Nothing new under the heavens: MIH in the past? A. R. Ogden*, R. Pinhasi**, W. J. White*** *Biological Anthropology Research Centre (BARC), Archaeological Sciences, University of Bradford, Bradford; **Dept. Archaeology, University of Cork, Ireland; ***Centre for Human Bioarchaeology, Museum of London, London Wall, London, England. Abstract Aim: This was to study an archaeological population of subadult teeth in 17th and 18th century skeletal material from a London (England) cemetery for enamel defects including molar-incisor-hypomineralisation (MIH). Methods: Dentitions of 45 sub-adults were examined using standard macroscopic methods and systematically recorded. A total of 557 teeth were examined with a *5 lens and photographed. Ages of the individuals were estimated from their dental crown and root development stages and not from charts that combine tooth eruption with development stages. The dental age of the individual and the approximate age of onset of enamel defects was then calculated on the basis of the chronological sequence of incremental deposition and calcification of the enamel matrix. Affected enamel was graded macroscopically as: - Mild: 50% of the tooth’s enamel surface area visibly disrupted. Results: Of the total number of individuals 41 (93.2%) showed signs of enamel developmental dysplasia or MIH, 28 of them showing moderate or severe lesions of molars, primary or permanent (63.6% of the sample). Incisors and canines, though surviving much less often, showed episodes of linear hypoplasia. Conclusion: The extensive lesions seen on many of the molars displayed cuspal enamel hypoplasia (CEH). Many of these teeth also exhibited Molar Incisal Hypomineralisation (MIH).
Introduction Bouts of malnutrition, disease and fever are known to depress the activity of the enamel-forming ameloblasts and to result in the formation of a thin and poorly calcified enamel matrix, with the formation of linearly distributed pits or grooves of defective enamel. Dental enamel hypoplasia (DEH) has therefore long been used as a non-specific indicator of systemic physiological stress during early life [Goodman and Rose, 1990; Gautelli-Steinberg et al., 1999]. Once formed, enamel is not remodelled during life and every individual’s enamel is a record of the first 8 or 9 years of their life when their crowns are formed [Smith, 1991; Skinner and Goodman, 1992; Hillson and Bond, 1997].
Two new types of enamel malformation have recently been identified. Molar-Incisor-Hypomineralisation (MIH) is characterised by demarcated and often indented defects involving an alteration in the translucency of the enamel, with the area being white, yellow or brown in colour [Beentjes 2003; Weerheijm 2003; Weerheim et al., 2003]. Until recent years many first permanent molars (FPM) decayed so rapidly during eruption that there was no possibility of diagnosing the initial state of the tooth or the cause of this rampant caries. There are few good clinical photographs of this condition because such teeth were always extensively carious or heavily restored by the time they were identified. SEM studies of such molars show the enamel bordering carious lesions to be poorly organised and porous [Jälevik et al., 2002]. Fagrell et al. [2008] have reported bacterial invasion of dentinal tubules beneath apparently intact enamel in such molars. A large cemetery was uncovered in 1985 in east central London during the demolition of Broad Street Railway station and the building of the Broadgate development [White, 1987; Harding, 2002]. The “New Graveyard” was founded in 1569 by the City of London as an overflow cemetery to relieve the congestion occurring in London’s parish burial grounds and it continued in use until the mid 18th century [Harding, 2002]. Only a small part of this cemetery was excavated during the development and some 388 individuals, of whom 45 were sub-adults (children and adolescents), were retrieved and stored at the Museum of London [White, 1987]. Examination of these sub-adults has revealed a quite exceptional level of disturbed enamel formation, not only in prevalence, but also in severity, compared with other archaeological populations [Ogden et al., 2007]. Much of this disturbed enamel would now be clinically diagnosed as showing MIH. In the same population we also identified the rare cuspal enamel hypoplasia (CEH). The only molar illustrated in the literature to show this degree of malformation appears in Jenkins’ textbook, [1978: page 262], and is simply labelled as “gross hypoplasia”. SEM images revealed many teeth with large areas of completely exposed dentinal tubules between the islands of enamel (Figure 1). When such teeth erupts into the mouth they will rapidly decay and, if left untreated may become non-vital, as bacteria can readily gain access to the
Key words: molar-incisor-hypomineralisation, archaeology Postal address: Dr A.R. Ogden. Biological Anthropology Research Centre (BARC), Archaeological Sciences, University of Bradford, Bradford; West Yorkshire, BD7 1DP, England. Email:
[email protected]
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unprotected dentinal tubules that lead directly to the pulp. Many of the affected teeth seen in this study were unerupted, owing to the early death of the children, but even erupted teeth had occasionally survived.
Materials and Methods This study was a follow-up of an investigation of the effects of rickets on long bone growth patterns in the 45 sub-adults retrieved from the Broadgate cemetery [Pinhasi et al., 2006 ]. The dentitions of all sub-adults were examined using standard macroscopic methods and systematically recorded. A total of 557 teeth were examined with a *5 lens and photographed. Ages of the individuals were estimated from their dental crown and root development stages and not from charts that combine tooth eruption with development stages [cf. Ubelaker, 1989], as it is known that one of the key signs of rickets is delayed eruption [Stuart-Macadam, 1989; Wharton and Bishop, 2003]. The dental age of each individual and the approximate age of onset of hypoplasia was then calculated on the basis of the chronologica sequence of incremental deposition and calcification of the enamel matrix [Moorees et al., 1969 a, b; Smith, 1991; Hillson, 1992]. These charts suggest the approximate ages at which disturbance of enamel formation began, and after which, in most individuals, amelogenesis returned to relative normality. The hypoplasia on many molars, both primary and permanent, was on such a scale that none of the conventional methods of assessment that are used to record the common linear and pitted lesions on canines and incisors were applicable [Hargreaves, 1989; Fédération Dentaire International, 1992; Ensor and Irish, 1995]. For the purposes of this study, therefore, the affected enamel was graded macroscopically as: ●
Mild
50% of the tooth’s enamel surface area visibly disrupted.
As all the individuals had died in early life it was possible to detect hypoplasia on the cusps of their relatively unworn primary or permanent molars. Many unerupted teeth were visible because of the poor preservation of the bone. Selected teeth were examined, uncoated, with Scanning Electron Microscopy (SEM), under low vacuum, using an FEI Quanta 400.
Results Many molars had grossly deformed cuspal architecture (Fig.1). Large areas of Tomes’ process pits, where the ameloblasts evidently ceased matrix production abruptly, are exposed between islands of more normal enamel [Ogden et al.,
2007]. As soon as such teeth erupt into the mouth they will rapidly decay, as bacteria can readily lodge on the rough and incompletely mineralised enamel. With all affected molars it was striking that the cervical third of the crowns was uninvolved, often with a clear demarcation between the cuspal and the cervical enamel. The smooth bulge of enamel, with perikymata grooves, apparently marks the return to normal enamel matrix formation. Of the total number of individuals 41 (93.2%) showed signs of enamel hypomineralisation or MIH, 28 of them showing moderate or severe lesions of molars, primary or permanent (63.6% of the sample) (Figures 1 and 2). Incisors and canines, though surviving much less often, showed episodes of linear hypoplasia [Ogden et al., 2007]. There were 10 of these children (24.4%) who also had cavitated carious lesions opening into dentine, even in their permanent teeth, although they had not long been erupted before death supervened. It is known that malnutrition leads to increased caries, certainly in the primary dentition, though the effect on caries of the permanent dentition is still uncertain [Psoter et al., 2005]. However, it is known that the pattern of caries development, as a function of age, is significantly altered in individuals with rickets, as a consequence of the delay in the eruption and exfoliation of the primary teeth [Alvarez, 1995; Psoter et al., 2005].
Discussion Suga [1989] suggested that ameloblasts are very sensitive to disorders at an early stage of maturation, and if a cell is damaged by systemic or local disorder at this stage, it cannot easily recover from dysfunction during the long period of maturation. He also claimed that the sensitivity to systemic disorders and the mode of reaction of the ameloblasts are not the same for each of the stages of the enamel development. For instance, in some cases, the cells at the matrix formation stage, when the disorder occurred, form highly mineralised sound enamel afterwards, whereas the enamel disturbed at the very early stage of maturation is prominently hypomineralised. The lesions seen on many of these molars were too extensive and complex to be simply described as “pitted” or “plane-form” and with the added disruption of cusp pattern this suggested that a new type of hypoplasia should best be described as “Cuspal Enamel Hypoplasia, CEH”. This type of hypoplasia, although very rare, is not unique to the Broadgate sub-adults, and needed to be designated as a distinct entity [Ogden et al., 2007]. Available modern clinical prevalence data for MIH, mostly from Northern Europe, ranges from 3.6% to 25%, with the highest rates apparently occurring in children from low fluoride areas whose mothers had been encouraged to practice extensive and prolonged breast-feeding [Weerheijm, 2003]. Histologically the disturbed enamel shows a severely hypomineralised enamel in the cuspal part of the tooth with 167 European Archives of Paediatric Dentistry // 9 (4). 2008
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Fig. 1 Photographs of molar teeth showing: a. Maxillary and mandibular permanent molars from a 5-6 year-old. These display Moon’s molar-like multiple small cusps but also have a wide band of pitting around the axial surfaces; b. Permanent lower molars from a 6-7 year-old. The cusps are almost devoid of enamel, however normal enamel resumes twothirds of the way down the crown. Note the indentations of the mesio-buccal cusps. This may be due to caries of what would have been the first cusps to erupt, or the result of MIH; c. Maxillary and mandibular primary second molars from a 3-4 year-old. Note the undulating and pitting of the enamel surface; d. SEM of cusp tip of primary mandibular molar seen in Fig. 1c.
Fig 2. Photographs of teeth showing: a. Probable MIH of the cusp tip of the mandibular left first permanent molar. Note the lack of wear of the other cusps; b. Probable MIH of the distobuccal cusp of the mandiublar left second primary molar; c. Probable MIH of the mesio-buccal cusp and medial marginal ridge of this secondprimary molar. Note the complexity of the cusp pattern and the lack of wear of the other cusp; d. View to show that mirrored defects existed on both sides.
a clearly defined border between hypomineralised and normal enamel. It is characteristic that the cervical third of the enamel always has a normal appearance compared with teeth without any opacities [Jälevik et al., 2001, 2005] and that is a prominent feature of the Broadgate teeth. Lewis [2002b] examined the prevalence of enamel hypoplasia among Anglo-Saxon, early medieval and post-medieval cemetery English populations from St. Helen-on-the-Walls, Christ Church Spitalfields or Raunds Furnells, respectively. She reported no DEH among infants younger than 6 months from any of these sites. At the age intervals of 0.5-2.5 years DEH was absent among infants from Raunds, low in frequency among those from St. Helen-on-the-Walls (5%) and moderate among infants from Spitalfields (20%). However, that investigator may have been looking for conventional clearly demarcated linear or pitted enamel hypoplasia in otherwise sound teeth. CEH or MIH, if present, may have been masked by occlusal destruction from caries, wear or taphonomic damage. King et al. [2005] examined the onset, frequency, and duration of linear enamel hypoplasia episodes among 30 specimens from the relatively privileged populations of Christ Church Spitalfields and St Bride’s London. They found that the earliest age at which enamel defects first occurred was at 1.2 years and the highest frequencies of enamel growth disruptions occur between ages 2–4 years. However these investigators were looking for linear or pitted enamel hypoplasia and again caries and attrition may have masked CEH and MIH, if present in these populations. Our findings therefore point to a sharp contrast between the age of onset and highest prevalence of enamel hypoplasias in Broadgate and Christ Church, Spitalfields. It is evident that equivalent teeth in the other quadrants of the mouth were all affected to a varying extent and the systemic disorder must have occurred during the first 2 years of life [Moorees et al., 1963 a, b; Smith, 1991]. The period of weaning is especially precarious for infants, with an increase in nutritional stress due to the sudden loss of nutrients provided by human milk, and a decrease in immunity due to the decreased immunoglobulin levels as well as the loss of immunity provided by the mother’s milk. The child is subjected also to the first real extramaternal contact with the environment and new pathogens [Larsen, 1987]. The reason why the FPM were more affected than the canines and incisors may be that the crowns of these teeth form in 3.8 years, i.e. half the time that canines take, and so are more vulnerable to short systemic disturbances [Ensor and Irish 1995; Fitzgerald, 1998]. As the cervical part of the enamel was relatively unaffected it could be that the insult only had potential to seriously disturb the ameloblasts during the child’s early years. Hillson [1992] suggested that this might be due to the abrupt change from widely spaced perikymata occlusally to closeley-spaced cervically, when de-
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fects would be less extensive and obvious. Another possible explanation is that the thickness of the enamel influences the ability of the ameloblasts to resist the insult [Jälevik and Norén, 2000]. It is of interest that Purvis et al. [1973] reporting on enamel hypoplasia in primary incisors, canines and molars in individuals known to have suffered from neonatal tetany, described and illustrated the presence of just such a hump separating the normal ivory-coloured enamel at the base from the yellow-coloured enamel nearer the tip. Neonatal tetany, due to low blood calcium, is a brief, self-limiting biochemical disturbance of only a few days duration, yet it had apparently led to major enamel disruption in 63 individuals out of the 112 reviewed. A Dutch pilot study of medical records from children with FPM with developmental defects found that 48% of the cases had problems related to birth and 67% suffered from respiratory disease [van Amerongen and Kreulen, 1995]. These figures were higher than normal, and the authors hypothesised that oxygen shortage might influence the mineralisation of the enamel. Chronic diarrhoea or environmental toxins, dioxins in particular, taken up directly with food or via breast milk have also been suggested as possible causes [Alaluusua et al., 1996]. Was rickets (Vitamin D deficiency) involved? Children in the crowded, sunless alleys of London were unable to synthesise vitamin D and we now know this was made even worse by the ability of a polluted atmosphere to absorb what little ultra-violet light there was [David, 1991; Wharton and Bishop, 2003; Mays 2003; Mays et al., 2006]. In recent years there have even been reports from Scandinavia and North America of the reappearance of rickets [Welch et al., 2000]. These are mild cases resulting from maternal vitamin D deficiency or prolonged breastfeeding without sufficient vitamin D supplementation. Kunzel [2003] has suggested that such deficiency might cause the appearance of MIH without the classical skeletal signs of rickets. Pinhasi et al. [2006] could find no significant relationship between enamel disturbance and skeletal rickets in the Broadgate population, but very few long-bones had survived. These authors suggested, however, that the low socioeconomic status of Broadgate must have played a significant role in the diet and health status of the sub-adults from this population. The apparently unique severity and frequency of severe hypoplasia in this population reported on here leads us to ask whether these lesions were perhaps the result of infection, in combination with the likely malnutrition of this population. The appearance of many of these teeth, with multiple small cusps is certainly reminiscent of that of the “Mulberry molars” or “Moon’s Molars” of congenital syphilis (Fig 1). However the channels of exposed poorly mineralised enamel between the islands of more normal smooth enamel are very different, as in congenital syphilis the enamel layer appears intact and smooth, even in the crevices, and only cusp architecture is
affected [Hillson et al., 1998, page 175]. Whatever the cause, the effects appear to have lasted for months rather than days and seem to have ceased suddenly, leading to a resumption of enamel production, of normal thickness and appearance. Hillson [2005] considered that the exposed plane “may occupy half the crown height, but still relate to a momentary disruption of amelogenesis” and suggested that two or more interacting factors are required to produce the lesions. Seow et al. [2005], studying primary dental enamel from modern preterm children, have reported that the incisal enamel is 20% thinner than in full-term children, but none of the teeth they examined showed visible hypoplasia, although 52% showed minor defects under SEM. This suggests that the massive disruptions seen in the teeth of the Broadgate subadults were not related to premature birth. Historical sources suggest that during the 17th and 18th centuries, mean weaning age in Britain dropped from 18 months to 7 months [Lewis, 2002a]. While weaning at Christ Church Spitalfields probably occurred around the age of 7 months, there are no indications of growth faltering after this age [Lewis, 2002b]. The high prevalence of DEH on the primary dentition of Broadgate infants at 0-6 months of age suggests that growth faltering started from birth or even in utero. It is therefore likely that the infants’ mothers were immunodeficient and malnourished to the extent that their colostrum could not buffer these infants from severe environmental stress and that the high prevalence of DEH and MIH in this population is not due to post-weaning stress. Industrialisation is associated with malnourishment, poor health and low stature [Floud and Wachter, 1982]. During the Industrial Revolution large European cities became a hub to people from diverse ethnic and socioeconomic backgrounds. In London, the distinction between the wealthy and the poor intensified during the first part of the 17th century. Inwood [1998] asserts that by 1650 East London had already acquired a working class complexion when new neighbourhoods of shacks were erected outside the city walls. The residents of these shacks lived in high density, without sufficient heating and with poor sanitation, environmental conditions that likely affected their overall growth status as well as their dental development. The New Graveyard’s peripheral location, with all its associations of moral marginality turned it from an amenity to a refuse burial dump within a 100-year period [Harding, 2002]. The variations in socioeconomic stress among urban populations are associated with variations in nutrition, living conditions, child labour and other factors [Bogin, 1998]. By 1695, residential differentiation within London was no longer characterised by occupation but rather the city became geographically divided according to wealth, and people of similar means were living in proximity to each other [Finlay, 1981]. Thus, 17th-18th century London was an economically and socially stratified city with a widening difference in health 169 European Archives of Paediatric Dentistry // 9 (4). 2008
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profile among its inhabitants that was associated to a large extent with the parish in which they dwelled. In modern populations minor hypoplasias and hypomineralisations can appear with surprising frequency in apparently healthy children’s teeth, being present in a frequency as high as 43-64% [Suckling and Pearce, 1984; Suckling et al., 1985; Dummer et al., 1986; Suckling 1989]. The sheer severity and incidence of enamel hypoplasia and caries in this archaeological population appears to be infrequent among archaeological populations. However, it is difficult to compare these figures with other work, as most published archaeological studies have reported on adults as well, when caries, attrition and taphonomy have destroyed much of the defective enamel and the primary teeth have been lost [Palumbeckaite et al., 2002]. An important aspect of the paper of Ogden et al. [2007] was to alert others in Paleopathology to look for evidence of CEH and MIH and to suspect it, if molars are unexpectedly carious or grossly worn for the age of the individual in their population. The teeth examined in this study provided a unique opportunity to examine gross developmental disruption of the early stages of crown formation. Image analysis will help more precisely quantify the surface area of enamel involved. Histological analysis using ground sections of the Broadgate dentition is enabling us to clarify the formation and sequence of these lesions. Electron microprobe analysis is allowing a detailed examination of enamel matrix formation and mineralisation. By examination of their relationship to the Striae of Retzius, neo-natal lines and evidence of weaning, and using the chronology of Reid and Dean [2006], we hope to better understand these lesions and to further our understanding of their aetiology.
Conclusions A group of 17th and 18th century sub-adults displays a high prevalence of moderate-to-severe non-linear enamel defects never previously reported in a systematic manner on a subadult sample. Molars, both primary and permanent, were affected with large areas of incompletely mineralised enamel with disruption of the normal cusp pattern. The enamel that was formed was often pitted and abnormal in morphology. The extensive lesions seen on many of these molars displayed cuspal enamel hypoplasia (CEH); many of these teeth also exhibited Molar Incisal Hypomineralisation (MIH). Future research will further investigate the formation and cause of CEH and MIH and will potentially shed more light on why this condition was so dramatically present in this archaeological population and whether these conditions were present, but unidentified in other archaeological populations. Acknowledgements The authors would like to thank Professor Martin Curzon of Leeds Dental Institute for supplying a clinical perspective and Stuart Fox of the Department of Archaeological Sciences, University of Bradford for his advice on SEM technique.
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