Original Paper Caries Res 2012;46:467–473 DOI: 10.1159/000339664 Received: March 9, 2012 Accepted after revision: May 21, 2012 Published online: July 13, 2012 Dental Caries in Rome, 50–100 AD O. Fejerskov a P. Guldager Bilde b M. Bizzarro d J.N. Connelly d J. Skovhus Thomsen a B. Nyvad c a Department of Biomedicine – Anatomy, b Department of Culture and Society, and c Department of Dentistry, Aarhus University, Aarhus, and d Centre for Star and Planet Formation, Natural History Museum of Denmark, University of Copenhagen, Copenhagen, Denmark Key Words Archaeology ⴢ Dental medicine in Imperial Rome ⴢ Dentin hypermineralization ⴢ Lead isotope ratio ⴢ Micro-computed tomography pipe. The Pb isotopic composition of the tooth did not match that of the tube, suggesting that the subjects were exposed to different Pb sources during their lifetime other than the lead tubes. Copyright © 2012 S. Karger AG, Basel Abstract Scarce information exists on the clinical features of dental caries in the Imperial Roman population and no structural data on caries lesions from this period have so far been published. We report on the findings of 86 teeth (50–100 AD) found during archaeological excavations of the temple of Castor and Pollux in the Forum Romanum. We found that nearly all teeth had large carious cavities extending into the pulp. The distribution and size of the caries lesions were similar to those found in contemporary adult populations in Africa and China living without access to dental care. Most lesions had a hypermineralized zone in the dentin at the advancing front of the carious cavities as revealed by microcomputed tomography. This biological dentin reaction combined with the morphology of the cavities might indicate that some temporary topical pain relief and intervention treatment slowed down the rate of lesion progression. This is indirectly supported by examination of cavities of similar size and depth from a contemporary population without access to dental health care. In contrast to the lesions in the Roman teeth, these lesions did not exhibit a hypermineralized dentin reaction. We investigated whether the Pb isotopic composition of enamel and/or dentin of a single tooth matched that of a sample of an ancient Forum water lead Despite a wealth of information about medicine, diseases, and their treatment in ancient Rome [Plinius, 1951– 1963; Celsus, 1960/61] there is limited knowledge about the prevalence of dental caries during the Roman Imperial Age (1st–3rd century AD). Studies of skeletal remains from central Italy (Latinum) suggest that the caries prevalence of slaves and middle-class people such as administrators and merchants was quite low, affecting no more than 4–6% of the teeth, corresponding to 36–52% of the population [Manzi et al., 1999]. Similar low caries figures have been reported for 78 children below the age of 12 [Prowse et al., 2008]. By contrast, excavation of a burial site for predominantly lower social class males near Rome showed a ‘high frequency’ of caries [Catalano et al., 2010] similar to reports from examination of 67 adults from the necropolis of Quadrella in central Italy originating from the same time period [Bonfiglioli et al., 2003]. Up until now there have been no reports on the caries status of the population from the city of Rome during the Imperial period, and no studies have described the microscopical characteristics of dental caries lesions in ancient Rome. During archaeological excavations in the Forum Romanum in the early 1980s, initiated by the Nordic Insti- © 2012 S. Karger AG, Basel 0008–6568/12/0465–0467$38.00/0 Fax +41 61 306 12 34 E-Mail [email protected] www.karger.com Accessible online at: www.karger.com/cre Prof. Ole Fejerskov Department of Biomedicine – Anatomy Wilhelm Meyers Allé 3, Aarhus University DK–8000 Aarhus C (Denmark) Tel. +45 8716 7638, E-Mail of @ ana.au.dk tutes in Rome [Guldager and Slej, 1986; Ginge et al., 1989], it became apparent that the Temple of Castor and Pollux had a peculiar arrangement with narrow tabernae in the podium on three sides of the temple. On the floor of one of these the presence of what was originally thought to be a grave was found and one of the authors (P.G.B.) became responsible for this particular excavation site. However, it appeared to be a channel, which led from the room to another channel in the foundation, eventually opening directly into the Cloaca Maxima [Bilde, 1999]. These channels had been overlooked by previous excavators. They were packed with soil and remains apparently swept from the floor of the room when in use around 50–100 AD. Coins dating back to the Flavian and Trajanic period were found at the bottom and in the more superficial part of the material filling the channels, respectively. The material contained more than 13,000 fragments of ceramics and numerous glass pieces with traces of makeup, medicine, and perfume along with a total of 86 teeth (no bone fragments were found) scattered throughout the plug. Consequently, the teeth could be dated to the period from approximately 50 AD to the end of emperor Trajan’s reign (117 AD). The material was only made available to the authors within the last decade and because of restrictions from the archaeological authorities we could only study the specimens using nondestructive techniques such as micro-computed tomography (CT). Having this unique material in hand we also wanted to investigate whether the Pb isotopic ratio in the teeth reflects the ratio prevailing in the water lead tubes existing at the time. This question was relevant as the literature contains several suggestions about lead poisoning from water pipes in antiquity [Nriagu, 1983; Reddy and Braun, 2010]. However, the analytical methods for these analyses are necessarily destructive. Therefore, the aim of the present study was to characterize the clinical and structural features of carious teeth retrieved from the Temple of Castor and Pollux in the Forum Romanum and to explore whether there were signs of restorative and/or palliative treatment at the time. Moreover, we investigated the Pb isotope composition of two loose fragments obtained from a single tooth. Material and Methods Teeth A total of 86 teeth from the archaeological excavation were available. Following excavation the teeth were rinsed and brushed to remove earth, but no attempts were made to clean the teeth mechanically. The teeth consisted of 81 molars, 3 premolars, and 468 Caries Res 2012;46:467–473 2 deciduous molars. The molars comprised 35 third upper and lower molars, 17 second molars, and 29 first molars with an equal distribution between the arches. In addition, 15 extracted teeth with deep caries lesions and extensive occlusal wear originating from a contemporary rural Tanzanian population without access to dental health care [Muya et al., 1984] were included for comparison. The latter teeth were chosen to compare teeth from a contemporary population exhibiting extensive occlusal wear and having no access to dental intervention. Moreover, the teeth should have milder degrees of dental fluorosis, indicating that the teeth originate from individuals exposed to fluoride levels in the environment that, from a caries point of view, would most likely slow down the rate of caries lesion progression. In addition, 1 molar extracted from a present-day adult in Copenhagen with known environmental Pb contamination served as a control for analyses of the Pb content and isotope composition of the Roman and Tanzanian teeth. All the teeth were examined under a stereomicroscope. Micro-Computed Tomography The teeth were wrapped in foam rubber and placed in a desktop CT scanner (CT35, Scanco Medical AG, Brüttisellen, Switzerland). The teeth were scanned in high resolution mode (1,000 projections/180°) with a spatial resolution of 10 ! 10 ! 10 m3, an X-ray tube voltage of 70 kVp, a current of 114 A, and an integration time of 800 ms. Images were reconstructed using the software supplied with the scanner. It has previously been shown that the bone morphology obtained by CT closely resembles that obtained by histology [Thomsen et al., 2005]. Subsequently, the image stacks were exported from the CT scanner as 16-bit DICOM image files for three-dimensional visualization. Three-dimensional reconstruction and interactive visualization of the image stacks were performed using Amira 4.1.2 (Mercury Computer Systems, Inc., Chelmsford, Mass., USA) running under Linux (openSUSE 11.2, www.opensuse.org). This three-dimensional visualization tool makes it possible to interactively scale, rotate, translate, and create virtual sections through the reconstructed three-dimensional image. Pb Content and Isotope Composition Pieces of enamel and dentin from a single Roman tooth that had broken away due to shrinkage and a sample of a lead water tube serving the Forum Romanum were analyzed by thermal ionization mass spectroscopy. Two Roman teeth and the above-mentioned fragments were first rinsed with very weak HCl (0.05 M) in an attempt to remove recently added Pb – the rinse from the 2 teeth was analyzed and is referred to in the text as ‘rinses’. Subsequently, the enamel and dentin fragments were sampled for Pb isotope analyses with dental drill bits using a computer-guided microdrilling instrument. The powder collected by this method was dissolved in 6 M HCl, dried down and converted to 1 M HBr in preparation for chemical purification. Pb from all samples was purified by an HBr-HNO3-based chemical separation scheme using anion resin as outlined by Connelly and Bizzarro [2009]. Purified Pb was loaded onto previously outgassed Re ribbon filaments using a high-emitter silica gel and analyzed by a VG Sector 54 thermal ionization mass spectrometer. Standard NBS-981 run during this project demonstrated linear mass fraction of 0.1%/ amu (80.02%/amu) that was applied to all analyses of unknowns. External reproducibility of standards for the ratios reported here Fejerskov /Guldager Bilde /Bizzarro / Connelly /Skovhus Thomsen /Nyvad were better than 0.03%. Error bars reported in figure 4 reflect internal errors of the individual analyses. For comparison we also attempted to determine the Pb isotopic composition of samples from 2 of the Tanzanian (enamel, dentin, and rinse) and 1 of the Danish teeth described above. Results The 86 Roman teeth were characterized by rather extensive cracks and partial fractures of both enamel and dentin as well as of the cementum surfaces at the root as a result of shrinkage following dehydration for 2,000 years. All but 2 teeth showed deep, rounded spoon-shaped caries cavities most of which extended close to or into the pulp chambers (fig. 1). Most lesions (n = 74) were located on approximal surfaces and in 43 cases the lesions also involved, or were confined to, the occlusal surfaces. Of the 74 approximal lesions 28 extended into or were predominantly originating from exposed root surfaces. In 3 cases noncavitated lesions were found below an approximal wear facet (fig. 1a). When examined in the stereomicroscope there were no obvious signs of mechanical scraping or drilling. However, on several of the molars there were clear superficial, horizontal traces of tools in the interproximal, cervical region, which were likely made by elevators used for extraction. Most teeth showed marked to extensive occlusal wear often with exposure of coronal dentin corresponding to cusp tips (fig. 1d). As a result most occlusal fissures were partly or totally worn away. Despite the extensive caries destruction of the tooth structure it was remarkable that the teeth had been extracted without apparent fractures of the teeth. In 20% of the teeth small fractures of curved root apices were recorded. Minor aggregations of mineral deposits (calculus) were occasionally found in most cases located close to the enamel-cementum border. In only 3 molar teeth such deposits were observed in the middle of the root surfaces at distal roots. In 1 upper third molar part of the buccal alveolar bone was still attached to the roots. The CT examinations revealed that in all cavities the typical extensive lesions were clearly demarcated along the advancing front by a zone of dentin hypermineralization (fig. 2). Towards the pulp this reaction was evident even when the lesions were in the outer part of the dentin. Along the walls of the lesion, where the dentinal tubules were affected predominantly sideways, the hypermineralization reaction was of limited extent (fig. 2d). At the interface between the bottom of the cavity and the surrounding dentin – where numerous odontoblast processDental Caries in Rome, 50–100 AD es had been involved – the hypermineralized reaction was rather extensive and extended towards the pulp (fig. 2). In addition to this vital response of the pulpodentinal organ, plugs of tertiary, reactive dentin were recorded in the pulp cavity corresponding to the involved dentinal tubules (fig. 2a). The few noncavitated lesions showed mineral loss of the outermost dentin with an early hypermineralization response (fig. 2b). The control teeth from Tanzania with extensive cavitated lesions exhibited a very different structural pattern (fig. 3). The zone of demineralization at the advancing front of the lesion was clearly visible as a rather narrow band, but in no case was a hypermineralization reaction observed. The preliminary Pb data are shown in figure 4. The overlapping Pb isotopic composition of the three analyses of the single Copenhagen tooth suggests that the individual was exposed to a common source of Pb during his/ her lifetime and that the tooth preserves a faithful record of this exposure. The African teeth had insufficient Pb content to measure the isotopic composition, consistent with these individuals living in an environment with very low levels of Pb and in their diet. The samples of the Roman tooth had Pb isotopic compositions of the enamel and dentin that were different from each other and different from that of the investigated lead pipe from the Forum Romanum. Discussion The present data are of historical interest because they are the first to document the pathology of dental caries in the Roman Empire. In addition, the findings have direct implications for the ongoing debate among dentists on the relevance of a more biological approach to treatment of carious cavities [Gruythuysen et al., 2011; Kidd, personal commun., 2011]. Thus, the treatment philosophy applied in these Roman teeth bears strong resemblance with the nonoperative cavity treatment recently ‘rediscovered’ by Gruythuysen [2010]. Our findings clearly show that the Roman teeth had caries lesions developing for years. Where attrition kept pace with lesion progression on occlusal surfaces the caries attack was arrested in accord with conditions also prevailing in contemporary populations in Africa and China without access to dental care [Manji et al., 1989; Luan et al., 2000]. At surfaces not easily accessible to regular cleaning, and hence prone to thick microbial deposits for long periods of time, lesion progression seems to have continued. However, approximal abrasion gradually wore Caries Res 2012;46:467–473 469 Fig. 1. Lower right molar: distal (a), buccal (b), mesial (c) and occlusal (d) surfaces. On the distal surface a noncavitated brownish caries lesion is located below a small abrasion facet, which is indicated with arrows. The occlusal fissure system is partly abraded away exposing the dentin corresponding to the 3 buccal cups. a a b CT images of the mesial carious cavity of figure 1. Note the reactive dentin formed in the pulp corresponding to the deep penetration of the caries lesion into and exposing the pulp (asterisk). The hypermineralized dentin reaction preceding the dentinal dissolution is marked by arrows and is particularly pronounced in c, 470 d c d c Fig. 2. a, b Three-dimensional reconstructed images based on Fig. 3. Three-dimensional reconstructed images based on CT images of an example of a deep approximal cavity from the Tanzanian teeth. Note that neither in the longitudinal nor in the horizontal plane there is any evidence of a hypermineralized dentin reaction. Instead a distinct zone of demineralization is seen along the walls (arrows). b a Caries Res 2012;46:467–473 which represents another cavity. d Horizontal view of the lateral wall of the cavity in c with a distinct thin zone of hypermineralization (arrows). The frame at the distal surface in b shows the noncavitated lesion in figure 1 with a demineralization extending through the enamel and an early demineralization of the dentin. b Fejerskov /Guldager Bilde /Bizzarro / Connelly /Skovhus Thomsen /Nyvad Pb fragment from aqueduct 15.70 15.68 Rinse tooth 1 15.65 Enamel tooth 1 15.64 15.63 Rinse tooth 2 15.62 18.42 a 207Pb/204Pb 207Pb/204Pb 15.66 Dentin tooth 1 15.66 15.64 15.62 Copenhagen dentin, enamel and rinse 15.60 Copenhagen rain water 15.58 18.43 18.44 206Pb/204Pb 18.45 15.56 17.8 18.46 Fig. 4. Uranogenic Pb-Pb diagrams. a Pb isotopic analyses of rinses from 2 Roman teeth and the enamel and dentin from a single tooth. The Pb isotopic composition of a single fragment obtained from a Roman aqueduct is also shown. Error bars reflect 2 uncertainties of the isotopic analyses. b Pb isotopic analyses of 17.9 b 18.0 18.1 18.2 206Pb/204Pb 18.3 18.4 18.5 rain water collected in Copenhagen in June 2007 and the Pb isotopic analyses of a rinse, enamel, and dentin from a long-term resident of Copenhagen. The Pb isotopic analyses from a are shown in the box. away the partly demineralized enamel and created abrasion facets, but lesion progression continued beneath such facets once the inflamed gingiva gradually retracted with age. Hence, with age this resulted in deep caries lesions. Restorative care has been known for thousands of years [Bennike and Fredebo, 1986], but from the extensive medical literature of Plinius and Celsus from ancient Rome [1951–1960] it is apparent that as long as pain could be relieved it was recommended to preserve the teeth in a functional state. The present sample set seems to indicate that the pain relief treatments must have been fairly successful in ancient Rome. Based on this sample of teeth, we believe that if successful pain relief was provided, teeth were not extracted before lesions penetrated into the pulp, resulting in necrosis and most likely painful periapical inflammatory reactions. According to the records of Celsus [1960/61] pain control might have been achieved by treating the lesion with opium, saffron, and pepper or more ‘exotic’ components, such as fried worms (Lumbricus terrestris), Nardus paste, or spider eggs! To obtain efficient pain relief, it might have been necessary to remove part or most of the soft content of the carious cavities prior to ‘pharmaceutical’ treatment. This is most likely the explanation for the rounded and almost circular cavities observed in this Roman material as small spoon-shaped metal instruments were available at the time [Milne, 1907]. This process, if performed regularly for months or years, might in and of itself have had a dramatic influence on the rate of caries lesion progression [Anderson, 1938; Kidd et al., 2008]. However, as such cavities have not been easily accessible for removal of the microbial mass by the patient, no long-lasting effect on further lesion progression could be expected. The present CT investigations strongly support this interpretation. When caries lesions progress slowly, the cellular response from odontoblasts in the pulpodentinal tissue will try to ‘seal off’ the mineral dissolution resulting in mineral deposits within the dentinal tubules as well as in the peritubular dentin at the advancing front of the lesion [Frank and Voegel, 1980]. This might be the explanation for the finding in the present teeth of a distinct hypermineralized zone deep to the lesion, even in lesions, which finally extended into the tertiary dentin and pulp and resulted in extraction. Similar phenomena are not likely to happen in carious cavities of similar size, had they not been temporarily ‘arrested’ during years of progression, as demonstrated by the CT findings in the carious cavities in the teeth from Tanzania. The contemporary control teeth from Tanzania all exhibited various degrees of dental fluorosis, and hence the individuals must have been exposed to relatively high levels of fluoride, which was incorporated into the dentin and, thus, was available in the oral cavity during the long-lasting periods of lesion development. Under such conditions, without regular removal of the microbial biomass from the cavities, even a constant fluoride exposure may not be strong enough to reduce the rate of lesion progression and hence stimulate a vital dentin response. Dental Caries in Rome, 50–100 AD Caries Res 2012;46:467–473 471 Moreover, it is remarkable that the treatment for pain relief in ancient Rome probably resulted in preserving the pulp vital until the moment when the pulp was exposed to the oral environment. This is indicated by the excessive formation of reactive dentin along the pulpodentinal interface corresponding to the dentinal tubules involved by the caries attack as well as in the adjacent parts of the pulp. The distribution of cavities according to tooth types is similar to observations reported from excavations in central Italy [Manzi et al., 1999] and in a Romano-British population from 320 to 420 AD [Whittaker et al., 1981]. Moreover, it is consistent with observations in contemporary populations around the world with no access to dental care and exhibiting marked occlusal wear [Manji et al., 1991]. It is striking that despite the commonly very large cavities the teeth had been extracted without breaking the crowns. Moreover, in only 22 teeth fractures of minute fragile root tips could be observed. This demonstrates that those removing the teeth were very skilled. There was no evidence of any restorative material that had been stuffed into the cavities prior to extraction to avoid fracture during removal. Several of the molar teeth exhibited obvious signs of ‘elevators’ being applied, which most likely have been widely used at the time [Milne, 1907]. Thus, medical and dental care must have been available to part of the population of Rome [Plinius, 1951–1963; Celsus, 1960/61]. The teeth did not show evidence of much calculus around the neck of the teeth and as such there is little evidence that extractions were eased because the teeth were loose as a result of periodontal breakdown of the marginal alveolar bone. With increasing age a gradual loss of bone around molar teeth is well documented in contemporary populations exhibiting excessive occlusal tooth wear without loosening of the teeth [Baelum and Fejerskov, 1986; Baelum et al., 1988; Manji et al., 1991; Baelum et al., 1996]. There is no reason to expect that it should be different in this ancient population and the findings of a number of the caries lesions developed from exposed interproximal cervical areas support this assumption. We do not know the identity of the persons from whom these teeth originate. It is tempting to suggest that the teeth belonged to persons of a certain social standing taking the location of the taberna into consideration. If correct, this sample of Roman teeth may reflect persons that, in contrast to previous findings from poor populations from rural areas [Manzi et al., 1999], had access to pain relief treatment and dental care. 472 Caries Res 2012;46:467–473 That the Pb isotope composition of the teeth was different from that of the lead pipe may best be explained by the fact that the drinking water in Rome was isolated from the inner side of the lead pipes by thick incrustations of calcium carbonates [Hodge, 1981]. The difference between dentin and enamel may suggest that this person was exposed to different Pb sources during his lifetime. The fact that the rinse of 1 tooth contained Pb with an isotopic composition that may have been a mixture of Pb from the enamel and the lead pipe indicates that a component of Pb in or on the tooth came from the aqueduct. However, we cannot determine whether this Pb was incorporated when the subject was alive or after the tooth was extracted and lay in the channel exposed to the local water for several years coming from the lead pipes in Rome. In fact it is more likely that the Pb intoxication commonly claimed to be a problem in ancient Rome [Nriagu, 1983; Reddy and Braun, 2010] may have originated from food and wine sweetened with lead salt. Anyhow, an in-depth analysis of the Pb isotopic composition of the teeth would require that portions of the unique archaeological material be destroyed, which was not allowed by the Italian authorities and could consequently not be performed in the present study. We conclude that it is likely that this taberna had functioned as a small pharmacy and beauty shop where it was possible also to seek pain relief treatment for toothache. In addition to pain relief many of the remedies used have most likely also had a certain bacteriostatic effect. This combined with the removal of the soft content of the cavities with small spoon-shaped instruments could explain the temporary arrest of lesion progression. As a protective zone of hypermineralization in the dentin was attainable relief of pain was obtained and the teeth remained functional for a longer period. 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