Letters to the Editor
2. Cennamo G, Rosa N, Iaccarino G, La Rana A, Pasquariello A. Macula study with standardized echography. Acta Ophthalmol Scand 1996;74:178-181. 3. Sbordone L, Levin L, Guidetti F, Sbordone C, Glikman A, Schwartz-Arad D. Apical and marginal bone alterations around implants in maxillary sinus augmentation grafted with autogenous bone or bovine bone material and simultaneous or delayed dental implant positioning. Clin Oral Implants Res 2011;22:485-491. Submitted February 19, 2013; accepted for publication February 19, 2013. doi: 10.1902/jop.2013.130120
Authors’ response: We would like to thank Drs. De Bernardo and Rosa for their interest in our article ‘‘Alveolar bone loss associated with age-related macular degeneration in males’’ published in the Journal of Periodontology.1 Drs. De Bernardo and Rosa may have misunderstood the methods used in our study to classify subjects as having a history of age-related macular degeneration (AMD) diagnosis. The diagnosis of AMD was not based on questionnaires; instead, interviews were used to collect the data on ‘‘previously diagnosed eye diseases.’’ As stated in our study, a subject was placed into the eye disease group if the study subject had previously been diagnosed with an eye disease by an ophthalmologist. We also cited the article by Laitinen et al.,2 where this is described in more detail. The home interview included several questions on eye diseases, such as: ‘‘Has a doctor diagnosed one of the following diseases: cataract, glaucoma, degenerative fundus changes, or other visual defect or injury?’’. Furthermore, in the Health 2000 Survey examination, the presence of eye diseases was specifically asked by the field physicians.2 In our article, this was expressed as ‘‘specifically assessed by the field physician’’ — perhaps the word ‘‘assessed’’ caused the misunderstanding. To be precise, these eye diseases were not diagnosed in the field examination of the Health 2000 Survey, but the data were collected by the field physician on ‘‘previously diagnosed eye diseases.’’ Drs. De Bernardo and Rosa expressed concern about the AMD diagnosis used in our study by stating that ‘‘. . . for ophthalmologists, degenerative fundus change does not mean ARMD; the correct statement should have been macular degenerative fundus change, because degenerative fundus change may develop in other regions of the fundus and has nothing to do with ARMD.’’ First, according to a very recent consensus report on the diagnosis of AMD,3 ‘‘At present there is no universally accepted precise definition, including both initial diagnosis and stag12
Volume 85 • Number 1
ing, of the AMD phenotype for either clinical or research purposes. There is not even consensus on basic terminology, with some groups using AMD and others using age-related maculopathy or ARM or ARMD.’’3 If we look at large-scale survey studies, the Framingham Eye Study accepted ‘‘a visual acuity of 20/30 or worse’’ as a diagnostic criterion of AMD.4 The Health and Nutrition Examination survey, on the other hand, accepted ‘‘typical fundus changes of AMD associated with a visual acuity of 20/25 or worse’’ as a case.5 Since AMD is characterized by the presence of drusen and geographic atrophy, and these fundus changes may predispose the eye to develop the neovascular/exudative stages of AMD,6 we accepted degenerative fundus changes as a diagnostic marker of AMD in our study. Drs. De Bernardo and Rosa wrote that a simple ophthalmoscopic exam or even a quick measurement with standardized echography could diagnose AMD. Although this approach would have been useful indeed, we emphasize that the national Health 2000 Survey was a large-scale epidemiological study, where data were collected from almost 10,000 study subjects in interviews and, further, from 8,000 study subjects in comprehensive health examinations. It is understandable that implementations of detailed medical checkups were beyond the limits of the survey (see survey at: http://www.terveys2000. fi/julkaisut/oral_health.pdf). In their letter, Drs. De Bernardo and Rosa stated that, in their opinion, self-reported diagnosis has a very low power, as sensitivity of only 55% and agreement ‘‘fair to good’’ do not sound very reliable. Firstly, these results presented by Laitinen et al.2 are based not only on sensitivity and specificity analyses but also kappa values. In our study, we used their report as a citation. Drs. De Bernardo and Rosa support their concerns by comparing the prevalence of AMD in Finland (12%) with the prevalence presented in our study (3%), and present it as ‘‘proof of the weakness in reliability of self-reported diagnosis.’’ By doing this, they ignore the fact that 12% is the prevalence of AMD in subjects aged 65 years and older.2 It is noteworthy that the prevalence of AMD in Finland is 1.2% in subjects aged 30 to 64 years, 8% in those aged 65 to 74 years, and 27% in those aged 85 years and older.2 In our study, the number of subjects aged 65 years and older was 319; among them, 31 had AMD diagnosis, bringing the prevalence up to 9.7%. Yet another argument by Drs. De Bernardo and Rosa was that the two groups appeared not to be homogeneous both for the number and the age of the study subjects. By arguing this, they ignore the nature of our study, which was an epidemiological one, not an age and gender-matched case-control study.
Letters to the Editor
J Periodontol • January 2014
In their letter, it was also suggested that the AMD population could be divided into two degenerative forms, to lend more information and significance to the study. Although this suggestion seems reasonable, it should be cautioned that the pathogenesis of AMD is not fully understood. The risk of dry AMD developing to advanced AMD (wet AMD) varies between 3.1% to 47.3% depending on the status (drusen) of dry AMD and the fellow eye.7 This means that the origin of these two diseases might be the same. Whether low-grade inflammation, hypoxia, or their combination is in their background is not yet thoroughly answered.8 Drs. De Bernardo and Rosa asked why we did not use self-reported diagnosis as a measure of periodontitis. In contrast to eye diseases, periodontitis often progresses without any subjective symptoms and easily remains unnoticed by the patient. Despite this, validation of self-reported periodontal disease has been discussed widely.9 As an example of such validations, the question of "Has any dentist/hygienist told you that you have deep pockets?" had a sensitivity of 55% and a specificity of 90%.10 Therefore, even a self-report measure could have been used. However, a dental examination, including radiographs, was already implemented into the Health 2000 Survey and, naturally, we preferred to use these outcomes in the diagnosis of periodontitis. Finally, Drs. De Bernardo and Rosa criticized our method of measuring alveolar bone loss, stating that it does not include an internal standard, in comparison to the use of implants as internal standards. We found the argument on the applicability of placing implants as internal standards on subjects in epidemiological studies totally groundless. We remind Drs. De Bernardo and Rosa that the internal standard in our study was the root, since the categorization was done as: 1 = bone pocket exceeding the middle third of the root, 2 = bone pocket exceeding the apical third of the root. Although self-reported measures bring some limitations in power of the studies, results and conclusions based on these measures are valuable especially in epidemiological studies, where a thorough clinical evaluation is not applicable. Ulvi K. Gursoy and Sisko Huumonen, Institute of Dentistry, University of Turku, Turku, Finland; Eija Vesti, Department of Ophthalmology, University of Turku; Pirkko J. Pussinen, Institute of Dentistry, University of Helsinki, Helsinki, Finland; Anna L. Suominen, Unit of Living Conditions, Health and
Well-Being, and Department of Environmental Health in Environmental Epidemiology Unit, National Institute for Health and Welfare (THL), and Institute of Dentistry, University of Eastern Finland, Kuopio, Finland; and Eija Ko€no€nen, Institute of Dentistry, University of Turku, Turku, and Department of Infectious Disease Surveillance and Control, National Institute for Health and Welfare (THL), Helsinki, Finland. The authors report no conflicts of interest related to this letter. REFERENCES 1. Karesvuo P, Gursoy UK, Pussinen PJ, et al. Alveolar bone loss associated with age-related macular degeneration in males. J Periodontol 2013;84:58-67. 2. Laitinen A, Laatikainen L, Ha¨rka¨nen T, Koskinen S, Reunanen A, Aromaa A. Prevalence of major eye diseases and causes of visual impairment in the adult Finnish population: A nationwide population-based survey. Acta Ophthalmol 2010;88:463-471. 3. Ferris FL 3rd, Wilkinson CP, Bird A, et al.; Beckman Initiative for Macular Research Classification Committee. Clinical classification of age-related macular degeneration. Ophthalmology 2013;120:844-851. 4. Krueger DE, Milton RC, Maunder LR. The Framingham Eye Study: Introduction to the monograph. Surv Ophthalmol 1980;24:614-620. 5. Mullins RF, Russell SR, Anderson DH, Hageman GS. Drusen associated with aging and age-related macular degeneration contain proteins common to extracellular deposits associated with atherosclerosis, elastosis, amyloidosis, and dense deposit disease. FASEB J 2000;14:835-846. 6. Bressler NM, Bressler SB, Fine SL. Age-related macular degeneration. Surv Ophthalmol 1988;32:375-413. 7. Davis MD, Gangnon RE, Lee LY, et al.; Age-Related Eye Disease Study Group. The Age-Related Eye Disease Study severity scale for age-related macular degeneration: AREDS Report No. 17. Arch Ophthalmol 2005;123:1484-1498. 8. Kaarniranta K, Salminen A, Haapasalo A, Soininen H, Hiltunen M. Age-related macular degeneration (AMD): Alzheimer’s disease in the eye? J Alzheimers Dis 2011; 24:615-631. 9. Buhlin K, Gustafsson A, Andersson K, Ha˚kansson J, Klinge B. Validity and limitations of self-reported periodontal health. Community Dent Oral Epidemiol 2002; 30:431-437. 10. Blicher B, Joshipura K, Eke P. Validation of selfreported periodontal disease: A systematic review. J Dent Res 2005;84:881-890. Submitted March 7, 2013; accepted for publication March 7, 2013. doi: 10.1902/jop.2013.130162
13
2. Cennamo G, Rosa N, Iaccarino G, La Rana A, Pasquariello A. Macula study with standardized echography. Acta Ophthalmol Scand 1996;74:178-181. 3. Sbordone L, Levin L, Guidetti F, Sbordone C, Glikman A, Schwartz-Arad D. Apical and marginal bone alterations around implants in maxillary sinus augmentation grafted with autogenous bone or bovine bone material and simultaneous or delayed dental implant positioning. Clin Oral Implants Res 2011;22:485-491. Submitted February 19, 2013; accepted for publication February 19, 2013. doi: 10.1902/jop.2013.130120
Authors’ response: We would like to thank Drs. De Bernardo and Rosa for their interest in our article ‘‘Alveolar bone loss associated with age-related macular degeneration in males’’ published in the Journal of Periodontology.1 Drs. De Bernardo and Rosa may have misunderstood the methods used in our study to classify subjects as having a history of age-related macular degeneration (AMD) diagnosis. The diagnosis of AMD was not based on questionnaires; instead, interviews were used to collect the data on ‘‘previously diagnosed eye diseases.’’ As stated in our study, a subject was placed into the eye disease group if the study subject had previously been diagnosed with an eye disease by an ophthalmologist. We also cited the article by Laitinen et al.,2 where this is described in more detail. The home interview included several questions on eye diseases, such as: ‘‘Has a doctor diagnosed one of the following diseases: cataract, glaucoma, degenerative fundus changes, or other visual defect or injury?’’. Furthermore, in the Health 2000 Survey examination, the presence of eye diseases was specifically asked by the field physicians.2 In our article, this was expressed as ‘‘specifically assessed by the field physician’’ — perhaps the word ‘‘assessed’’ caused the misunderstanding. To be precise, these eye diseases were not diagnosed in the field examination of the Health 2000 Survey, but the data were collected by the field physician on ‘‘previously diagnosed eye diseases.’’ Drs. De Bernardo and Rosa expressed concern about the AMD diagnosis used in our study by stating that ‘‘. . . for ophthalmologists, degenerative fundus change does not mean ARMD; the correct statement should have been macular degenerative fundus change, because degenerative fundus change may develop in other regions of the fundus and has nothing to do with ARMD.’’ First, according to a very recent consensus report on the diagnosis of AMD,3 ‘‘At present there is no universally accepted precise definition, including both initial diagnosis and stag12
Volume 85 • Number 1
ing, of the AMD phenotype for either clinical or research purposes. There is not even consensus on basic terminology, with some groups using AMD and others using age-related maculopathy or ARM or ARMD.’’3 If we look at large-scale survey studies, the Framingham Eye Study accepted ‘‘a visual acuity of 20/30 or worse’’ as a diagnostic criterion of AMD.4 The Health and Nutrition Examination survey, on the other hand, accepted ‘‘typical fundus changes of AMD associated with a visual acuity of 20/25 or worse’’ as a case.5 Since AMD is characterized by the presence of drusen and geographic atrophy, and these fundus changes may predispose the eye to develop the neovascular/exudative stages of AMD,6 we accepted degenerative fundus changes as a diagnostic marker of AMD in our study. Drs. De Bernardo and Rosa wrote that a simple ophthalmoscopic exam or even a quick measurement with standardized echography could diagnose AMD. Although this approach would have been useful indeed, we emphasize that the national Health 2000 Survey was a large-scale epidemiological study, where data were collected from almost 10,000 study subjects in interviews and, further, from 8,000 study subjects in comprehensive health examinations. It is understandable that implementations of detailed medical checkups were beyond the limits of the survey (see survey at: http://www.terveys2000. fi/julkaisut/oral_health.pdf). In their letter, Drs. De Bernardo and Rosa stated that, in their opinion, self-reported diagnosis has a very low power, as sensitivity of only 55% and agreement ‘‘fair to good’’ do not sound very reliable. Firstly, these results presented by Laitinen et al.2 are based not only on sensitivity and specificity analyses but also kappa values. In our study, we used their report as a citation. Drs. De Bernardo and Rosa support their concerns by comparing the prevalence of AMD in Finland (12%) with the prevalence presented in our study (3%), and present it as ‘‘proof of the weakness in reliability of self-reported diagnosis.’’ By doing this, they ignore the fact that 12% is the prevalence of AMD in subjects aged 65 years and older.2 It is noteworthy that the prevalence of AMD in Finland is 1.2% in subjects aged 30 to 64 years, 8% in those aged 65 to 74 years, and 27% in those aged 85 years and older.2 In our study, the number of subjects aged 65 years and older was 319; among them, 31 had AMD diagnosis, bringing the prevalence up to 9.7%. Yet another argument by Drs. De Bernardo and Rosa was that the two groups appeared not to be homogeneous both for the number and the age of the study subjects. By arguing this, they ignore the nature of our study, which was an epidemiological one, not an age and gender-matched case-control study.
Letters to the Editor
J Periodontol • January 2014
In their letter, it was also suggested that the AMD population could be divided into two degenerative forms, to lend more information and significance to the study. Although this suggestion seems reasonable, it should be cautioned that the pathogenesis of AMD is not fully understood. The risk of dry AMD developing to advanced AMD (wet AMD) varies between 3.1% to 47.3% depending on the status (drusen) of dry AMD and the fellow eye.7 This means that the origin of these two diseases might be the same. Whether low-grade inflammation, hypoxia, or their combination is in their background is not yet thoroughly answered.8 Drs. De Bernardo and Rosa asked why we did not use self-reported diagnosis as a measure of periodontitis. In contrast to eye diseases, periodontitis often progresses without any subjective symptoms and easily remains unnoticed by the patient. Despite this, validation of self-reported periodontal disease has been discussed widely.9 As an example of such validations, the question of "Has any dentist/hygienist told you that you have deep pockets?" had a sensitivity of 55% and a specificity of 90%.10 Therefore, even a self-report measure could have been used. However, a dental examination, including radiographs, was already implemented into the Health 2000 Survey and, naturally, we preferred to use these outcomes in the diagnosis of periodontitis. Finally, Drs. De Bernardo and Rosa criticized our method of measuring alveolar bone loss, stating that it does not include an internal standard, in comparison to the use of implants as internal standards. We found the argument on the applicability of placing implants as internal standards on subjects in epidemiological studies totally groundless. We remind Drs. De Bernardo and Rosa that the internal standard in our study was the root, since the categorization was done as: 1 = bone pocket exceeding the middle third of the root, 2 = bone pocket exceeding the apical third of the root. Although self-reported measures bring some limitations in power of the studies, results and conclusions based on these measures are valuable especially in epidemiological studies, where a thorough clinical evaluation is not applicable. Ulvi K. Gursoy and Sisko Huumonen, Institute of Dentistry, University of Turku, Turku, Finland; Eija Vesti, Department of Ophthalmology, University of Turku; Pirkko J. Pussinen, Institute of Dentistry, University of Helsinki, Helsinki, Finland; Anna L. Suominen, Unit of Living Conditions, Health and
Well-Being, and Department of Environmental Health in Environmental Epidemiology Unit, National Institute for Health and Welfare (THL), and Institute of Dentistry, University of Eastern Finland, Kuopio, Finland; and Eija Ko€no€nen, Institute of Dentistry, University of Turku, Turku, and Department of Infectious Disease Surveillance and Control, National Institute for Health and Welfare (THL), Helsinki, Finland. The authors report no conflicts of interest related to this letter. REFERENCES 1. Karesvuo P, Gursoy UK, Pussinen PJ, et al. Alveolar bone loss associated with age-related macular degeneration in males. J Periodontol 2013;84:58-67. 2. Laitinen A, Laatikainen L, Ha¨rka¨nen T, Koskinen S, Reunanen A, Aromaa A. Prevalence of major eye diseases and causes of visual impairment in the adult Finnish population: A nationwide population-based survey. Acta Ophthalmol 2010;88:463-471. 3. Ferris FL 3rd, Wilkinson CP, Bird A, et al.; Beckman Initiative for Macular Research Classification Committee. Clinical classification of age-related macular degeneration. Ophthalmology 2013;120:844-851. 4. Krueger DE, Milton RC, Maunder LR. The Framingham Eye Study: Introduction to the monograph. Surv Ophthalmol 1980;24:614-620. 5. Mullins RF, Russell SR, Anderson DH, Hageman GS. Drusen associated with aging and age-related macular degeneration contain proteins common to extracellular deposits associated with atherosclerosis, elastosis, amyloidosis, and dense deposit disease. FASEB J 2000;14:835-846. 6. Bressler NM, Bressler SB, Fine SL. Age-related macular degeneration. Surv Ophthalmol 1988;32:375-413. 7. Davis MD, Gangnon RE, Lee LY, et al.; Age-Related Eye Disease Study Group. The Age-Related Eye Disease Study severity scale for age-related macular degeneration: AREDS Report No. 17. Arch Ophthalmol 2005;123:1484-1498. 8. Kaarniranta K, Salminen A, Haapasalo A, Soininen H, Hiltunen M. Age-related macular degeneration (AMD): Alzheimer’s disease in the eye? J Alzheimers Dis 2011; 24:615-631. 9. Buhlin K, Gustafsson A, Andersson K, Ha˚kansson J, Klinge B. Validity and limitations of self-reported periodontal health. Community Dent Oral Epidemiol 2002; 30:431-437. 10. Blicher B, Joshipura K, Eke P. Validation of selfreported periodontal disease: A systematic review. J Dent Res 2005;84:881-890. Submitted March 7, 2013; accepted for publication March 7, 2013. doi: 10.1902/jop.2013.130162
13
