12 Dental Anthropology 2019 │ Volume 32 │ Issue 02 Periodontal Health and the Lifecourse Approach in Bioarchaeology Alexandra Tuggle 1 and James T. Watson 2,3* 1 Department of Anthropology, The Ohio State University 2 Arizona State Museum, University of Arizona 3 School of Anthropology, University of Arizona Periodontal tissues historically receive little atten- tion in bioarchaeological research. Periodontal ‘health’, however, is essential to maintaining a foundation for attachment, stability, and retention of teeth. The concept of ‘health’ is more than the absence of disease and is therefore problematic among both clinicians and bioarchaeologists (see Pilloud and Fancher, this issue). Mariotti and Hefti’s (2015) call for redefinition of periodontal health among clinicians, using a modified wellness model, includes both physical (functional dentition and periodontal attachment stability) and psycho- social (pain and individual well-being) characteris- tics. The challenge for bioarchaeologists is defining what physical expression/degree within a disease process would begin to affect an individual’s well- being. Here we therefore apply a lifecourse ap- proach to the measurement of periodontal disease in a prehistoric sample from the American South- west to test the hypothesis that age and sex differ- ences bear the greatest impact on the expression of periodontitis. Periodontal disease (PD) is the clinical charac- terization of destruction of the periodontium—the oral structure containing the teeth, composed of both fibrous (gingival and periodontal ligament) and mineralized (cementum and alveolar bone) tissues. Periodontal disease has a multifactorial etiology, but is primarily associated with inflam- matory host response resulting from bacterial in- fection of periodontal tissues. Many bacterial spe- cies have been associated with the pathogenic colo- nization of subgingival biofilm (dental plaque) (Adriaens, De Boever, & Loesche, 1988; Boutin et al., 2017; Socransky & Haffajee, 2005) and the peri- odontal pocket provides an ideal eco-system for these organisms, containing a diverse microbiota of up to 700 prokaryote species (Boutin et al., 2017; Chen et al., 2010). Martelli and colleagues (2017) identify that the progression and severity of PD depends on the aggressiveness of the subgingival ABSTRACT Healthy periodontal tissues are essential to maintaining attachment, stability, and retention of teeth. The concept of ‘health’ is problematic however and includes both physical and psycho-social characteristics. The challenge for bioarchaeologists is defining what physical expression begins to affect an individual’s well-being. Here we apply a lifecourse approach to periodontal tissue health in a pre- historic sample (N = 166) from the American Southwest to test the hypothesis that age and sex differ- ences bear the greatest impact on the expression of periodontitis. Tooth loss, tooth wear, periodontal depth (CEJ-AC), and alveolar crest (AC) morphology were recorded at M1. T-tests identify that females exhibit significantly higher values across each variable. In addition, general linear modeling analyses demonstrate that values increased significantly across five age stages (15-20yo, 20-30yo, 30-40yo, 40- 50yo, 50+yo) with females exhibiting significantly higher values in the fourth and fifth decades of life. Results support the hypothesis that periodontal tissue loss differentially affects females across the lifecourse. Bacterial infection, chronic gingivitis, and attachment loss cause the physical symptoms of periodontal disease but may not be accompanied by pain or altered functionality. The outcome of the disease process is tooth loss, which can affect functionality and quality of life. Periodontal ‘health’ is therefore best interpreted in bioarchaeological samples around the point that attachment loss results in tooth loss and altered functionality. *Correspondence to: James T. Watson Arizona State Museum University of Arizona PO Box 210026, Tucson, AZ 85721 watsonjt@email.arizona.edu Keywords: periodontal disease, dental anthropology, lifecourse 13 Dental Anthropology 2019 │ Volume 32 │ Issue 02 plaque biofilm and individual host immune re- sponse, which can be further affected by genetic and epigenetic contexts and environmental factors (i.e., age, sex, smoking, oral hygiene, etc.). Today, PD is also correlated with various systemic disor- ders, including cancer, diabetes, rheumatoid arthri- tis, cardiovascular diseases, and preterm birth (Jepsen et al., 2018; Martelli et al., 2017). Studies of modern and prehistoric patterns of periodontal disease demonstrate that men general- ly have a higher prevalence than women (DeWitte, 2012; Shiau & Reynolds, 2010; Wasterlain et al., 2011). DeWitte (2012) proposes that this is likely due to immuno-buffering from estrogen among women (Klein and Huber, 2010). But there is other clinical evidence to suggest that hormonal fluctua- tions, particularly associated with pregnancy, may have adverse effects on periodontal health (Carrillo -de-Albornoz et al., 2010; Laine, 2002; Lukacs and Largaespada, 2006; Silk et al., 2008; Wu, Chen, & Jian, 2015). During pregnancy, production of estro- gens and progesterone is increased. Estrogen levels rise to over 100 times more than pre-pregnancy levels, with progesterone levels surpassing this even more. During labor, hormone concentrations drop, reaching their pre-pregnancy levels within 2- 3 days after delivery (Laine, 2002). After the second trimester, the placenta begins regulating hormone production to maintain the pregnancy, including maintenance of the endometrium, preparation for lactation, increase in basal metabolic rate, and reg- ulation of the immune system. The affiliated vascu- larization of bodily tissues often causes the gingiva to become inflamed and retain fluid, resulting in pregnancy gingivitis and edema (Bobetsis et al., 2006; Laine, 2002). While pregnancy does not actually cause gingi- vitis or periodontitis, the hormonal activity in gin- gival tissues can exacerbate pre-existing periodon- tal disease. With increased gingival inflammation and edema, the periodontium can become weak- ened (Laine, 2002; Silk et al., 2008). Especially in the presence of accumulated plaque and calculus, the gingiva can become detached from the tooth exposing the periodontium (Coventry et al., 2000). When bacteria infiltrate the weakened periodonti- um, their toxins activate a chronic inflammatory response, causing the ligaments and bone support- ing the teeth to break down (Silk et al., 2008). Current research has identified some specific pathophysiology that may contribute to PD associ- ated with hormonal activity during pregnancy. Pregnant women experience pronounced fluctua- tions in the sex hormone estrogen. Estrogen acts as a ligand for estrogen receptor ß (ERß), which plays an important role in periodontal ligament cell func- tion and proliferation (Jönsson et al., 2004; Liang et al., 2008; Mamalis et al., 2011; Wattanaroonwong et al., 2011). The periodontal ligament (PDL) is a con- nective tissue that bonds the cementum of the tooth to the alveolar bone. Collagen-producing PDL cells restore mineralized tissue and thus are essential in maintaining the structural and func- tional integrity of the periodontium. Human PDL cells have receptors for estrogen (ERß), which in turn has an inhibitory effect on bone-resorbing os- teoclast formation in the periodontium (Wattanaroonwong et al., 2011). Fluctuations in estrogen levels during pregnancy may affect subse- quent PDL cell proliferation and consequently per- iodontal integrity (Mamalis et al., 2011). Changes in progesterone levels associated with pregnancy can make the subgingival microbiota significantly more anaerobic (Kornman & Loesche, 1982; Paropkari et al., 2016). Less well explored is how salivary sex hormones affect the supragingi- val microbiota, which also experiences an ecologi- cal shift in association with pregnancy. Recently, Lin et al. (2018) explored the bacterial diversity and ecological shifts in the supragingival plaques of pregnant women and observed it is highly correlat- ed with the subgingival microbiota and may equal- ly contribute to oral dysbiosis during pregnancy. Lin et al. (2018) posited that consistent with surges in progesterone and estradiol during the third tri- mester, pregnancy constructs an environment con- ducive to some bacterial strains including mem- bers of the Neisseria and Poryphromonas genera. Progesterone may also downregulate IL-6 produc- tion by gingival fibroblasts, resulting in gingival inflammation and bacterial proliferation (Lapp et al., 1995). Other hormones associated with significant fluctuations during pregnancy have also been ex- plored as possible contributors to PD in women. Parathyroid hormone, a calcitropic hormone re- sponsible for calcium metabolism, decreases in early pregnancy. This is followed by a spike in the first trimester, a decline at the middle, and another rise towards the end of a pregnancy (Hameedi, 2017). Osteocalcin, an osteoblastic hormone, mir- rors parathyroid hormone fluctuations throughout pregnancy with corresponding effects on bone- formation processes (Seki et al., 1991). Progester- one levels also are negatively associated with calci- um levels in pregnant women (Hameedi, 2017). 14 Dental Anthropology 2019 │ Volume 32 │ Issue 02 Fertility in prehistoric agricultural communities The Holocene is characterized in part by the sub- stantial increase in human populations that oc- curred in a relatively small amount of time, mark- edly in areas that adopted agriculture (Larsen, 1995). Although the transition from foraging to farming is generally characterized by a decline in overall health (including a decline in skeletal ro- busticity and dental health), the archaeological rec- ord displays evidence of a "Neolithic demographic transition" (Ndt), wherein populations expanded in most agricultural communities throughout the world (Bocquet-Appel, 2002; Bocquet-Appel & Du- bouloz, 2004; Bocquet-Appel & Naji, 2006). While population growth is apparent, sedentary settle- ment is also commonly associated with a reduction in mean age-at-death and high prevalence of skele- tal lesions, often ascribed to nutritional deficiencies or infectious disease (Cohen & Armelagos, 1984). A decline in health and mean age-at-death coupled with an increase in population seems paradoxical, but many contend that this trend indicates an in- crease in fertility rather than an increase in mortali- ty due to poor general health (Wood, 1992). In ad- dition, the greater prevalence of skeletal lesions evidenced in agricultural samples could alterna- tively reflect enhanced resilience to illness and stress (Wood, 1992). Multiple causes for an increase in fertility among sedentary agriculturalists have been pro- posed. Cultivation of domestic crops such as maize in the New World would not only increase the car- rying capacity of the environment, but also result in lifestyle shifts leading to increased fertility (Lukacs, 2008). More dependable, higher calorie food supplies, a reduction in workload, and more readily available weaning foods would both in- crease the energy available to mothers and de- crease the necessary weaning time. Fecundity (the biological potential for childbearing) can be sensi- tive to energetic stress, and even moderate energet- ic stress appears to suppress ovarian hormone lev- els (Ellison et al., 2012). With decreased mobility associated with an agricultural lifestyle and a car- bohydrate-based, calorie-dense diet, women would likely be under less energetic stress and thus more fecund. A shorter weaning period may also influence fertility by a reduction in interbirth intervals. Lac- tation suppresses ovulation and often has a contra- ceptive effect due to the results of lactational amen- orrhea (Kennedy & Visness, 1992; WHO, 1999). However, variation in the contraceptive effect seems to be related to maternal energetic state. Re- search shows that maternal physiology acts to low- er the chance of another conception when energetic investment in the current child is still high. Lacta- tion is energetically expensive, and if the weaning age is decreased due to supplementation of wean- ing foods, the mother may return to a fecund state more quickly (Ellison, Bogin, & O'Rourke, 2012). Ethnographic comparisons with modern foraging societies show that they generally exhibit longer interbirth intervals (generally 3-4 years) and de- creased fertility due to longer breastfeeding peri- ods, higher mobility/activity level, and seasonal weight fluctuations with resource availability (Eshed et al., 2004; Hitchcock, 1982; Howell, 1979). In addition, higher rates of infant mortality (as ex- perienced by early agricultural populations) can increase fertility by returning a mother to a fecund state after the loss of a breastfeeding child (Ellison, Bogin, & O'Rourke, 2012). Given the complex interplay between repro- ductive hormones and the reproductive burden associated with burgeoning population growth among prehistoric agricultural groups, the cumula- tive effects of high fertility rates would differential affect women in these prehistoric communities. We therefore suggest that age and sex differences have the greatest impact on the expression of periodon- tal disease, which may be a function of high fertili- ty. Here we apply a lifecourse approach to the measurement of periodontal disease in a prehistor- ic sample from the American Southwest to test this hypothesis. Materials and Methods The samples analyzed in this study were recovered from a series of archaeological sites associated with the Mogollon archaeological culture (Fig. 1). The Mogollon archaeological culture is associated with Ancestral Puebloan occupation of the rugged inter- montane region of east-central Arizona and west- central New Mexico (Reid & Whittlesey, 1997). The Mogollon area is physiographically diverse with low valleys containing desert and grassland eco- systems and high elevations (~6,000 feet) character- ized by large, Ponderosa pine forests and juniper/ piñon woodlands (Reid, 2006; Woodbury, 1961). Although agriculture, particularly reliant on maize, was the foundation of their subsistence economy, a variety of local wild resources continued to pro- vide an important role in the diet (Reid & Whittle- sey, 1997; Woodbury, 1961). The Pueblo Period of Mogollon development in Arizona began around A.D. 1100 with the transi- tion from pit houses to masonry construction and 15 Dental Anthropology 2019 │ Volume 32 │ Issue 02 lasted until about A.D. 1400 when the pueblos were abandoned and populations became effec- tively archaeologically invisible (Reid & Whittle- sey, 1997). This period is characterized by rapid population growth and nucleation into fewer, larg- er villages. Nucleation resulted in denser popula- tion concentrations within groups but larger dis- tances between groups (Tuggle, 1970). As popula- tion densities increased, pueblo residents became more dependent on cultivated crops and relied less on foraging wild resources. Sometime around A.D. 1400, as most communities neared the maximum population density that could be supported by available agricultural technologies and exhausted their wild resources, Mogollon villages were large- ly abandoned. Environmental pressure was aggra- vated by several periods of drought, resulting in migration out of the region (Reid & Whittlesey, 1997; Tuggle, 1970). There is also evidence of sig- nificant economic and social tensions (Reid and Whittlesey, 1997). Skeletal remains from five Mogollon sites were analyzed for evidence of periodontal disease. The sites include Point of Pines, Turkey Creek, Kinishba, King Ruin, and AZ:W:10:52(ASM), which represent a series of large, multi-room pueb- los that emerged in the Mogollon region with occu- pations that ranged between A.D. 1225 to 1450 (East, 2008; Haury, 1989; Lowell, 1991; Welch, 2016). Together these samples represent a 225-year sequence of population growth, until social col- lapse, reorganization, migration, and partial aban- donment of the Mogollon area. Based in successful agricultural adaptations, it is likely that a combina- tion of environmental and social stressors led to eventual collapse. The demographic profile, in- cluding generally a higher infant mortality fits the curve proposed by Bocquet-Appel (2002) as repre- senting high fertility populations and therefore make ideal samples to test the relationship be- tween periodontal disease and sex across the lifecourse. The Mogollon samples are part of the Bioar- chaeology Collection at the Arizona State Museum (ASM), University of Arizona in Tucson, Arizona. Sex and age data were obtained from the Arizona State Museum Human Remains Database, estimat- ed previously by ASM curators using macroscopic aspects of the pelvis and/or cranium for sex (Buikstra and Ubelaker, 1994), and macroscopic changes in the pubic symphysis (Buikstra & Ub- elaker, 1994) and relative rates of dental attrition (Brothwell, 1989) for age. Individuals of indetermi- nate sex or age were excluded from the analysis. Table 1 displays the distribution of samples by site, age, and sex. The 166 individuals were sepa- rated into five decadal age sets representing the sequence from late juvenile to senescence. We fo- cused our analysis on the first permanent mandib- ular molar (M1) because periodontal disease differ- entially affects posterior teeth (Kerr, 1989) and the first molar is in occlusion the longest among the posterior teeth, thereby having the greatest poten- tial for the expression of PD over the lifecourse. The remains were analyzed at the ASM by James Watson and Theodora Burbank and included 1) an inventory of teeth including antemortem loss, 2) recording occlusal surface wear (Wear) according Figure 1. Map of Southwest US/Northwest Mexi- co with the Mogollon archaeological culture area defined by dashed line, and location of sites plot- ted (marked by squares). Map reproduced with permission from Arizona State Museum. Site Sex 15-20 20-30 30-40 40-50 50+ Point of Pines M 1 9 9 3 1 F 5 12 10 3 0 Turkey Creek M 2 4 10 13 4 F 2 5 9 11 6 Kinishba M 3 5 7 0 1 F 7 4 4 2 0 King Ruin M 0 0 0 1 0 F 0 1 1 1 0 AZ:W:10: 52 M 0 3 3 1 0 F 0 2 0 1 0 Table 1. Archaeological samples used in analysis 16 Dental Anthropology 2019 │ Volume 32 │ Issue 02 to Scott (1979), 3) measuring distance of the alveo- lar crest (AC) from the cemento-enamel junction (CEJ) on the buccal surface of M1 (CEJ-AC) with a periodontal probe (Hu-Friedy UNC-15 color-coded periodontal probe), and 4) alveolar crest (AC) mor- phology according to Kerr (1988). Independent samples t-tests are used to com- pare mean values for Wear, CEJ-AC, and AC and a Mann-Whitney U test to compare frequency of tooth loss between sexes. In addition, general line- ar modeling analysis (Gill, 2001)—with age as the covariate and sex as the grouping factor— compares mean values between sexes across age groups. All statistical procedures were performed using IBM SPSS Statistics for Windows, v25.0 (SPSS Inc., Chicago, IL., USA). Results Preliminary comparisons by sex identify signifi- cant differences in mean values, with females ex- hibiting higher rates of wear, deeper CEJ-AC depths, and more compromised alveolar crest mor- phology (Table 2). In addition, the Mann-Whitney U test indicates that tooth loss was greater for fe- males (mean rank: 76.01) than males (mean rank: 91.55), U= 6537.0, p= .006. Comparisons across age groups demonstrate the general age-related progression of periodontal attachment loss that is typical of the general trend in clinical studies (Billings et al., 2018; Eke et al., 2018). The results of the general linear modeling analysis show similar significant differences in tooth wear, alveolar crest depth, and alveolar crest morphology between males and females across age grades (Table 3). Figures 2-4 plot the means and 95% confidence intervals of each variable across age groups demonstrating similar patterns over the life course. Mean values are similar between males and females in the youngest age cohorts but begin to separate in the fourth and fifth decades of life, only to return to closer values in the final decade (s). In addition to measurable attachment loss of the alveolar crest, tooth loss at M1 was significant. Tooth loss is again more pronounced among fe- males compared to males in the middle decades of life; 30-40yo and 40-50 (Fig. 5). Discussion Our results support the hypothesis that periodon- tal disease can be measured across the lifecourse (using the proxy measurements observed here) and demonstrate that females suffered dispropor- tionately from tooth and periodontal tissue loss. Periodontal attachment loss differed over the lifecourse; however, with both sexes experiencing similar (non-significant) periodontal tissue depths and morphology in the early age grades and expe- riencing significant increases after roughly age 30. Males appear to display a steady, age-related de- cline in periodontal tissue quality that only again approaches higher female levels in the oldest age Variable Sex N Mean s.d. t df Sig. Wear M 80 3.59 1.17 -4.682 164 <0.001 F 86 4.58 1.53 CEJ-AC M 80 2.11 1.21 -3.695 164 <0.001 F 86 2.81 1.23 AC M 80 2.09 0.93 -5.656 164 <0.001 F 86 2.94 1.01 Variable Sex 15-20 20-30 30-40 40-50 50+ F df Sig. Wear M 3.0 3.0 4.0 4.0 4.0 31.030 2 <0.001 F 3.0 4.0 5.0 5.0 6.0 CEJ-AC M 1.0 2.0 2.0 2.0 3.0 20.659 2 <0.001 F 2.0 2.0 3.0 3.0 4.0 AC M 2.0 2.0 2.0 2.0 3.0 30.433 2 <0.001 F 2.0 3.0 3.0 3.0 4.0 Table 2. Results of independent samples t-tests for variables by sex Table 3. Results for general linear modeling by sex and age groups 17 Dental Anthropology 2019 │ Volume 32 │ Issue 02 grade; and this is more related to greater variabil- ity in expression among males rather than a final spike in tooth and tissue loss. Significant differ- ences between sexes from 30 to 50 years suggests an underlying biological phenomenon negatively affecting women's oral health. We propose that hormonal fluctuations associ- ated with reproduction and higher parity in prehis- toric Mogollon communities are the cause of dis- parities in periodontal retreat and tooth loss be- tween sexes. Tooth loss specifically can also result from dental caries, pulp exposure from heavy wear, and trauma; but the co-occurring trends ob- served in the data suggest inter-related processes contributing to tooth loss. It is likely that trends in caries frequency in the sample would mirror those observed in periodontal tissues but is beyond the scope of the current study. Tooth wear also ap- pears to have played a role in destabilizing perio- dontal tissues through continuous eruption in re- sponse to heavy tooth wear. Yet, tooth wear also increases significantly in the interval from 30 to 50 years where female periodontal health incremen- tally declines compared to males and is perhaps exacerbated by tooth loss, loss of contact, and mal- occlusion. Clinical and epidemiological research shows that the hormonal fluctuations associated with re- productive physiology play a substantial role in maintaining healthy periodontal tissues (Laine, 2002; Wu et al., 2015). Evidence from ethnographic accounts and the archaeological record suggests a Figure 2. Mean wear score (from Scott, 1979) at M1 plotted by age groups for males and females. Error bars represent 95% confidence intervals. Figure 3. Mean distance (mm) from the cemento-enamel junction on the buccal surface of M1 to the alveolar crest plotted by age groups for males and females. Error bars rep- resent 95% confidence intervals. Figure 4. Mean alveolar crest morphology score (from Kerr, 1988) at M1 plotted by age groups for males and females. Error bars represent 95% confidence intervals. Figure 5. Frequency (%) of tooth loss at M1 plotted by age groups for males and females. 18 Dental Anthropology 2019 │ Volume 32 │ Issue 02 general pattern of increased fertility with the adop- tion of agriculture in most areas (Bocquet-Appel & Naji, 2006; Eshed et al., 2004). Sedentism is associ- ated with lifestyle changes that could critically im- pact fertility, including increased availability of energy-dense foods, decreased mobility, and short- er interbirth intervals (Ellison et al., 2012; Lukacs, 2008). A cariogenic diet reliant on maize undoubt- edly played a crucial role in the overall decline in oral health observed in prehistoric agricultural populations of the Southwest US/Northwest Mexi- co. Dietary composition and high fertility likely led to an environment in which women experienced exacerbated oral pathology (Watson et al., 2009). This study contributes some insights into the oral health of women in prehistoric agricultural com- munities in Arizona. The impact of pregnancy and reproduction has been largely avoided in archaeological literature, in part due to the difficulty associated with its study. While this study barely scratches the surface of the problem, it highlights a need to engage with life history theory and acknowledge the influences of reproductive life history on women's health in ar- chaeological research. Although current medical and dental therapy place emphasis on improving the well-being of pregnant women and their un- born children (Jared & Boggess, 2008; Russell & Mayberry, 2008; Sanz & Kornman, 2013), data show that increased parturition is still related to increased tooth loss in a woman’s lifespan (Christensen et al., 1998; Russell et al., 2008). This trend of increased tooth loss extends across cultur- al and socio-economic boundaries. It probably is related to the ongoing problem of untreated dental disease, which includes maternal periodontitis (Jeffcoat et al., 2001; Offenbacher et al., 1996). Our results specifically demonstrate that cu- mulative effects among reproductive-age and post reproductive-age females caused disproportionate tooth and periodontal tissue loss. Hormone fluctu- ations associated with reproductive physiology play a substantial role in maintaining healthy peri- odontal tissues (Wu, Chen, & Jiang, 2015). Bacterial infection, chronic gingivitis and attachment loss cause the physical signs and symptoms of perio- dontal disease. However, this inflammatory de- struction of the periodontium often is not accom- panied by pain or altered function until advanced degrees of destruction. The penultimate outcome of the disease process is tooth loss, which can affect functionality and quality of life. Periodontal ‘health’ is therefore best interpret- ed/conceptualized in bioarchaeological samples around the point that attachment loss destabilizes the tooth and results in loss and altered functional- ity. Although still stemming from a ‘disease- focused’ approach, we consider how functional occlusion plays a significant role in health. In addi- tion, the pain and process involved in tooth loss and removal will significantly impact quality of life, followed by altered functionality and differen- tial wear. This allows bioarchaeologists to relate past people’s physical conditions to modern clini- cal and epidemiological understandings of health and pathology. Acknowledgements We would like to express our gratitude to Theo Burbank for assisting with data collection on sever- al of the skeletal collections, to Marin Pilloud and J. P. Fancher for their invitation to contribute to the 2018 AAPA poster symposium dedicated to “Reevaluating the meaning of ‘oral health’ in bio- archaeology”, to Marin Pilloud for the invitation to contribute to this special issue of Dental Anthropolo- gy, and again to J. P. Fancher for extensive com- ments that led to a much improved manuscript. REFERENCES Adriaens, P.A., De Boever, J.A., Loesche, W.J. (1988). Bacterial invasion in root cementum and radicular dentin of periodontally diseased teeth in humans. A reservoir of periodonto- pathic bacteria. Journal of Periodontology, 59, 222 -230. Billings, M., Holtfreter, B., Papapanou, P.N., Mit- nik, G.L., Kocher, T., and Dye, B.A. (2018). Age -dependent distribution of periodontitis in two countries: Findings from NHANES 2009 to 2014 and SHIP-TREND 2008 to 2012. Journal of Periodontology, 89, S1, S140-S158. Bobetsis, Y.A., Barros, S.P., and Offenbacher, S. (2006). Exploring the relationship between per- iodontal disease and pregnancy complications. Journal of the American Dental Association, 137 (Suppl), 7S–13S. Boquet-Appel, J-P. (2002). The paleoanthropologi- cal traces of the Neolithic demographic transi- tion. Current Anthropology, 43, 638-650. Boquet-Appel, J-P. and Dubouloz, J. (2004). Ex- pected paleoanthropological and archaeologi- cal signal from a Neolithic demographic transi- tion on a worldwide scale. Documenta Praehis- torica, 31, 25-33. Boquet-Appel, J-P. and Naji, S. (2006). Testing the hypothesis of a worldwide Neolithic demo- graphic transition. Current Anthropology, 47, 19 Dental Anthropology 2019 │ Volume 32 │ Issue 02 341-365. Boutin, S., Hagenfeld, D., Zimmermann, H., El Sayed, N., Höpker, T., Greiser, H.K., Becher, H., Kim, T-S. ,& Dalpke, A.H. (2017). Cluster- ing of Subgingival Microbiota Reveals Microbi- al Disease Ecotypes Associated with Clinical Stages of Periodontitis in a Cross-Sectional Study. Frontiers in Microbiology, 8, 340-353. Brothwell, D. (Ed.). (1989). The relationship of tooth wear to aging. In Işcan MY, Age Markers in the Human Skeleton (pp. 303-318). Spring- field: Charles C. Thomas Publisher. Buikstra, J.E. & Ubelaker, D.H. (1994). Standards for data collection from human skeletal re- mains. Arkansas Archeological Survey Research Series, 44. Carrillo-de-Albornoz, A.E., Figuero, D., Herrera, P., & Bascones-Martínez, A. (2010). Gingival changes during pregnancy: II. Influence of hor- monal variations on the subgingival biofilm. Journal of Clinical Periodontology, 37( 3), 230-40. Carrillo-de-Albornoz, A.E., Figuero, D., Herrera, P., & Bascones-Martínez, A. (2012). Gingival changes during pregnancy: III. Impact of clini- cal, microbiological, immunological, and socio- demographic factors on gingival inflammation. Journal of Clinical Periodontology, 39, 272-83. Chen, T., Yu, W-H., Izard, J., Baranova, O.V., Lak- shmanan, A., & Dewhirst, F.E. (2010). The hu- man oral microbiome database: a web accessi- ble resource for investigating oral microbe taxonomic and genomic information. Database (Oxford); 2010 baq013. Christensen, K., Gaist, D., Jeune, B., & Vaupel, J.W. (1998). A tooth per child? The Lancet, 352 (9123), 204. Christian, L.M. (2015). Stress and immune function during pregnancy: an emerging focus in mind -body medicine. Current Directions in Psycho- logical Science, 24(1), 3-9. Cohen, M.N. & Armelagos, G.J. (Eds.). (1984). Pale- opathology at the origins of agriculture. New York, NY: Academic Press. Cohen, M.N. & Crane-Kramer, G.M.M. (Eds.). (2007). Ancient health: Skeletal indicators of Aari- cultural and economic intensification. Gaines- ville, FL: University Press of Florida. Coventry, J., Griffiths, G., Scully, C., & Tonetti, M. (2000). ABC of oral health: periodontal dis- ease. British Medical Journal, 321(7252), 36-39. East, A. (2008). Reproduction and prenatal care in Ari- zona prehistory: An examination of patterns of health in perinates and children at Grasshopper, Point of Pines, and Turkey Creek Pueblos. Ph.D. dissertation, University of New Mexico. Ann Arbor, MI: ProQuest LLC. Eke, P.I., Thornton-Evans, G.O., Wei, L., Borgnakke, W.S., Dye, B.A., & Genco, R.J. (2018). Periodontitis in US adults: National health and nutrition examination survey 2009- 2014. The Journal of the American Dental Associ- ation, 149(7), 576-588.e576. Ellison, P.T., Bogin, B., & O'Rourke, M.T. (2012). Demography part 2: Population growth and fertility regulation. In S. Stinson, B. Bogin, and D. O'Rourke (Eds.), Human Biology: An Evolu- tionary and Biocultural Perspective (pp. 757- 803). Hoboken, NJ: Wiley Blackwell. Eshed, V., Gopher, A., Gage, T.B., & Hershkovitz, I. (2004). Has the transition to agriculture re- shaped the demographic structure of prehis- toric populations? New evidence from the Levant. American Journal of Physical Anthropol- ogy, 124, 315-329. Fields, M., Herschaft, E.E., Martin, D.L., & Watson, J.T. (2009). Sex and the agricultural transition: Dental health of early farming females. Journal of Dentistry and Oral Hygiene, 1(4), 42-51. Gill, J. (2001). General linear models: A unified ap- proach. Thousand Oaks, CA: Sage Publica- tions. Hameedi, B.H. (2017). Estimation of parathyroid hormone, progesterone and prolactin, with some electrolyte in sera of first trimester Iraqi pregnant women. International Journal of Sci- ence and Nature, 8(3), 710-713. Haury, E.W. (1989). Point of Pines, Arizona: A his- tory of the University of Arizona archaeologi- cal field school. In Anthropological Papers of the University of Arizona No. 50. Tucson, AZ: Uni- versity of Arizona Press. Hillson, S. (2002). Dental anthropology. Cambridge: Cambridge University Press. Hitchcock, R.K. (1982). Patterns of sedentism among the Besarwa of eastern Botswana. In E. Leacock and R.B. Lee (Eds.), Politics and Histo- ry in Band Societies, (pp. 223-268). Cambridge: Cambridge University Press. Howell, N. (1979). Demography of the Dobe !Kung!. New York, NY: Academic Press. Jared, H., & Boggess, K. (2008). Periodontal diseas- es and adverse pregnancy outcomes: a review of the evidence and implications for clinical practice. Journal of Dental Hygiene, 82(3), 2-20. Jeffcoat, M.K., Geurs, N.C., Reddy, M.S., Cliver, S.P., Goldenberg, R L., & Hauth, J.C. (2001). Periodontal infection and preterm birth: Re- sults of a prospective study. The Journal of the 20 Dental Anthropology 2019 │ Volume 32 │ Issue 02 American Dental Association, 132(7), 875-880. Jepsen, S., Caton, J.G., Albandar, J.M., Bissada, N F., Bouchard, P., Cortellini, P., & Yamazaki, K. (2018). Periodontal manifestations of systemic diseases and developmental and acquired conditions: Consensus report of workgroup 3 of the 2017 world workshop on the classifica- tion of periodontal and peri-implant diseases and conditions. Journal of Periodontology, 89 (S1), S237-S248. Jönsson, D., Andersson, G., Ekblad, E., Liang, M., Bratthall, G., & Nilsson, B.-O. (2004). Im- munocytochemical demonstration of estrogen receptor β in human periodontal ligament cells. Archives of Oral Biology, 49, 85-88. Kennedy, K.I. & Visness, C.M. (1992). Contracep- tive efficacy of lactational amenorrhoea. The Lancet, 339(8787), 227-230. Kerr, N.W. (1988). A method of assessing perio- dontal status in archaeologically derived skele- tal material. Journal of Paleopathology, 2(2) 67-78. Kerr, N.W. (1989). The periodontal status of a Scot- tish Mediaeval Cohort. Journal of Paleopatholo- gy, 2, 119-128. Klein, S.L., & Huber, S. (2010). Sex differences in susceptibility to viral infection. In S.L. Klein, and C. Roberts, (Eds.), Sex Hormones and Im- munity to Infection (pp 93–122). Heidelberg: Springer. Kornman, K.S. & Loesche, W.J. (1982). Effects of estradiol and progesterone on Bacterioides mela- ninogenicus and Bacterioides gingivalis. Infection and immunity, 35(1), 256-263. Laine, M.A. (2002). Effect of pregnancy on perio- dontal and dental health. Acta Odontologica Scandinavica, 60, 257-264. Lapp, C.A., Thomas, M.E., & Lewis, J.B. (1995). Modulation by progesterone of interleukin-6 production by gingival fibroblasts. Journal of Periodontology, 66, 279-284. Larsen, C.S. (1995). Biological changes in human populations with agriculture. Annual Review of Anthropology, 24, 185-213. Larsen, C.S. (1998). Gender, health, and activity in foragers in the American Southeast: implica- tions for social organization in the Georgia Bight. In A.L. Grauer and P. Stuart-Macadam (Eds.), Sex and Gender in Paleopathological Per- spective (pp. 165-187). Cambridge: Cambridge University Press. Larsen, C.S. (2002). Bioarchaeology: The lives and lifestyles of past people. Journal of Archaeologi- cal Research, 10, 2, 119-166. Larsen, C. S. (2015). Bioarchaeology: Interpreting be- havior from the human skeleton (second edition). Cambridge: Cambridge University Press. Liang, L., Yu, J.-F., Wang, Y., Wang, G., &Ding, Y. (2008). Effect of estrogen receptor beta on the osteoblastic differentiation function of human periodontal ligament cells. Archives of Oral Biol- ogy, 53, 553-557. Lin, W., Jiang, W., Hu, X., Gao, L., Ai, D., Pan, H., & Huang, Z. (2018). Ecological shifts of su- pragingival microbiota in association with pregnancy. Frontiers in Cellular and Infection Microbiology, 8, 24. Lowell, J.C. (1991). Prehistoric households at Tur- key Creek Pueblo, Arizona. In Anthropological Papers of the University of Arizona No. 54. Tuc- son, AZ: University of Arizona Press. Lukacs, J.R. (2008). Fertility and agriculture accen- tuate sex differences in dental caries rates. Cur- rent Anthropology, 49, 901-914. Lukacs, J.R. & Largaespada, L.L. (2006). Explaining sex differences in dental caries prevalence: sali- va, hormones and “life-history” etiologies. American Journal of Human Biology, 18, 540-555. Mamalis, A., Markopoulou, C., Lagou, A., & Vrot- sos, I. (2011). Oestrogen regulates proliferation osteoblastic differentiation, collagen synthesis and periostin gene expression in human perio- dontal ligament cells through oestrogen recep- tor beta. Archives of Oral Biology, 56, 446-455. Martelli, M.L., Brandi, M.L., Martelli, M., Nobili, P., Medico, E., &Martelli, F. (2017). Periodontal disease and women’s health. Current Medical Research and Opinion, 33(6), 1005-1015. Nelson, G.C. (2016). A host of other dental diseases and disorders. In J.D. Irish and G.R. Scott (Eds.), A Companion to Dental Anthropology (pp. 465-483). West Sussex, UK: Wiley Blackwell. Offenbacher, S., Katz, V., Fertik, G., Collins, J., Boyd, D., Maynor, G., & Beck, J. (1996). Perio- dontal infection as a possible risk factor for preterm low birth weight. Journal of Periodontol- ogy, 67(10s), 1103-1113. Paropkari, A.D., Leblebicioglu, B., Christian, L.M., & Kumar, P.S. (2016). Smoking, pregnancy, and the subgingival microbiome. Scientific Re- ports, 6, 30388. Pearce-Duvet, J.M.C. (2006). The origin of human pathogens: Evaluating the role of agriculture and domestic animals in the evolution of hu- man disease. Biology Review, 81, 369-382. Reid, J.J. (2006). A Grasshopper perspective on the Mogollon of the Arizona mountains. In L.S. Cordell and G.J. Gumerman (Eds.), Dynamics of Southwest Prehistory. Tuscaloosa, AL: Universi- 21 Dental Anthropology 2019 │ Volume 32 │ Issue 02 ty of Alabama Press. Reid, J.J. & Whittlesey, S. (1997). The Archaeology of Ancient Arizona. Tucson, AZ: University of Ari- zona Press. Russell, S.L., Ickovics, J.R., & Yaffee, R.A. (2008). Exploring potential pathways between parity and tooth loss among American women. Amer- ican Journal of Public Health, 98(7), 1263-1270. Russell, S.L., & Mayberry, L. (2008). Pregnancy and oral health: A review and recommendations to reduce gaps in practice and research. MCN Am J Matern Child Nurs, 33(1), 32-37. Sanz, M., &Kornman, K. (2013). Periodontitis and adverse pregnancy outcomes: consensus report of the Joint EFP/AAP Workshop on Periodon- titis and Systemic Diseases. Journal of Periodon- tology, 84(4-s), S164-S169. Scott, E. C. (1979). Dental wear scoring technique. American Journal of Physical Anthropology, 51, 213-218. Seki, K., Makimura, N., Mitsui, C., Hirata, J., & Na- gata, I. (1991). Calcium-regulating hormones and osteocalcin levels during pregnancy: A longitudinal study. American Journal of Obstet- rics and Gynecology, 164(5), 1248-1252. Shiau, H.J., & Reynolds, M.A. (2010). Sex differ- ences in destructive periodontal disease: A sys- tematic review. Journal of Periodontology, 81, 1379-1389. Silk, H., Douglass, A.B., Douglass, J.M., & Silk, L. (2008). Oral health during pregnancy. American Family Physician, 77(8), 1139-1144. Socransky, S.S. & Haffajee, A.D. (2005). Periodontal microbial ecology. Periodontology 2000, 38(1), 135-187. Tuggle, H.D. (1970). Prehistoric Community Relation- ships in East Central Arizona. Ph.D Dissertation, University of Arizona. Ann Arbor, MI: Univer- sity Microfilms. Wasterlain, S. N., Cunha, E. & Hillson, S. (2011). Periodontal disease in a Portuguese identified skeletal sample from the late nineteenth and early twentieth centuries. American Journal of Physical Anthropology, 145, 30–42. Watson, J.T., Fields, M., & Martin, D.L. (2009). In- troduction of agriculture and its effects on women’s oral health. American Journal of Hu- man Biology, 22, 92-102. Wattanaroonwong, N., Schoenmaker, T., de Vries, T.J., & Everts, V. (2011). Oestrogen inhibits os- teoclast formation induced by periodontal liga- ment fibroblasts. Archives of Oral Biology, 56, 212-219. Welch, J.R. (2016). The site that nobody really knows: Kinishba revisited. Archaeology South- west, 30(1). Whittlesey, S.M., & Reid, J.J. (2001). Mortuary ritu- al and organizational inferences at Grasshop- per Pueblo, Arizona. In D.R Mitchell & J.L. Brunson-Hadley (Eds.), Ancient Burial Practices in the American Southwest: Archaeology, Physical Anthropology, and Native American Perspectives (pp. 68-96). Albuquerque: University of New Mexico Press. WHO. (1999). The World Health Organization multinational study of breast-feeding and lac- tational amenorrhea. III. Pregnancy during breast-feeding. Fertility and Sterility, 72(3), 431- 440). Wood, J.W., Milner, G.R., Harpending, H.C., & Weiss, K.M. (1992). The osteological paradox: Problems of inferring prehistoric health from skeletal samples. Current Anthropology, 33(4), 343-358. Woodbury, R.B. (1961). Prehistoric Agriculture at Point of Pines, Arizona. Salt Lake City, UT: Uni- versity of Utah Press. Wu, M., Chen, S-W., & Jiang, S-Y. (2015). Relation- ship between gingival inflammation and preg- nancy. Mediators of Inflammation, vol. 2015, Ar- ticle ID 623427, 11 pages.