiotherapy, through evaluation of halitosis and sialometry in patients who had undergone radiotherapy in comparison to patients with periodontal disease.

This study was approved by the Human Research EthicsCommittee of Bauru Dental School, University of São Paulo,Brazil (process #104/2005) and is in accordance with the Helsinki Declaration of 1975, revised in 1983. All volunteers signed an informed consent form. The sample was composedof 38 patients, divided into two groups: Group I: 13 patients from the screening sector of the Bauru Dental School , with generalized chronic periodontal disease previously diagnosed but not treated; Group II: 25 volunteers selected among patients from Manoel de Abreu Hospital, referenced for cancer treatment in the city of Bauru, SP, Brazil. The sample sizewas justified by the fact of many patients have not finished the radiotherapy treatment at the moment of the consultation and only volunteers with the treatment completed were included in the study. In Group I, patients with localized ortreated periodontal disease were excluded, which reduced the initial sample size. All patients were selected among apopulation of each Institution, both with spontaneous demand. Careful exam and screening of these patients according tothe exclusion and inclusion criteria led to the reduction of the sample; however, according to the statistician responsible for this study, the sample size was appropriated.

Patients of Group I presented periodontal pockets > 5mm in all molars and incisors, bleeding on probing andgeneralized vertical bone loss observed radiographically. The diagnosis of these patients was chronic generalizedperiodontal disease. Patients of Group II were subjected toradiotherapy as the main or complementary treatment of headand neck tumors. The radiation area covered at least one of the major salivary glands or part of them. The radiotherapy treatment of all patients had already been concluded andthey were under continuous monitored from 1 to 6 monthsafter the last radiotherapy session. It is important toemphasize that all patients of Group II were periodontally healthy, that is, they did not present bleeding on probing or periodontal pockets > 4 mm). Also, the sequelae of the radiotherapy treatment (e.g.: radiation caries and mucositis)were treated in the period between the radiotherapy and this research.

The management of the patients was similar to a previous study⁷. All patients underwent two appointments conductedby the same examiner. In the first one, the patients receivedsome guidelines for the procedures to be carried out in afurther moment: avoid spicy and/ or flavored food 24 h before the clinical appointment; avoid brushing the teeth, using dental floss, chewing gum, drinking alcoholic drinks and smoking 3 h before the clinical appointment and not being using perfume at the moment of the appointment.

The halimetry values in all individuals were obtained using a sulfide monitor (Halimeter; Interscan Corporation,Chatsworth, NJ, USA). Before measurements, patients werekept seated, relaxed and without talking for 1 min, with theirmouth closed. A disposable plastic tube connected to themonitor was introduced 4 cm inside the patient´s mouth⁷. The patients were instructed to leave their mouth slightly opened on the tube without inhaling or exhaling during the analysis. Those measures were taken three times, which resulted in a final average.

After removing the excess of humidity of the tonguewith gauze, the tongue coating was removed with a tonguecleaner and placed in a previously weighted filter paper.The material was stored for 24 h for drying and weighing.The tongue coating weight was obtained using a digitalprecision scale (A&D System Co., Ltd. Tokyo, Japan).Immediately after removing the tongue coating, halimetrywas performed again, in order to identify possible variationsin the VSCs concentrations⁷.

The test was performed to identify a possible relationbetween the presence of microorganisms BANA positive andthe values of halimetry. A small amount of tongue coatingwas collected and transferred to the BANA test strip(BANAMet LLC, Ann Arbor, MI, USA). A drop of distilled water was poured on the reagent strip, which was folded and kept this way with a paperclip, so that the reagent would bein contact with the organic material, left undisturbed for 24h, as indicated by the manufacturer. After that period, thereaction was noted and the result obtained, classified as negative and positive, according to the obtained color⁷.

After remaining 5 min at rest, with the eyes opened, without stimulating salivation, each patient spit out all salivaobtained in that period in a recipient graded in millimeters(mL) to obtain the non-stimulated salivary flow. After this procedure, each patient was given a piece of sterile hyperboloid which was used to stimulate salivation through mastication for 5 min, and the saliva obtained was also placed in a recipient graded in mL to obtain the stimulated salivary flow⁷.

The radiotherapy treatment protocol was the same forall patients of Group II. All selected patients have had atleast one of the major salivary glands involved in the areaof radiation and the protocol of radiotherapy was the same used in the patients of a previous study⁷.

The results were analyzed by ANOVA and Tukey' s for the variables that quantified halitosis before and after removing tongue coating. The relationship among oral halimetry, dry weight of tongue coating and stimulated/nonstimulated salivary flow rate were analyzed by Pearson's correlation test. Student's t-test was used to verify the correlation between halimetry and BANA test. A significance level of 5% was used for all analyses. The computer software used was Microsoft Office Excel 2007.

Group I presented lower initial halimetry average (148.102 ppb) when compared to Group II (143.747 ppb),with no statistically significant difference (Table 1). The dryweight of tongue coating in Group II (0.016mg) was smaller than in Group I (0.0245 mg), but this difference was not significant (Table 1). Group II showed a decrease in salivary flow, in stimulated and non-stimulated sialometry, with a statistically significant difference (p<0.001) (Table 1).

In the evaluation of the correlation between the studied variables and halitosis, in Group I this correlation was notedbetween initial halimetry and presence of tongue coating(p=0.012) and between initial and final halimetry(p<0.001) (Table 2). Group II, showed a significantcorrelation between initial halimetry and presence of tonguecoating (p=0.043), between initial and final halimetry(p<0.001) and between stimulated and non-stimulated salivary flow (p<0.001) (Table 3).

In both groups, the number of negative BANA_TM tests (n=25) was greater than the positive results (n=23), with astatistically significant difference among the negative andpositive results and halimetry in Group I (p=0.017) and when the entire sample was analyzed together (p=0.003)(Table 4).

Discussion

Regarding oral halimetry, Group I presented lower initialaverage when compared to Group II (Table 1), but withoutstatistically significant difference. However, in the present study, the use of the sulfide monitor enabled the evaluationonly of the relation between VSCs and halitosis. This is alimitation of methodology since bad breath is caused byother volatile organic compounds and other gases⁸.

Final halimetry was performed soon after tonguecleaning. A previous study⁷ demonstrated that the values of halimetry can decrease substantially immediately after thetongue cleaning. It is known that tongue coating is animportant etiological factor of halitosis⁹. Waler¹⁰ showed that the largest production of VSCs is in the tongue dorsum.Yaegaki and Sanada¹¹ reported that removing tongue coatingreduced by 50% the production of VSCs. Albuquerque etal.⁷ found a relationship between presence of tongue coating and VSCs levels, with a decrease in the values of halimetry after removing tongue coating. Boever and Loesche¹² noticed that the score of oral breath was highly connected to theodor of the tongue, presence and extension of coating. In this work, the values of initial halimetry were greater than final halimetry in both groups. However, there was nostatistically significant difference (Table 1). Since the tongue cleaner shows a higher percentage of reduction of VSCs than the tooth brush¹³, it justifies the use of this tool in the methodology of this research. In our study, the amount oftongue coating was evaluated quantitatively after drying, confirming methodologies used by other studies^7,11,14. The dry weight of tongue coating in patients with periodontal disease was greater than in the irradiated patients, but the differencewas not statistically significant. This finding is a little surprising because it is well established that the tongue coating is a resultof the hypossalivation⁷. Salivary reduction provides theimplantation of the tongue coating because the saliva becomesmore viscous, with higher amounts of mucin, increasing theadherence of microorganisms and epithelial debris in the tongue.As the bacteria present in the tongue coating and in theperiodontal pockets are similar (anaerobic proteolytic),colonization of the tongue can be favored in patients with periodontal disease. However, it does not explain the higheramounts of tongue coating in Group I than in Group II, sinceirradiated patients have an outstanding decrease in salivary flow,the main etiological factor of tongue coating. Perhaps the poor hygiene, which is common in patients with periodontal disease, can explain this finding of the present work.

Regarding salivary flow, there was significant difference between the groups in stimulated and non-stimulatedsialometry (Table 1). All patients in Group II showed a decrease in the amount of saliva. The value of 0.1 mL/minfor salivary flow without stimulus was considered severe glandular hypofunction. There was a decrease in sialometry without stimulus from group II of 66.03% compared to Group I. Albuquerque et al.⁷ found a decrease in sialometry without stimulus in irradiated patients of 56.51% when compared to healthy patients.

In Group I, correlation between the studied variablesand halitosis was noted between initial halimetry and presenceof tongue coating and between stimulated and non-stimulated salivary flow (Table 2). In group II, a significant correlation was observed between initial and final halimetry, between initial halimetry and presence of tongue coating and between stimulated and non-stimulated salivary flow (Table 3).

The BANA_TM test - an enzymatic method used as anindicator of the presence of microorganisms responsible forperiodontal diseases - was performed in Groups I and II.Similarly to a previous study⁷, in both groups the number ofnegative tests was greater than positive results. In Table 4, itis noted that there was a significant difference among thenegative and positive results and halimetry in Group I andwhen the entire sample was together. Some authors have notnoted relation between the levels of VSCs and the results of lingual BANA_TM test¹⁵. According to Monteiro-Amado et al.¹⁴, there is not a relation between the value of BANA_TM test and the values of halimetry.

Irradiated patients did not have main complaint of halitosis. However, when they were questioned about oralbad breath, the majority answered that felt it. Patients withperiodontal disease did not ask for treatment of halitosis,but they had complaints of bad breath and presentedindication for periodontal treatment.

According to Conceição et al.¹⁶, halimetry above 100ppb can be considered as halitosis. In this study, all evaluated patients, of both groups, presented halitosis, since the valuesof initial and final halimetry were greater than 100 ppb. However, there was no statistically significant difference between the groups, confirming the fact that the oral health condition is an important etiological factor of halitosis, andbad breath is strongly associated with periodontal disease. It is known that saliva incubation of patients with periodontal disease produces VSCs quickly, inducing an intense bad breath. The saliva of these patients produces more VSCs thanthe saliva of healthy people. Halitosis may occur in anyindividual, but it is emphasized when inflammatory anddegenerative processes are present. For example, gingivitis and periodontitis are almost always associated with halitosis,which corroborates the findings of the present study.

The present work is a continuation of a previous study,which detected halitosis and hyposalivation in irradiated patients when comparing them with healthy people⁷. It is believed that the comparison of periodontally healthy irradiated patients, which recognizably have halitosis,) andpatients with periodontal disease can show the true degreesof halitosis in each group as well as demonstrate that both conditions play important roles in bad breath development.

It is known that hyposalivation is a definitive sequel ofhead and neck radiotherapy and that this condition plays a key rule in halitosis pathogenesis⁶. We believe that the significant reduction in the amount of saliva is the most important parameter in the bad breath development inirradiated patients, since, in this research, they had asatisfactory oral condition. On the other hand, the significant differences among the negative and positive results and halimetry of the BANA_TM tests in Group I show the substantial role of periodontopathogenic microorganisms in the development of halitosis in patients periodontally affected. Additionally, despite the lack of statistical significance, the dry weight of tongue coating in Group I was greater than in Group II, showing a close relationship between periodontitis and tongue coating, since the bacteria that colonize the tongueand periodontal pockets are the same. For these reasons, we agree that the most expressive factors that influence thehalitosis formation in patients with periodontal disease aretongue coating and presence of periodontopathogenic microorganisms.

Summarizing our findings, halitosis was detected inpatients with periodontal disease and patients subjected tohead and neck radiotherapy and that there was relation betweenpresence of tongue coating and VSCs levels in the studiedgroups. There was a significant decrease in the values of halimetry after removing tongue coating in both groups. Also, stimulated and non-stimulated salivary flow was extremelyreduced in irradiated patients. According to the results obtained under the tested conditions, it is possible to conclude that halitosis is an adverse effect of head and neck radiotherapy and is strongly associated with periodontal disease.

The authors would like to thank Professor José Roberto Lauris for the support in the statistical analysis of this study.This investigation was supported by CAPES.

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