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 Table of Contents  
ORIGINAL ARTICLE
Year : 2013  |  Volume : 9  |  Issue : 4  |  Page : 630-637

Assessment of periodontal changes in patients undergoing radiotherapy for head and neck malignancy: A hospital-based study


1 Department of Periodontics, Government Dental College, Calicut, India
2 Department of Oral Pathology and Microbiology, Government Dental College, Trivandrum, India
3 320 Fd Hospital 99 APO, Kerala, India

Date of Web Publication11-Feb-2014

Correspondence Address:
Rafeek Rahim Ammajan
Department of Periodontics, Government Dental College, Calicut, Kerala
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0973-1482.126461

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 > Abstract 

Background: Surgical resection, radio and chemotherapy, either used singly or in combination, are the three most common modalities used in head and neck cancer treatment. These modalities are effective in eradicating the tumor; they also negatively impact the normal head and neck structures surrounding the tumor. Direct damage to the oral structures (soft and hard tissue) frequently occurs from radio and chemotherapy, and indirect damage may also arise from systemic toxicity.
Materials and Methods: This prospective study was designed to analyze the effect of radiotherapy on periodontal parameters in oncology patients prior to irradiation in the head and neck area, compared with 6 months following treatment. The statistical analysis was done using SPSS.
Results: The study sample consisted of total 29 patients of head and neck malignancy (M = 17, F = 12), of mean age 45.66 years. Only 22% of patients had various habits (smoking, tobacco chewing, and alcohol consumption) and majority (27.59% patients) had tongue malignancy. All periodontal parameters - oral hygiene index Siller (OHIS), clinical attachment level (CAL), gingival recession (GR), except probing pocket depth (PPD) - were significantly increased after radiotherapy. When comparison was made between doses and fractions, only in mandible statistically significant difference were observed in GR.
Conclusion: Although there was no significant change in PPD, there was increased GR, CAL, and plaque index associated with radiotherapy. In this study, 61.5% cases of mandibular teeth and 34.4% cases of maxillary teeth showed attachment loss greater than 0.2 mm. So, all patients with head and neck malignancy should undergo an oral examination before the initiation of cancer therapy with adequate prophylaxis.

Keywords: Head and neck malignancy, periodontal therapy, radiation therapy


How to cite this article:
Ammajan RR, Joseph R, Rajeev R, Choudhary K, Vidhyadharan K. Assessment of periodontal changes in patients undergoing radiotherapy for head and neck malignancy: A hospital-based study. J Can Res Ther 2013;9:630-7

How to cite this URL:
Ammajan RR, Joseph R, Rajeev R, Choudhary K, Vidhyadharan K. Assessment of periodontal changes in patients undergoing radiotherapy for head and neck malignancy: A hospital-based study. J Can Res Ther [serial online] 2013 [cited 2018 May 27];9:630-7. Available from: http://www.cancerjournal.net/text.asp?2013/9/4/630/126461


 > Introduction Top


Cancer is currently the cause of 12% of all deaths worldwide and is a significant global health problem with more than 10 million new cases and 6 million deaths each year worldwide. [1],[2] Among them, head and neck neoplasia (HNN) is a major form of cancer in India, accounting for 23% of all cancers in males and 6% in females; the 5-year survival varies from 20% to 90% depending upon the sub-site of origin and the clinical extent of the disease. [3] Surgical resection, radio- and chemotherapy, either used singly or in combination, are the three most common modalities used in head and neck cancer treatment. Although these modalities are effective in eradicating the tumor, they also negatively impact the normal head and neck structures surrounding the tumor. Radiation therapy has cytotoxic effects on both normal cells and malignant cells. Direct damage to the oral structures (soft and hard tissue) frequently occurs from radio- and chemotherapy, and indirect damage may also arise from systemic toxicity. These oral complications may occur during and following cancer therapy and are generally grouped into two broad categories: acute and chronic. [4]

The reported acute oral complications are mucositis, xerostomia, dysphagia, dysguisia, and opportunistic infections, and chronic complications such as trismus, irradiation caries, osteoradionecrosis, and changes in periodontal attachment. The long-term effects include alteration in vascularity of soft tissue and bone, salivary gland damage, reduction in cellularity of connective tissue, and risk of increased collagen synthesis which results in fibrosis. [5]

Radiation treatment induces obliterative endarteritis that result in the soft tissue ischemia and fibrosis while the irradiated bone become hypovascular and hypoxic. [6]

The peridontium is sensitive to the effect of radiation at high doses. Decreased vascularity and cellularity of the periodontal membrane with rupturing, thickening, and disorientation of Sharpey's fibers and widening of periodontal space have been reported. [7] The direct and indirect effect of high-dose radiotherapy (RT) on the periodontium results in an increased risk of periodontal attachment loss and tooth loss and even an increased risk for the development of osteoradionecrosis. [8],[9] The rampant periodontal destruction may occur in the absence of good oral hygiene.

Periodontitis in patients scheduled for head and neck RT results in acute and chronic complications such as osteoradionecrosis. Maintenance of good oral hygiene in patients undergoing RT may reduce morbidity of the known oral and periodontal side effects. Patient scheduled to receive the head and neck radiation therapy require dental consultation at the earliest possible time. Pre-irradiation treatment depends on patient prognosis, compliance, and residual dentition, in addition to fields, ports, dose and, immediacy of RT. The purpose of the study was to evaluate changes in peridontium in patients receiving radiation therapy for head and neck malignancy.


 > Materials and Methods Top


This prospective study was designed to analyze the effect of RT on periodontal parameters in oncology patients prior to irradiation in the head and neck area compared with 6 months following treatment. The study population consisted of 29 dentate patients with malignant neoplasm in head and neck region. The study was conducted during the period 2 May 2007 to 24 October 2007 in Department of Periodontia, Government Dental College, Calicut, Kerala, India. Also, patients were recruited from Radiotherapy Department, Medical College, Calicut. All patients who agreed to participate in the dental examination signed informed consent forms. The study was approved by Institutional Ethics Committee.

The mode of RT consisted of external beam radiation by megavolt machine following the conventional scheme of high dose fractions. RT alone or as an adjunct to surgery or chemotherapy was also considered. The area of administration of RT are considered as maxilla alone, mandible alone, whole of maxilla and part of mandible, and whole of mandible and most of the maxilla. All patients were evaluated using a detailed questionnaire. The dental treatment planning and procedures were carried out according to individual patient requirement. Prior to RT, the periodontal examination was done and necessary extraction was carried out. A traumatic extraction of periodontally compromised teeth was done before 6 weeks of therapy.

Patients undergoing RT were selected based on type of tumor, site, irradiation dose, and irradiation field. Patients included for study were: Dentate patients ≤60 years without any systemic conditions causing periodontal changes; those with primary malignancy; and patients with no history of any periodontal treatment in the past 6 months. Patient undergoing RT for the secondary malignancy, tooth with poor prognosis (periodontal attachment loss greater than 8 mm, caries, or non-restorable teeth), patient who had undergone periodontal therapy within 6 months duration, and patients with diabetes mellitus were excluded from the study. The general examination include gender, age, smoking, pan chewing, alcohol consumption, family history, oral hygiene practices, type of neoplasm, and area of irradiation. The RT data including dosage, radiation fields, number of fractions of radiation, and associated therapy were recorded in the Performa.

Statistical analysis

Periodontal data were collected from computing the mean in millimeters of each tooth from four probed sites (mesial, distal, buccal, and lingual/palatal). The sum of means of each tooth was divided by the number of teeth examined to obtain the mean of each parameter. The different periodontal parameters measured before and after RT include probing pocket depth (PPD), clinical attachment level (CAL), gingival recession (GR), bleeding on probing (BOP), and oral hygiene index Siller (OHIS).

The other data obtained from patients' files from RT department includes gender, age, socioeconomic status, education, history of systemic illness, family history of malignancies, oral hygiene practices, site of neoplasm, associated therapies, dosage and fraction of radiation, and area of irradiation.

The obtained periodontal data were subjected to statistical analysis and correlated with dosage, fraction of radiation, and area of irradiation. The statistical analysis was done using SPSS 13 for windows SPSS INC Chicago IL program.

The initial and final periodontal parameters were based on means, using paired t-test for continuous variables. P values <0.05 were considered statistically significant.

The correlation frequencies were developed using the cutoff 0.2 mm. The patients were grouped into those with loss of <0.2 mm and those with loss of >2 mm. We used the Pearson Chi-square test in double entry contingency tables, replacing it with Fisher's exact test whenever needed.


 > Results Top


The present study consisted of totally 29 patients (17 males and 12 females) with a mean age of 45.66 years. Only 22% of patients had various habits (smoking, tobacco chewing, and alcohol consumption). The tumor site in the study population is shown in [Figure 1]. Majority (27.59%) of the patients had tongue malignancy. Therapy associated with radiation and direction of radiation is shown in [Table 1], [Table 2]a and b, respectively. Radiation doses and fraction are shown in [Table 3] and [Table 4], respectively. Change (mm) in periodontal parameters in maxillary (n = 29) and mandibular (n = 26) teeth were examined prior to (1) and following RT (2) using paired t-test. All periodontal parameters [OHIS, calculus index (CAL), and GR] except PPD were significantly increased after RT [Table 5]. The correlation of radiation dosage with difference in periodontal parameters in maxilla and mandible did not reach statically significant values [Table 6] and [Table 7] when correlation of radiation fraction with difference in periodontal parameters in maxilla and mandible was assessed [Table 8] and [Table 9]. There was a statistically significant correlation between GR in mandibular teeth and the radiation fractions applied (P value 0.048 < 0.05).
Figure 1: Distribution of tumor sites

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Table 1: Therapies associated with radiation

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Table 2:

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Table 3: Radiation dosage

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Table 4: No of fractions

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Table 5: Change (mm) in periodontal parameters when maxillary (n = 29) and mandibular (n = 26) teeth were examined prior to (1) and following radiotherapy (2) using paired t-test

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Table 6: Correlation* of radiation dosage with difference in periodontal parameters in maxilla

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Table 7: Correlation* of radiation dosage with difference in periodontal parameters in mandible

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Table 8: Correlation* of radiation fraction with difference in periodontal parameters in maxilla

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Table 9: Correlation* of radiation fraction with difference in periodontal parameters in mandible

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{Figure 1}


 > Discussion Top


Diseases of teeth and supporting structures are a worrisome finding in a patient about to undergo tumoricidal RT for a malignant condition in the maxillofacial region because oral pain and infection are common and a potentially serious sequence to RT for head and neck tumors in patients with healthy mouth. The loss of integrity of the gingival crevicular tissues, as a result of periodontitis and RT induced thinning of these tissues together with xerostomia, mucositis, altered diet, and poor oral hygiene that often follow high-dose RT to the jaws, can create oral problems that affect the quality of life, which can cause interruption to cancer therapy. [10],[11]

Blood vessels in the periodontium are affected leading to widening of periodontal ligament space and destruction of bony trabeculae. These changes may result in increased risk of periodontal disease and altered healing with impaired capacity for bone remodeling and repair. [12]

The present study was conducted as a prospective clinical trial assessing progression of periodontal attachment loss at 6 months intervals for patients undergoing RT of head and neck tumors.

A total of 30 patients were recruited in the study who were undergoing RT for head and neck tumors; 6 months after RT 29 patients turned up for follow-up examination. The age of patients recruited for this study ranged from 22 to 60 years, with a mean age of 45.66 ± 9.6 years. The study population comprised 17 (58.6%) males and 12 (41.4%) females.

Oral hygiene habits in these cases were evaluated by recording oral hygiene method, frequency, and the material used. Oral hygiene status of the patient was examined using OHIS index by Green and Vermillion, prior to RT (mean of 3.13 mm) and 6 months after RT (mean of 3.38 mm). They were analyzed using paired t-test. The test showed a statistically significant correlation for OHIS before and after RT.

The increase in OHIS score may be due to hyposalivation and poor oral hygiene maintenance by patients during and after the course of RT. Anxiety or lack of physical and emotional motivation as well as decreased salivary flow and trismus are the other important factors in making oral hygiene more difficult. Plaque control in irradiated patients is necessary to prevent colonization of microorganisms in the gingival crevice.

Llory et al. in 1972 showed a radiation-induced downshift of periopathogens. [13] Markitziu et al.[14] in 1992 and Leung et al.[15] in 1998 reported the risk of periodontal infection is also increased due to radiation-induced hyposalivation and a concomitant increased plaque accumulation and shift in oral micro flora. This may explain the increased plaque rates in our study.

In this study, the PPD was calculated; for maxillary teeth, the mean PPD was 3.16 mm and for mandibular teeth, the mean PPD was 2.97 mm at baseline, and 6 months after RT, mean values of 3.13 mm for maxillary teeth and 3 mm for mandibular teeth were obtained. The paired t-test was used for analysis and no statistical significance was found.

Shwarze et al. in 1999 found a higher number of shallow periodontal pockets in radiated patients. [16] There is no statistically significant increase in PPD in this study, which does not indicate that there is improvement in clinical gain or stability of periodontal attachment. This may be due to increase in GR resulting in greater loss of periodontal attachment. The reduced PPD does not indicate the histological pocket depth since the probe normally penetrates coronal level of junctional epithelium due to inflammation of underlying connective tissue or may be due to disparity between probing technique, probing force, or angle of insertion of the probe.

The mean GR scores obtained in this study were 0.54 mm and 0.59 mm for maxillary and mandibular teeth, respectively, at baseline. Six months after RT, the mean scores obtained were 0.68 mm and 0.9 mm for maxillary and mandibular teeth, respectively. These results showed statistical significance when analyzed using a paired t-test.

The increased GR observed after RT may be due to changes in vascularity and cellularity of periodontal ligament and hypovascular, hypocellular, and hypoxic changes in alveolar bone. Rampant periodontal destruction may occur in the absence of good oral hygiene. The GR associated with RT is mainly due to reduction in gingival blood flow and alteration in immune response. The GR represents loss of attachment, which is an indicator of disease progression.

Toljanic et al. in 1984 reported gingiva is sensitive to irradiation, and also reported increased GR even without signs and symptoms of periodontal inflammation, perhaps due to the hypovascularity induced by irradiation. [17]

Epstein et al. in 1994 showed periodontal attachment loss in patients after head and neck RT. [12] Their results showed GR of 1.8 mm in facial aspects and 2.1 mm in lingual aspects of irradiated teeth for a span of 6.01 years.

The exposed root surfaces due to GR are susceptible to caries, abrasion, or erosion. The cementum exposed by recession leaves an underlying dentinal surface that can be sensitive. Hyperemia of the pulp and associated symptoms may also result from excessive exposure of the root surface.

The mean CAL values were assessed and found to be 3.66 mm for maxillary teeth and 3.61 mm for mandibular teeth before RT and 3.81 mm and 3.89 mm for maxillary and mandibular teeth, respectively, 6 months after RT.

Machtei et al. in 1993 showed a 0.2 mm annual loss of clinical attachment in patient with established periodontitis. [18] In this study, we set a 0.2 mm mark to separate the patients into two groups with attachment loss greater than0.2 mm and below it.

In this study, 61.5% cases of mandible (16 out of 26 cases) showed mandibular attachment loss and 34.4 maxillary cases showed clinical attachment loss greater than 0.2 mm. In the study sample, 20% cases (6) in mandible and 15% cases (4) in maxilla did not show clinical attachment loss.

Epstein et al. in 1998 found that increased attachment loss occurs over time in the teeth treated for RT of head and neck or intraoral cancers. [9]

Yusuf and Bakri in 1993 showed that direct and indirect effects of high-dose RT on the periodontium result in increased risk of attachment loss and bone loss, and even an increased risk for development of osteoradionecrosis. [8]

Twenty-two patients showed at least 20% bleeding sites on probing during the initial examination, and 6 months after RT, 19 patients showed at least 20% bleeding sites. There is decrease in bleeding on probing compared to initial examination. This may be due to hypocellularity and hypovascularity caused by radiation.

Markitziu et al. in 1992 reported low bleeding rates in irradiated area despite a high plaque index. [14]

A study by Marques in 2004 showed no statistical significance between plaque and bleeding on probing index in initial and final examination, but a tendency toward lower percentage of bleeding site in mandible. [19]

The dosage and fraction of radiation were categorized into two groups by dividing dosage into ≤4000 cGy and ≥4000 cGy and fraction into ≤20 fractions and≥20 fractions, and then compared with mean difference of PPD, CAL, and GR in both maxilla and mandible before and 6 month after RT. The relationship was correlated using Fisher's exact test, and all the tests did not show statistical significance except GR in mandible to fraternization of radiation, and PPD and dosage showed no relation.

Studies by Epstein [20] and Yusuf and Bakri [8] showed that direct and indirect effects of high dose of RT on periodontium resulted in increased attachment loss.

Marx et al. in 1987 reported that generally increasing the doses of irradiation above 7000 rad increased dose rates (fractions >200 rad/day), implant sources, neutron beam, concomitant surgery, concomitant chemotherapy or hyperthermy, and the risk and severity of osteoradionecrosis. [21]

Marciani et al. in 1992 reported that dosage can indicate potential irradiation injury. [22] Smaller irradiation doses administered at higher dose rates may be more injurious than higher doses dispensed at lower dose rates.

Marques et al. in 2004 stated that RT may contribute to a greater or lesser degree to progression of attachment loss. [19] In patients with irradiation restricted to cervical field (excluding maxilla), there was no attachment loss to maxilla and loss was greater when maxilla was directly irradiated. They concluded that irradiation may be a factor responsible for more extensive attachment loss, related to anatomic site of irradiation.

Our results are in accordance with the results of the study conducted by Marques et al. in 2004. [19] Also, our study is the second only in English literature on this topic, to the best of our knowledge, after Marques et al.'s study in 2004. [19] Yet, no other study has been published.

The post-radiation questionnaire included patient reporting complications like mucositis, sensitivity, difficulty in swallowing, pain in tempero- mandibular joint TMJ, xerostomia, and dental caries. 68.9% experienced mucositis, 44.8% had sensitivity of teeth, 17.2% had xerostomia, 20.6% had dental caries 24% reported having difficulty in swallowing, and 13.7% had pain in TMJ.

Oral mucositis is the most distressing of all the complications following head and neck RT. [23] Damage to oral mucosa is strongly related to radiation dose, fraction size, volume of irradiated tissue, fraternization scheme, and type of ionizing radiation. The acute mucosal response to RT is a result of mitotic death of epithelial cells, since the cell cycle time of the basal keratinocytes is about 4 days. [23]

The GR may lead to sensitivity, dental caries, and difficulty in maintenance of oral hygiene.

Xerostomia results from inflammatory and degenerative changes of ionizing radiation on the salivary gland parenchyma, especially serous acinar cells. Xerostomia has the potential to affect mastication, speech, and patients' overall quality of life. [23]

Difficulty in swallowing is encountered because the reduction in salivary flow diminishes lubrication and liquefaction of food, and irritation of mucosa makes chewing painful. Irradiation also causes fibrosis and atrophy of muscles in the pharynx.

The increased rate of caries may be due to the indirect effect of radiation caused by reduced salivary flow rate and its related consequences.

The pain in TMJ may be due to edema, cell destruction, and fibrosis resulting from radiation. Limited mouth opening complicates oral hygiene procedures and provision of dental care. [23]

Anxiety or lack of physical and emotional motivation, as well as decreased salivary flow, trismus, and other important factors make oral hygiene more difficult and accelerate loss of attachment.

The presence of microorganisms associated with these dental diseases increases the probability of compromised bones being infected.

Plaque control in irradiated patients is necessary to prevent colonization of microorganisms in the gingival crevice. Altered nature of microorganisms and reduced host defense mechanism toward plaque caused by RT may lead to attachment loss.

There is a need for more carefully controlled studies for definitive guidelines for management of dental structures in the field of irradiation.

In the present study, the periodontal parameter evaluation was done in a short period of time. A larger sample and long-term evaluation are needed for determining the effects of radiation on peridontium accurately.

The periodontist is an important member in the oncological team as increased oral hygiene maintenance can lead to reduction in post-radiation complications of peridontium.

In our study, it is observed that there are radiation-related changes in the oral and periodontal tissues. We observed an increase in GR and clinical attachment loss in patients who underwent RT.

As PPD did not increase in our study population, this can be explained on the basis on a review presented by Delanian et al. in 2004. [24] According to the authors, schematically, three successive clinical and histopathologic phases can be distinguished: a pre-fibrotic specific inflammatory phase, a constitutive fibrotic cellular phase, and a matrix densification and remodeling phase, possibly ending in terminal tissue necrosis. A fibroblastic stromal hypothesis is suggested revolving around a "gravitational effect" exerted by the couple reactive oxygen species (ROS) fibroblasts, and partly mediated by transforming growth factor (TGF)-b1. A variety of strategies have been tested for the management of radiation-induced fibrosis (RIF). In the light of the mechanisms described, a curative procedure has been proposed via the antioxidant pathway. In particular, it was shown that superoxide dismutase and combined pentoxifylline-tocopherol treatment enable the process of established radiation-induced fibroatrophy to be greatly reduced or even reversed, both in clinical practice and in animal experiments. The efficacy of combined pentoxifylline-tocopherol treatment in superficial RIF was confirmed in a randomized clinical trial, and then in successful phase II trials, especially in uterine fibroatrophy and osteoradionecrosis. It is of critical importance to evaluate these new management approaches in larger clinical trials and to improve the recording of results for better outcome analysis. They also suggested that mechanistic studies are always necessary to improve the understanding of the RIF process and the antifibrotic drug action. [24] As fibroblasts are the major cellular components of the periodontal tissue, adverse effect of radiation on fibroblast will definitely alter the periodontal health, which may represent as fibrotic changes and GR and clinical attachment loss. Even we did not use this therapeutic approach in the present study. But from the above-mentioned discussion, it is clear that oral hygiene maintenance measure with pentoxifylline-tocopherol administration can give better outcome in maintenance of periodontal health during and after RT. Furthermore, based on this study, we give the strong recommendation that dental treatment should be aimed at improving the oral hygiene status of patients through professional dental care. Patients should be constantly motivated toward maintaining a meticulous oral hygiene status before, during, and after RT to prevent and control the oral and periodontal sequelae.


 > Conclusion Top


In this prospective clinical trial, a total of 29 patients undergoing RT for head and neck malignancy were examined before and 6 months after RT. From our study it was found that there are highly significant changes in periodontal parameters following RT. Although there is no significant change in PPD, there is increased GR, CAL, and plaque index associated with RT. In this study, 61.5% cases of mandibular teeth and 34.4% cases of maxillary teeth showed attachment loss greater than 0.2 mm. So, all patients with head and neck malignancy should undergo an oral examination before the initiation of cancer therapy. Treatment of pre-existing oral disease is essential in minimizing oral complications in such patients. Periodontists have an important role in identifying and preventing oral and periodontal sequelae associated with cancer therapy and they help the patients to lead a better quality of life.

Kindly add name of A. Sudhakaran, former head of radiotherapy department, medical college, Calicut, Kerala, India.

 
 > References Top

1.World Health Organization. The World Health Report 2004: changing history. Geneva: WHO; 2004.  Back to cited text no. 1
    
2.Petersen PE. Oral cancer prevention and control--the approach of the World Health Organization. Oral Oncol 2009;45:454-60.  Back to cited text no. 2
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3.Mehrotra R, Singh M, Gupta RK, Singh M, Kapoor AK. Trends of prevalence and pathological spectrum of head and neck cancers in North India. Indian J Cancer 2005;42:89-93.  Back to cited text no. 3
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4.Hancock PJ, Epstein JB, Sadler GR. Oral and dental management related to radiation therapy for head and neck cancer. J Can Dent Assoc 2003;69:585-90.  Back to cited text no. 4
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5.Dreizen S, Daly TE, Drane JB, Brown LR. Oral complications of cancer radiotherapy. Postgrad Med 1977;61:85-92.  Back to cited text no. 5
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6.Marx RE. Osteoradionecrosis: a new concept of its pathophysiology. J Oral Maxillofac Surg 1983;41:283-8.  Back to cited text no. 6
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7.Silverman S Jr, Chierici G. Radiation therapy of oral carcinoma. I. Effects on oral tissues and management of the periodontium. J Periodontol 1965;36:478-84.  Back to cited text no. 7
    
8.Yusof ZW, Bakri MM. Severe progressive periodontal destruction due to radiation tissue injury. J Periodontol 1993;64:1253-8.  Back to cited text no. 8
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9.Epstein JB, Lunn R, Le N, Stevenson-Moore P. Periodontal attachment loss in patients after head and neck radiation therapy. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1998;86:673-7.  Back to cited text no. 9
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10.Marx RE, Johnson RP. Studies in the radiobiology of osteoradionecrosis and their clinical significance. Oral Surg Oral Med Oral Pathol 1987;64:379-90.  Back to cited text no. 10
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11.Wescott WB. Dental management of patients being treated for oral cancer. CDA J 1985;13:42-7.  Back to cited text no. 11
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12.Epstein JB, Corbett T, Galler C, Stevenson-Moore P. Surgical periodontal treatment in the radiotherapy-treated head and neck cancer patient. Spec Care Dentist 1994;14:182-7.  Back to cited text no. 12
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13.Llory H, Dammron A, Gioanni M, Frank RM. Some population changes in oral anaerobic microorganisms, Streptococcus mutans and yeasts following irradiation of the salivry glands. Caries Res 1972;6:298-311.  Back to cited text no. 13
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14.Marciani RD, Ownby HE. Treating patients before and after irradiation. J Am Dent Assoc 1992;123:108-12.  Back to cited text no. 14
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15.Leung WK, Jin LJ, Samaranayake LP, Chiu GK. Subgingival microbiota of shallow periodontal pockets in individuals after head and neck irradiation. Oral Microbiol Immunol 1998;13:1-10.  Back to cited text no. 15
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16.Schwarz E, Chiu GK, Leung WK. Oral health status of southern Chinese following head and neck irradiation therapy for nasopharyngeal carcinoma. J Dent 1999;27:21-8.  Back to cited text no. 16
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17.Susen JY, Myers EN. Cancer Of Head and Neck. ???: Churchill Living stone; 1981.  Back to cited text no. 17
    
18.Machtei EE, Norderyd J, Koch G, Dunford R, Grossi S, Genco RJ. The rate of periodontal attachment loss in subjects with established periodontitis. J Periodontol 1993;64:713-8.  Back to cited text no. 18
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19.Marques MA, Dib LL. Periodontal changes in patients undergoing radiotherapy. J Periodontol 2004;75:1178-87.  Back to cited text no. 19
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20.Epstein JB, Stevenson-Moore P. Periodontal disease and periodontal management in patients with cancer. Oral Oncol 2001;37:613-9.  Back to cited text no. 20
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21.Marx RE, Johnson RP. Studies in the radiobiology of osteoradionecrosis and their clinical significance. Oral Surg Oral Med Oral Pathol 1987;64:379-90.  Back to cited text no. 21
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22.Marciani RD, Ownby HE. Treating patients before and after irradiation. J Am Dent Assoc 1992;123:108-12.  Back to cited text no. 22
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23.Scully C, Epstein JB. Oral health care for the cancer patient. Eur J Cancer B Oral Oncol 1996;32B:281-92.  Back to cited text no. 23
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24.Delanian S, Lefaix JL. The radiation-induced fibroatrophic process: Therapeutic perspective via the antioxidant pathway. Radiother Oncol 2004;73:119-31.  Back to cited text no. 24
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