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    Periodontal Disease, Hypertension,and Blood Pressure Among Older Adults

    in Puerto RicoSona Rivas-Tumanyan,* Maribel Campos,* Juan C. Zevallos, and Kaumudi J. Joshipura*

    Background: Current scientific evidence addressing the re-lationship between periodontitis and hypertension is limitedto studies producing inconsistent results.

    Methods: All participants of an ongoing representative co-hort of Puerto Rican elderly who were 70 years old and resid-ing in the San Juan metropolitan area were invited to thiscross-sectional study. Periodontal probing depth (PD) and at-

    tachment loss (AL) were summarized using the Centers forDisease Control and Prevention and the American Academyof Periodontology definition for severe periodontitis (2 teethwith AL 6 mm and 1 tooth with PD 5 mm). Three repeatedblood pressure (BP) measurements taken were averaged us-ing a standardized auscultatory method. Information on hy-pertension history, use of antihypertensive medications, andpotential confounders (age, sex, smoking, heavy and bingedrinking, diabetes, use of preventive dental services, flossing,body mass index, consumption of fruits, vegetables, wholewheat bread, and high-fiber cereal) was collected during in-person interviews. High BP was defined as average systolicBP 140 mm Hg or diastolic 90 mm Hg. Multivariate logisticregression models were used to study the relationship be-tween severe periodontitis, hypertension history, and high BP.

    Results: The study population comprised 182 adults. Inmultivariate analysis, there was no association betweensevere periodontitis and hypertension history (odds ratio[OR] = 0.99; 95% confidence interval [CI]: 0.40 to 2.48). Se-vere periodontitis was associated with high BP, with ORof 2.93 (95% CI: 1.25 to 6.84), after adjusting for age, sex,smoking, and binge drinking. This association was strongerwhen restricted to those with hypertension or taking antihyper-tensive medications: OR = 4.20 (95% CI: 1.28 to 13.80).

    Conclusion: The results of this study suggest that peri-

    odontitis may contribute to poor BP control among olderadults. J Periodontol 2013;84:203-211.

    KEY WORDS

    Blood pressure; hypertension; periodontal diseases;periodontitis.

    Hypertension is one of the major

    causes of cardiovascular diseaseand other serious health condi-tions. Hypertension-related mortality inthe United States was estimated toreach 54,000 deaths in 2004.1 As re-ported by Garcia-Palmieri,2 hypertensionaccounted for 43 deaths per 100,000inhabitants in Puerto Rico in 2002.

    Periodontal disease has recently drawnincreasing attention because of its po-tential relationship with cardiovasculardisease, as a chronic inflammatory con-dition linked with systemic markers ofinflammation and endothelial dysfunc-tion.3 A number of research studies havesuggested a possible link betweenchronic inflammation and hyperten-sion, emphasizing the need for furtherresearch.4-7 However, to date, only afew studies8-12 have reported on therelationship between oral health and hy-pertension, producing inconsistent re-sults. In a large cross-sectional study,Holmlund et al.8 reported an increasedrisk of self-reported history of antihy-

    pertensive treatment was associatedwith the number of periodontal pockets,as well as a l inear trend betweenperiodontal disease severity and anti-hypertension treatment. A recent pro-spective study on periodontal diseaseand incident hypertension among Japa-nese workers showed similar results.9

    The scientific evidence was further sup-ported by an intervention study.10 Ina randomized controlled trial, intensive

    * Center for Clinical Research and Health Promotion, University of Puerto Rico School ofDental Medicine, San Juan, Puerto Rico

    Endowed Health Services Research Center, University of Puerto Rico School of Medicine,San Juan

    doi: 10.1902/jop.2012.110748

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    treatment for periodontal disease (subgingival scaling,root planing, and local antimicrobial treatment) led toa statistically significant decrease in systolic bloodpressure (SBP) at the end of the second month offollow-up (7 mm Hg change in the treatment arm)compared to the baseline measurements; the reduc-

    tion was greater among smokers (14 mm Hg decreasefrom baseline).10 On the other hand, our recentanalysis of the Health Professionals Follow-Up Studydid not show any significant associations between self-reported periodontal disease and hypertension di-agnosis over 20 years of follow-up.11Similarly, analysisof the Third National Health and Nutrition Examina-tion Survey data did not reveal any associationbetween periodontal disease severity and BP.12

    In this study, the authors aim to evaluate the as-sociation between clinically measured periodontaldisease and clinically assess hypertension in a re-

    presentative sample of elderly Puerto Ricans.

    MATERIALS AND METHODS

    Study PopulationParticipants were recruited for the Puerto Rican El-derly Dental Health Study (PREDHS) from August toDecember 2007, from an ongoing representativecohort of Puerto Rican elderly (the Puerto Rican El-derly: Health Conditions [PREHCO] study). ThePREHCO study used probability-based sampling toidentify houses across Puerto Rico with 1 adult of60 years of age from census track data.

    The PREDHS study population included residentsof the San Juan metropolitan area who were 70years of age at the time of recruitment to PREDHS(2007). PREHCO participants who were earlier invitedto participate in another clinical study and those whodid not pass the Caban Mini-Mental Status Test13

    (scored11 points) andtherefore were not consideredmentally competent to complete the in-person ex-amination and interview without the assistance ofa proxy were excluded.

    A total of 392 elderly were contacted regarding thePREDHS study by letters, phone calls, and home visits.Twenty-three participants could not be reached aftermultiple attempts using all means of communication.Of 369 participants who we attempted to contact todiscuss the goals and procedures of the study, 107refused participation and 19 were deceased, hospi-talized, or bedridden. After initial screening by phone,participants were excluded if they had conditions thatcould potentially lead to systemic complicationsfrom the periodontal examination. Participants werealso ineligible if they were instructed by a physicianto take antibiotics prior to any dental examination,were undergoing renal dialysis, taking anticoagulants,or had any of the following diseases, conditions, and

    medical procedures: 1) specific heart conditions (i.e.,

    congenital heart murmurs, valve problems, congen-ital heart disease, or endocarditis); 2) hip bone orjoint replacement, 3) rheumatic fever; 4) hemophilia;5) a pacemaker; 6) an automatic defibrillator; or 7)artificial material in the cardiovascular system. Thefinal sample of the PREDHS was composed of 185

    participants (62 males and 123 females, aged 70 to97 years). This study was conducted in accordancewith the Helsinki Declaration of 1975, as revised in2000, and approved by the Institution Review Boardfor Human Subjects at the University of PuertoRico. All participants signed a written informed con-sent form prior to all research procedures.

    Three teams of dental examiners (Dr. EnriqueSantiago, Dr. Maria L. Aguilar, Dr. Mauricio Montero,University of Puerto Rico School of Dental Medicine,San Juan, Puerto Rico) and recorders (Ms. Yari Valle,Dr. Vanesza Robles, Mr. Michael Brunelle, Ms. Jeniffer

    Torres, University of Puerto Rico School of DentalMedicine, San Juan, Puerto Rico) completed datacollection by performing home visits. All dental exam-iners received training and calibration on oral healthassessment and BP measurement.

    All participants completed an in-person interviewon: 1) current oral health status; 2) history of dentaldiseases and procedures; 3) use of dental services; 4)oral hygiene habits; 5) physical activity; and 6) foodintake. Resting BP was measured and a list of currentprescription medications was recorded. A total of183 participants also agreed to participate in the

    clinical assessment of periodontal disease status;two individuals declined. Original participants in-cluded in the final sample were similar to those whorefused participation in terms of age, smoking, anddiabetes and included a somewhat higher number ofmen (P values for t test for age differences and forx2 test for sex, smoking and, diabetes differences>0.05).

    Assessment of Periodontal Disease StatusPeriodontal disease was assessed by clinical mea-surements of probing depth (PD) and attachment loss(AL) at four sites per tooth (mid-buccal, mesio-buccal,

    disto-buccal, and distal-lingual) using a full-mouthdesign (excluding third molars). All measurementswere taken with a periodontal probe and roundedoff upward to the nearest millimeter. Clinical ALwas computed as the difference of gingival recessionand PD measurements for all sites. Three inter-proximal sites (mesio-buccal, disto-buccal, and dis-tal-lingual) per tooth were used to derive periodontaldisease status, according to the Centers for DiseaseControl and Prevention and the American Academyof Periodontology definition for severe and moderateperiodontal disease.14 Severe periodontal disease

    PCP2, Hu-Friedy, Chicago, IL.

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    was defined as the presence of 2 teeth with AL6 mm in any of the interproximal sites and 1 toothwith PD 5 mm at any interproximal site. Moderateperiodontal disease was defined as the presence of2 teeth with AL 4 mm or 2 teeth with PD 5 mm.

    Prior to the study, all dental examiners were trained

    in accordance with the NHANES standards15 andcalibrated by a NHANES reference examiner (Dr.Bruce Dye, National Center for Health Statistics,Centers for Disease Control, Hyattsville, Maryland).Periodontal measurements taken by trained exam-iners were in absolute agreement with the referenceexaminer 87% to 94% of the time, with weighted kcoefficients ranging between 0.75 and 0.87.

    Assessment of Hypertension and BPDuring in-person interviews, all participants wereasked: Have you ever been diagnosed by a doctoror another health professional with high blood pres-sure? Those who responded positively to thequestion were classified as having a hypertensiondiagnosis history.

    Dental examiners were additionally trained andcalibrated by a cardiologist (JZ) in a standardizedindirect BP determination by the auscultatorymethod. Participants arm length and circumferencewere first measured to determine the correct cuffsize. After the participant rested for 5 minutes, SBPand diastolic BP (DBP) measurements were takenthree times within 1- to 2-minute intervals, in a sittingposition, on the right arm of the participant, using

    a bell stethoscope and a mercury sphygmomanome-ter. Measurements were rounded upward to the near-est 2 mm Hg, recorded, and later averaged. BP wasclassified as high if average SBP was 140 mm Hg oraverage DBP was 90 mm Hg. We also used a sec-ondary outcome of three-category severity of hy-pertension, based on SBP and DBP cutoff pointssuggested by the JNC7 report16 (stage0ifSBP1

    drink daily for women. Men consuming 5 drinks ona single occasion and women consuming 4 drinkson a single occasion were classified as binge drinkers.Information on some additional potential confounders(food intake,useofpreventive dental services, physicalactivity) was collected during PREDHS in-personinterviews. Fruit and vegetable, whole wheat bread,and high-fiber cereal consumption was assessed inPREDHS as the number of servings per day or weekand later categorized into tertiles.

    Data AnalysesStatistical analysis was conducted using statisticalsoftware. A multivariate logistic regression modelsto evaluate the associations between periodontaldisease and hypertension, as well as periodontaldisease and BP was used, while adjusting for potentialconfounders. Odds ratios (ORs) and 95% CI (confi-dence interval) were reported. The relationship be-tween severe periodontal disease and severity ofhypertension (stages 0 to 2) was also explored usingpolynomial regression analysis. The authors consid-ered the following potential confounders in this mul-tivariate models: 1) age; 2) sex; 3) smoking (never/past/current); 4) heavy and binge drinking (yes/no);

    5) history of diabetes diagnosis; 6) physical activitywithin the past month (yes/no); 7) overweight/obesity(BMI 25 kg/m2); 8) use of preventive dental serviceswithin the past year (yes/no); 9) daily flossing (yes/no);and 10) consumption of fruit and vegetables (tertiles),whole wheat bread (tertiles), and cereal (tertiles). Toarrive at more parsimonious models for our analysison hypertension and high BP, a backward elimina-tion technique applying a 10% change-in-estimaterule17 was used while forcing age, sex, and smokinginto the model. The final multivariate models (model2) for hypertension diagnosis history included all the

    considered confounders; the final model for BP in-cluded only: 1) age; 2) sex; 3) smoking; and 4) bingedrinking. Additional models on high BP also includedthe number of antihypertensive medications andnumber of teeth (1 to 10, 11 to 16, 17 to 24, 25 to 32).

    To evaluate the effect of periodontal disease on highBP with regard to specific at-risk criteria, we repeatedour analysis on high BP within strata by antihyper-tensive medication use, smoking, diabetes, and num-ber of teeth (1 to 16, 17 to 32). A Wald test to testfor effect modification by diabetes, smoking, numberof teeth, and antihypertensive medication use was

    SAS v. 9.2, SAS Institute, Cary, NC.

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    Table

    1.

    Age-andSex-AdjustedCha

    racteristicsofthePREDH

    SPopulation,

    WithorWithoutSeverePeriodontalD

    isease*

    Characteristic

    OverallPopulation

    ParticipantsWithSeverePeriodontalDisease

    ParticipantsWithoutSeverePeriodontalDisease

    Numberofparticipants

    182

    43

    139

    Age,mean(SD)

    78(6.0)

    77(7.2)

    78(5.5)

    Male(%)

    34

    58

    26

    Smokinghabits(%)

    Never

    74

    67

    77

    Past

    21

    23

    20

    Current

    5

    10

    3.1

    Diabetesdiagnosis(%)

    22

    36

    26

    Overweight(BMI25kg/m2)(%)

    65

    65

    64

    Nophysicalactivitywithinthelastmonth

    (%)

    61

    60

    60

    Heavydrinking(%)

    3.3

    8

    0.6

    Bingedrinking(%)

    5.5

    14

    2.7

    Consuming5fruitsandvegetables/day(%)

    12

    9.3

    12

    Dentalcheckupvisitwithinthepastyear(%)

    34

    20

    37

    Periodontaldiseasestatus(%)

    Moderate

    59

    0

    79

    Severe

    24

    100

    0

    Hypertensiondiagnosis(%)

    63

    64

    70

    HighBP(%)

    58

    75

    55

    *V

    aluesforparticipantswithandwithoutsever

    eperiodontaldiseasearestandardizedtoageandsexdistributionofthePREDHSpopulation,unlessotherwiseindicated.

    V

    aluesarenotageandsexadjusted.

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    used. In addition, the authors restricted the analysisto participants with hypertension diagnosis or takingantihypertensive medications, as well as those with iso-lated systolic (ISH) hypertension, and those with isolatedsystolic or systolic-diastolic (SDH) hypertension, andcompared them to participants with normal SBP and

    DBP.Missing data: Thirty-two (17.5%) participants had

    missing information on 1 of the confounders. Missingdata on physical activity; weight; and fruit and vege-table, whole-wheat bread, and cereal intake werenot associated with the self-reported hypertensiondiagnosis or high BP (Pvalues for all x

    2tests >0.05).

    One participant was excluded with missing in-formation on use of preventive dental services andcreated missing indicator variables for the remainingconfounders and adjusted for them in regressionanalysis. After conducting sensitivity analysis, miss-

    ing values in food intake questions were assigned tothe lowest consumption tertile (reference group),which provided the most conservative effect estimatein logistics regression analysis.

    RESULTS

    The final sample for this analysis included 182 par-ticipants (Table 1). Participants with severe peri-odontal disease were more likely than those withoutperiodontal disease to be male (58% versus 26%among those without severe periodontitis), smokers(current smokers: 10% versus 3.1%), heavy (8%

    versus 0.6%) and binge (14% versus 2.7%) drinkers,and to have diabetes (36% versus 26%). They were alsoless likely to consume five or more servings of fruitsand vegetables a day (9.3% versus 12%) or have adental checkup within the past year (20% versus 37%).

    The authors identified 126 participants who re-ported history of hypertension diagnosis by a physi-cian and 106 participants with high BP. Of those with

    high BP, 68 were classified as having stage 1 and 38participants as stage 2 hypertension. After adjustingfor all potential confounders, the authors did not ob-serve any association between severe periodontaldisease and history of hypertension diagnosis (Table2; OR = 0.99; 95% CI: 0.40 to 2.48). Participants with

    severe periodontal disease had 2.93 times higherodds of having high BP on examination (multivariate-adjusted OR = 2.93; 95% CI: 1.25 to 6.84). The ORestimate for severe periodontal disease remainedstrong and statistically significant after additionaladjustment for antihypertensive medications (OR=3.00; 95% CI: 1.28 to 7.03) or for number of teeth(model 4, OR = 2.87; 95%CI: 1.22 to 6.74). In ourpolynomial regression analysis between severe peri-odontal disease and stages of hypertension, we ob-served an OR of 3.54 for stage 1 hypertension (model2, 95% CI: 1.41 to 8.85); however, the OR for stage 2

    hypertension was not statistically significant (model 2,OR = 2.05; 95% CI: 0.69 to 6.07).

    When the analysis was restricted to participantstaking antihypertensive medications (Table 3), morethan a four-fold increase in odds of high BP associatedwith severe periodontal disease (model 2, OR = 4.63;95%CI:1.20to17.94)wasobserved.Theassociationswere similar among participants with a history of hy-pertension diagnosis or taking antihypertensive med-ications or both (OR = 4.20; 95% CI: 1.28 to 13.80).The association between severe periodontitis andBP was not statistically significant among past and

    current smokers (OR=

    1.99; 95% CI: 0.49 to 8.12).The authors did not observe a statistically significantassociation among participants with (model 2, OR =3.76; 95% CI: 0.74 to 19.01) or without historyof diabetes (model 2, OR = 2.00; 95% CI: 0.75 to5.35, P for effect modification = 0.51). When the au-thors restricted their analysis to participants withisolated systolic or systolic-diastolic hypertension

    Table 2.

    OR (95% CI) for Hypertension and BP According to Severe Periodontal Disease Status

    Outcome Number of Participants Model 1* OR (95% CI) Model 2

    OR (95% CI)

    History of hyper tension diagnosis 126/182 0.80 (0.38 to 1.71) 0.99 (0.40 to 2.48)

    High BP, stage 1 and 2 (SBP 140 or DBP 90

    mm Hg)

    106/182 2.35 (1.08 to 5.14) 2.93 (1.25 to 6.84)

    Stage 2 hypertension (SBP 160 or DBP

    100 mm Hg)

    38 1.79 (0.66 to 4.86) 2.05 (0.69 to 6.07)

    Stage 1 hypertension (140 SBP

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    Table

    3.

    OR(95%CI)forHighBPA

    ccordingtoSeverePeriod

    ontalDiseaseStatusforSelectedSubgroupsof

    PREDHSPopulation

    Subgroup

    Numberof

    Participants

    Model1*OR(95%CI)

    M

    odel2

    OR(95%CI)

    PVa

    lueforEffect

    M

    odification

    Participantstakingantihypertensivemedic

    ations

    70/115

    2.69(0.90to8.02)

    4.63(1.20to17.94)

    0.67

    Participantsnottakingantihypertensivem

    edications

    36/67

    2.34(0.68to8.10)

    3.06(0.78to11.98)

    Participantswithhypertensiondiagnosiso

    rtaking

    antihypertensivemedications

    78/135

    2.49(0.94to6.60)

    4.20(1.28to13.80)

    Never-smokers

    76/134

    3.09(1.12to8.57)

    3.09(1.12to8.57)

    0.62

    Pastandcurrentsmokers

    30/48

    1.77(0.45to6.90)

    1.99(0.49to8.12)

    Patientswithdiabetes

    34/52

    3.42(0.70to16.76)

    3.76(0.74to19.01)

    0.51

    Patientswithoutdiabetes

    72/130

    1.82(0.72to4.62)

    2.00(0.75to5.35)

    Participantswith17teeth

    60/103

    2.24(0.76to6.63)

    2.36(0.74to7.53)i

    0.77

    Participantswith44 years of age (OR =1.36; 95% CI: 0.80 to 2.33). This study12 used thesame periodontal measures as the current study.However, periodontal data were collected only inrandomly assigned half-mouths of each participant,rather than the whole mouth. This may have resultedin non-differential misclassification (under diagnosis)of periodontal disease and, therefore, underestima-tion of the magnitude of the association betweenperiodontitis and BP.

    The first two reports cited here8,9 and the present

    study all found a significant association betweenperiodontal disease and hypertension/blood pressure;however, the effect estimates (OR) for the presentstudy are stronger. PREDHS participants with severeperiodontal disease have an almost three-fold increase inodds of having high BP, compared with those withoutsevere periodontal disease (multivariate OR = 2.93;95%CI: 1.25 to 6.84).This association remains strongand statistically significant even after adjusting forantihypertensive medication use and number of teeth.The present study population is older compared toprevious publications,8-12 which suggests that local

    and perhaps consequent systemic inflammation mightplay a greater role in BP control among the elderly.The authors analysis on stages of hypertension

    suggests a threshold relationship between periodontaldisease and BP, rather than a linear trend. However,the authors have limited statistical power amongparticipants with stage 2 hypertension (SBP160 mmHg and DBP 100 mm Hg).

    The relationship between severe periodontitis andBP appears to be stronger among participants witha known diagnosis of hypertension and those takingantihypertensive medications, suggesting that el-derly with severe periodontitis may have poorer re-sponse to antihypertensive treatment compared tothose who have a healthier periodontium. Inasmuchas the majority of PREDHS participants with hyper-tension presented with ISH (N = 76) or SDH (N = 26),results from the stratified analysis limited to ISH andSDH were similar to those obtained from the overallpopulation.

    Smoking and diabetes have been shown previouslyto be effective modifiers of the relations betweenperiodontal disease and cardiovascular outcomes;27

    however, no effect modification by these variables wasobserved. In age and sex analyses among never-

    smokers, periodontal disease was associated with an

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    OR of 3.09 (95% CI: 1.12 to 8.57); however, theauthors were unable to adjust for binge drinking inmodel 2, due to small power and instability of themodel. The association between periodontitis and BPwas somewhat weaker and not significant amongparticipants without diabetes history (model 2, OR =

    2.00;95%CI:0.75to5.35),comparedtotheestimatesfrom the overall population, which might be explainedby limited sample size in this stratum. At the sametime, a weaker association among participants with-out diabetes suggests potential residual confoundingof our main results by severity of undetected diabetesand prediabetes.

    The present study has several strengths, includingcollection of high-quality clinical data on periodontaldisease and BP. A full-mouth oral examination wasconducted on all participants; all dental examiners weretrained according to NHANES criteria and showed

    excellent agreement with the reference examiner.Detailed information on potential confounders wasalso collected, including variables reflecting healthbehavior, such as use of preventive dental services,fruit and vegetable intake, and flossing. The presentstudy participants were not requested to refrain fromtheir medications prior to the examination; hence, theBP measurements obtained from participants re-ceiving antihypertensive treatment reflect their truelevel of BP control.

    This study also has several limitations. The cross-sectional nature of our study does not allow causal

    interpretations of our findings, because we do not haveinformation on temporality of the relationship betweenperiodontal disease and BP. However, hypertensionis not likely to cause periodontal disease. Inasmuch asour BP measurements were taken on only one occa-sion, day-to-day variations in BP may have resultedin random misclassification of our outcome measureof high BP. However, the authors expect that thismisclassification was non-differential with regard toperiodontal disease status, which would result in un-derestimation of the true OR between periodontaldisease and high BP. Also, due to a relatively smallsample size, there was not enough statistical powerfor some of the subgroup analysis (e.g., analysislimited to participants with diabetes, and never, past,and current smokers). The authors information ondiabetes, one of major potential confounders of thisrelationship, was self-reported, which does not excludepossible residual confounding; hence, the resultsshould be interpreted with caution. In addition, thisstudy was limited to Hispanic elderly of Puerto Ricandescent, which may limit the generalizability of ourfindings to other populations. Despite these limita-tions, the present study demonstrates a possiblestrong relationship between periodontal health and

    BP control, which may have a major public health

    impact among the elderly. Given the limitations of thisstudy, further studies are needed to confirm this as-sociation in other populations.

    ACKNOWLEDGMENTS

    This work was partially funded by National Institute Den-

    tal and Craniofacial Research Grants R01AG1620904,G12RR03051, and K24DE16884 from the NationalInstitutes of Health (Bethesda, Maryland). We wouldlike to acknowledge the PREDHS team (Dr. EnriqueSantiago, Dr. Maria L. Aguilar, Dr. Ana L. Davila,Dr. Alberto Garcia, Ms. Sasha Martinez, Ms. Yari Valle,Ms. Vanesza Robles, Mr. Francisco Munoz, Mr. MichaelBrunelle, Ms. Mildred Rivera, Ms. Jennifer Torres, Ms.Jennifer Guadalupe, and Dr. Monik Jimenez) for theirhelp with the study. The authors report no conflictsof interest related to this study.

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    Correspondence: Dr. Sona Rivas-Tumanyan, Center forClinical Research and Health Promotion, P.O. Box 365067,San Juan, PR 00936-50667. Fax: 787/763-4868; e-mail:[email protected].

    Submitted December 24, 2011; accepted for publicationMarch 6, 2012.

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    mailto:[email protected]:[email protected]