Abstract
OBJECTIVE:
Oral health can affect a patient’s general health and quality of life. Given the increase in breast cancer survival rates, investigations of factors influencing the quality of life of survivors have gained importance. Therefore, the objective of our study was to characterize oral health in postmenopausal breast cancer survivors.
METHODS:
We conducted a matched case-control study. Forty-eight women who survived breast cancer (age 62.1±9.1 years) and 48 healthy controls (age 61.8±8.6 years) were included. For each case and control, a complete oral evaluation chart was completed.
RESULTS:
The prevalence of chronic periodontal disease was 98% in breast cancer survivors and 87% in controls. The breast cancer survivors had a median of 16 remaining teeth, whereas controls had a median of 22 remaining teeth (p = 0.03). The percentage of sites with gingival bleeding was 16.05% (0-100%) in breast cancer survivors and 0% (0-72%) in controls (p = 0.04).
CONCLUSION:
Chronic periodontal disease and tooth loss were highly prevalent in postmenopausal breast cancer survivors. To improve survivors’ quality of life, a preventive oral health evaluation should be available prior to cancer treatment.
Breast Cancer; Periodontal Disease; Tooth Loss
INTRODUCTION
Breast cancer mortality has declined dramatically since 1990 (11. Parkin DM, Bray FI, Devesa SS. Cancer burden in the year 2000.
The global picture. Eur J Cancer. 2001;37(Suppl
8):S4-66.). In the U.S., breast cancer death rates have decreased by
34% (22. DeSantis C, Ma J, Bryan L, Jemal A. Breast cancer statistics,
2013. CA Cancer J Clin 2014;64(1):52-62.). This epidemiological change can be
attributed to a combination of screening programs and improvements in adjuvant
therapy (33. Berry DA, Cronin KA, Plevritis SK, Fryback DG, Clarke L, Zelen M,
et al. Effect of screening and adjuvant therapy on mortality from breast cancer.
N Engl J Med. 2005;353(17):1784-92.). In this context, an important
issue faced by clinicians caring for these women is how to improve their long-term
quality of life. Many latent clinical disorders can emerge during or after cancer
treatment that eventually may attenuate the survival gains obtained via recent
advances in curative-intent therapies (44. Jones LW, Haykowsky MJ, Swartz JJ, Douglas PS, Mackey JR. Early
breast cancer therapy and cardiovascular injury. J Am Coll Cardiol.
2007;50(15):1435-41,
http://dx.doi.org/10.1016/j.jacc.2007.06.037.
http://dx.doi.org/10.1016/j.jacc.2007.06...
).
Good oral health is important to quality of life and overall health. Chronic
periodontal disease (CPD) is associated with low flow-mediated dilation of the
brachial artery and high levels of systemic inflammation markers (55. Amar S, Gokce N, Morgan S, Loukideli M, Van Dyke TE, Vita JA.
Periodontal disease is associated with brachial artery endothelial dysfunction
and systemic inflammation. Arterioscler Thromb Vasc Biol. 2003;23(7):1245-9,
http://dx.doi.org/10.1161/01.ATV.0000078603.90302.4A.
http://dx.doi.org/10.1161/01.ATV.0000078...
). CPD is also associated with atherogenesis
(66. Beck JD, Elter JR, Heiss G, Couper D, Mauriello SM, Offenbacher
S. Relationship of periodontal disease to carotid artery intima-media wall
thickness: The atherosclerosis risk in communities (aric) study. Arterioscler
Thromb Vasc Biol. 2001;21(11):1816-22,
http://dx.doi.org/10.1161/hq1101.097803.
http://dx.doi.org/10.1161/hq1101.097803...
) and a risk of myocardial infarction
and stroke (77. Scannapieco FA, Bush RB, Paju S. Associations between periodontal
disease and risk for atherosclerosis, cardiovascular disease, and stroke.
A systematic review. Ann Periodontol. 2003;8(1):38-53,
http://dx.doi.org/10.1902/annals.2003.8.1.38.
http://dx.doi.org/10.1902/annals.2003.8....
). Oral care during cancer
treatment primarily focuses on the management of acute complications, such as
mucositis, oral pain and infection (88. Mosel DD, Bauer RL, Lynch DP, Hwang ST. Oral complications in the
treatment of cancer patients. Oral Dis. 2011;17(6):550-9,
http://dx.doi.org/10.1111/j.1601-0825.2011.01788.x.
http://dx.doi.org/10.1111/j.1601-0825.20...
).
Chronic oral diseases have the potential to impair survivors’ quality of life
after oncological treatment and are frequently neglected.
In this study, we report the results of a systematic oral evaluation after breast cancer treatment in postmenopausal women. Our objective was to characterize the oral health in breast cancer survivors treated in the public health system.
MATERIALS AND METHODS
Subjects
This case-control study included 48 voluntary post-menopausal breast cancer survivors and 48 age-matched healthy women volunteers. The cases and matched controls were recruited from the public health system in Brazil.
Oral examination
The oral examinations were conducted by a single calibrated dental examiner who collected the complete clinical history of the patients and performed the clinical oral examination. The oral examinations were performed after the end of oncological treatment for all breast cancer survivors. The data included the following: the total number of teeth, full-mouth plaque score (the number of sites with detectable dental plaque divided by the total number of sites per mouth, multiplied by 100), full-mouth gingival bleeding on probing score (the number of sites with gingival bleeding on probing divided by the total number of sites per mouth, multiplied by 100), full-mouth periodontal lesion score (the number of sites with a probing depth ≥4 mm divided by the total number of sites per mouth, multiplied by 100) and the mean probing attachment level.
Statistics
The data for each variable were tested using the D' Agostino & Pearson normality test. The mean and standard deviation or median and range were determined. Student’s t test or the Mann-Whitney test was performed as appropriate. All analyses were performed using GraphPad Software¯ 5.0 for Windows (GraphPad Software Inc, La Jolla, CA, USA).
Ethics
The study was approved by the local institutional review board, and all subjects signed a written informed consent form. All procedures were in accordance with the Helsinki Declaration.
RESULTS
The medical parameters associated with breast cancer are presented in Table 1. The mean age was 62.1±9.1 years for breast cancer survivors and 61.8±8.6 years for controls.
Oral health data are presented in Table 2. CPD was identified in 98% of breast cancer survivors (mild periodontitis: 30 cases; moderate periodontitis: 11 cases; severe periodontitis: 6 cases) and 87% of controls (mild periodontitis: 23 cases; moderate periodontitis: 12 cases; severe periodontitis: 7 cases).
The median number of teeth was 16 (3-28) for breast cancer survivors and 22 (4-31) for controls (p = 0.03, Mann-Whitney test). The median full-mouth plaque score was 50 (0-100) for cancer survivors and 36.57 (0-100) for controls (p = NS, Mann-Whitney test). The median full-mouth gingival bleeding on probing score was 16.05 (0-100) for the cases and 0 (0-72) for the controls (p = 0.04, Mann-Whitney test). The median full-mouth periodontal lesion score was 3.3 (0.0-46.7) for breast cancer survivors and 3.6 (0.0-51.6) for controls. The probing attachment level was 2.8 (1.3-5.9) in breast cancer survivors and 3.1 (1.5-5.2) in controls (p = NS, Mann-Whitney test).
DISCUSSION
We identified a very high prevalence of CPD in postmenopausal breast cancer survivors; only one of our patients did not exhibit signs of the disease. The controls also presented a high prevalence of CPD; however, breast cancer survivors had significantly higher indices of gingival bleeding and tooth loss. These findings are highly relevant for the multidisciplinary management of breast cancer.
The quality of life and long-term survival of breast cancer survivors may be affected
by lack of oral health care. CPD is associated with several unpleasant symptoms that
can range from mild to severe, including swelling, bluish purple discoloration of
the gingiva, bleeding after eating or brushing and halitosis. CPD can also induce
loss of supportive connective tissues, including alveolar bone, thereby resulting in
loss of attachment of the periodontal ligament to the cementum and eventual tooth
loss (mainly among older individuals) (99. Murray Thomson W. Epidemiology of oral health conditions in older
people. Gerodontology. 2014;31 Suppl 1:9-16,
http://dx.doi.org/10.1111/ger.12085.
http://dx.doi.org/10.1111/ger.12085...
).
The prevalence of CPD increased significantly with age and remained constant after
the 50-59 age group (1010. Holtfreter B, Schwahn C, Biffar R, Kocher T. Epidemiology of
periodontal diseases in the study of health in pomerania. J Clin
Periodontol. 2009;36(2):114-23,
http://dx.doi.org/10.1111/j.1600-051X.2008.01361.x.
http://dx.doi.org/10.1111/j.1600-051X.20...
). The prevalence of
CPD in postmenopausal women not taking hormonal replacement is approximately 64.4%,
whereas the prevalence is 46.3% in postmenopausal women taking hormonal replacement
(1111. Haas AN, Rosing CK, Oppermann RV, Albandar JM, Susin C.
Association among menopause, hormone replacement therapy, and periodontal
attachment loss in southern brazilian women. J Periodontol.
2009;80(9):1380-7, http://dx.doi.org/10.1902/jop.2009.090082.
http://dx.doi.org/10.1902/jop.2009.09008...
). Overall, 87% of the individuals in
our control group had CPD; this prevalence is comparable to that observed in Germany
(1010. Holtfreter B, Schwahn C, Biffar R, Kocher T. Epidemiology of
periodontal diseases in the study of health in pomerania. J Clin
Periodontol. 2009;36(2):114-23,
http://dx.doi.org/10.1111/j.1600-051X.2008.01361.x.
http://dx.doi.org/10.1111/j.1600-051X.20...
) and higher than that observed in the
U.S. (1212. Dye BA, Tan S, Smith V, Lewis BG, Barker LK, Thornton-Evans G,
et al. Trends in oral health status: United states, 1988-1994 and 1999-2004.
Vital Health Stat 11. 2007(248):1-92.). The association between breast
cancer treatment and oral health has not previously been explored, but it is well
known that “potentially complicating oral disease should be identified and
corrected as early as possible before commencement of anticancer therapy”
(1313. Consensus statement: Oral complications of cancer therapies.
National institutes of health consensus development panel. NCI Monogr.
1990(9):3-8.). A comprehensive dental examination
performed prior to treatment can identify approximately 80% of the patients with
chronic odontogenic pathology who should receive treatment to prevent local
exacerbation or systemic spread of ongoing infection while avoiding long-term oral
complications, such as tooth loss (1414. Toljanic JA, Bedard JF, Larson RA, Fox JP. A prospective pilot
study to evaluate a new dental assessment and treatment paradigm for patients
scheduled to undergo intensive chemotherapy for cancer. Cancer.
1999;85(8):1843-8,
http://dx.doi.org/10.1002/(SICI)1097-0142(19990415)85:8<1843::AID-CNCR26>3.0.CO;2-R.
http://dx.doi.org/10.1002/(SICI)1097-014...
).
On the other hand, the association between CPD and cardiac morbidity is well
established. Cardiac complications have a serious impact on the life expectancy and
quality of life of breast cancer survivors. The risk for cardiac disease may be
increased in breast cancer survivors due to various reasons other than CPD. Data
from The Late Effects Breast Cancer Cohort have revealed that 62.9 excess cases of
cardiovascular events per 10,000 patient-years are associated with long-term breast
cancer treatment and the main risk factors are associated with radiotherapy of the
internal mammary chain, radiation with adjuvant chemotherapy and smoking (1515. Hooning MJ, Botma A, Aleman BM, Baaijens MH, Bartelink H, Klijn
JG, et al. Long-term risk of cardiovascular disease in 10-year survivors of
breast cancer. J Natl Cancer Inst. 2007;99(5):365-75,
http://dx.doi.org/10.1093/jnci/djk064.
http://dx.doi.org/10.1093/jnci/djk064...
). After breast conservation treatment for
early stage disease, the subsequent development of cardiac disease is more frequent
in women with cancer of the left breast (1616. Harris EE, Correa C, Hwang WT, Liao J, Litt HI, Ferrari VA, et
al. Late cardiac mortality and morbidity in early-stage breast cancer patients
after breast-conservation treatment. J Clin Oncol. 2006;24(25):4100-6,
http://dx.doi.org/10.1200/JCO.2005.05.1037.
http://dx.doi.org/10.1200/JCO.2005.05.10...
).
Anthracyclines, which are largely used in breast cancer chemotherapy, have long been
recognized as a cause of cardiac dysfunctions, such as cardiomyopathy and heart
failure. These side effects are dose-dependent (1717. Von Hoff DD, Layard MW, Basa P, Davis HL, Jr., Von Hoff AL,
Rozencweig M, et al. Risk factors for doxorubicin-induced congestive heart
failure. Ann Intern Med. 1979;91(5):710-7,
http://dx.doi.org/10.7326/0003-4819-91-5-710.
http://dx.doi.org/10.7326/0003-4819-91-5...
) and occur more frequently in older patients (1818. Pinder MC, Duan Z, Goodwin JS, Hortobagyi GN, Giordano SH.
Congestive heart failure in older women treated with adjuvant anthracycline
chemotherapy for breast cancer. J Clin Oncol. 2007;25(25):3808-15,
http://dx.doi.org/10.1200/JCO.2006.10.4976.
http://dx.doi.org/10.1200/JCO.2006.10.49...
). Trastuzumab, a monoclonal antibody that blocks the HER-2
receptor and improves the survival of women with HER-2-positive breast cancer, is
also associated with an increased risk of cardiac dysfunction (1919. Seidman A, Hudis C, Pierri MK, Shak S, Paton V, Ashby M, et al.
Cardiac dysfunction in the trastuzumab clinical trials experience. J Clin
Oncol. 2002;20(5):1215-21,
http://dx.doi.org/10.1200/JCO.20.5.1215.
http://dx.doi.org/10.1200/JCO.20.5.1215...
).
High-quality management of breast cancer patients should include strategies for
identifying patients who are at high risk for cardiac disease and developing
effective interventions to prevent the development of late toxicities and minimize
their effects on quality of life (2020. Giordano SH, Hortobagyi GN. Local recurrence or cardiovascular
disease: Pay now or later. J Natl Cancer Inst. 2007;99(5):340-1,
http://dx.doi.org/10.1093/jnci/djk085.
http://dx.doi.org/10.1093/jnci/djk085...
).
Epidemiological (77. Scannapieco FA, Bush RB, Paju S. Associations between periodontal
disease and risk for atherosclerosis, cardiovascular disease, and stroke.
A systematic review. Ann Periodontol. 2003;8(1):38-53,
http://dx.doi.org/10.1902/annals.2003.8.1.38.
http://dx.doi.org/10.1902/annals.2003.8....
) and experimental (55. Amar S, Gokce N, Morgan S, Loukideli M, Van Dyke TE, Vita JA.
Periodontal disease is associated with brachial artery endothelial dysfunction
and systemic inflammation. Arterioscler Thromb Vasc Biol. 2003;23(7):1245-9,
http://dx.doi.org/10.1161/01.ATV.0000078603.90302.4A.
http://dx.doi.org/10.1161/01.ATV.0000078...
,2121. Tonetti MS, D'Aiuto F, Nibali L, Donald A, Storry C, Parkar
M, et al. Treatment of periodontitis and endothelial function.
N Engl J Med. 2007;356(9):911-20.)
evidence indicates that periodontal disease is linked to an increased risk of
cardiovascular disease. Despite the limitations of our case-control design and a
lack of diversity in the therapeutic methods employed, our data consistently
revealed a high prevalence of periodontal disease and tooth loss after breast cancer
treatment in post-menopausal women. We believe that the current evidence warrants
the inclusion of a recommendation for a comprehensive oral examination and treatment
of identified lesions in the breast cancer management protocols in the public health
system. Efforts have been made to screen for and reduce or eliminate risk factors
for cardiac disease, such as smoking, elevated lipid levels and hypertension, in
patients who have breast cancer after menopause. However, these efforts should also
include the prevention and treatment of oral diseases.
REFERENCES
-
1Parkin DM, Bray FI, Devesa SS. Cancer burden in the year 2000. The global picture. Eur J Cancer. 2001;37(Suppl 8):S4-66.
-
2DeSantis C, Ma J, Bryan L, Jemal A. Breast cancer statistics, 2013. CA Cancer J Clin 2014;64(1):52-62.
-
3Berry DA, Cronin KA, Plevritis SK, Fryback DG, Clarke L, Zelen M, et al. Effect of screening and adjuvant therapy on mortality from breast cancer. N Engl J Med. 2005;353(17):1784-92.
-
4Jones LW, Haykowsky MJ, Swartz JJ, Douglas PS, Mackey JR. Early breast cancer therapy and cardiovascular injury. J Am Coll Cardiol. 2007;50(15):1435-41, http://dx.doi.org/10.1016/j.jacc.2007.06.037.
» http://dx.doi.org/10.1016/j.jacc.2007.06.037 -
5Amar S, Gokce N, Morgan S, Loukideli M, Van Dyke TE, Vita JA. Periodontal disease is associated with brachial artery endothelial dysfunction and systemic inflammation. Arterioscler Thromb Vasc Biol. 2003;23(7):1245-9, http://dx.doi.org/10.1161/01.ATV.0000078603.90302.4A.
» http://dx.doi.org/10.1161/01.ATV.0000078603.90302.4A -
6Beck JD, Elter JR, Heiss G, Couper D, Mauriello SM, Offenbacher S. Relationship of periodontal disease to carotid artery intima-media wall thickness: The atherosclerosis risk in communities (aric) study. Arterioscler Thromb Vasc Biol. 2001;21(11):1816-22, http://dx.doi.org/10.1161/hq1101.097803.
» http://dx.doi.org/10.1161/hq1101.097803 -
7Scannapieco FA, Bush RB, Paju S. Associations between periodontal disease and risk for atherosclerosis, cardiovascular disease, and stroke. A systematic review. Ann Periodontol. 2003;8(1):38-53, http://dx.doi.org/10.1902/annals.2003.8.1.38.
» http://dx.doi.org/10.1902/annals.2003.8.1.38 -
8Mosel DD, Bauer RL, Lynch DP, Hwang ST. Oral complications in the treatment of cancer patients. Oral Dis. 2011;17(6):550-9, http://dx.doi.org/10.1111/j.1601-0825.2011.01788.x.
» http://dx.doi.org/10.1111/j.1601-0825.2011.01788.x -
9Murray Thomson W. Epidemiology of oral health conditions in older people. Gerodontology. 2014;31 Suppl 1:9-16, http://dx.doi.org/10.1111/ger.12085.
» http://dx.doi.org/10.1111/ger.12085 -
10Holtfreter B, Schwahn C, Biffar R, Kocher T. Epidemiology of periodontal diseases in the study of health in pomerania. J Clin Periodontol. 2009;36(2):114-23, http://dx.doi.org/10.1111/j.1600-051X.2008.01361.x.
» http://dx.doi.org/10.1111/j.1600-051X.2008.01361.x -
11Haas AN, Rosing CK, Oppermann RV, Albandar JM, Susin C. Association among menopause, hormone replacement therapy, and periodontal attachment loss in southern brazilian women. J Periodontol. 2009;80(9):1380-7, http://dx.doi.org/10.1902/jop.2009.090082.
» http://dx.doi.org/10.1902/jop.2009.090082 -
12Dye BA, Tan S, Smith V, Lewis BG, Barker LK, Thornton-Evans G, et al. Trends in oral health status: United states, 1988-1994 and 1999-2004. Vital Health Stat 11. 2007(248):1-92.
-
13Consensus statement: Oral complications of cancer therapies. National institutes of health consensus development panel. NCI Monogr. 1990(9):3-8.
-
14Toljanic JA, Bedard JF, Larson RA, Fox JP. A prospective pilot study to evaluate a new dental assessment and treatment paradigm for patients scheduled to undergo intensive chemotherapy for cancer. Cancer. 1999;85(8):1843-8, http://dx.doi.org/10.1002/(SICI)1097-0142(19990415)85:8<1843::AID-CNCR26>3.0.CO;2-R.
» http://dx.doi.org/10.1002/(SICI)1097-0142(19990415)85:8<1843::AID-CNCR26>3.0.CO;2-R -
15Hooning MJ, Botma A, Aleman BM, Baaijens MH, Bartelink H, Klijn JG, et al. Long-term risk of cardiovascular disease in 10-year survivors of breast cancer. J Natl Cancer Inst. 2007;99(5):365-75, http://dx.doi.org/10.1093/jnci/djk064.
» http://dx.doi.org/10.1093/jnci/djk064 -
16Harris EE, Correa C, Hwang WT, Liao J, Litt HI, Ferrari VA, et al. Late cardiac mortality and morbidity in early-stage breast cancer patients after breast-conservation treatment. J Clin Oncol. 2006;24(25):4100-6, http://dx.doi.org/10.1200/JCO.2005.05.1037.
» http://dx.doi.org/10.1200/JCO.2005.05.1037 -
17Von Hoff DD, Layard MW, Basa P, Davis HL, Jr., Von Hoff AL, Rozencweig M, et al. Risk factors for doxorubicin-induced congestive heart failure. Ann Intern Med. 1979;91(5):710-7, http://dx.doi.org/10.7326/0003-4819-91-5-710.
» http://dx.doi.org/10.7326/0003-4819-91-5-710 -
18Pinder MC, Duan Z, Goodwin JS, Hortobagyi GN, Giordano SH. Congestive heart failure in older women treated with adjuvant anthracycline chemotherapy for breast cancer. J Clin Oncol. 2007;25(25):3808-15, http://dx.doi.org/10.1200/JCO.2006.10.4976.
» http://dx.doi.org/10.1200/JCO.2006.10.4976 -
19Seidman A, Hudis C, Pierri MK, Shak S, Paton V, Ashby M, et al. Cardiac dysfunction in the trastuzumab clinical trials experience. J Clin Oncol. 2002;20(5):1215-21, http://dx.doi.org/10.1200/JCO.20.5.1215.
» http://dx.doi.org/10.1200/JCO.20.5.1215 -
20Giordano SH, Hortobagyi GN. Local recurrence or cardiovascular disease: Pay now or later. J Natl Cancer Inst. 2007;99(5):340-1, http://dx.doi.org/10.1093/jnci/djk085.
» http://dx.doi.org/10.1093/jnci/djk085 -
21Tonetti MS, D'Aiuto F, Nibali L, Donald A, Storry C, Parkar M, et al. Treatment of periodontitis and endothelial function. N Engl J Med. 2007;356(9):911-20.
-
No potential conflict of interest was reported.
Publication Dates
-
Publication in this collection
Oct 2014
History
-
Received
2 Feb 2014 -
Reviewed
28 Feb 2014 -
Accepted
18 Mar 2014