smoking, cigarette smoking, periodontal disease, LA, Community Dent, subjects, smoking cessation, periodontal pockets, J Periodontol, cardiovascular disease, non-smokers, periodontitis, cross-sectional study, chronic periodontitis, smokers, risk factor, risk factors, periodontal diseases, Brazil, J Clin Periodontol, Oral Health Surveys, Oral Health, Preventive Dentistry, Bergstrom J, periodontal tissues, prospective study, Bergstrom J. Periodontitis, Bergstrom, European Workshop, van der Velden U. Teeth, smoking cigarettes, Attributable risk, periodontal pocket, Department of Pediatric and Social Dentistry, southern Brazil, Paulo State University, Ara�tuba School of Dentistry, score, National Health and Nutrition Examination Survey, Cannabis smoking, World Health Organisation, CPI, percentage of smokers, Claffey N. Advances
Smoking and Periodontal Disease: Clinical Evidence for an Association
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Suzely Adas Saliba Moimaza/Lнvia Guimarгes Zinab/Orlando Salibac/ Cleб Adas Saliba Garbina
Purpose: The aim of the present study was to assess the periodontal condition and smoking status, according to dose and duration information, and to estimate the percentage of subjects with periodontitis attributable to cigarette smoking in a representative adult rural population in Southern Brazil
Materials and Methods: Bivariate Statistical Analysis
was used to evaluate the association of smoking status with periodontitis in a cross-sectional study comprising 165 dentate individuals, aged 35 to 66 years, subjected to oral Clinical Examination
of six sites per tooth in all sextants. Results: The prevalence of periodontitis (having 1 pocket of 4 mm around the index teeth) in the population was 35.2%. Overall, 13.9% had a cumulative loss of attachment > 4 mm; 35.7% of subjects were current smokers, classified as heavy (average 25.3 pack years), moderate (average 14.6 pack years) and light smokers (average 3.1 pack years). Statistical analysis showed that current smokers had an 11 times (95% confidence interval [CI] = 4.69 to 26.62) and former smokers had a nine times (95% CI = 3.29 to 25.96) greater probability of having established periodontitis compared with non-smokers. The number of pack years (P = 0.0004) and years of smoking exposure (P = 0.0013) were associated with an increased prevalence of periodontitis. The number of current smokers with periodontitis might be reduced by 80%, had they not smoked cigarettes. Of the subjects with periodontitis, 64% could be prevented among current smokers by eliminating tobacco consumption.
Conclusions: Cigarette smoking was strongly associated with periodontitis, and there was a relationship with dose and duration of smoking. These findings contributed to the evidence of smoking as a risk factor
for periodontal disease and support the importance of dose-response analysis on determining the strength of this association.
Key words: periodontal diseases, primary prevention, risk factors
Oral Health Prev Dent 2009; 7: 369376.
Submitted for publication: 02.04.08; accepted for publication: 20.07.08.
Periodontal diseases are chronic diseases, and the causative factors act throughout life (Nicolau et al, 2003). These diseases have historically been a Discipline of Dental Public Health, Department of Pediatric and Social Dentistry, Araзatuba School of Dentistry, Sгo Paulo State University (UNESP), Brazil. b Postgraduate Program in Preventive and Social Dentistry, Araзatuba School of Dentistry, Sгo Paulo State University (UNESP), Brazil. c Discipline of Biostatistics, Department of Pediatric and Social Dentistry, Araзatuba School of Dentistry, Sгo Paulo State University (UNESP), Brazil. Correspondence: Suzely AS Moimaz, Department of Pediatric and Social Dentistry, Araзatuba School of Dentistry, Sгo Paulo State University, Rua Josй Bonifбcio 1193, Araзatuba, SP 16015 050, Brazil. Tel: +55 18 3636 3249. Fax: +55 18 3636 3332. Email: [email protected]
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considered one of the most important global oral health burdens (Petersen, 2005). The distribution and the severity of periodontal diseases can vary in different parts of the world, as it can be observed through the percentage of subjects with periodontitis (Community Periodontal Index [CPI] scores 3 and 4), aged 35 to 44 years in regions such as the Americas (60%), Europe (48%), Africa (40%) and Western Pacific (38%), according to the Global Data Bank of the World Health Organization
(Petersen and Ogawa, 2005). Smoking has been identified as one of the most important risk factors for periodontal diseases that can be accumulated throughout life (Bergstrom, 2006; Heasman et al, 2006; Johnson and Guthmiller, 2007; Thomson et al, 2008); risk calculations suggest that 40% of subjects with chronic periodontitis 369
Moimaz et al may be attributable to smoking, with an increased odds ratio of 5.4 for chronic periodontitis in smokers (Brothwell, 2001). Also, smoking has been implicated in a substantial proportion of the global burden of periodontal diseases (Ezzati et al, 2002). The majority of contemporary studies suggest that smoking increases the risk of periodontal diseases between two and six times, and the differences in the size of the association can be found between current and former smokers (Thomson et al, 2007). The influence of smoking on periodontal health is shown on the effectiveness of treatments of chronic periodontitis in smokers and non-smokers. There are significantly greater reductions in probing depth and bleeding on probing, and greater gain of clinical attachment following non-surgical and surgical treatments in non-smokers compared with smokers (Heasman et al, 2006). Evidence of risk factor status is strengthened by the ability to demonstrate a dose-response, and `years of exposure' to tobacco products is a statistically significant risk factor for periodontal disease (Grossi et al, 1995). A study conducted at Peking University compared smoking status, number of pack years and plasma cotinine levels with bone loss in a group of untreated periodontal patients (Xu et al, 2002). The authors found that cigarette smoking affected the number of teeth with or without periodontal bone loss, and that this effect was related to the degree of smoking exposure, showing the importance of reporting the dose-response relationship. The lack of adequate adjustment for smoking can cause false-positive associations between microbial colonisation, periodontal diseases and systemic diseases. The ideal would be to include the variable smoking in statistical model
s by separating current, former and never smokers with or without additional information such as dose, duration or a combination of both (e.g. pack years and age at which the smoking habit was initiated). Given that smoking is an important risk factor, the control for alternative causal explanations in the periodontal field is an important task in epidemiology and is necessary in the quest for reliable evidence (Spiekerman et al, 2003). In general, there is a substantial body of evidence to support the observation that the more a patient smokes, the greater the degree of periodontal disease. However, there is a need for studies evaluating the strength of this association through dose and duration of smoking, and few data are available on the proportion of periodontal disease that may be attributed to smoking. The goals of the present study were, therefore, to assess the periodontal condition and smoking status, according to dose and duration 370
ictpnoeofnopctruiamglagaaetriteoiotontnefi,nssaumsnbodojuektctihnotesgreniwsntBitiamhraarzpetileep.rrietohsdeeoNnnntotauitttmiisvftbeoeCearsaorttsPdpraeiuubynlbuntdrtlircaigupcebreaalertl-ion MATERIALS AND METHODS The target population of this cross-sectional study was adults aged 30 years or above living in the rural area of Araзatuba in the Brazilian state of Sгo Paulo. This state is located in the southeast part of Brazil. The present survey covered the rural area of the Araзatuba region with about 1,500 inhabitants. A total of 200 individuals with an age range of 35 to 66 years were invited to participate in the present study; 165 subjects were clinically examined and interviewed (82.5% response rate). Those who did not participate were unable to attend the examination or refused to participate. The sample was randomly selected and weighted to represent the 35- to 66year-old adult population of this rural area. These selected individuals were patients who looked for medical and/or dental care at the health centres of the rural districts. The researchers explained to the patients about the aims of the present study and solicited their participation. Exclusion criteria were the presence of diseases/conditions that might pose health risks to the participant or the examiner, or that might interfere with the clinical examination. Clinical examinations were conducted by two clinicians, assisted by a recorder and an assistant, and they were conducted in the health centres, under standardised conditions. The examinations were carried out in natural light. Gauze squares, cotton buds, sterile sets of plane mouth mirrors and CPI probes were packed in sufficient quantities for each working day. Strict procedures for the control of infection were followed. The examinations lasted an average of 10 min per adult. The World Health Organization (WHO, 1997) recommends the CPI and loss of attachment (LA) for periodontal assessment in oral surveys. CPI was recorded for each sextant. Six sites per index tooth (17, 16, 11, 26 and 27 in the maxilla and 47, 46, 31, 36 and 37 in the mandible) per six sextants were probed, and the highest scores were recorded for each sextant on the following basis: 0: healthy; 1: gingival bleeding after gentle probing; 2: the presence of supra- or subgingival calculus or other plaque retentive factors; 3: 4- to 5-mm deep periodontal pockets; 4: 6-mm or deeper periodontal pockets; x: excluded sextant; and 9: not recorded. Information on LA was collected from the same index teeth immediately after recording the CPI score for Oral Health & Preventive Dentistry
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each particular sextant. The extent of LA was recorded using the following codes: 0: 0 to 3 mm; 1: 4 to 5 mm; 2: 6 to 8 mm; 3: 9 to 11 mm; 4: 12 mm or more; x: excluded sextant; and 9: not recorded (WHO, 1997). Eligible subjects who consented to participate were interviewed after oral examination. Two interviewers performed the interviews using a pretested structured written questionnaire that included questions on age, gender and smoking habits (the presence of habit, the number of cigarettes and the period of use). Interviewers and examiners were blinded to both individuals' oral health and smoking condition. Dental examiners participated in a 10-day training and calibration session that focused on the interpretation of indexes measuring pathologies sought during examinations. Intra- and interexaminer reliability and agreement with gold standard clinician were assessed during and at the end of the session. Later, a pilot study was carried out on adults aged 35 to 66 years who attended the Araзatuba School of Dentistry Clinic for testing the feasibility of the study and dental examination. There was no need to change the methodology that was previously proposed. The present study was aware of the Code of Ethics of the World Medical Association
(Declaration of Helsinki), and it received ethical approval from the Research Ethics Committee of the Araзatuba School of Dentistry. The examinations and interviews were undertaken with the understanding and written consent of each subject. Confidentiality was assured to participants, and all recording forms were numbered, but not named. Data analysis The outcome variable was the presence of periodontal pockets, classified as periodontitis and defined as subjects having 1 periodontal pocket of 4 mm around the index teeth (CPI scores: 3 and 4). Exposure to cigarette smoking was calculated for current and former smokers. Classification of smoking status was based on answers given at the moment of data collection
. Current smoker was defined as a person who has been smoking every day or occasionally; former smoker was defined as a person who had smoked in the past, but did not smoke any more; and non-smoker was a person who had never smoked. The number of cigarettes smoked per day was multiplied by the number of days of habit and divided by 20 (i.e. one pack) for calculating the total number of packs of cigarettes smoked. Smokers were classified using smoking thresholds selected Vol 7, No 4, 2009
aeagocrnacrditoeenrsdo(2inan7-rgse3mt5ocoottkemoer7rptsila3er(0sa<0bin1lpetoapwcahkicetskha)),v.aylTig(ch>hoetn7f(so31uNu0mtro0ospt2pmtiaM7fotooec3noCkkrsi4oimsnosPp)gpafe,uzya>mcbncerakotl2ictisgdeca0e)a--l tion pack years, 7.5 to 20 pack years, 0.1 to 7.4 pack years and < 0.1 pack years, respectively. This classification was based on previously published studies (Susin et al, 2004). Attributable risk (AR) among smokers estimated the absolute excess risk for periodontitis because of smoking, or the fraction of smokers who would not have periodontitis if smoking had not occurred. Attributable risk per cent (AR%) converts the attributable fraction among exposed into the percentage of smokers with periodontitis because of smoking. Attributable risk to the population (PAR) is the proportion of reduction of periodontitis risk that could be achieved by eliminating smoking from population, while other risk factors remain unchanged. Attributable risk to the population per cent (PAR%) converts the PAR into the percentage of subjects with periodontitis that is preventable (Koepsell and Weiss, 2003). For the descriptive statistical analysis of the periodontal parameters, mean values were calculated for each patient. Bivariate statistical analyses were used to associate smoking status, duration and quantity with periodontal condition. Level of statistical significance
was chosen at P < 0.05. RESULTS Patients presenting to oral examination and consenting to participate were aged 35 to 66 years (mean = 39.2 years; SD = 5.1 years); 67.9% were females. Intra- and interexaminer reliability was considered excellent (kappa coefficient [j] was 0.85 and 0.81, respectively). The majority (96.4%) reported brushing their teeth one or more times per day, whereas only 25.5% flossed their teeth at least once per day. Overall, 52.7% of the adult population was exposed to cigarette smoking. Of the 165 individuals, 35.8% (59/165), 16.9% (28/165) and 47.3% (78/165) were current, former and nonsmokers, respectively. Among current smokers (59/165), the mean years of exposure to smoking was 17.5: 17% (10/ 59) consumed a mean number of 25.3 pack years (1 pack/day for 25 years), classified as heavy smokers; 23.7% (14/59) consumed a mean number of 14.6 pack years (1 pack/day for 14 years), moderate smokers; and 59.3% (35/59) consumed a mean number of 3.1 pack years (1 pack/day for 3 years), light smokers. 371
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Moimaz et al
Periodontal condition (CPI) 13%
Healthy (score 0) Bleeding (score 1)
Calculus (score 2)
Periodontal pocket (score 3)
Fig 1 Percentage distribution of subjects according to periodontal condition, assessed through the Community Periodontal Index (CPI).
Loss of periodontal attachment (LA) 2% 12%
LA 0-3 mm (score 0) LA 4-5 mm (score 1) LA 6-8 mm (score 2)
cesaumrnsrdroevkheneetrrsassuv;mysmosnkmooednores-ksreamvrteseorksvseuemrsrsso;nuksoliegnnrh-ssotmnvs-oesmkrmNsoeuokrossket;ersnrfftsoooevC.rnresmoS-rssPpsetmeauurytsbnosirskmlicntiegcieocorasankt;l--ion analysis showed that current smokers had an 11 times (95% confidence interval [CI] = 4.69 to 26.62) and former smokers had a nine times (CI = 3.29 to 25.96) greater probability of having periodontal pockets than non-smokers (Table 2). The number of pack years--heavy and moderate versus light smokers (P = 0.0004)--was associated with an increased prevalence of periodontitis among current smokers. Years of exposure to tobacco was a statistically significant risk factor for periodontal disease, with an increased odds ratio of 12.11 (CI = 2.30 to 63.69) for periodontitis in patients smoking cigarettes
for 10 years or more. Among current smokers, the rate of periodontitis that was attributable to smoking was 47.8/100 (AR = 0.478), which means that 81% of the incidence of periodontitis among smokers was due to smoking (AR%). Approximately 64% of the cases of periodontitis could be prevented among current smokers (PAR%) by eliminating tobacco consumption (Table 2). Among the demographic variables, only age (P = 0.0023) was associated with the prevalence of periodontitis, with older people being more susceptible to periodontal disease (Table 1).
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Fig 2 Percentage distribution of subjects according to loss of periodontal attachment, assessed through the LA index. The prevalence of periodontitis (having 1 pocket of 4 mm around the index teeth) in the study population
was 35.2% (58/165), corresponding to CPI scores 3 and 4. Gingivitis, represented by bleeding and calculus (scores 1 and 2), was the most frequent periodontal alteration (Fig 1). Overall, 13.9% (23/165) had LA between 4 and 8 mm, corresponding to LA scores 1 and 2. No subjects showed LA > 9 mm (Fig 2). Periodontitis was significantly more prevalent among current (P < 0.0001) and former smokers (P < 0.0001) than among non-smokers. Table 1 shows chi-square tests conducted between the groups, comparing specific characteristics such as age, gender and smoking status according to the presence (CPI scores 3 and 4) or the absence (CPI scores 0 to 2) of periodontitis: 35 to 44 years versus 45 to 54 years versus 55 to 66 years; female versus male; 372
DISCUSSION The findings of the present study indicate that gingivitis was more prevalent in the rural adult Brazilian population than periodontitis, and the rate of this condition was lower than that reported for the Americas in the Global Data Bank of WHO (2003). The healthier periodontal condition of this specific population may be due to a better socioeconomic status
and a greater access to oral health care
than that of the Americas regions overall. In addition, half of the subjects were smokers, and cigarette smoking was a strong risk factor for periodontitis. The number of pack years had a significant correlation with the size of the association. The available information on dose and duration of cigarette smoking in the present study allowed a more precise evaluation of the association between periodontal disease and smoking. The classification of individuals into current, former and non-smokers minimised the bias and contributed to a better analysis of the evidence. The authors also estimated that the number of smokers having 1 pocket of 4 mm around the Oral Health & Preventive Dentistry
Table 1 Variable
characteristics and smoking status of individuals in
Individuals with probing depth 4 mm (CPI1 scores 3 and 4)
Not study population Individuals with probing depth < 4 mm (CPI1 scores 0 to 2)
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Current smokers (overall)
1CPI: Community Periodontal Index. 2Reference Group
% 66.9 27.3 0 69.8 62.5 88.5 50 40.7 60 7.2 20
0.0023 0.3876 < 0.0001 < 0.0001 < 0.0009 < 0.0001 < 0.0001
Table 2 Estimated ORs with 95% CI and AR, AR% and PAR% due to smoking on the occurrence of periodontitis1
Prevalence of periodontitis1
Current smokers Former smokers Non-smokers2 Overall
35/59 14/28 9/78 58/165
59.3 50.0 11.5 35.2
1Defined as having 1 pocket of 4 mm around the index teeth (CPI scores 3 and 4). 2Reference group.
index teeth may be reduced by approximately 80% if these individuals had not been smokers. A smoking cessation programme could result in a reduction in the percentage of subjects by up to 64% in this population. Clearly, the projected number of preventable cases would depend on the success of the smoking cessation programme. The findings of the present study were similar to those of other studies in evaluating smoking dose and duration. Xu et al (2002) reported a positive association between heavy smokers and the number of
teeth with moderate bone loss (P < 0.001) compared with non-smokers, and a positive correlation between pack years and the number of teeth with light bone loss (P < 0.005). Although the present results can be compared with these, the authors analysed the periodontal pocket depth (Xu et al, 2002) and not bone loss. Hence, the periodontal disease and smoking association was confirmed using different measures of periodontal disease throughout the dose-response evaluation. Also, the authors reported that plasma cotinine levels correlated significantly
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Moimaz et al with the number of cigarettes smoked per day, justifying that the self-reported smoking status was precise. Recent studies estimate different potential reductions in the percentage of periodontal disease cases compared with this study (Hyman and Reid, 2003; Susin et al, 2004). Several case definitions (loss of clinical attachment versus periodontal pocket depth versus bleeding) may be causing differences in the size of reductions. Susin et al (2004) verified the percentage of cases attributable to smoking in the southern Brazilian population and defined subjects as those with 30% of their teeth showing periodontal attachment loss 5 mm; it was estimated that 28% and 48% of cases were attributable to moderate and heavy smokers, respectively. On the other hand, Hyman and Reid (2003) defined cases as 10% of the population with the greatest mean attachment loss within each age group, and estimated that the smoking attributable fraction for US current smokers was 82% and 84% subjects in the 20- to 49- and > 50year-old groups, respectively. Tooth loss and impaired oral function are expected to grow as a public health problem in many developing countries
(Petersen, 2005). Severe periodontitis, which may result in tooth loss, is found in 5 to 15% of most population (WHO, 2003). Scientific evidence represented by the present study and many other good quality studies show that the usage of tobacco is a major factor for adult periodontal disease. With the growing consumption of tobacco in many countries, the risk of periodontal disease and tooth loss, therefore, may increase. The incidence of periodontitis in past decades can even be estimated by the prevalence of smoking (Hujoel et al, 2003). Disease definition can have an impact on the prevalence, and relative risks may vary as a function of prevalence (Bergstrom, 2003). The most common description used for periodontal diseases is the CPI, which was used in the present study and was the method recommended by WHO (1997) for population screening purposes. The Fifth European Workshop on Periodontology issued new case definition for periodontitis, which aimed at better uniformity within the literature (Tonetti and Claffey, 2005). Although CPI has certain shortcomings when used as a stand-alone means of assessing the extent and severity of periodontal disease, it has been widely used for descriptive periodontal epidemiological studies and needs assessment in developed and developing countries (Petersen and Ogawa, 2005). Although many studies reported their findings using different periodontal index and case definitions, the present findings are consistent with other studies 374
st12hh90eo80wo90ic;,ncguB2rae0rer0gsn6sicg;tenroiBfiomecfacpkenettreieaotfldf,eoac2nl,tt0ao10lf90dc9;iisg7TeNa;oaroemsAtteltabesfrtaoes(nCaBrsmdonesPapdorerugkysAibnenrtslrtigciomgcemoaaanlt,,,ion 2000; Hanioka et al, 2007; Kibayashi et al, 2007; Ojima et al, 2007; Thomson et al, 2007, 2008; Wang et al, 2007), demonstrating the power of smoking as a risk factor for periodontitis. Only age showed a statistically significant association with periodontitis among the demographic variables. The relationship between these two conditions is well established in the literature (Persson, 2006). The strengths of the present study include a high dose-response (> 80%), the analysis by dose and duration of smoking and the size of the association, reporting that the lower limit of 95% CI was > 3. When the lower limit of the relative risk measure is large, the need for detailed control for competing causal explanations is minimal. In the present study, the lower limit of the odds ratio for periodontal disease in current smokers exceeds 400, which minimises the potential that alternative causal explanations would explain away this strong association. The weaknesses of the present study include the outcome assessment. Although probing depth and loss of clinical attachment are a common measure of periodontal disease assessment in the majority of studies (Tomar and Asma, 2000; Hyman and Reid, 2003; Susin et al, 2004; Tonetti and Claffey, 2005; Geismar et al, 2006; Ojima et al, 2006; Thomson et al, 2007), it is a surrogate and not a true outcome. The best measure for diagnosis of periodontitis would be tooth loss, a true outcome that reflects unequivocal evidence of tangible consequence perceived by the patient, instead of probing depth or attachment level, which are physical signs that are used as a substitute for a clinically meaningful end point. However, due to several advantages, such as standardisation, validation and ease of measurement by clinician and universal use, which allows comparison among studies, these measures have been considered the gold standard for evaluating periodontal diseases and have been used for many decades in periodontal studies, recommended by international organisations and centres of research (Cutress et al, 1987; Williams et al, 2001; Heitz-Mayfield et al, 2002; Kingman and Albandar, 2002; WHO, 2003). Studies based on true end points may be of a long duration and require the recruitment of thousands of patients and high costs (Hujoel et al, 2000), therefore in some situations the use of current surrogates that can be evaluated any Oral Health & Preventive Dentistry
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time is more feasible. Based on these reasons, probing depth and LA level were chosen as outcome measures in the present study. Data accumulated over the past 20 years offer convincing evidence that smokers exhibit greater bone loss and attachment loss, as well as more pronounced frequencies of periodontal pockets, than non-smokers do. The harmful effects manifest themselves by interfering with vascular and immunological reactions, as well as by undermining the supportive functions of the periodontal tissues. The interference with vascular and inflammatory phenomena may be one potential mechanism for the destructive effects of smoking on periodontal tissues (Bergstrom, 2004). Smoking and unhealthy eating
habits lead to destructive periodontal disease as well as to chronic non-Communicable diseases
such as diabetes (Willi et al, 2007), cardiovascular disease (Scannapieco et al, 2003) and certain cancers in late adulthood (Doll et al, 2004); successful smoking prevention and cessation programmes aimed at reducing cancer and cardiovascular mortality may have inadvertently reduced the incidence of destructive periodontal disease, even before tobacco use became widely recognised as a cause of destructive periodontal disease (Hujoel, 2008). Dental policy, as smoking cessation programmes, and research priorities aimed at the primary prevention of destructive periodontal disease can also help reduce the occurrence of other systemic diseases, due to their common risk factors. Primary prevention of periodontal diseases may lead to benefits beyond dental health and may have greater implications for general health. In conclusion, the prevalence of periodontitis in the present study population was not considered high. Cigarette smoking was strongly associated with periodontitis, and there was a relationship with dose and duration of smoking. A significant percentage of cases might have been prevented if smoking cessation intervention had been implemented. These findings contribute to the evidence of smoking as a risk factor for periodontal diseases and support the importance of dose-response analysis on determining the strength of this association. Populationbased smoking cessation programmes should be implemented in an attempt to reduce the incidence of periodontal disease in populations with a high level of smoking exposure. ACKNOWLEDGEMENT The present research was supported by the FAPESP Foundation (The State of Sгo Paulo (Brazil) Research Foundation), Grant No. 01/08989-4.
R1E.FApdEiilpsbReeaa,nEsdaNeanrdCaJcMEnidg,SaSrtetortoettechksfumlososCksiF.n,gJAadPseesrraiisonkdyoafanMctNotRolo,rs2Wt0fioMfn0trone0oCpr;sDio7emsMr1Ppiaoe:.u1zydC8bnoeri7gntlicait4gcaaer,all tion 1881. 2. Beck JD, Cusmano L, Green-Helms W, Koch GG, Offenbacher S. A 5-year study of attachment loss in community-dwelling OLDER ADULTS
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