Birth Order, Sibship Size, and Housing Density in Relation to Tooth Loss and Periodontal Disease: A Cohort Study among Swedish Twins

Lorelei A. Mucci1,2,3 , Chung-cheng Hsieh1,2, Paige L. Williams4, Paul W. Dickman2,5, Lars Björkman6 and Nancy L. Pedersen2,7

1 Department of Epidemiology, Harvard School of Public Health, Boston, MA.
2 Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, Sweden.
3 Department of Oral Health Policy and Epidemiology, Harvard School of Dental Medicine, Boston, MA.
4 Department of Biostatistics, Harvard School of Public Health, Boston, MA.
5 Department of Oncology and Pathology, Karolinska Institutet, Stockholm, Sweden.
6 Adverse Reaction Unit, Dental Biomaterials, University of Bergen/UNIFOB, Bergen, Norway.
7 Department of Psychology, University of Southern California, Los Angeles, Los Angeles, CA.

Received for publication March 7, 2003; accepted for publication September 25, 2003.


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 APPENDIX
 REFERENCES
 
For diseases with an infectious etiology, birth order may dictate the age of exposure to childhood infection, while sibship size may be a proxy for the probability of exposure. The authors examined whether birth order, sibship size, and childhood housing density affect risk of tooth loss and periodontal disease. The study included 28,690 adults aged >=42 years who were participating in a 1998–2002 follow-up of persons listed in the Swedish Twin Registry. Logistic regression was used to calculate odds ratios and 95% confidence intervals, with adjustment for age, sex, education, and smoking and mutual adjustment for family composition (sibship size and/or birth order). Tooth loss and periodontal disease affected 8% and 19% of the twins, respectively. Each additional sibling increased the odds of tooth loss by 10% (95% confidence interval (CI): 1.06, 1.15) and the odds of periodontal disease by 5% (95% CI: 1.02, 1.08). Later birth order was associated with lower odds of periodontal disease. Each additional person per room in the childhood home increased the odds of tooth loss (odds ratio = 1.28, 95% CI: 1.03, 1.60) but lowered the odds of periodontal disease (odds ratio = 0.65, 95% CI: 0.48, 0.89). These findings are compatible with the hypotheses that adult oral diseases are associated with the probability of exposure in childhood and that earlier age at exposure lowers risk.

birth order; communicable diseases; family characteristics; oral health; periodontal diseases; siblings; tooth loss; twins

Abbreviations: Abbreviations: CI, confidence interval; SALT, Screening Across the Lifespan of Twins.


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 APPENDIX
 REFERENCES
 
Periodontal disease is a chronic condition with an infectious origin. Oral bacteria stimulate host inflammation as part of the healing process. However, perturbation of host defense mechanisms can result in the destruction of bone and connective tissue that support teeth, leading to tooth mobility, pain, and ultimately tooth loss. Periodontal disease represents an important public health burden among adults in Europe and the United States, with more than 15 percent having a severe form of the disease (1, 2). Given its possible association with severe systemic conditions such as cardiovascular disease, periodontal status may itself be a risk factor for mortality (3).

Birth order and sibship size have consistently been associated with other diseases hypothesized to have an infectious etiology, including peptic ulcer (4), allergies and asthma (5), and certain cancers (6, 7). Birth order may dictate the age of exposure to common childhood infections, under the assumption that firstborn children are not exposed until they enter school, while later-born children are exposed at an earlier age through their older siblings (8, 9). Sibship size may be a proxy for the probability of exposure to infectious agents during childhood. Greater sibship size is associated with a greater probability of exposure to infectious agents and thus generally increases risk of disease later in life. For birth order, however, the direction of the effect is dependent on the infectious agent and its relation to clinical disease. For example, exposure to Epstein-Barr virus earlier in life is hypothesized to reduce the risk of Hodgkin’s disease (8), whereas exposure to hepatitis B virus at an earlier age appears to increase the risk of hepatocellular carcinoma (6).

Person-to-person transmission of periodontal pathogens occurs via saliva, and increased frequency of exposure to infectious saliva increases the likelihood of bacterial colonization (10). Periodontal pathogens can be transmitted among family members (10), and familial transmission may be a risk factor for progression to periodontal disease (11). In addition, the bacteria involved in the pathogenesis of oral diseases are often colonized and already established in childhood, although risk of colonization appears to be higher among children not exposed to bacteria until later in childhood (12, 13). Once colonization occurs, the bacteria remain present and thus may determine a person’s future periodontal status (10).

On the basis of these previous studies, we would hypothesize that larger sibship size, by increasing the probability of exposure, and earlier birth order, by delaying age at exposure, would increase the risk of periodontal disease and tooth loss. Housing density might influence the timing of exposure, through greater person-to-person contact with parents or other family members as an infant, or may reflect lower socioeconomic status during childhood and thus less access to dental treatment. To our knowledge, no previous study has tested these hypotheses. To this end, we examined the associations between birth order, sibship size, and housing density and risk of tooth loss and periodontal disease in a population-based cohort of Swedish adults.


    MATERIALS AND METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 APPENDIX
 REFERENCES
 
Study population
The data for the present investigation were obtained from the Swedish Twin Registry (14, 15). The Swedish Twin Registry is currently the largest population-based twin registry in the world, with entries on more than 70,000 twin pairs born in Sweden since 1886. The Registry was assembled in the late 1950s and early 1970s, and the twins have been prospectively followed through postal questionnaires, telephone interviews, and in-person screenings. Between 1998 and 2002, all twins who were born before 1958 were invited to participate in Screening Across the Lifespan of Twins (SALT), a computer-assisted telephone interview eliciting information on health outcomes, risk factors, preventive behaviors, and familial and demographic factors. Twins were interviewed regardless of the vital status or participation of their co-twin. The SALT study was approved by the institutional review board of the Karolinska Institutet, and the twins provided oral consent to participate in the study.

As of February 2002, 37,432 twins had completed the SALT screening. To reduce the length of the interview, questions on selected topics were limited to a subsample of the cohort during the latter 2 years. Questions on oral health were asked of all twins interviewed through 2000 but were limited to persons aged 65 years or younger in 2001 and 2002. It is unlikely that this would have led to any bias, since twins were selected randomly each month for participation. Thus, information on dental health was available from 10,718 complete twin pairs and 7,254 single-responding twins (N = 28,690 twins (2 x 10,718 + 7,254)).

Study variables
The principal exposure variables were birth order, sibship size, and childhood housing density. Each twin reported the number of liveborn siblings in his or her family and the order of his or her birth with respect to other siblings. Sibship size was defined as the total number of siblings plus the two twins. Data on housing density were available for the 456 SALT twins who had previously participated in the Swedish Adoption/Twin Study of Aging (16). Briefly, twin pairs reared apart and matched control twin pairs reared together were part of this longitudinal study of aging. Twins in the Swedish Adoption/Twin Study of Aging reported the number of rooms in their childhood home and the number of persons who had shared that home. An index of housing density was created by dividing the number of individuals by the number of rooms.

Oral health status was based on self-reported information from the SALT screening. All twins were asked, "Do you have your own teeth?". Tooth loss was defined as not having any of one’s own teeth. Participants who were not edentulous were also asked, "Have you been diagnosed by a dentist as having loose teeth or periodontal disease?" and "Do you have or have you ever had any teeth which are loose or move around?". Participants who responded that a dentist had told them they had periodontal disease or who reported that they had ever had tooth mobility were defined as having periodontal disease.

Statistical analysis
Logistic regression analyses were used to assess the roles of sibship size, birth order, and housing density in risk of tooth loss and periodontal disease, controlling for potential confounders. Covariates that changed the odds ratio for the main effect by more than 10 percent or that were significant at {alpha} = 0.20 and that were not on the causal pathway were kept in the final model (17). We evaluated the linearity of variables for sibship size, birth order, housing density, and age on the log scale to determine whether the relations followed linear trends. Higher-order terms for continuous variables were also explored.

All analyses were conducted using the GENMOD procedure in SAS (version 8.2; SAS Institute, Inc., Cary, North Carolina). Because of potential cluster-correlation within twin pairs, confidence intervals calculated under the assumption of independence may be biased (usually too narrow). Thus, we adapted the alternating logistic regression model proposed by Carey et al. (18) to account for the correlated data of twin pairs. We further allowed for twin pair correlations for the outcome to vary for monozygotic and dizygotic twins (the relevant SAS code is presented in the Appendix). Odds ratios and 95 percent confidence intervals were calculated. The results of trend tests are also presented. Results were adjusted for age (continuous variable), age squared, sex, education (categorical—university, gymnasium, military/vocational, compulsory, elementary, other), and smoking status (categorical—current daily smoker, current nondaily smoker, former daily smoker, former nondaily smoker, never smoker) and were mutually adjusted for sibship size and/or birth order.


    RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 APPENDIX
 REFERENCES
 
Information on tooth loss and periodontal disease was analyzed for 28,690 participants. In this population-based sample of Swedish adults aged 42 years or more, the cumulative risk of tooth loss was 8 percent and the lifetime prevalence of periodontal disease was 19 percent (table 1). Almost 15 percent of the twins had a sibship size of seven or more, and 60 percent had been born first or second among their siblings. In the subsample of 456 twins who also participated in the Swedish Adoption/Twin Study of Aging, 38 percent grew up in a household with a density of two or more people per room.


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TABLE 1. Prevalence of oral conditions among 28,690 participants in Screening Across the Lifespan of Twins aged >=42 years, Swedish Twin Registry, 1998–2002
 
The likelihood of tooth loss and periodontal disease according to characteristics of the study population is presented in table 2. Tooth loss and periodontal disease were more common among those with larger sibship sizes and those born later with respect to other siblings in the family. Twins living in the most crowded homes during childhood were more likely to have complete tooth loss. In contrast, periodontal disease was higher for those who had lived in a home with less than one person per room during childhood.


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TABLE 2. Percentages of persons with tooth loss and periodontal disease according to demographic, lifestyle, and family characteristics among 28,690 participants in Screening Across the Lifespan of Twins aged >=42 years, Swedish Twin Registry, 1998–2002
 
Crude and adjusted odds ratios for tooth loss and periodontal disease by sibship size are presented in table 3. After adjustment for age, sex, education, and smoking, sibship size was positively associated with both tooth loss and periodontal disease. Further adjustment for birth order did not substantially change the odds ratios. For each additional sibling in the family, the odds of tooth loss increased 10 percent (95 percent confidence interval (CI): 1.06, 1.15). Respondents with eight or more siblings in the family had 1.8 times’ greater odds of tooth loss than those with two siblings. Similarly, the odds ratio for periodontal disease per additional sibling was 1.05 (95 percent CI: 1.02, 1.08). Persons with six or more siblings in the family had approximately 30 percent greater odds of periodontal disease than those with two siblings.


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TABLE 3. Crude and adjusted odds ratios for the relation of sibship size to tooth loss and periodontal disease, Swedish Twin Registry, 1998–2002
 
Data on birth order and oral disease are presented in table 4. The apparently higher risk of oral disease associated with later birth order was attenuated after adjustment for age, sex, education, and smoking. There was no evidence of a linear trend or any association between birth order and tooth loss. The effect of birth order on periodontal disease was inverted upon mutual adjustment by sibship size, so that later birth was protective against periodontal disease later in life (per increase in (later) birth order, odds ratio = 0.97, 95 percent CI: 0.94, 1.00). Persons born sixth or later among their siblings had almost 20 percent lower odds of periodontal disease than those born first.


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TABLE 4. Crude and adjusted odds ratios for the relation of birth order to tooth loss and periodontal disease, Swedish Twin Registry, 1998–2002
 
Data on the relation of childhood housing density to risk of tooth loss and periodontal disease among the 456 twins who provided this information are presented in figure 1. After results were controlled for birth order, sibship size, and other factors, the odds of tooth loss increased with increasing crowding in the childhood home (per additional person per room, odds ratio = 1.28, 95 percent CI: 1.03, 1.60). In comparison with a childhood housing density of less than one person per room, the odds ratios were 1.2 (95 percent CI: 0.4, 4.2) for a density of 1–1.9 people per room, 1.5 (95 percent CI: 0.4, 5.1) for a density of 2–3.9 people per room, and 2.8 (95 percent CI: 0.7, 10.8) for a density of >=4 people per room. In contrast, exposure to more crowded living conditions during childhood was associated with lower odds of periodontal disease (per additional person per room, odds ratio = 0.65, 95 percent CI: 0.48, 0.89). The odds ratios for periodontal disease were 0.45 (95 percent CI: 0.22, 0.93) for a density of 1–1.9, 0.32 (95 percent CI: 0.14, 0.71) for a density of 2–3.9, and 0.33 (95 percent CI: 0.09, 1.16) for a density of >=4, as compared with a density of less than one person per room.



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FIGURE 1. Adjusted odds ratios (ORs) for the relation of childhood housing density to tooth loss (top) and periodontal disease (bottom) among twins participating in Screening Across the Lifespan of Twins who also participated in the Swedish Adoption/Twin Study of Aging (n = 456), Swedish Twin Registry, 1998–2002. Childhood housing density was defined as the number of people in the household divided by the number of rooms in the household during childhood. The odds ratio represents the odds of disease per additional person per room, modeled as an ordinal variable. Odds ratios were adjusted for age (continuous variable), age squared, sex, education (categorical—university, gymnasium, compulsory/elementary, military/vocational, other), smoking status (current, former, never), birth order, and sibship size. CI, confidence interval.

 

    DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 APPENDIX
 REFERENCES
 
To our knowledge, this is the first study to provide informative data on the effect of familial characteristics on periodontal disease and tooth loss. These analyses demonstrated an important role for childhood family environment in the etiology of oral diseases in adulthood. Our findings will help in developing an infectious model for understanding these oral diseases. Sibship size was positively related to periodontal disease, suggesting that the risk is increased with increasing probability of exposure to infectious agents during childhood. The inverse association with birth order and periodontal disease suggests that earlier exposure to infectious agents is protective against disease in adulthood.

We found no evidence of an association between birth order and tooth loss. In addition to periodontal disease, however, dental caries is an important contributor to tooth loss. Two earlier epidemiologic studies, without controlling for confounding, examined the effect of birth order on dental caries. Zadik (19) observed that the prevalence of caries among children was lower among those with an earlier birth order, while Mansbridge (20) noted the opposite. The lack of an association with respect to birth order and tooth loss may highlight the complexity of oral pathogen immunity involved in this condition. A positive effect of sibship size on dental caries in children has been consistently noted (19–22). In line with the data on periodontal disease, this observation is consistent with the higher risk of tooth loss noted with larger sibship size.

Information on housing density in childhood provided additional evidence for a role of transmission during childhood. The number of people per room in the childhood home was positively associated with risk of tooth loss but negatively associated with periodontal disease. These opposing effects of household crowding are intriguing, and we can only hypothesize a possible mechanism. Tooth loss is the ultimate outcome of untreated oral disease, particularly periodontal disease and dental caries. Thus, risk factors for tooth loss will reflect both the infectious mechanisms of oral disease and predictors of a lack of access to dental treatment. Housing density might influence the timing of exposure, through greater person-to-person contact with parents or other family members as an infant. In addition, a more crowded home may reflect lower socioeconomic status during childhood and less access to dental treatment. Thus, the inverse association between household crowding and periodontal disease may be indicative of the infectious disease process. Whether or not a person receives treatment for oral disease during childhood will predict tooth loss during adult life, which is reflected in the positive association between housing density and tooth loss.

The data from our study agree with data from other research exploring the infectious etiology of oral diseases. The person-to-person transmission of pathogens involved in both periodontal disease (10) and dental caries (23) has been documented. Indeed, genotyping of Streptococcus mutans, a bacterium causing dental caries, suggests direct transmission of the bacterium within families (24). One interpretation of our study, in light of these data, is that sibship size is a proxy for the probability of exposure to oral infection during childhood.

One of the responsible bacteria in the pathogenesis of periodontal disease, Actinobacillus actinomycetemcomitans, appears to be resistant to colonization among infants and toddlers but can become established in the oral cavity when children are first exposed at 5–7 years of age (12, 13). Periodontal bacteria remain present long after colonization occurs, and they may become active during transient bacteremia (10). Age at initial exposure is a major determinant of the outcome of infection, that is, immunity versus clinical disease. For many infections, early exposure is associated with durable immunity, whereas delayed exposure results in a higher ratio of clinical disease to immunity (8). Our data on an association between birth order and periodontal status provide supportive evidence that this is true. The observed reduction in periodontal disease risk may be a function of exposure to maternal antibodies, priming and maturation of the immune system during early life (25), or earlier development of herd immunity (26).

Our study had a number of strengths and limitations to consider. We took a retrospective approach to assessing the impact of exposure to childhood infection on oral disease risk in adult life using existing resources. The Swedish Twin Registry is population-based, and participation in the follow-up study was high (~75 percent). Thus, selection bias is likely to have been minimal. Given the sample size, we had substantial statistical power to detect an effect of birth order and sibship size. Although the number of persons who provided information on housing density was lower, power calculations conducted after the fact suggested that we had 98 percent power to detect an odds ratio of 0.33 for the highest group versus the lowest.

The SALT interview collected extensive data on covariates, and we adjusted for the major risk factors for these conditions. It is possible that residual confounding may exist. Given the strength of the association between cigarette smoking and periodontal health, we systematically evaluated possible residual confounding due to smoking. In analyses restricted to never smokers, the odds ratios were similar to those obtained for all participants, providing evidence of no residual confounding by smoking.

The data collected through SALT were based on self-report and may have been subject to a degree of misclassification. For birth order and sibship size, we assessed the percentage of agreement between twins. We found that 76 percent of twins were concordant for sibship size, and 96 percent gave a sibship size plus or minus one sibling. For birth order, twins were 86 percent concordant, and 98 percent gave a birth order plus or minus one order. The fact that some twins were off by one sibling or one birth order may reflect some respondents’ interpretation of the question and the fact that they were twins. For example, some twins who were asked about the number of siblings may or may not have included themselves. The extent of exposure misclassification was fairly minimal and therefore should not have distorted the findings.

The validity of self-reported information on periodontal measures has created considerable debate among oral health professionals, though few studies have directly examined this issue. Self-reported tooth loss appears to have good validity compared with clinical assessment in community-based samples (27). Among health professionals, the validity of self-reporting for periodontal disease is high, particularly among those with severe disease (28). The applicability of these findings is potentially limited, given the health awareness of this population. In one study of a community sample of Swedish adults, agreement between self-reported assessment of periodontal pockets and clinical examination was relatively high (29), while the correlation between tooth mobility and clinical examination was lower. Since the survey questions differed from those in SALT, we cannot directly extrapolate those results to the present study. Within our own data, we find supportive evidence for minimal misclassification of data on the oral health measures. First, tooth loss and periodontal disease in this study were associated with their established risk factors, that is, smoking, age, and education. Second, reliability data from a small sample of twins who were recontacted 2 weeks after the initial SALT interview suggested that there was excellent reliability for both tooth loss ({kappa} = 86.5 percent) and periodontal disease ({kappa} = 89.0 percent). If there was misclassification of disease, it is unlikely to have been related to family characteristics and thus would have been nondifferential. In general, this would have tended to bias estimates toward the null. Thus, if anything, our findings would have underestimated the true associations.

In this study, we used birth order, sibship size, and housing density as proxy measures. Given the length of time between exposure during childhood and onset of adult oral diseases, it is difficult to study early-life exposures by other means. Although the association between family characteristics and periodontal health is consistent with a role of childhood infection, these proxy measures may be indicative of some other underlying process occurring during childhood. For example, sibship size may be indicative of other family effects, such as influences on oral hygiene and dental habits later in life, or it could indicate a lower level of access to health services earlier in life. Notwithstanding this limitation, the data support a role of early familial environment in the risk of periodontal disease and edentulism occurring in adulthood.

Given the disease burden caused by periodontal disease and tooth loss, it is important both to understand the etiology of the disease and to design public health interventions for prevention. This study may have potential use from both perspectives, by identifying possible windows of opportunity during childhood to reduce transmission of oral pathogens and by contributing information to the infectious disease model of oral health.


    ACKNOWLEDGMENTS
 
Dr. Lorelei Mucci was supported by training grant 2T32 DE07151 from the US National Institute of Dental and Craniofacial Research. Funding for this study came from a STINT (Swedish Foundation for International Cooperation in Research and Higher Education) grant supporting collaboration between the Karolinska Institutet and Harvard University. The Screening Across the Lifespan of Twins (SALT) project was supported by grants from the Swedish Council for the Planning and Coordination of Research (FRN) and the US National Institute on Aging (grant AG 08724). The Swedish Twin Registry is supported by grants from the Swedish Department of Higher Education, the Swedish Research Council, and AstraZeneca (Stockholm, Sweden). The Swedish Adoption/Twin Study of Aging is supported by the US National Institute on Aging (grants AG 04563 and AG 10175).

The authors thank Drs. Hans-Olov Adami, Dimitrios Trichopoulos, and Chester Douglass for their thoughtful comments and suggestions.


    APPENDIX
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 APPENDIX
 REFERENCES
 
Below we present the SAS code for alternating logistic regression models. Use of this method allows twin pair correlations for the outcome to vary for monozygotic and dizygotic twins.

proc genmod data = twins;

class twinid mz;

model perio = sibship/type 3 error = bin link = logit;

repeated subject = twinid/logor = logorvar (mz) covb;

run;

In this model, "twinid" represents the identification for each twin pair, and mz is a binary variable indicating monozygotic twins. "Perio" is the outcome variable for periodontal disease, and "sibship" is the ordinal exposure for sibship size. The statement "logor = logorvar (mz)" allows for the effect of zygosity to differ as a function of the odds ratio.


    NOTES
 
Correspondence to Dr. Lorelei A. Mucci, Department of Epidemiology, Harvard School of Public Health, 677 Huntington Avenue, 9th floor, Boston, MA 02115 (e-mail: lmucci{at}hsph.harvard.edu). Back


    REFERENCES
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 APPENDIX
 REFERENCES
 

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