Periodontal Bone Loss in Pleistocene Hominins.

Already 50 years ago, the terms resistance and susceptibility in relation to the treatment of gingivitis were introduced by Cheraskin and Ringsdorf [1]. In the same year, the famous “experimental gingivitis in man” study by Löe and coworkers [2] was published, demonstrating that not all participants developed gingivitis at the same rate. Because most information about periodontal diseases at that time came from cross-sectional studies, Löe and coworkers initiated a prospective longitudinal study in 1969 [3]. The natural history of a disease has been defined as the “natural course of a disease from the time immediately prior to its inception, progressing, through its pre-symptomatic phase and different clinical stages to the point where it has ended and the patient is either cured, chronically disabled or dead without external intervention [4]. By natural course,” it is meant that no external intervention is applied that might change this pathway from health to disease expression [5]. In this regard the Sri Lanka branch of “The natural history of periodontal disease in man” study [3] fulfills that criterion. In the 1980s, a number of experimental gingivitis studies were carried out in individuals highly resistant to periodontitis and highly susceptible to periodontitis. Results of the experimental gingivitis study in individuals highly resistant to periodontitis [6] (mean age 58 years, no history of interdental cleaning and no attachment loss) showed that after 33 days of no oral hygiene, these participants developed only a few point bleeding sites after probing. In contrast, experimental gingivitis in highly susceptible periodontal patients with a reduced but healthy periodontium [7] (mean age 34 years) showed point bleeding sites after probing already after a few days. Over the last few decades there is increased awareness about the role of nutrition in periodontal diseases. This is evident from the numerous studies published over the years. A systematic review on this issue found inverse associations between a poor dietary intake of omega-3 fatty acids, vitamin C, vitamin E, beta-carotene, fiber, calcium, dairy, fruits and vegetables and an increased risk of periodontal disease in older adults [11]. On the basis of NHANES data it was shown that patients with a higher healthy eating index had a lower prevalence of periodontitis [12]. A systematic review further demonstrated that higher Healthy Eating Index scores, higher Mediterranean Diet scores, and lower Dietary Inflammatory Index scores were associated with a reduced risk of periodontitis and improved periodontal conditions [13]. In an 11 year follow-up study among middle-aged adults, poor-quality diet appears to be associated with the development of periodontal disease [14]. Another study using NHANES data showed that a healthy plant-based diet was inversely related to an increased risk of periodontitis [15]. Results of a 4-week replica study of “Stone Age” life and diet showed that gingivitis decreased, although plaque scores increased due to the lack of oral hygiene [16]. Since “Stone Age” living conditions, and especially a diet without refined sugars, are able to reduce gingivitis it can be hypothesized that it may also prevent the development of periodontitis. To investigate the influence of diet on the onset and progression of periodontitis in the absence of oral hygiene measures would require another natural history of periodontitis study. It is important to recognize, however, that the Sri Lanka and Java studies were initiated at a time when medical ethics committees did not yet mandate approval for such investigations. Today, ethics committees would not permit longitudinal studies in which treatment is withheld once disease is detected. Therefore, in our view, it is no longer feasible to conduct new longitudinal studies that examine, for example, the influence of diet on the onset and natural course of periodontitis using a natural history study design. Consequently, it may be of interest to investigate periodontal bone loss in fossils of Pleistocene ancestors predating the Neolithic period, when regular oral hygiene was absent and after which major lifestyle changes occurred, particularly in terms of diet. In human evolutionary history, it is evident that members of the genus Homo exhibited high versatility, inhabiting diverse environments during the Early Pleistocene (2.58 million to 774 000 years ago). Early Homo were dietary opportunists, capable of adapting to a wide range of paleohabitats [17]. Until the advent of agriculture, their diet consisted primarily of gathered plant-based foods (approximately 80%), including leafy greens, sweet grasses, nuts, seeds, tubers, berries, roots, fruits, and legumes, alongside animal protein from wild animals and fish (approximately 20%) [18]. It has been suggested that the prevalence of oral diseases such as caries and periodontitis was relatively low among our Pleistocene ancestors [19]. However, Lacy [20] concluded that periodontal disease was widespread in humans living from the Middle to Late Paleolithic (300 000–11 700 years before the year 2000). The aim of the present study, therefore, is to systematically assess the prevalence of interdental periodontal bone loss in fossils of hominins living in the Pleistocene. For this study the National Library of Medicine, Washington D.C. (MEDLINE-PubMed) database was used to retrieve articles on Pleistocene fossils with teeth present in the jawbone. A list of exclusion criteria is provided in Table 2. Following this selection procedure, 34 articles were included in the final evaluation, comprising 47 fossil hominin samples [21-54]. To estimate the age of the fossilized hominins, the age classification system proposed by Bolter et al. [27] was used (see Table 3). This system was applied directly by the original authors to15 hominins. Authors provided age estimates for 16 hominids, which were subsequently fitted into the Bolter system. The age classification “adult,” as used by the original authors for six hominins, was reclassified into two young adults and four old adults based on the Bolter criteria. Using this system, the remaining 10 hominins were classified as follows: Early Juvenile (1) Late Juvenile (2) Young Adult (3) and Old Adult (3). The age class of one fossil could not be determined. All classification procedures were carried out by author UvdV. Additionally, the division of the Pleistocene geological time period was established as follows: Early Pleistocene, Middle Pleistocene, and Late Pleistocene. After identifying the best available photograph of a fossil in each article, two interdental measurement sites at non-adjacent teeth were selected by UvdV, based on optimal accessibility for measurements and the greatest visible interdental bone loss. Locations situated too close to fracture planes were excluded. A list was compiled describing the measurement locations in each article. These included 58 molars, 18 premolars, 7 canines, 8 incisors, and 3 deciduous molars. At 300× magnification, the size of the scale bar in the photographs was measured by UvdV, and two independent researchers (MMD and UvdV) separately assessed the estimated distance between the cemento-enamel junction and the alveolar bone level using a digital caliper. A comparison of their measurements showed that in 68% of cases, the difference between the two was ≤ 1 mm. For these cases, the mean value was calculated. If the difference exceeded 1 mm, a new measurement was performed after discussion and agreement between both researchers. Due to the limited evaluable fossil material in some photographs, it was not possible to apply the criterion of bone loss at two non-adjacent teeth in 22 of the 47 fossils. In such cases, an alternative criterion was used: bone loss not occurring at the same interdental area. Due to the nature of the study material, only descriptive statistics are presented, and no statistical analyses were performed. The Pleistocene era was subdivided into the Early Pleistocene (2.58–0.774 millon years ago), the Middle Pleistocene (774 000–129 000 years before present), and the Late Pleistocene (129 000–11 000 years before the year 2000), following the classification of the Subcommission on Quaternary Stratigraphy. The present sample of 47 fossils includes 7 hominins (14.9%) without interdental bone loss, that is, both measurement sites showed a distance of ≤ 2 mm between the cemento-enamel junction and the alveolar bone level. Nine hominins (19.1%) exhibited bone loss at one site but not at the other. Based on individual bone loss severity, 29.8% of the hominins had minor bone loss, 31.9% had moderate bone loss, and 23.4% had severe bone loss (Table 4). Further evaluation identified 33 periodontal cases, defined as bone loss > 2 mm at 2 sites, representing 70% of the total sample. Among these: 5 hominins (15.2%) had severe bone loss (> 5 mm) at both sites, 7 hominins (21.2%) had a combination of severe and moderate bone loss, and 8 hominins (24.2%) had moderate bone loss (3–5 mm). The majority of hominins were young adults (40.4%) and old adults (25.5%). In both groups, approximately 33% exhibited severe bone loss. As shown in Table 4, 10 out of 12 old adults (83.3%) had moderate to severe bone loss, compared to 52.6% of young adults and 42.9% of subadults. Among the three early juveniles, one had two primary molars with no bone loss, another had two permanent molars with no bone loss, and the third had one exfoliating primary molar and one permanent molar, both without bone loss. Table 5 shows the distribution of fossilized hominins by age and severity of periodontal bone loss across the Late, Middle, and Early Pleistocene. It is evident that interdental periodontal bone loss was present in hominins throughout the entire Pleistocene. The eight hominins from the Late Pleistocene included five Homo sapiens (Hs), two Homo neanderthalensis (Hn), and one Homo floresiensis (Hf). The Hs group comprised two subadults (one with minor bone loss and one with moderate bone loss), two young adults (both with severe bone loss), and one old adult (with moderate bone loss). The two Hn individuals were early juveniles with no bone loss, and the Hf individual was an old adult with severe bone loss. Based on case reports, there is no doubt that periodontitis occurred in our ancestors long before the Holocene [56, 57]. In an extensive study of fossil material from 123 individuals living during the Middle to Late Paleolithic period, including 79 modern humans and 44 Neanderthals, it was concluded that periodontal disease was widespread among humans of that era [20]. In that study, the distance from the cemento-enamel junction (CEJ) to the alveolar crest (AC) was measured at the buccal and lingual midpoints using digital calipers. The author noted: “More than the standard two measurements (mid-point buccal and lingual) were taken when CEJ-AC distances varied greatly around the tooth, a condition more common in multi-rooted teeth. CEJ-AC distances were averaged per tooth, per tooth type, and individual with locations of severe angular defects noted.” In the present study, the decision was made to focus exclusively on the interdental areas of fossilized teeth when assessing periodontal bone loss. This approach was taken because buccal and lingual bone may already have been absent during life in cases of dehiscence, and because skeletal material becomes brittle over time, making it susceptible to postmortem damage and bone loss. As a result, buccal and lingual alveolar bone loss may be overestimated and may not accurately reflect the true extent of periodontitis-related bone loss. Nevertheless, the findings of the present study also indicate a high prevalence of periodontal bone loss in Pleistocene hominin fossils, with over 60% of subadult and older individuals exhibiting moderate to severe interdental bone loss. Although the number of fossils in the present study is extremely limited, no clear differences in the prevalence of interdental periodontal bone loss are evident among the three geological subdivisions of the Pleistocene, suggesting a high prevalence of this condition throughout the entire epoch. As discussed in the introduction, a poor diet may contribute to the development of periodontitis. In the replica “Stone Age” study by Baumgartner et al. (2009) [16], participants followed a restricted diet for 4 weeks consisting primarily of whole grains (barley, wheat, and spelt), along with small amounts of salt, herbs, honey, milk, and meat from domestic animals (goats and hens). Because this diet was not nutritionally complete, participants were required to supplement it with natural foraged foods such as berries, edible plants, and fish (caught without nets). It was suggested that a healthy diet free of refined sugars may have contributed to the reduction in gingival inflammation. Since refined sugars were absent in the Pleistocene, the findings of the present study do not support the idea that such a diet also may help prevent periodontitis. During human evolution, the diet shifted from being heavily plant-based to including more meat during the Early Pleistocene [58]. Isotopic analysis of Late Pleistocene fossils suggests that both animal and plant proteins contributed to an omnivorous diet, indicating a significant intake of meat alongside a clear consumption of plant-based foods [59]. Our closest relatives, the great apes (chimpanzees, bonobos, gorillas, and orangutans), primarily consume plant-based foods but also include animal-source foods in their diet [60]. A common feature among all of them is the presence of periodontitis [61], suggesting that susceptibility to periodontitis is a shared trait among primates, including humans. In the present study, the age classification of Bolter et al. [27] was used, as it provides the most effective framework for presenting data based on publications in which individual authors estimated the ages of fossils from various hominins that lived over a time span of more than 2.5 million years, likely exhibiting differences in developmental aging and lifespan. In order to facilitate comparison of periodontal bone loss prevalence in the studied fossils with data from contemporary epidemiological studies, the probable age ranges in years for the following Bolter groups are provided: sub-adult (12–20 years), young adult (20–35 years), and old adult (35+ years). Since the introduction of the EFP/AAP classification in 2018, several epidemiological studies have been conducted using or evaluating this system. The results showed that the prevalence of severe periodontal bone loss (i.e., stages III and IV) varies considerably across different countries. The following prevalences have been reported in young individuals: 8.1% in individuals aged 15–19 years (South America) [62], 22.0% in those aged 20–34 years (Cote d’Ivoire) [63], 22.8% in individuals aged 13–35 years (Saudi Arabia) [64]. In the present study, the prevalence of periodontal bone loss in fossil specimens classified as sub-adults and young adults combined was 26.9%, which is comparable to today's prevalence. In older age groups, much greater variation in prevalence was observed between countries: 8.9% in individuals aged 40–49 years (Norway) [65], 19.7% in those aged 35–44 years (Turkey) [66], 35.1% in individuals aged ≥ 30 years with a mean age of 50.5 years (USA) [67], 35.4% in the 35–44 age group (Côte d’Ivoire) [63], 74.1% in those aged 35–80 years (Saudi Arabia) [64], and 94.1% in the 35–44 age group of five South American countries [62]. Comparison of these data with the small number of 12 older adult fossils, of which 33% showed severe periodontal bone loss, is difficult, but again suggests a similar prevalence. Notably, one older adult exhibited no periodontal bone loss, indicating that not all hominins were susceptible to periodontitis. It is evident that both primates and hominins have faced significant stress throughout their evolutionary history. Environmental challenges (such as climate change), food scarcity, intraspecies competition, and social stress all contributed to natural selection and likely increased the risk of developing periodontitis, a trade-off seemingly taken for granted in the course of survival. Indeed, there is now strong evidence supporting the role of psychological stress and anxiety in the progression of periodontitis [68]. A major limitation of the present study is the small number of fossils; nevertheless, it can be concluded that the natural history of periodontitis in the Pleistocene does not differ markedly from that of today. Furthermore, in the absence of oral hygiene measures, a diet consisting of plant-based foods combined with either small or large amounts of animal-source products is likely to result in the development of periodontitis in the majority of primates and humans. This manuscript is part of “The Past, the Present, the Future” series, celebrating the 60th anniversary of the Journal of Periodontal Research [69]. AI statement: This manuscript did not use artificial intelligence in any capacity. The authors declare no conflicts of interest. The data that support the findings of this study are available from the corresponding author upon reasonable request.