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Periodontal disease as one possible explanation for the Mexican paradox
Medical Hypotheses (2006) 67, 1348–1354
http://intl.elsevierhealth.com/journals/mehy
Periodontal disease as one possible explanation for the Mexican paradox X. Xiong
a,*
, P. Buekens a, S. Vastardis b, T. Wu
c
a
Department of Epidemiology, School of Public Health and Tropical Medicine, Tulane University, Tidewater Building Suite 2022, SL-18, 1440 Canal Street, New Orleans, LA 70112, USA b Department of Periodontics, Louisiana State University, USA c Departments of Public Health and Family Medicine, East Tennessee State University, USA Received 30 March 2006; accepted 15 May 2006
Summary Mexican-American women have similar low socio-economic status as compared to Non-Hispanic Blacks. However, Mexican-American women have consistently been shown to have a lower rate of low birth weight births as compared to Non-Hispanic Blacks and similar to Non-Hispanic Whites. This phenomenon is referred to as the ‘‘Mexican paradox’’, and the explanation for this is still unclear. We used data from the third US National Health and Nutrition Examination Survey (NHANES III) to compare the rate of periodontal disease in Non-Hispanic Black, Non-Hispanic White and Mexican-American pregnant and non-pregnant women. We found that Mexican-American women have a lower rate of periodontal disease before and during pregnancy when compared to Non-Hispanic Blacks. Since periodontal disease has been associated with an increased risk of preterm birth and low birth weight, we hypothesize that the lower prevalence of periodontal disease before and during pregnancy among Mexican-American women may contribute to the ‘‘Mexican paradox’’. c 2006 Elsevier Ltd. All rights reserved.
Introduction Despite their low socio-economic status (SES), Mexican-American women have consistently been shown to have lower rates of low birth weight births as compared to Non-Hispanic Blacks and similar rates as compared to Non-Hispanic Whites, a phenomenon that is referred to as the ‘‘Mexican (epidemiological) paradox’’ [1–4]. Recent studies suggested that periodontal disease may be a risk fac* Corresponding author. Tel.: +1 504 988 1379; fax: +1 504 988 1568. E-mail address: [email protected] (X. Xiong).
tor for poor pregnancy outcomes [5–9]. Periodontal disease is more prevalent and severe in those with lower SES as compared to those with higher SES [10–14], and it is more common in Non-Hispanic Blacks than in Non-Hispanic Whites and MexicanAmericans [15–17]. We speculate that a lower prevalence of periodontal disease in Mexican-American women (irrespectively of pregnancy status) may be a potential partial explanation to the phenomenon of the Mexican paradox. In this article, we (1) briefly summarize the Mexican Paradox as well as the current evidence of periodontal disease as a risk factor for adverse pregnancy outcomes; (2) present data of the prevalence of periodontal disease between
0306-9877/$ - see front matter c 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.mehy.2006.05.059
Periodontal disease as one possible explanation for the Mexican paradox Non-Hispanic Black, Non-Hispanic White, and Mexican-American pregnant and non-pregnant women; and (3) discuss the plausibility of race and ethnicity disparities in periodontal disease prevalence contributing to the Mexican paradox.
The Mexican (epidemiological) paradox Great disparities in perinatal morbidity and mortality among different racial and ethnic women still exist in the US For example, based on data from the California linked infant birth/death certificate files of 1, 622, 324 infants from 1995 to 1997, Gould et al. found that the rate of low birth weight (birth weight <2500 g) was 5.7% among Non-Hispanic White infants, 12.5% among Non-Hispanic Black infants and 5.2% among Mexican-American infants, respectively. Neonatal mortality (death before 28 days of age) was 2.7& among Non-Hispanic White infants, 4.9& among Non-Hispanic Black infants and 2.6& among Mexican-American infants, respectively [18]. Compared to Non-Hispanic Whites, Non-Hispanic Black women have been consistently shown to have markedly higher rates of low birth weight and infant mortality. The increased risk for Non-Hispanic Black women has been attributed in part to poor demographics and low socio-economic status (SES) [19–23]. Ironically, despite their poor demographics and low SES, Mexican-American women have consistently been shown to have lower rates of low birth weight births as compared to Non-Hispanic Blacks and similar rates as compared to NonHispanic Whites, a phenomenon that is referred to as the ‘‘Mexican (epidemiological) paradox’’. Mexican-American women have relatively few low birth weight babies because they have few preterm births [18,24]. The reasons why pregnant Mexican-American women and their babies are protected from the harmful effects of their adverse living conditions are still elusive [24–26]. Many theories have been proposed to explain the ‘‘Mexican paradox’’, including selective migration, a protective culture (diet, social support), and healthy behaviors (less smoking) [27–33]. However, much controversy still remains and none of these hypotheses/theories fully explain this phenomenon [32,34].
Periodontal disease and adverse pregnancy outcomes Periodontal disease is one of the most common chronic disorders of infectious origin known in humans, with a reported prevalence varying between
1349
10% and 60% in adults, depending on diagnostic criteria [6,35–37]. Periodontal disease refers to gingivitis (an inflammatory condition of the soft tissues surrounding a tooth or the gingiva) and periodontitis (involving the destruction of such supporting structures as the periodontal ligament, bone, cementum or soft tissues) [38]. Periodontal disease is initiated by overgrowth of certain bacterial species, with a majority of gram-negative, anaerobic bacteria growing in subgingival sites. The host response to periodontal pathogens causes persistent inflammation and the destruction of periodontal tissues that support teeth [38,39], leading to clinical manifestations of disease. There is increasing evidence suggesting that periodontal disease may be associated with an increased risk of systemic diseases such as atherosclerosis, myocardial infarction, stroke, diabetes mellitus, and adverse pregnancy outcomes [5,40– 42]. We have recently published a systematic review of existing studies on the relationship between periodontal disease and adverse pregnancy outcomes [9]. Adverse pregnancy outcomes that have been linked to periodontal disease include preterm birth, low birth weight, miscarriage or early pregnancy loss and pre-eclampsia. Although several studies reported no associations, the majority of studies suggested that periodontal disease was associated with increased risk of adverse pregnancy outcomes such as preterm birth and low birth weight, in particular in African–American and low SES populations [5–9]. Periodontal disease, as a source of sub-clinical and persistent infection, may induce systemic inflammatory responses that increase the risk of adverse pregnancy outcomes [9]. Oral mechanical manipulation (e.g., tooth brushing, dental procedures, and even routine mastication) can cause bacteremia [43]. Chronic periodontal infections can produce local and systemic host responses leading to transient bacteremia. Lipopolysaccharide (LPS) endotoxins and other bacterial substances can gain access to gingival tissue, initiate and perpetuate local inflammatory reactions, and consequently produce high levels of proinflammatory cytokines (e.g., tumor necrosis factor). In addition, LPS, bacteria from subgingival plaque, and proinflammatory cytokines from inflamed periodontal tissue can enter the bloodstream, reach the maternal-fetal interface, trigger or worsen maternal inflammatory response, and increase plasma levels of prostaglandin and cytokines [40– 42,45]. Such activations of maternal inflammatory responses and cytokine cascades play important roles in the pathophysiological processes of preterm labor and low birth weight [40,44].
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Periodontal disease in pregnant and non-pregnant women by race and ethnicity: data from the third US national health and nutrition examination survey (NHANES III) Periodontal disease, often initiated by poor oral hygiene, is more prevalent and severe in those with lower SES as compared to those with higher SES [10–14]. Studies have also found that periodontal disease is more common in Non-Hispanic Blacks than in Non-Hispanic Whites and Mexican-Americans [15–17]. However, to our knowledge, there is no study that has examined the prevalence of periodontal disease in pregnant women and non-pregnant women of childbearing age by race and ethnicity. NHANES III was a nationally representative crosssectional survey of the US civilian, non-institutional population between 1988 and 1994 [46]. The data included for this analysis was restricted to women who reported to be pregnant during the survey and women who were at childbearing age of 15– 44 years.
Xiong et al. the ‘‘Women, Infant and Children’’ (WIC) supplemental food program, years of education (<12 years, P12 years), smoking status (current smoker, former smoker, never smoker), insurance coverage (general, dental, no), time elapsed since last dental visit (66 months, >6 months, P1 year), and poverty income ratio (low: 61.850, middle: 1.851–3.500, high: P3.501) [16].
Statistical analyses Univariate analysis was performed to examine the prevalence of periodontal disease in different ethnic groups according to pregnant and non-pregnant status. Odds ratios (OR) and 95% confidence intervals (CI) of periodontal disease were calculated for Mexican-Americans and Non-Hispanic Whites relative to Non-Hispanic Blacks. Multivariate logistic regression was performed to adjust for potential confounding variables. Because of the complex survey design used in NHANES III, all analyses were conducted by using the software SUDAAN [49], which provided unbiased standard error estimates by taking into consideration the sampling weights provided in the data set.
Study variables Results In NHANES III, oral health examinations were conducted in mobile examination centers by trained and calibrated dental examiners [47]. The periodontal examination was performed in two randomly chosen quadrants-one maxillary and one mandibular. Two sites, midbuccal and mesiobuccal, were examined for each tooth, with a maximum of 14 teeth and 28 sites examined for each participant. Using a periodontal probe, the examiners measured clinical attachment level (CAL, the distance between the cemento-enamel junction and the apical part of the pocket) and probing depth (PD, the distance from the gingival margin to the apical part of the pocket) and presence of bleeding on probing. Since there is no universally accepted standard for periodontal disease diagnosis, most studies have used their own case definitions that combined PD and CAL [9,15,16,48]. For this study, periodontal disease was defined as at least one site with CAL or PD P4 mm. The independent variables of interest were race and ethnicity and pregnancy status. Race and ethnicity was defined as Non-Hispanic Black, Non-Hispanic White and Mexican-American. Pregnancy status was derived from the question: ‘‘Are you now pregnant?’’ The covariates included age at interview (recoded as <20, 20–35, >35 years old), marital status (married, single, divorced, widowed), participation in
The present study sample includes 268 pregnant women and 3115 non-pregnant childbearing aged women of 15–44 years. Table 1 and Fig. 1 present the frequency of periodontal disease and otherw demographic characteristics in pregnant and nonpregnant women by race and ethnicity. In general, both pregnant and non-pregnant Mexican-American women, (similar to Non-Hispanic Blacks), were younger, poorer, less educated and less likely to have insurance coverage as compared to NonHispanic Whites. However, Mexican-American women were less likely to smoke, especially during pregnancy. In the cohort of the 286 pregnant women, the prevalence of periodontal disease in pregnant women was 29.1% for Non-Hispanic Blacks, 20.6% for Mexican-Americans and 10.7% for Non-Hispanic Whites. Compared to Non-Hispanic Blacks, Mexican-American women had a lower risk of having periodontal disease (adjusted OR: 0.55, 95% CI: 0.16–1.97) after adjusting for age, marital status, education, poverty income ratio, smoking, time elapsed since last dental visit and insurance coverage, although the difference was not statistically significant. Non-Hispanic Whites had a significantly lower risk of having periodontal disease (adjusted OR: 0.31, 95% CI: 0.10–0.99) as
Periodontal disease as one possible explanation for the Mexican paradox
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Table 1 Periodontal disease and demographic characteristics in pregnant and non-pregnant women by race and ethnicity, based on NHANES III, 1988–1994 Periodontal disease and demographic characteristicsa
Pregnant women (N = 268)
Non-Hispanic MexicanBlacks Americans (N = 84) (N = 119)
Non-pregnant women (N = 3115)
Non-Hispanic Non-Hispanic MexicanWhites Blacks Americans (N = 65) (N = 1184) (N = 1033)
Non-Hispanic Whites (N = 899)
Periodontal disease (%) 29.1 OR & 95% CI 1.00 (ref.) aOR & 95% CIb 1.00 (ref.)
20.6 10.7 0.63 0.29 (0.28–1.40) (0.11-0.74) 0.55 0.31 (0.16–1.97) (0.10–0.99)
26.0 1.00 (ref.)
Age (%) < 20 20–35 > 35
20.5 74.5 5.0
19.9 70.2 9.9
13.5 86.2 0.3
5.4 59.6 35.0
5.1 61.6 33.3
2.4 52.9 44.7
Marital status (%) Married Single Divorced Widow
41.2 50.7 – –
77.3 12.3 9.6 0.8
76.1 18.3 5.6 –
39.9 36.0 22.8 1.3
73.4 12.4 13.2 1.0
76.2 8.6 14.9 0.3
Education (%) < 12 year P 12 years
34.7 65.3
58.5 41.5
17.9 82.1
22.3 77.7
56.3 43.7
16.3 83.7
WIC coverage (%) Yes No
35.0 65.0
39.5 60.5
14.9 85.1
8.8 91.2
14.2 85.8
4.0 96.0
Poverty income ratio (%) Low 79.1 Middle 11.1 High 9.9
74.8 14.3 10.9
37.4 28.2 34.5
59.8 27.7 12.5
70.0 20.5 9.5
27.6 36.6 35.8
Smoking (%) Current smokers Former smokers Never smokers
4.7 11.8 83.6
20.1 22.7 57.2
32.4 8.1 59.5
15.3 10.5 74.2
37.2 20.1 42.7
Presence of health insurance (%) General 27.4 Dental 39.8 No 32.9
26.5 24.8 48.7
31.9 47.4 20.7
25.2 50.2 24.6
24.7 31.9 43.4
33.3 52.0 14.7
Time since last dental visit (%) 6 6 months 35.4 > 6 months 26.0 P 1 year 38.6
34.4 24.3 41.3
47.1 19.3 33.6
39.3 24.2 36.5
40.7 21.4 37.9
51.8 21.2 27.0
20.9 8.2 70.9
1.00 (ref.)
15.4 16.9 0.52 0.58 (0.39–0.68) (0.41–0.82) 0.42 0.50 (0.29–0.61) (0.35–0.71)
a
Excluding missing values. Adjusted OR: adjusted for age, marital status, education, poverty income ratio, smoking, time elapsing since last dental visit, insurance coverage. b
compared to Non-Hispanic Blacks. Mexican-American women had a higher prevalence of periodontal disease than Non-Hispanic Whites, with adjusted OR of 1.79 (95% CI: 0.50–6.47). In the cohort of
non-pregnant women (n = 3115), the prevalence of periodontal disease was markedly higher in Non-Hispanic Blacks (26.0%) than in MexicanAmericans (15.4%) and Non-Hispanic Whites
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Xiong et al.
Periodontitis (%)
60
Black
Mexican-American
White
40
29.1
26 20.6
20
10.7
15.4
16.9
0
Pregnant women
Non-pregnant women
Figure 1 Periodontal disease in pregnant and nonpregnant women by race and ethnicity, based on NHANES III, 1988–1994.
(16.9%). Compared to Non-Hispanic Blacks, Mexican-American women had significantly lower rates of periodontal disease (adjusted OR = 0.42, 95% CI:0.29–0.61).
Comment In the present analysis, Mexican-American women had lower rates of periodontal disease when compared to Non-Hispanic Black women, and rates similar to Non-Hispanic White women. This finding is consistent with another study of NHANES III general population including 12,399 persons at least 17 years of age, which found that Non-Hispanic Blacks had a significantly higher prevalence of periodontal disease than both Mexican-Americans and NonHispanic Whites, and Mexican-Americans had rates similar to Non-Hispanic Whites [16]. In the present study, although Mexican-American pregnant women had lower rate of periodontal disease than NonHispanic Black pregnant women, the difference was not statistically significant. In addition, there was an unexpected trend for Mexican-American pregnant women to have more periodontal disease than the general population of Mexican-American women, and an opposite trend among Non-Hispanic Whites. These results may be due to the fact that the number of pregnant women by race-ethnicity groups included in NHANES III was relatively small, which thus suffered a lack of statistical power and resulted in imprecise estimates of prevalence. Another limitation of NHANES III is that data on birth outcomes were not available.
Hypothesis: periodontal disease as one possible explanation for the Mexican paradox Based on the data from the NHANES III, we found that Mexican-American women had similar poverty
rates, education and medical insurance coverage to Non-Hispanic Black women. Mexican-American women were less likely to smoke, which is consistent with previous reports [27,32,33]. Smoking is a well-established risk factor for both adverse pregnancy outcomes and poor periodontal status [50,51]. However, the disparity in periodontal disease between Mexican-American and Non-Hispanic Black women remained even after adjusting for potential confounding factors. Because periodontal disease could lead to an increased risk of preterm birth and low birth weight [5–9], and because the prevalence of periodontal disease is relatively low in Mexican-American women during and outside pregnancy, we speculate that this lower prevalence may explain (at least partially) the observed lower rate of low birth weight and preterm birth in Mexican-American women. In summary, our hypothesis is that the paradox of lower rates of low birth weight and preterm birth in Mexican-American women may be explained by the lower prevalence of periodontal disease in this population before and during pregnancy. Future studies, especially of a prospective design, are needed to test this hypothesis. Current theories do not sufficiently explain perinatal outcomes in different racial and ethnic populations. Should our hypothesis be confirmed by future studies, it will open doors to new intervention strategies to eliminate the racial and ethnic disparities in infant morbidity and mortality. Periodontal disease is both preventable and curable. Improving periodontal health before or during pregnancy may prevent or reduce occurrences of preterm birth and low birth weight and therefore reduce perinatal morbidity and mortality.
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[28] Scribner R, Dwyer JH. Acculturation and low birthweight among Latinos in the Hispanic HANES. Am J Public Health 1989;79:1263–7. [29] Notzon FC, Bobadilla JL, Coria I. Birthweight distributions in Mexico City and among US Southwest Mexican-Americans: the effect of altitude. Am J Public Health 1992;82:1014–7. [30] James SA. Racial and ethnic differences in infant mortality and low birth weight. A psychosocial critique. Ann Epidemiol 1993;3:130–6. [31] Collins Jr JW, Shay DK. Prevalence of low birth weight among Hispanic infants with United States-born and foreign-born mothers: the effect of urban poverty. Am J Epidemiol 1994;139:184–92. [32] Scribner R. Paradox as paradigm–the health outcomes of Mexican-Americans. Am J Public Health 1996;86:303–5. [33] Cobas JA, Balcazar H, Benin MB, Keith VM, Chong Y. Acculturation and low-birthweight infants among Latino women: a reanalysis of HHANES data with structural equation models. Am J Public Health 1996;86:394–6. [34] Abraido-Lanza AF, Dohrenwend BP, Ng-Mak DS, Turner JB. The Latino mortality paradox: a test of the ‘‘salmon bias’’ and healthy migrant hypotheses. Am J Public Health 1999;89:1543–8. [35] Papapanou PN. Periodontal diseases: epidemiology. Ann Periodontol 1996;1:1–36. [36] Albandar JM. Periodontal diseases in North America. Periodontol 2000 2002;29:31–69. [37] Albandar JM, Rams TE. Global epidemiology of periodontal diseases: an overview. Periodontol 2000 2002;29:7–10. [38] Kinane DF. Causation and pathogenesis of periodontal disease. Periodontol 2000;25:8–20. [39] Kornman KS, Page RC, Tonetti MS. The host response to the microbial challenge in periodontitis: assembling the players. Periodontol 2000;14:33–53. [40] Garcia RI, Henshaw MM, Krall EA. Relationship between periodontal disease and systemic health. Periodontol 2000;25:21–36. [41] Champagne CM, Madianos PN, Lieff S, Murtha AP, Beck JD, Offenbacher S. Periodontal medicine: emerging concepts in pregnancy outcomes. J Int Acad Periodontol 2000;2:9–13. [42] Paquette DW. The periodontal infection-systemic disease link: a review of the truth or myth. J Int Acad Periodontol 2002;4:101–9. [43] Sconyers JR, Crawford JJ, Moriarty JD. Relationship of bacteremia to toothbrushing in patients with periodontitis. J Am Dent Assoc 1973;87:616–22. [44] Gibbs RS. The relationship between infections and adverse pregnancy outcomes: an overview. Ann Periodontol 2001;6:153–63. [45] Offenbacher S, Jared HL, O’Reilly PG, et al. Potential pathogenic mechanisms of periodontitis associated pregnancy complications. Ann Periodontol 1998;3:233–50. [46] Plan and operation of the Third National Health and Nutrition Examination Survey, 1988–94. Series 1: programs and collection procedures. Vital Health Stat 1 1994:1–407. [47] Drury TF, Winn DM, Snowden CB, Kingman A, Kleinman DV, Lewis B. An overview of the oral health component of the 1988–1991 National Health and Nutrition Examination Survey (NHANES III-Phase 1) J Dent Res 75 1996: Spec No: 620–30. [48] Machtei EE, Christersson LA, Grossi SG, Dunford R, Zambon JJ, Genco RJ. Clinical criteria for the definition of ‘‘established periodontitis. J Periodontol 1992;63:206–14. [49] Institute RT. SUDAAN software for the statistical analyses of correlated data, SAS-Callable SUDAAN. Version 9.0. Research Triangle Park (NC): Research Triangle Institute; 2004.
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http://intl.elsevierhealth.com/journals/mehy
Periodontal disease as one possible explanation for the Mexican paradox X. Xiong
a,*
, P. Buekens a, S. Vastardis b, T. Wu
c
a
Department of Epidemiology, School of Public Health and Tropical Medicine, Tulane University, Tidewater Building Suite 2022, SL-18, 1440 Canal Street, New Orleans, LA 70112, USA b Department of Periodontics, Louisiana State University, USA c Departments of Public Health and Family Medicine, East Tennessee State University, USA Received 30 March 2006; accepted 15 May 2006
Summary Mexican-American women have similar low socio-economic status as compared to Non-Hispanic Blacks. However, Mexican-American women have consistently been shown to have a lower rate of low birth weight births as compared to Non-Hispanic Blacks and similar to Non-Hispanic Whites. This phenomenon is referred to as the ‘‘Mexican paradox’’, and the explanation for this is still unclear. We used data from the third US National Health and Nutrition Examination Survey (NHANES III) to compare the rate of periodontal disease in Non-Hispanic Black, Non-Hispanic White and Mexican-American pregnant and non-pregnant women. We found that Mexican-American women have a lower rate of periodontal disease before and during pregnancy when compared to Non-Hispanic Blacks. Since periodontal disease has been associated with an increased risk of preterm birth and low birth weight, we hypothesize that the lower prevalence of periodontal disease before and during pregnancy among Mexican-American women may contribute to the ‘‘Mexican paradox’’. c 2006 Elsevier Ltd. All rights reserved.
Introduction Despite their low socio-economic status (SES), Mexican-American women have consistently been shown to have lower rates of low birth weight births as compared to Non-Hispanic Blacks and similar rates as compared to Non-Hispanic Whites, a phenomenon that is referred to as the ‘‘Mexican (epidemiological) paradox’’ [1–4]. Recent studies suggested that periodontal disease may be a risk fac* Corresponding author. Tel.: +1 504 988 1379; fax: +1 504 988 1568. E-mail address: [email protected] (X. Xiong).
tor for poor pregnancy outcomes [5–9]. Periodontal disease is more prevalent and severe in those with lower SES as compared to those with higher SES [10–14], and it is more common in Non-Hispanic Blacks than in Non-Hispanic Whites and MexicanAmericans [15–17]. We speculate that a lower prevalence of periodontal disease in Mexican-American women (irrespectively of pregnancy status) may be a potential partial explanation to the phenomenon of the Mexican paradox. In this article, we (1) briefly summarize the Mexican Paradox as well as the current evidence of periodontal disease as a risk factor for adverse pregnancy outcomes; (2) present data of the prevalence of periodontal disease between
0306-9877/$ - see front matter c 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.mehy.2006.05.059
Periodontal disease as one possible explanation for the Mexican paradox Non-Hispanic Black, Non-Hispanic White, and Mexican-American pregnant and non-pregnant women; and (3) discuss the plausibility of race and ethnicity disparities in periodontal disease prevalence contributing to the Mexican paradox.
The Mexican (epidemiological) paradox Great disparities in perinatal morbidity and mortality among different racial and ethnic women still exist in the US For example, based on data from the California linked infant birth/death certificate files of 1, 622, 324 infants from 1995 to 1997, Gould et al. found that the rate of low birth weight (birth weight <2500 g) was 5.7% among Non-Hispanic White infants, 12.5% among Non-Hispanic Black infants and 5.2% among Mexican-American infants, respectively. Neonatal mortality (death before 28 days of age) was 2.7& among Non-Hispanic White infants, 4.9& among Non-Hispanic Black infants and 2.6& among Mexican-American infants, respectively [18]. Compared to Non-Hispanic Whites, Non-Hispanic Black women have been consistently shown to have markedly higher rates of low birth weight and infant mortality. The increased risk for Non-Hispanic Black women has been attributed in part to poor demographics and low socio-economic status (SES) [19–23]. Ironically, despite their poor demographics and low SES, Mexican-American women have consistently been shown to have lower rates of low birth weight births as compared to Non-Hispanic Blacks and similar rates as compared to NonHispanic Whites, a phenomenon that is referred to as the ‘‘Mexican (epidemiological) paradox’’. Mexican-American women have relatively few low birth weight babies because they have few preterm births [18,24]. The reasons why pregnant Mexican-American women and their babies are protected from the harmful effects of their adverse living conditions are still elusive [24–26]. Many theories have been proposed to explain the ‘‘Mexican paradox’’, including selective migration, a protective culture (diet, social support), and healthy behaviors (less smoking) [27–33]. However, much controversy still remains and none of these hypotheses/theories fully explain this phenomenon [32,34].
Periodontal disease and adverse pregnancy outcomes Periodontal disease is one of the most common chronic disorders of infectious origin known in humans, with a reported prevalence varying between
1349
10% and 60% in adults, depending on diagnostic criteria [6,35–37]. Periodontal disease refers to gingivitis (an inflammatory condition of the soft tissues surrounding a tooth or the gingiva) and periodontitis (involving the destruction of such supporting structures as the periodontal ligament, bone, cementum or soft tissues) [38]. Periodontal disease is initiated by overgrowth of certain bacterial species, with a majority of gram-negative, anaerobic bacteria growing in subgingival sites. The host response to periodontal pathogens causes persistent inflammation and the destruction of periodontal tissues that support teeth [38,39], leading to clinical manifestations of disease. There is increasing evidence suggesting that periodontal disease may be associated with an increased risk of systemic diseases such as atherosclerosis, myocardial infarction, stroke, diabetes mellitus, and adverse pregnancy outcomes [5,40– 42]. We have recently published a systematic review of existing studies on the relationship between periodontal disease and adverse pregnancy outcomes [9]. Adverse pregnancy outcomes that have been linked to periodontal disease include preterm birth, low birth weight, miscarriage or early pregnancy loss and pre-eclampsia. Although several studies reported no associations, the majority of studies suggested that periodontal disease was associated with increased risk of adverse pregnancy outcomes such as preterm birth and low birth weight, in particular in African–American and low SES populations [5–9]. Periodontal disease, as a source of sub-clinical and persistent infection, may induce systemic inflammatory responses that increase the risk of adverse pregnancy outcomes [9]. Oral mechanical manipulation (e.g., tooth brushing, dental procedures, and even routine mastication) can cause bacteremia [43]. Chronic periodontal infections can produce local and systemic host responses leading to transient bacteremia. Lipopolysaccharide (LPS) endotoxins and other bacterial substances can gain access to gingival tissue, initiate and perpetuate local inflammatory reactions, and consequently produce high levels of proinflammatory cytokines (e.g., tumor necrosis factor). In addition, LPS, bacteria from subgingival plaque, and proinflammatory cytokines from inflamed periodontal tissue can enter the bloodstream, reach the maternal-fetal interface, trigger or worsen maternal inflammatory response, and increase plasma levels of prostaglandin and cytokines [40– 42,45]. Such activations of maternal inflammatory responses and cytokine cascades play important roles in the pathophysiological processes of preterm labor and low birth weight [40,44].
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Periodontal disease in pregnant and non-pregnant women by race and ethnicity: data from the third US national health and nutrition examination survey (NHANES III) Periodontal disease, often initiated by poor oral hygiene, is more prevalent and severe in those with lower SES as compared to those with higher SES [10–14]. Studies have also found that periodontal disease is more common in Non-Hispanic Blacks than in Non-Hispanic Whites and Mexican-Americans [15–17]. However, to our knowledge, there is no study that has examined the prevalence of periodontal disease in pregnant women and non-pregnant women of childbearing age by race and ethnicity. NHANES III was a nationally representative crosssectional survey of the US civilian, non-institutional population between 1988 and 1994 [46]. The data included for this analysis was restricted to women who reported to be pregnant during the survey and women who were at childbearing age of 15– 44 years.
Xiong et al. the ‘‘Women, Infant and Children’’ (WIC) supplemental food program, years of education (<12 years, P12 years), smoking status (current smoker, former smoker, never smoker), insurance coverage (general, dental, no), time elapsed since last dental visit (66 months, >6 months, P1 year), and poverty income ratio (low: 61.850, middle: 1.851–3.500, high: P3.501) [16].
Statistical analyses Univariate analysis was performed to examine the prevalence of periodontal disease in different ethnic groups according to pregnant and non-pregnant status. Odds ratios (OR) and 95% confidence intervals (CI) of periodontal disease were calculated for Mexican-Americans and Non-Hispanic Whites relative to Non-Hispanic Blacks. Multivariate logistic regression was performed to adjust for potential confounding variables. Because of the complex survey design used in NHANES III, all analyses were conducted by using the software SUDAAN [49], which provided unbiased standard error estimates by taking into consideration the sampling weights provided in the data set.
Study variables Results In NHANES III, oral health examinations were conducted in mobile examination centers by trained and calibrated dental examiners [47]. The periodontal examination was performed in two randomly chosen quadrants-one maxillary and one mandibular. Two sites, midbuccal and mesiobuccal, were examined for each tooth, with a maximum of 14 teeth and 28 sites examined for each participant. Using a periodontal probe, the examiners measured clinical attachment level (CAL, the distance between the cemento-enamel junction and the apical part of the pocket) and probing depth (PD, the distance from the gingival margin to the apical part of the pocket) and presence of bleeding on probing. Since there is no universally accepted standard for periodontal disease diagnosis, most studies have used their own case definitions that combined PD and CAL [9,15,16,48]. For this study, periodontal disease was defined as at least one site with CAL or PD P4 mm. The independent variables of interest were race and ethnicity and pregnancy status. Race and ethnicity was defined as Non-Hispanic Black, Non-Hispanic White and Mexican-American. Pregnancy status was derived from the question: ‘‘Are you now pregnant?’’ The covariates included age at interview (recoded as <20, 20–35, >35 years old), marital status (married, single, divorced, widowed), participation in
The present study sample includes 268 pregnant women and 3115 non-pregnant childbearing aged women of 15–44 years. Table 1 and Fig. 1 present the frequency of periodontal disease and otherw demographic characteristics in pregnant and nonpregnant women by race and ethnicity. In general, both pregnant and non-pregnant Mexican-American women, (similar to Non-Hispanic Blacks), were younger, poorer, less educated and less likely to have insurance coverage as compared to NonHispanic Whites. However, Mexican-American women were less likely to smoke, especially during pregnancy. In the cohort of the 286 pregnant women, the prevalence of periodontal disease in pregnant women was 29.1% for Non-Hispanic Blacks, 20.6% for Mexican-Americans and 10.7% for Non-Hispanic Whites. Compared to Non-Hispanic Blacks, Mexican-American women had a lower risk of having periodontal disease (adjusted OR: 0.55, 95% CI: 0.16–1.97) after adjusting for age, marital status, education, poverty income ratio, smoking, time elapsed since last dental visit and insurance coverage, although the difference was not statistically significant. Non-Hispanic Whites had a significantly lower risk of having periodontal disease (adjusted OR: 0.31, 95% CI: 0.10–0.99) as
Periodontal disease as one possible explanation for the Mexican paradox
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Table 1 Periodontal disease and demographic characteristics in pregnant and non-pregnant women by race and ethnicity, based on NHANES III, 1988–1994 Periodontal disease and demographic characteristicsa
Pregnant women (N = 268)
Non-Hispanic MexicanBlacks Americans (N = 84) (N = 119)
Non-pregnant women (N = 3115)
Non-Hispanic Non-Hispanic MexicanWhites Blacks Americans (N = 65) (N = 1184) (N = 1033)
Non-Hispanic Whites (N = 899)
Periodontal disease (%) 29.1 OR & 95% CI 1.00 (ref.) aOR & 95% CIb 1.00 (ref.)
20.6 10.7 0.63 0.29 (0.28–1.40) (0.11-0.74) 0.55 0.31 (0.16–1.97) (0.10–0.99)
26.0 1.00 (ref.)
Age (%) < 20 20–35 > 35
20.5 74.5 5.0
19.9 70.2 9.9
13.5 86.2 0.3
5.4 59.6 35.0
5.1 61.6 33.3
2.4 52.9 44.7
Marital status (%) Married Single Divorced Widow
41.2 50.7 – –
77.3 12.3 9.6 0.8
76.1 18.3 5.6 –
39.9 36.0 22.8 1.3
73.4 12.4 13.2 1.0
76.2 8.6 14.9 0.3
Education (%) < 12 year P 12 years
34.7 65.3
58.5 41.5
17.9 82.1
22.3 77.7
56.3 43.7
16.3 83.7
WIC coverage (%) Yes No
35.0 65.0
39.5 60.5
14.9 85.1
8.8 91.2
14.2 85.8
4.0 96.0
Poverty income ratio (%) Low 79.1 Middle 11.1 High 9.9
74.8 14.3 10.9
37.4 28.2 34.5
59.8 27.7 12.5
70.0 20.5 9.5
27.6 36.6 35.8
Smoking (%) Current smokers Former smokers Never smokers
4.7 11.8 83.6
20.1 22.7 57.2
32.4 8.1 59.5
15.3 10.5 74.2
37.2 20.1 42.7
Presence of health insurance (%) General 27.4 Dental 39.8 No 32.9
26.5 24.8 48.7
31.9 47.4 20.7
25.2 50.2 24.6
24.7 31.9 43.4
33.3 52.0 14.7
Time since last dental visit (%) 6 6 months 35.4 > 6 months 26.0 P 1 year 38.6
34.4 24.3 41.3
47.1 19.3 33.6
39.3 24.2 36.5
40.7 21.4 37.9
51.8 21.2 27.0
20.9 8.2 70.9
1.00 (ref.)
15.4 16.9 0.52 0.58 (0.39–0.68) (0.41–0.82) 0.42 0.50 (0.29–0.61) (0.35–0.71)
a
Excluding missing values. Adjusted OR: adjusted for age, marital status, education, poverty income ratio, smoking, time elapsing since last dental visit, insurance coverage. b
compared to Non-Hispanic Blacks. Mexican-American women had a higher prevalence of periodontal disease than Non-Hispanic Whites, with adjusted OR of 1.79 (95% CI: 0.50–6.47). In the cohort of
non-pregnant women (n = 3115), the prevalence of periodontal disease was markedly higher in Non-Hispanic Blacks (26.0%) than in MexicanAmericans (15.4%) and Non-Hispanic Whites
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Xiong et al.
Periodontitis (%)
60
Black
Mexican-American
White
40
29.1
26 20.6
20
10.7
15.4
16.9
0
Pregnant women
Non-pregnant women
Figure 1 Periodontal disease in pregnant and nonpregnant women by race and ethnicity, based on NHANES III, 1988–1994.
(16.9%). Compared to Non-Hispanic Blacks, Mexican-American women had significantly lower rates of periodontal disease (adjusted OR = 0.42, 95% CI:0.29–0.61).
Comment In the present analysis, Mexican-American women had lower rates of periodontal disease when compared to Non-Hispanic Black women, and rates similar to Non-Hispanic White women. This finding is consistent with another study of NHANES III general population including 12,399 persons at least 17 years of age, which found that Non-Hispanic Blacks had a significantly higher prevalence of periodontal disease than both Mexican-Americans and NonHispanic Whites, and Mexican-Americans had rates similar to Non-Hispanic Whites [16]. In the present study, although Mexican-American pregnant women had lower rate of periodontal disease than NonHispanic Black pregnant women, the difference was not statistically significant. In addition, there was an unexpected trend for Mexican-American pregnant women to have more periodontal disease than the general population of Mexican-American women, and an opposite trend among Non-Hispanic Whites. These results may be due to the fact that the number of pregnant women by race-ethnicity groups included in NHANES III was relatively small, which thus suffered a lack of statistical power and resulted in imprecise estimates of prevalence. Another limitation of NHANES III is that data on birth outcomes were not available.
Hypothesis: periodontal disease as one possible explanation for the Mexican paradox Based on the data from the NHANES III, we found that Mexican-American women had similar poverty
rates, education and medical insurance coverage to Non-Hispanic Black women. Mexican-American women were less likely to smoke, which is consistent with previous reports [27,32,33]. Smoking is a well-established risk factor for both adverse pregnancy outcomes and poor periodontal status [50,51]. However, the disparity in periodontal disease between Mexican-American and Non-Hispanic Black women remained even after adjusting for potential confounding factors. Because periodontal disease could lead to an increased risk of preterm birth and low birth weight [5–9], and because the prevalence of periodontal disease is relatively low in Mexican-American women during and outside pregnancy, we speculate that this lower prevalence may explain (at least partially) the observed lower rate of low birth weight and preterm birth in Mexican-American women. In summary, our hypothesis is that the paradox of lower rates of low birth weight and preterm birth in Mexican-American women may be explained by the lower prevalence of periodontal disease in this population before and during pregnancy. Future studies, especially of a prospective design, are needed to test this hypothesis. Current theories do not sufficiently explain perinatal outcomes in different racial and ethnic populations. Should our hypothesis be confirmed by future studies, it will open doors to new intervention strategies to eliminate the racial and ethnic disparities in infant morbidity and mortality. Periodontal disease is both preventable and curable. Improving periodontal health before or during pregnancy may prevent or reduce occurrences of preterm birth and low birth weight and therefore reduce perinatal morbidity and mortality.
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