close

Вход

Забыли?

вход по аккаунту

?

Dental caries in a Portuguese identified skeletal sample from the late 19th and early 20th centuries.

код для вставкиСкачать
AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 140:64–79 (2009)
Dental Caries in a Portuguese Identified Skeletal Sample
From the Late 19th and Early 20th Centuries
Sofia N. Wasterlain,1* Simon Hillson,2 and Eugénia Cunha1
1
Centro de Investigação em Antropologia e Saúde, Department of Anthropology, University of Coimbra,
Coimbra 3000-056, Portugal
2
Institute of Archaeology, University College London, London, UK
KEY WORDS
paleopathology; epidemiology; Coimbra; diet; antemortem tooth loss
ABSTRACT
Dental caries was investigated in 600
adult dentitions belonging to the identified osteological
collections of the Museum of Anthropology, University of
Coimbra, Portugal (late 19th/early 20th centuries). The
main advantage of this sample compared to an archaeological source is the presence of known demographic parameters such as age, sex, and occupation. The aim of
this study is to investigate the issues involved in comparing caries data derived from archaeological death
assemblages with statistics compiled from clinical studies of the living. When only the upper dentition was considered, higher rates were observed in females than in
males. No differences were found between sexes for
lower teeth. In both sexes, both the percentage of carious
teeth and the severity of lesions were found to increase
with age, demonstrating that caries activity continued
throughout life. The slight decrease observed for the age
group 70–79 years is probably due to the increased antemortem tooth loss in the elderly. Caries was most common at contact areas (32.9%) and rarest at smooth crown
surfaces (6.5%). Root surface caries was graphed in relation to the exposure of roots, and it was confirmed that
the degree of root exposure was not strongly related to
the frequency of carious lesions on the exposed root surface, although both increased with age. Molars were
attacked more frequently by caries as a whole than premolars, canines or incisors. The results are similar to
studies of recent living populations with a limited access
to professional dental care. Am J Phys Anthropol
140:64–79, 2009. V 2009 Wiley-Liss, Inc.
Dental caries is one of the most widely studied pathological conditions in archaeological and anthropological
collections. It produces highly characteristic changes
that are distinguishable from other causes of tooth
destruction, so it is possible to record lesions with a high
degree of confidence in archaeological assemblages. It
has also been the subject of widespread clinical research,
so that the etiology and epidemiology of the disease during the latter part of the 20th century are well established. Caries has a multifactorial etiology but of prime
importance is the amount and type of carbohydrate in
the diet, which makes the disease a particularly useful
tool in reconstructing dietary change in the archaeological record. In interpreting the palaeopathology of dental
caries, it is logical to make comparisons with epidemiological studies of caries in living people, but there are
several important issues that need to be taken into
account. The aim of this study is to investigate the
issues involved in comparing caries data derived from
archaeological death assemblages with statistics compiled from clinical studies of the living.
The first issue concerns the nature of archaeological
collections. Recent clinical studies are based upon dental
examinations of living people. An archaeological collection of dentitions is fundamentally different—it is a
death assemblage. This has a very different age distribution from that of a living population, with much higher
proportions of young children and older adults. Further,
such assemblages also encompass a particular subset of
people—the sick and infirm—who might well have a different caries experience from the main bulk of the living.
After all, caries in modern times shows a strong relationship with general health (Sheiham, 1997). Consequently,
one may legitimately query whether the structure of a
death assemblage produces a markedly different caries
epidemiology from that seen in a living population.
The second issue is the patterning of caries between
teeth, with different ages and sexes. Epidemiological
studies of living people (Thylstrup and Fejerskov, 1994)
have concentrated on caries in children. These studies
have identified a strong pattern of susceptibility for different teeth within the dentition (Batchelor and Sheiham, 2004) that focuses on the permanent and deciduous
molar crowns, so that the caries experience of modern
children is clearly related to the sequence of dental eruption. These studies also identify sex differences in caries
prevalence, usually with higher caries rates in girls,
although this is not universal. There are far fewer
reports on the epidemiology of caries in living adults
(Luan et al., 1989; Manji et al., 1989). All, however,
report a strong progression with age and this progression occurs for caries rate, the type of lesion and the specific teeth affected. Although these studies do not always
distinguish between men and women, Luan et al. (1989)
reported higher caries rates in Chinese women. By con-
C 2009
V
WILEY-LISS, INC.
C
Additional Supporting Information may be found in the online
version of this article.
*Correspondence to: Sofia N. Wasterlain, Departamento de Antropologia, Universidade de Coimbra, Coimbra 3000-056, Portugal.
E-mail: sofiawas@antrop.uc.pt
Received 28 April 2008; accepted 23 December 2008
DOI 10.1002/ajpa.21036
Published online 17 March 2009 in Wiley InterScience
(www.interscience.wiley.com).
CARIES IN A PORTUGUESE IDENTIFIED SKELETAL SAMPLE
trast, Mack et al. (2004) found no consistent differences
by sex among elderly Germans. In yet another study,
Manji et al. (1989) found no overall differences between
the sexes among adult Kenyans. Nevertheless, older
Kenyan women had higher caries rates than their male
counterparts. In sum, patterning in children and rate
differences among adults were found in some but not all
studies.
Most archaeological studies of caries have calculated
caries rates from the total number of teeth without distinguishing between different regions of the dentition. Those
studies that have made this distinction (Moore and Corbett, 1971, 1973, 1975; Corbett and Moore, 1976; Varrela,
1991) report marked contrasts between different teeth. If
this is so then, where all teeth are combined together, it is
implicitly assumed that all teeth throughout the dentition
have an equal chance of preservation, in all assemblages
studied. This is not the case for most archaeological or
museum collections. Teeth are quite often lost postmortem
and the single rooted anterior teeth are much more frequently lost than cheek teeth, which are held more firmly
in their sockets. At the same time, antemortem tooth loss
(AMTL) must complicate reliable comparisons of caries
data because it is likely that many teeth with carious
lesions would be lost earlier than those without lesions.
This is not necessarily so, however, as teeth may also be
lost through periodontal disease or, in heavy wear rate
groups, through the processes of fracturing and rapid continuous eruption. For all these reasons, the assumptions
made in archaeological studies are likely to have a profound influence on caries rates. So, for example, if caries
rates are expressed as a proportion of total teeth, variation between sites could well be due to differential preservation of anterior versus cheek teeth. The only way to
avoid this problem is to provide separate statistics for different teeth. Clinical studies make different assumptions,
depending on the methodology used. Postmortem tooth
loss need not be considered, so all teeth absent at the time
of examination are assumed to have been lost through the
process of disease, trauma or congenital absence. Some
studies also assume that missing teeth have been lost by
extraction following a deeply penetrating caries lesion
that exposed the pulp to infection (see discussion in
Thylstrup and Fejerskov, 1994, p 184). While this may be
true in children, which make up the bulk of epidemiological studies, in adults such assumptions ignore periodontal
disease which is an important cause of tooth loss. Once
again, it is important to be clear about the assumptions
being made before comparing clinical studies.
Relatively few archaeological studies have examined
caries affectation in relation to estimated age-at-death.
In those studies where this has been attempted, such
studies have found a marked progression in caries affectation that parallels indicators of increasing age-at-death
(Moore and Corbett, 1971, 1973, 1975; Corbett and
Moore, 1976; Varrela, 1991). Recent epidemiological
studies are based upon carefully selected, equally sized
groups representing a full range of ages from the living
population. Archaeological and museum collections are
often too small to allow selection of similarly sized
groups throughout the full age range and, in any case,
age estimation from the skeletal remains of older adults
is not only uncertain but also often based on factors such
as increasing tooth wear which are themselves not independent of dental caries. The nature of age groupings in
most archaeological assemblages therefore differs fundamentally from age groupings in clinical studies.
65
By contrast, sexual dimorphism in the adult skeleton
allows a reasonably confident identification of sex in
many archaeological collections, and most archaeological
studies report higher caries rates in females than in
males (Lukacs and Thompson, 2008). As these studies
are usually based on total tooth counts, no distinction is
made between adults and children, although it seems
reasonable to assume they were adults since it is difficult to distinguish between the skeletons of boys and
girls. Archaeological collections often have fewer than
expected female skeletons (see discussion in Waldron,
1994, p 23), perhaps due to a preference in burial, or to
taphonomic factors. Furthermore, an examination of statistical tables in the United Nations Demographic Yearbooks (available online at http://unstats.un.org/unsd/demographic/products/dyb/dyb2.htm) shows that the sexes
are never evenly distributed by age in death assemblages–there tend to be more girls than boys in the infant
age group, fewer girls/women throughout most of childand adulthood, and more women in the oldest age
groups. This might well have an impact on the sex differences in caries rates seen in archaeological studies.
Once more, clinical studies usually select carefully equal
numbers of males and females for each age group. This
is difficult to achieve in the typical archaeological collection and again, the nature of the assemblage needs to be
borne in mind when comparing the age and sex variation
of caries between different sites, and between archaeological and modern clinical studies.
Until the development of large urban centers following
the industrial revolution, human dentitions seem to
have been characterized by a much more rapid rate of
wear than seen today. In addition, refined sugar was not
readily available to all socioeconomic groups until after
the 18th century, when there was massive growth in the
international sugar market. These two factors—very
light wear and high sugar consumption—set the past
200 years apart from the bulk of human history (Moore
and Corbett, 1975; Corbett and Moore, 1976; Hillson,
2008). For example, Victorian era dentitions from Christchurch, Spitalfields in London (Whittaker, 1993) show a
caries experience much more in common with the present day than with medieval times. Like today, caries
affected primarily the tooth crowns starting with newly
erupted teeth in childhood, with adults accumulating
more crown lesions and adding root caries as the root
surfaces were exposed in the oral cavity by periodontal
disease. By contrast, many ancient archaeological collections tend to be characterized by lesions that started at
the cement-enamel junction (CEJ) as the roots were
exposed in older adults—not by periodontal disease—but
by continuous eruption to compensate for heavy wear
(Hillson, 2008). Hence, the type of lesions and the pattern of occurrence with age contrast strongly between
archaeological collections and recent clinical studies.
Because of this, a simple comparison of caries rates calculated for all teeth and all ages combined is likely to be
affected by many hidden factors. It is therefore important to take these fundamental changes in caries epidemiology into account.
In light of these issues, there are several important
questions to be addressed when comparing archaeological collections with data collected from living people:
1. Are caries data gathered from a death assemblage
consistent with data gathered from clinical studies of
the living?
American Journal of Physical Anthropology
66
S.N. WASTERLAIN ET AL.
2. Does a death assemblage, in which teeth are lost postmortem and there is a different distribution of ages,
show similar differences in caries rates between different teeth to those shown in recent living populations?
3. Is there a similar progression of caries with age, despite the differences between a death assemblage and
a living population?
4. What are the potential effects of the patterns of antemortem and postmortem tooth loss in different age
groups within the death assemblage?
5. Are there differences between males and females in the
age-related progression of caries and do these vary
between different age groups in a way that might be
affected by the nature of the death assemblage?
To test for these, it is necessary to isolate, as far as
possible, the different factors. Such a test requires a
collection of dentitions from a death assemblage that
represents a well-defined group of people who lived
under conditions that differ little from those of living
people, particularly in not being subjected to the very
rapid wear, which characterizes most archaeological
collections that antedate the early years of the 19th century. To be directly comparable to the demographic characteristics of a clinical study, ages-at-death and sex need
to be known independently from the skeletal remains
themselves. This is especially important for age-at-death
since age is extremely difficult to estimate reliably in
older adult skeletons. In addition, there should be a relatively even spread of age groups across the full range of
adult life. Such collections are rare, but one exists in the
Coimbra identified osteological collections of the Museum
of Anthropology at the University of Coimbra in Portugal. These collections encompass around 2,000 skulls
and dentitions of people from the central region of Portugal, who were mostly of low socioeconomic status and
who died during the late 19th and early 20th centuries.
This places them at a point temporally intermediate
between the large clinical studies of the 1980s and the
archaeological collections of the 19th centuries in other
European countries. The study presented here uses a
sample selected from the Coimbra identified osteological
collections to address the six questions posed above.
MATERIALS AND METHODS
The Coimbra identified osteological collections
The sample evaluated for this analysis comes from the
Coimbra identified osteological collections, curated by
the Museum of Anthropology of the University of Coimbra (MAUC). There are three osteological collections at
the MAUC that make up the Coimbra identified osteological collections. These include the Medical School
(MS, 585 skulls), the International Exchange (IE, 1075
skulls) and the Identified Skeletal (IS, 505 skeletons) collections. The skulls belonging to the medical school collection were acquired from the Schools of Medicine in
Lisbon and Porto and also from the Anatomical Theatre
of the University of Coimbra, whereas skeletal material
from both International exchange and identified skeletal
collections was recovered from the ‘‘Cemitério Municipal
da Conchada’’ in Coimbra.
In Portuguese cemeteries it is common practice to perform exhumations after a period of 5 years. The bones
are then required to be transferred for deposition in an
American Journal of Physical Anthropology
ossuary. However, if relatives do not claim the remains
following exhumation or cease payment of ossuary fees
the remains are either placed in a communal grave or
cremated. It was at that time that the Coimbra University intervened and asked to house the remains for
research purposes (Cunha and Wasterlain, 2007).
Individuals in the MS, IE, and IS collections died
between the years 1895–1903, 1904–1938, and 1904–
1938, respectively. As these were fully identified individuals, detailed information about each, namely birthplace,
sex and age at death, year and place of death, illness or
cause of death, and occupation, amongst others, is compiled in a Record Book. These records make clear the
low socioeconomic status of most individuals in the collections. According to these records, the women were
almost exclusively engaged as housewives whereas men
were employed mainly as rural workers and artisans.
Furthermore, the provenance of their bodies can also be
considered a sign of their low socioeconomic status, for
in most cases their families could not afford adequate
burials (Cunha and Wasterlain, 2007).
The sample
In some dental studies based on skeletal collections,
the specimens were selected on the basis of degree of
completeness or state of preservation (Whittaker et al.,
1981; Kerr, 1990; Kerr et al., 1990; Whittaker and Molleson, 1996). However, exclusion of damaged specimens
might result in an unrealistically low frequency of
caries, as bones and teeth weakened by disease are more
likely to suffer diagenic damage in the ground than
those with normal structure (Watt et al., 1997). To avoid
this, the individuals of the present study were selected
regardless of the state of preservation.
Since previous studies (Kerr, 1990; Kerr et al., 1990)
have shown an increase in the frequency of dental caries
in adults with advancing age, it was important to analyze individuals by age group. Therefore, 600 specimens
were randomly selected in order to have six age groups
(age Group 1: 20–29 years; age Group 2: 30–39 years;
age Group 3: 40–49 years; age Group 4: 50–59 years; age
Group 5: 60–69 years; and age Group 6: 70–79 years)
composed of 100 individuals, with 50 males and 50
females in each. The selected individuals died in the
centre of Portugal between 1896 and 1938. Nonadults
were deliberately excluded from the study due to the
insufficient number of children and juveniles in the collections. Ideally it would be known if these individuals
had life-long, or at least long-term, residence in the
same geographic region, but this information was not
available. It is known, however, that all of the selected
individuals had been born and had died in the centre of
Portugal.
The dental collection analyzed in this research (9,562
permanent teeth) is one of the largest and best preserved studied anywhere. This is important because low
numbers of individuals could easily result in false high
or low values for caries statistics (Vodanovic et al.,
2005).
Context of the collection in late
19th/early 20th century Portugal
Diet. The daily diet in the centre of Portugal at the beginning of the 20th century was very simple, consisting
CARIES IN A PORTUGUESE IDENTIFIED SKELETAL SAMPLE
essentially of bread (mostly made of maize, but also
wheat, barley, and rye), green and dry vegetables eaten
as soups and broths accompanied by potatoes. Soups
were also prepared with maize flour (Roque, 1982). Additionally, a small (but not daily) intake of fish (usually
sardine and salted codfish), bacon, olive oil and honey
could complement the dietary staples (Bocquet-Appel
and Morais, 1987).
Oral hygiene. Despite the availability of some modern
methods of cleaning teeth during the 19th and early
20th centuries, such methods were certainly not widely
used in Portugal. Based on general accounts of the history of oral hygiene, toothbrushes were already manufactured in France and England by the 18th century
(Saunders et al., 1997), and even though described in
great detail in the Portuguese literature by A. De Vitry
Júnior in 1843, they remained luxury items due to the
high cost of production (Boléo, 1965).
Access to professional dental care. Professional dentistry was available in the late 19th and early 20th centuries, though on a limited basis. As in Europe in general, there were only a very small number of practicing
dentists in Portugal (in 1887, only two medical doctors
practiced dentistry in Portugal). Gradually, others
began to practice, but dental treatment, mainly dental
extraction, was predominantly provided by people without any qualification and as a sideline to other primary
businesses, such as barbering (Ribeiro, 1935; Costa,
1961; Capelas and Pereira, 1976). Tooth extraction is
one of the oldest surgical procedures, and would quite
possibly have been performed by many people in the
past, particularly when pulp exposing lesions led to
periapical inflammation which can produce the most
violent toothache (Hillson, 2000, 2008). More complex
procedures, such as fillings and crowns, would have
been limited, even for qualified dental practitioners,
since there were no anesthetics, the instruments and
materials were unsophisticated and, most importantly,
there was a lack of knowledge of the etiology and pathology of caries. Consequently, preventive practices
hardly existed (Capelas and Pereira, 1976) and the
treatment offered by qualified practitioners would have
been limited by their cost and the ability of patients to
pay.
Fluorine levels. The cariostatic properties of fluorine
are well known (Thylstrup and Fejerskov, 1994), but
fluoridation was never introduced in Portugal, despite
some experiments in a few places later in the 20th century. Natural soil fluorine levels in Portugal are generally very low (ranging between 0.03 mg F2/l and 0.19
mg F2/l in the region of Coimbra) (Pinto et al., 1999).
In fact, a recent study performed in 275 Portuguese
‘‘concelhos’’ (administrative division) reveals that in
only one (Vila Flôr, district of Bragança, Northeast
region of the country) are the natural soil fluorine levels sufficiently high to dispense fluorine supplements
(Pinto et al., 1999). Consequently, aside these few
exceptions, the individuals living in Portugal would
probably not have ingested fluorides in any significant
amounts, until more recent times, when fluoridated
toothpastes were introduced.
67
Dental examination
Initially, teeth were examined for presence, postmortem absence, antemortem absence, partial eruption,
anomalous eruption, or no eruption (as a result of young
age, impaction or agenesis). The assessment of which
teeth had been lost before death and which after death
was done by considering the condition of the socket margins. It was assumed that a tooth had been lost postmortem if there was an empty alveolus with no sign of
remodeling. AMTL was assumed when there was at
least a trace of remodeling in the socket or alveolar process. Third molars were only recorded as lost antemortem when they had left distinct traces of approximal
wear on the distal surface of the adjacent second molar.
All retained roots were recorded as remaining teeth.
Only fully erupted teeth were used for further calculations because there is the possibility that partially
erupted teeth may have been covered by soft tissue
(Lingström and Borrman, 1999). In all, 19,188 tooth
positions and 9,562 permanent teeth were analyzed.
In this paper the phrase ‘‘tooth type’’ is used to refer
to a specific tooth in the dentition regardless of side
(e.g., mandibular first molars) rather than to an entire
class of tooth (e.g., molars).
Recording dental caries
For a detailed comparison with modern epidemiological studies of living adults, it was necessary to record
caries in more detail than has been the case in many
archaeological studies. For this reason, the caries recording scheme of Hillson (2001) has been adopted here.
The dentitions were examined under standardized
lighting conditions by careful visual inspection, with the
aid of a low-power microscope. When possible, teeth
were removed from the alveolus for better evaluation.
Lesions were judged to be caries if there was a discernable, even if small, white or brown spot in the otherwise
translucent enamel, which serves to identify the early
stages of the condition (Hillson, 2001). Most surveys to
date have only recorded carious cavities about which the
examiner was absolutely certain (O’Sullivan et al., 1993;
Whittaker and Molleson, 1996; Watt et al., 1997; Lingström and Borrman, 1999; Cucina and Tiesler, 2003;
Vodanovic et al., 2005). It is now recognized that such
procedure underestimates the frequency of caries and
that recording of noncavitated lesions is not as unreliable as had been believed when carefully trained and
calibrated examiners are used to conduct the survey
(Ismail, 1997). Radiographs could not be made of all
specimens in this very large collection but their use was
not considered essential. The visual method of caries
identification has previously been shown to be reliable
when compared to both radiographic and histological
studies (Whittaker et al., 1981) and serves to minimize
interobserver error (Rudney et al., 1983). Also the dry
surfaces, bright lighting and use of a microscope greatly
improve the visibility of lesions.
The position, site of origin, stage of development and
extent of lesions were recorded where possible. Several
locations were considered: occlusal surfaces, pit sites,
mesial and distal contact areas, mesial and distal root
surfaces, buccal/labial and lingual enamel smooth surface sites, and buccal/labial and lingual root surfaces. A
cavity was classified as gross when it was too large for
the initial location of the site of attack to be determined
American Journal of Physical Anthropology
68
S.N. WASTERLAIN ET AL.
with certainty, and as gross gross when involving the
loss of so much of the tooth that it was not possible to
determine whether the lesion was initiated in the crown
or root.
Root exposure on each side of the tooth was assessed by
measuring maximum vertical distance (to the nearest
millimetre) between the CEJ to the alveolar bone lining
the socket (ABLS) with a graduated periodontal probe
(roots were considered exposed when CEJ-ABLS [2 mm).
Before commencement of the main study, several calibration exercises were carried out to ensure that diagnostic criteria were precisely defined and a high level of
reproducibility achieved. Data were collected by one observer (S.W.). Every 2 weeks, checks for intra-examiner
variability were made by repetition of the first individual
recording made during that time period. In all, 22
repeats were involved in this intra-observer assessment.
The kappa statistics on intra-examiner consistency in
the diagnosis of caries lesions was 0.93.
Calculating caries occurrence
The expression of caries frequency in an assemblage of
skeletons has always been problematic. Given the fragmentary nature of osteological material, it is rather difficult to estimate the proportion of individuals affected by
dental caries, as the status of missing teeth can never be
known. For the same reason, modern caries indices such
as DMFT (decayed, missing and filled teeth) or DMFS
(decayed, missing and filled surfaces) are unsuitable
(Watt et al., 1997). The most accurate method of expressing caries rate would seem to be the calculation of the
number of teeth observed to be affected by caries as a
percentage of all teeth present that have erupted into
functional positions (Kerr et al., 1990). Some individuals
are likely to have lost some teeth during their lives and
it is reasonable to think that some of these had been lost
due to dental caries. Some researchers (Whittaker et al.,
1981; Lukacs, 1995) have felt that to exclude those teeth
would yield caries rates lower than the true ones and
have attempted to apply corrective factors derived from
the numbers of teeth lost antemortem. However, teeth
are frequently lost antemortem due to reasons other
than caries; namely periodontal disease and trauma.
Most frequently, it is impossible to know what proportion
of AMTL may have resulted from dental caries, and the
current view seems to be that such corrections should
not be applied (Kerr et al., 1990; Whittaker and Molleson, 1996; Watt et al., 1997; Hillson, 2001; Oxenham and
Matsumura, 2008). This was the position adopted in this
study.
In life the teeth are held in the jaw by the soft tissues.
However, after death, as these decay, the teeth become
more susceptible to loss in the burial environment. Some
researchers have considered the proportion of postmortem tooth loss to be a useful measure of the ‘‘quality" of
the dentitions in excavated skeletal material. If, however, as in the present study incisors and canines are
more often lost postmortem than cheek teeth and at the
same time they are much less affected by caries than
cheek teeth (Varrela, 1991; Watt et al., 1997; Lingström
and Borrman, 1999), then the pattern of loss must have
a strong effect on caries statistics.
With all this in mind it was decided that a single
index of caries rate could not express the true complexities of dental caries and would be affected by differential preservation of different tooth classes, parts of teeth,
American Journal of Physical Anthropology
age groups and sexes (Hillson, 2001). Separate tabulations for the different categories of carious lesions, at the
different sites where they may be initiated on different
teeth were made. AMTL was calculated as the percentage of tooth positions in the jaws from which the tooth
had been lost during life. The statistical significance of
the recorded values was tested with independent
samples chi-square.
RESULTS
Missing teeth
Of the 19,188 observable sockets, 2,222 teeth were lost
postmortem (11.6%) and 7,131 (37.2%) were lost before
death. Additionally, two roots remained as support to
prosthetic crowns. Partial eruption was observed in 38
teeth (third molars only) whereas anomalous eruption
was found in 32 teeth (third molars and upper canines).
Much more common was complete failure to erupt (as a
result of young age, impaction or agenesis), registered in
109 tooth positions (mainly third molars, but also upper
lateral incisors, lower canines and lower premolars). Of
the 9,654 fully erupted teeth, 92 were excluded from the
present study due to severe postmortem damage that
prevented evaluation. Therefore, it has been possible to
study caries in 9,562 teeth. The percentages of teeth
present, antemortem losses, postmortem losses, postmortem fractures, and those with eruption related problems
(with sides pooled) by age group are provided in Figure
1 (Supporting Information Table S-1).
In age Groups 1 and 2, between 53 and 95% of all
teeth were present. The number of teeth present
decreased with age particularly in the posterior region,
as AMTL increased. In fact, AMTL increased steadily
from 4.6% in age Group 1 to 73.2% in age Group 6. Loss
of molar teeth was especially marked from age Group 5
onwards. Canines were the least frequently missing
teeth as age progressed. Postmortem tooth loss was
higher between age Groups 2 and 4 whereas tooth damage was broadly similar in all age groups. In age Group
6, between 6 and 28% of all teeth were present. Molars
suffered AMTL with higher frequency but were lost postmortem less often than incisors or canines. In general,
premolars occupied an intermediate position in both
types of tooth loss.
Caries experience
Though dental caries may attack one side of the dentition to a greater degree in an individual, there is no reason why it should systematically favor one side or the
other in a population (Watt et al., 1997). A pilot comparison showed no consistent side-specific differences in
caries frequency in the current sample, and hence data
from both sides were combined as is normal for most epidemiological studies (Thystrup and Fejerskov, 1994).
In the whole assemblage, 62.0% (5,932/9,562) of the
surviving permanent teeth and 99.4% (511/514) of individuals with permanent teeth were affected by caries. If
only cavitated lesions are considered, these values drop
to 27.9% (2,666/9,562) and 92.6% (476/514), respectively.
Of 514 individuals with dentitions, only 17 (3.3%) had
only one decayed tooth.
When consideration is limited to the upper dentition,
higher rates were observed in females than in males
(Chi-square 5 28.451, df 5 1, P 5 0.000). No differences
CARIES IN A PORTUGUESE IDENTIFIED SKELETAL SAMPLE
69
Fig. 1. Percentages of teeth present, missing antemortem, lost postmortem, fractured postmortem, and with eruption related
problems in each tooth type (numbered from eight for third molar to one for first incisor), and age group. Upper dentition is above
the line and lower below.
Fig. 2. Caries and antemortem tooth loss frequency rates for each tooth type (numbered from eight for third molar to one for
first incisor) and age group, in males. Upper dentition is above the line and lower below.
were found between the sexes for lower teeth (Chisquare 5 0.087, df 5 1, P 5 0.768).
In Figures 2 and 3 (males and females, respectively;
Supporting Information Tables S-2 and S-3), caries and
AMTL frequency rates are presented for each tooth by
age group. Although the frequency of carious lesions was
age-associated it was still remarkably high among members of age Group 1. In the youngest males some 49.1%
of all teeth were carious. This rose to a maximum of
74.7% in age Group 5 and fell to 72.8% in age Group 6.
In females, the percentage of carious teeth rose from
53.6% in age Group 1 to 71.7% in age Group 2, than fell
to 64.2% in age Group 3 to increase again until age
Group 5. As with men, caries experience decreased in
the oldest group of females. This decrease in the oldest
age group may have been influenced by increasing levels
of AMTL, for the most carious teeth would also be the
ones most likely to be lost. In both sexes, the eldest age
group showed a marked increase in AMTL, an unknown
proportion of which may have been due to caries. Furthermore, a slight trend was evident towards a more anterior location of the lesions from molars, to premolars,
to canines and incisors in the older age categories. In
the younger age classes caries attacked the incisor and
American Journal of Physical Anthropology
70
S.N. WASTERLAIN ET AL.
Fig. 3. Caries and antemortem tooth loss frequency rates for each tooth type (numbered from eight for third molar to one for
first incisor) and age group, in females. Upper dentition is above the line and lower below.
Fig. 4. Caries frequency rates for each tooth type (numbered from eight for third molar to one for first incisor) and age group,
according to the severest lesion type on any surface of the tooth, in males. Upper dentition is above the line and lower below.
canine teeth less frequently than the molars and premolars, whereas in the older age groups caries progressed
from posterior to anterior teeth, so that in some cases
posterior and anterior teeth were affected by caries with
almost equal frequency. This pattern may be a consequence of AMTL. With preferential loss of the molars, often due to caries, more anterior teeth are the only ones
left to be at risk of caries in older individuals. Hence,
caries frequency tends to increase. Caries occurred more
frequently in the upper than in the lower jaw, both in
males (Chi-square 5 34.859, df 5 1, P 5 0.000) and
females (Chi-square 5 110.227, df 5 1, P 5 0.000).
American Journal of Physical Anthropology
The overall coronal and root surface caries frequency
for all incisors and canines was 44.6%, for premolars
70.6%, and molars 77.2%. The most caries-involved teeth
were first molars, independently of sex. Nevertheless,
the largest value for caries frequency in a particular
tooth class was 100%, observed in maxillary second
molars and mandibular third molars among 70 to 79year-old males. By contrast, the least affected teeth were
the lower incisors.
In Figures 4 and 5 (for males and females, respectively), caries frequency rates are presented for each
tooth by age group, according to the severest lesion type
71
CARIES IN A PORTUGUESE IDENTIFIED SKELETAL SAMPLE
Fig. 5. Caries frequency rates for each tooth type (numbered from eight for third molar to one for first incisor) and age group,
according to the severest lesion type on any surface of the tooth, in females. Upper dentition is above the line and lower below.
on any surface of the tooth (Supporting Information
Table S-4). The pattern of lesions changed progressively
with age as well. Lesions confined to the enamel of the
crown were the most common form in young adults,
declining with age, particularly from the age Group 4 in
females and from age Group 5 in males onward. On the
other hand, the proportion of teeth with lesions penetrating to the dentine and to the pulp chamber rose
gradually with age. Overall, enamel lesions, fillings, and
pulp exposing lesions predominated in the posterior
teeth, while in the anterior teeth dentine lesions predominated. Fillings were extremely rare in all age groups
and were not found in any individual in the oldest age
class (age Group 6). Only 12 individuals possessed
fillings. These include three individuals (two males, one
female) with three filled teeth, four individuals (three
males, one female) with fillings in two teeth, and five
males had a filling in a single tooth. Overall, only 0.4%
of the carious teeth (22/5,932) and 2.3% of the individuals had fillings. First molars were the most frequently
filled teeth (11), followed by the second molars (4). The
remaining filled teeth were incisors (1), canines (2), first
premolars (2), and second premolars (2). Fifty per cent of
those teeth had fillings on only one surface: seven teeth
had fillings involving the occlusal surface, and four teeth
had the approximal area filled.
Since carious lesions fall into several different categories, in relation to their site of initiation on the tooth
surface, and that these categories have contrasting etiologies, and develop in different ways with increasing age,
they are also presented separately here. On the crown, it
is possible that a carious lesion might have initiated in
the enamel of the occlusal fissures, grooves or fossae, in
a buccal or lingual pit, in an occlusal attrition facet, at
either the mesial or the lingual contact point, or in the
enamel of the smooth surface.
For occlusal caries (Table 1), the percentages of surfaces involved were calculated as a percentage of fissure
and fossa occlusal sites (only molar and premolar teeth
have them) present in each individual and at risk. As no
TABLE 1. Occlusal caries frequency rates for each tooth
by age group
Upper
Lower
Age group
Tooth
N
% Carious
N
% Carious
1
(20–29 year)
8
7
6
5
4
8
7
6
5
4
8
7
6
5
4
8
7
6
5
4
8
7
6
5
4
8
7
6
5
4
127
178
175
157
173
105
148
125
123
126
76
116
88
106
90
47
76
72
76
68
23
42
35
41
38
11
28
22
22
20
29.9
34.8
29.7
3.8
2.9
46.7
45.9
28.8
8.1
4.8
27.6
39.7
28.4
3.8
7.8
38.3
30.3
25.0
7.9
7.4
56.5
38.1
28.6
14.6
10.5
36.4
39.3
31.8
9.1
5.0
129
168
145
168
186
96
138
108
146
150
86
108
85
135
142
43
66
51
90
106
23
34
28
49
60
13
19
16
36
40
43.4
45.2
29.0
6.0
2.2
51.0
58.7
35.2
6.2
4.0
43.0
37.0
23.5
6.7
1.4
32.6
43.9
33.3
5.6
2.8
39.1
41.2
39.3
10.2
6.7
46.2
31.6
18.8
8.3
5.0
2
(30–39 year)
3
(40–49 year)
4
(50–59 year)
5
(60–69 year)
6
(70–79 year)
sexual differences were found for occlusal caries (Chisquare 5 0.660, df 5 1, P 5 0.416), males and females
were pooled. Of all the occlusal surfaces examined, some
22.9% (1,189 of 5,197) showed evidence of caries. Overall, molars were significantly more affected by occlusal
caries (37.4%) than premolars (5.3%) (Chi-square 5
American Journal of Physical Anthropology
72
S.N. WASTERLAIN ET AL.
TABLE 2. Pit caries frequency rates for each tooth by age group and sex
Male
Female
Upper
Lower
Upper
Lower
Age group
Tooth
N
% Carious
N
% Carious
N
% Carious
N
% Carious
1
(20–29 year)
8
7
6
3
2
1
8
7
6
3
2
1
8
7
6
3
2
1
8
7
6
3
2
1
8
7
6
3
2
1
8
7
6
3
2
1
0
0
1
12
17
6
0
0
2
7
12
1
1
0
0
4
8
0
1
0
0
3
1
3
0
2
0
4
4
3
0
0
0
1
0
0
0.0
0.0
100.0
0.0
11.8
0.0
0.0
0.0
100.0
14.3
16.7
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
14.3
0.0
0.0
50.0
0.0
25.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
10
19
35
0
0
0
8
18
26
0
0
0
11
10
29
0
0
0
3
12
14
1
0
0
4
4
4
0
0
1
0
1
1
0
0
0
10.0
15.8
5.7
0.0
0.0
0.0
37.5
38.9
26.9
0.0
0.0
00
27.3
40.0
20.7
0.0
0.0
0.0
66.7
58.3
21.4
0.0
0.0
0.0
50.0
50.0
0.0
0.0
0.0
0.0
0.0
100
100
0.0
0.0
0.0
0
1
1
5
20
5
2
0
1
8
11
5
1
1
1
1
14
0
1
0
0
3
4
0
0
1
0
1
2
1
0
0
0
1
0
0
0.0
100.0
100.0
0.0
0.0
0.0
50.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
7.1
0.0
100.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
100.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
4
11
24
1
1
1
12
11
21
0
0
0
4
6
12
0
0
0
3
4
1
0
0
0
1
3
5
0
0
0
1
0
2
0
0
0
40.0
18.2
4.2
0.0
0.0
0.0
41.7
9.1
14.3
0.0
0.0
0.0
25.0
0.0
25.0
0.0
0.0
0.0
0.0
50.0
0.0
0.0
0.0
0.0
0.0
0.0
40.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
2
(30–39 year)
3
(40–49 year)
4
(50–59 year)
5
(60–69 year)
6
(70–79 year)
751.720, df 5 1, P 5 0.000). The teeth most affected
were second molars and the teeth least affected were
first premolars. Interestingly, the frequency of occlusal
caries increased between age-Groups 1 and 2 then
remained relatively stable until showing another rise in
age Group 5. No differences were found between lower
teeth (22.8%) and upper teeth (22.8%), for occlusal caries
(Chi-square 5 0.003, df 5 1, P 5 0.955).
For pit caries (Table 2), each discrete pit present in
the dentitions was counted and evaluated. Not all dentitions have them, but there is often one buccal pit on
molars and, sometimes, a lingual pit in upper incisors
(rarely canines) (Hillson, 2001). The frequency of pit
caries was lower than that of occlusal caries, totaling
17.8% of 533 sites at risk. Central incisors were never
affected by pit lesions, neither were lower canines. No
pits were even present in lower lateral incisors. Overall,
molars were significantly more affected by pit caries
(24.2%) than anterior teeth (5.1%) (Chi-square 5 29.743,
df 5 1, P 5 0.000). Besides, the frequency of pit caries in
lower teeth (22.6%) was higher than that of upper teeth
(9.0%) (Chi-square 5 15.290, df 5 1, P 5 0.000). In
males, the percentage of pit caries rose from 9.0% in the
20–29 year-olds to 66.7% in the oldest group. In females,
the frequency of pit caries increased more or less steadily through the age groups from 11.3% in age Group 1 to
21.4% in age Group 5. Males had a significantly (ChiAmerican Journal of Physical Anthropology
square 5 5.179, df 5 1, P 5 0.023) greater involvement
of pit sites (21.0%) than females (13.4%).
For occlusal attrition facet dentine caries (Table 3),
5,906 facets were at risk and of these 16.0% were
involved. For both males and females, occlusal attrition
facet dentine caries was more common in upper than in
lower teeth (Chi-square 5 100.055 df 5 1, P 5 0.000).
No differences were found between anterior and posterior teeth (Chi-square 5 2.069, df 5 1, P 5 0.150), nor
did occlusal attrition facet dentine caries show any significant preference for a particular tooth type. In the
youngest men (age Group 1), 15.6% of attrition facets
were carious and, as with occlusal caries, the frequency
rose to a maximum of 27.5% in age Group 5 only to fall
to 20.3% in age Group 6. In females, the frequency of
attrition facet caries was lowest among age Group 2
(10.6%) and highest in age Group 5 (19.5%). Males had
significantly (Chi-square 5 17.579, df 5 1, P 5 0.000)
more involvement of attrition facets (17.8%) than
females (13.8%).
Contact areas between neighboring teeth (Table 4)
were the most frequently sites attacked by caries. Of the
17,617 approximal surfaces (mesial and distal) at risk,
5,800 (32.9%) were carious. In both sexes, contact caries
was significantly more common in posterior (60.0%) than
in anterior teeth (28.8%) (Chi-square 5 813.248, df 5 1,
P 5 0.000) and in upper (54.2%) than in lower teeth
73
CARIES IN A PORTUGUESE IDENTIFIED SKELETAL SAMPLE
TABLE 3. Occlusal attrition facet dentine caries frequency rates for each tooth by age group and sex
Male
Female
Upper
Lower
Upper
Lower
Age group
Tooth
N
% Carious
N
% Carious
N
% Carious
N
% Carious
1
(20–29 year)
8
7
6
5
4
3
2
1
8
7
6
5
4
3
2
1
8
7
6
5
4
3
2
1
8
7
6
5
4
3
2
1
8
7
6
5
4
3
2
1
8
7
6
5
4
3
2
1
6
12
44
19
30
73
52
67
9
29
58
25
47
79
64
69
9
22
39
35
37
71
54
54
18
32
37
35
29
51
36
28
14
22
19
21
21
37
22
25
1
8
8
21
7
12
8
13
33.3
8.3
22.7
26.3
23.3
31.5
15.4
20.9
55.6
27.6
19.0
36.0
23.4
16.5
15.6
17.4
0.0
22.7
20.5
17.1
21.6
25.4
22.2
27.8
0.0
6.3
2.7
14.3
31.0
15.7
30.6
39.3
50.0
22.7
15.8
28.6
14.3
29.7
45.5
68.0
0.0
37.5
12.5
28.6
28.6
16.7
0.0
23.1
8
14
53
9
23
72
77
76
19
43
61
34
36
64
66
70
20
32
52
24
42
75
74
66
21
36
38
33
50
64
48
38
18
22
20
29
36
46
42
31
0
10
6
12
14
21
13
10
12.5
35.7
11.3
22.2
21.7
6.9
3.9
2.6
15.8
11.6
14.8
20.6
13.9
12.5
3.0
4.3
15.0
9.4
9.6
0.0
7.1
10.7
12.2
18.2
14.3
25.0
21.1
0.0
8.0
21.9
16.7
23.7
27.8
31.8
15.0
27.6
22.2
23.9
19.0
16.1
0.0
100.0
16.7
25.0
35.7
19.0
15.4
20.0
2
12
38
18
31
71
54
55
9
20
41
25
34
57
42
52
7
21
30
27
33
58
44
46
6
13
29
25
32
52
27
32
2
3
13
12
13
26
10
22
3
9
11
11
7
32
15
18
50.0
16.7
28.9
33.3
29.0
26.8
25.9
27.3
22.2
5.0
12.2
16.0
11.8
14.0
14.3
23.1
28.6
9.5
10.0
14.8
18.2
27.6
18.2
15.2
0.0
7.7
6.9
20.0
25.0
7.7
18.5
21.9
50.0
33.3
7.7
33.3
23.1
23.1
10.0
22.7
33.3
11.1
36.4
27.3
42.9
15.6
6.7
5.6
0
14
47
12
23
80
80
83
10
28
40
17
32
61
56
52
10
20
30
22
28
65
60
59
8
13
9
12
31
55
51
46
2
4
9
8
16
34
18
13
6
6
9
12
16
24
23
16
0.0
21.4
12.8
8.3
8.7
7.5
5.0
3.6
10.0
10.7
7.5
11.8
9.4
3.3
1.8
7.7
30.0
15.0
13.3
13.6
7.1
9.2
5.0
8.5
12.5
7.7
0.0
8.3
6.5
9.1
11.8
15.2
0.0
0.0
22.2
25.0
12.5
20.6
11.1
23.1
16.7
0.0
22.2
8.3
6.3
4.2
4.3
0.0
2
(30–39 year)
3
(40–49 year)
4
(50–59 year)
5
(60–69 year)
6
(70–79 year)
(41.4%) (Chi-square 5 143.500, df 5 1, P 5 0.000). Overall, contact caries was more common in first molars and
premolars. Interestingly, the frequency of contact caries
was much lower in third molars. Even so, central incisors were the least affected of all teeth. In males, a trend
towards increasing caries frequency on the approximal
surface with age until age Group 4 was noted. In
females, 28.5% of contact areas were caries-involved in
age Group 1, rising to a maximum of 47.2% in age Group
2, a rate very different from that in age Group 6 (32.9%).
Females had a significantly greater involvement (Chisquare 5 57.115, df 5 1, P 5 0.000) of distal and mesial
surfaces (both upper and lower) than did the males.
Smooth surfaces (Table 5) were the least affected by
caries. As no sexual differences were found for smooth
surfaces caries (Chi-square 5 1.934, df 5 1, P 5 0.164),
males and females were lumped together. Lesions were
seen on the buccal or lingual surfaces in only 1,174 cases
of 18,148 surfaces observed (6.5%). Overall, third molars
were the most commonly affected teeth. By contrast, second premolars and the incisors were the least involved
teeth in the upper and lower jaws, respectively. In men,
smooth surfaces caries was more frequent in age Group 5
whereas in females it was more common in age Group 2.
In living individuals, it is possible to determine
whether a root surface carious lesion was initiated at
the CEJ or on the root surface nearby, but in archaeologically-derived specimens it is usually not possible to distinguish between the two initiation sites. It is, therefore,
more practical to combine the two as ‘root surface caries’,
as in clinical studies (Fejerskov et al., 1993). A
root caries index (Kerr, 1990) was calculated from the
American Journal of Physical Anthropology
74
S.N. WASTERLAIN ET AL.
TABLE 4. Contact caries frequency rates for each tooth by age group and sex
Male
Female
Upper
Lower
Upper
Lower
Age group
Tooth
N
% Carious
N
% Carious
N
% Carious
N
% Carious
1
(20–29 year)
8
7
6
5
4
3
2
1
8
7
6
5
4
3
2
1
8
7
6
5
4
3
2
1
8
7
6
5
4
3
2
1
8
7
6
5
4
3
2
1
8
7
6
5
4
3
2
1
143
187
172
155
170
175
158
138
117
155
130
130
148
165
136
133
99
114
102
112
91
147
119
105
60
81
70
84
65
102
70
53
33
58
38
47
44
70
43
48
4
16
15
18
11
21
11
18
14.0
24.1
43.0
41.3
34.1
13.1
20.9
13.0
29.9
28.4
36.9
48.5
40.5
21.8
25.7
21.8
20.2
27.2
31.4
51.8
39.6
25.2
32.8
28.6
31.7
43.2
60.0
65.5
64.6
30.4
34.3
20.8
42.4
34.5
55.3
59.6
61.4
28.6
32.6
27.1
0.0
31.3
26.7
61.1
54.5
28.6
18.2
16.7
141
174
152
173
188
174
170
164
111
165
137
169
163
153
138
140
102
124
105
145
156
164
153
131
49
95
78
95
123
132
96
70
34
46
39
62
74
86
86
66
24
20
11
29
27
37
22
9
20.6
42.5
58.6
35.8
21.8
6.9
2.4
0.6
32.4
45.5
55.5
40.2
19.0
10.5
6.5
5.0
14.7
26.6
49.5
30.3
22.4
11.0
4.6
3.1
44.9
63.2
67.9
55.8
44.7
16.7
8.3
4.3
29.4
65.2
61.5
62.9
51.4
23.3
16.3
10.6
33.3
25.0
45.5
62.1
44.4
18.9
0.0
0.0
113
176
179
160
173
175
160
113
98
142
127
117
109
132
128
108
54
116
84
105
92
136
99
93
39
71
74
68
73
111
63
61
9
27
32
34
31
52
21
40
18
36
25
26
27
68
38
37
21.2
22.2
45.8
43.1
45.7
23.4
25.6
25.7
44.9
54.9
63.0
76.9
67.9
38.6
51.6
39.8
38.9
39.7
51.2
68.6
54.3
35.3
27.3
33.3
30.8
47.9
54.1
58.8
52.1
35.1
23.8
21.3
22.2
55.6
65.6
61.8
58.1
40.4
33.3
22.5
55.6
33.3
56.0
73.1
77.8
48.5
26.3
29.7
118
164
141
160
186
184
180
165
80
116
84
123
140
153
124
103
69
93
75
130
127
142
123
115
38
42
20
88
90
112
103
92
9
21
18
36
39
63
30
24
22
17
20
42
53
57
39
30
23.7
39.6
57.4
37.5
26.9
9.2
7.8
4.2
42.5
57.8
70.2
62.6
47.9
17.0
13.7
15.5
39.1
44.1
60.0
48.5
34.6
19.0
7.3
4.3
36.8
61.9
50.0
56.8
40.0
22.3
6.8
7.6
44.4
19.0
44.4
63.9
30.8
27.0
16.7
12.5
36.4
35.3
65.0
66.7
45.3
26.3
5.1
6.7
2
(30–39 year)
3
(40–49 year)
4
(50–59 year)
5
(60–69 year)
6
(70–79 year)
number of lesions in each sex and age group related to
the surfaces at risk (Table 6, Supporting Information
Figs. S-1 and S-2). Of the 36,567 root surfaces analyzed,
55.9% were presumably exposed (maximum vertical distance between CEJ to alveolar bone lining socket [2
mm) by continuous eruption, or the recession of the gingivae and underlying supporting tissues related to periodontal disease. Although root exposure affected all
tooth classes, a characteristic pattern could be identified
in both sexes. In upper teeth, root exposure was more
commonly seen in molars whereas in lower teeth affected
mainly incisors and canines. The percentage of exposed
root surfaces increased steadily with age, in both sexes,
from 26% in age Group 1 to around 89% in the oldest
individuals. Of the 20,432 exposed root surfaces, 2,161
(10.6%) were carious. Overall, molars were more affected
American Journal of Physical Anthropology
by root surface caries than anterior teeth, but this was
not evident for every age group. Root surface caries was
relatively uncommon amongst young adults, only 7.4
and 7.9% of male and female surfaces being affected, but
showed a steady rise with age, reaching the maximum of
16.6% and 11.4%, respectively, in age Group 4. In age
Group 6, the frequency of root caries was 13.2% for
males and 10.5% for females. Root caries was lower in
females (9.7%) than in males (11.3%). In both sexes, buccal root surfaces were more heavily affected by caries
(men: 10.0%; women: 7.4%) than lingual surfaces (men:
3.2%; women: 2.4%).
Overall, caries was most common at contact areas
(32.9%) and rarest at smooth surfaces (6.5%). In some
teeth the lesions were so large that they involved more
than one surface. Of the 9,562 analyzed teeth, 252
CARIES IN A PORTUGUESE IDENTIFIED SKELETAL SAMPLE
TABLE 5. Smooth surfaces caries frequency rates for each tooth
by age group
Upper
Lower
Age group
Tooth
N
% Carious
N
% Carious
1
(20–29 year)
8
7
6
5
4
3
2
1
8
7
6
5
4
3
2
1
8
7
6
5
4
3
2
1
8
7
6
5
4
3
2
1
8
7
6
5
4
3
2
1
8
7
6
5
4
3
2
1
256
365
352
324
345
359
325
237
212
300
268
249
260
304
279
260
152
234
188
218
187
293
234
213
97
153
151
152
142
220
146
128
47
86
70
78
77
127
77
100
22
54
44
45
42
94
48
62
10.5
8.2
5.1
1.9
2.9
3.3
4.6
5.5
24.5
7.0
6.0
4.0
5.4
3.9
5.0
4.6
9.2
6.8
3.2
0.5
2.7
5.1
5.1
4.2
12.4
3.3
7.9
1.3
2.8
5.5
6.2
5.5
6.4
11.6
4.3
2.6
7.8
8.7
11.7
17.0
9.1
5.6
0.0
2.2
9.5
4.3
4.2
3.2
260
338
293
335
374
365
361
336
189
277
225
294
306
319
279
250
171
220
182
277
285
320
297
258
92
138
102
185
218
257
209
172
47
68
56
98
118
168
131
92
25
37
30
73
81
105
74
50
18.1
14.5
10.6
3.6
3.7
1.9
1.4
1.8
32.8
17.3
11.6
6.1
7.2
7.5
1.8
2.4
19.9
9.5
6.6
4.0
2.8
5.3
1.0
1.9
20.7
13.8
6.9
5.4
5.5
4.7
3.3
2.3
21.3
7.4
10.7
14.3
10.2
4.8
4.6
2.2
16.0
2.7
10.0
11.0
3.7
3.8
2.7
0.0
2
(30–39 year)
3
(40–49 year)
4
(50–59 year)
5
(60–69 year)
6
(70–79 year)
(2.6%) had gross cavities. Of these, the great majority
(49.6%) were gross contact area or cervical caries (where
a carious cavity bridges the CEJ and the edge of the
approximal attrition facet), 15.9% were gross buccal or
lingual caries (where a carious cavity bridges the CEJ
and the buccal or lingual smooth surface), 14.3% were
gross coronal caries (where the lesion has progressed so
far that it was only possible to say that it was initiated
on the crown), 11.9% were gross mesial or distal caries
(where a carious cavity bridges the entire crown side
from the CEJ to the edge of the occlusal surface), and
8.3% were gross contact area/occlusal caries (where it
was not possible to tell whether it was initiated in the
occlusal surface or at the contact point). Gross gross
lesions where there was no indication where the lesion
was initiated affected 4.2% of all teeth.
75
DISCUSSION
In summer, our study of the Coimbra collection found
that:
1. The proportion of teeth lost antemortem increased
markedly with age particularly in the molars and premolars. In the oldest age group, the great majority of
cheek teeth were missing. Postmortem tooth loss or
fracturing stayed at a similar level throughout, with
anterior teeth affected substantially more than cheek
teeth.
2. A larger proportion of molars and premolars was
affected by carious lesions than incisors and canines.
There was no significant difference between left and
right, but upper teeth were more often carious than
lower. The proportion of surviving teeth affected by
caries increased with age (particularly in the cheek
teeth), but reduced slightly in the oldest group. As
the number of surviving teeth decreased markedly
with age, when caries and AMTL are considered together the proportion of tooth positions showing a carious lesion fell. Both males and females showed a similar pattern of lesions–only in upper teeth did females
show significantly higher frequencies of lesions than
males.
3. Overall, in both males and females, cheek teeth
lesions were most often confined to enamel or penetrating the pulp, while in anterior teeth they were
more commonly confined to dentine. There was, however, a progression with increasing age. For most
teeth, enamel lesions were commonest in the youngest
age group and declined steadily to the oldest group.
Dentine and pulp penetrating lesions were least common in the youngest group and increased to the oldest. This trend was particularly marked in anterior
teeth. Even in the oldest age group, a substantial proportion of lesions was confined to the enamel. This
might be taken to imply that lesions were slowly
developing but, given that the proportion of teeth lost
antemortem increased markedly with age and that
many of those teeth are likely to have been heavily
affected by caries, it suggests that new lesions continued to develop in the crown enamel.
4. Molar occlusal fissures were much more commonly
affected by carious lesions than those of premolars,
and there was no significant difference between upper
and lower teeth. There was no strong trend with age
and the oldest age group had just as many fissures
affected as the youngest. Pits on the crown sides were
much less commonly affected than occlusal fissures
and mainly the buccal pits of lower molars were
involved. In males, lesions at these sites showed a
pronounced increase with age.
5. Contact areas were the most common sites of all carious lesions. A greater proportion of cheek teeth than
anterior teeth was involved, especially the first
molars and the premolars. Females showed slightly
higher proportions of contact areas with caries than
males, while males showed a stronger trend with age
than females.
6. The smooth surfaces of crown sides just above the
gingivae were the least common caries sites. This
type of lesion could be found in any tooth, but the
most commonly affected were the third molars. There
was no significant difference between males and
females and there was not a strong trend with age.
American Journal of Physical Anthropology
76
S.N. WASTERLAIN ET AL.
TABLE 6. Root surface caries frequency rates for each tooth by age group and sex
Male
Upper
Age group
Tooth
N
%
Exposed
root
surfaces
1
(20–29 year)
8
7
6
5
4
3
2
1
8
7
6
5
4
3
2
1
8
7
6
5
4
3
2
1
8
7
6
5
4
3
2
1
8
7
6
5
4
3
2
1
8
7
6
5
4
3
2
1
285
377
343
315
343
358
324
290
230
317
273
260
301
336
291
284
197
231
203
227
195
310
253
220
113
165
146
169
131
210
164
117
67
113
75
95
89
156
106
116
8
31
29
39
27
47
32
47
14.0
27.3
38.8
23.8
27.4
22.3
30.9
27.2
50.0
45.7
59.7
50.4
58.1
50.9
54.3
53.5
56.9
73.6
80.8
72.7
72.8
72.3
70.8
74.5
72.6
78.2
77.4
74.6
72.5
73.8
62.2
60.7
77.6
80.5
80.0
74.7
71.9
69.2
60.4
63.8
75.0
87.1
96.6
92.3
74.1
66.0
68.8
76.6
2
(30–39 year)
3
(40–49 year)
4
(50–59 year)
5
(60–69 year)
6
(70–79 year)
Female
Lower
%
Carious
root
surfaces
1.1
3.4
1.7
0.6
1.5
1.1
1.9
1.7
3.5
6.3
4.8
2.3
2.0
2.7
3.4
4.2
7.1
5.6
4.4
5.7
3.1
1.6
3.2
1.4
12.4
12.7
15.8
14.2
12.2
12.4
12.8
17.1
14.9
12.4
16.0
16.8
15.7
14.7
17.0
20.7
12.5
12.9
3.4
5.1
14.8
12.8
9.4
8.5
N
%
Exposed
root
surfaces
%
Carious
root
surfaces
287
347
308
347
377
352
352
336
221
336
277
341
329
322
288
291
199
250
211
292
316
338
317
269
105
192
157
192
250
269
204
159
74
92
79
124
155
199
183
134
4
40
22
60
55
83
56
38
3.1
8.6
12.0
16.1
24.4
30.1
47.4
57.7
23.1
31.0
44.8
41.6
42.6
55.0
60.1
73.2
41.7
55.2
58.3
61.6
61.1
69.2
83.6
86.2
56.2
56.8
66.2
71.4
69.2
75.8
78.4
79.9
63.5
72.8
69.6
78.2
75.5
78.4
78.1
85.8
0.0
75.5
81.8
81.7
87.3
83.1
78.6
92.1
0.7
1.7
2.3
2.6
2.7
3.7
2.6
3.3
7.2
9.5
5.4
6.2
6.1
3.4
5.6
6.2
10.6
10.8
10.0
9.2
7.9
4.1
6.0
4.8
15.2
18.2
19.1
16.7
15.2
10.8
9.3
14.5
6.8
6.5
19.0
12.1
14.8
13.1
17.5
9.0
25.0
12.5
13.6
16.7
9.1
16.9
19.6
5.3
7. Root surface caries lesions were strongly related to
exposure of the roots through continuous eruption or
periodontal disease. Both exposure and caries showed
a steady increase until 50 years of age. Males showed
a somewhat larger proportion of exposed root surfaces
with caries than females.
One of the main aims of this study was to test the
effect on caries statistics of a death assemblage, with its
very different age distribution to a living population. It
was therefore necessary to find comparative studies of
adults of all ages, divided into age groups. In addition,
because of the uneven distribution of teeth lost postmortem, it was necessary to find studies which reported
American Journal of Physical Anthropology
Upper
Lower
N
%
Exposed
root
surfaces
%
Carious
root
surfaces
223
349
359
327
347
352
326
241
195
282
261
237
222
270
268
230
108
231
174
212
184
278
213
204
76
140
149
136
151
231
134
139
22
54
62
68
63
106
48
85
36
72
51
52
55
138
70
79
9.9
16.0
27.6
17.7
17.0
23.9
26.7
28.2
34.9
41.5
56.7
39.2
36.5
43.0
42.9
37.8
60.2
65.4
74.7
56.1
59.2
58.3
54.5
56.9
65.8
76.4
79.9
72.8
69.5
69.7
65.7
69.8
40.9
53.7
66.1
70.6
71.4
69.8
43.8
64.7
55.6
83.3
74.5
88.5
65.5
84.8
77.1
89.9
0.9
0.3
3.1
0.9
1.4
2.0
1.5
2.0
2.6
2.8
5.0
3.0
3.2
1.5
1.9
1.7
4.6
7.4
9.2
1.9
7.1
3.6
2.8
3.9
9.2
10.0
8.1
4.4
8.6
8.7
10.4
7.2
22.7
16.7
8.1
4.4
11.1
6.6
10.4
10.6
19.4
9.7
13.7
0.0
18.2
6.5
7.1
2.5
N
%
Exposed
root
surfaces
%
Carious
root
surfaces
240
329
281
321
371
370
365
332
164
233
176
247
279
307
259
206
139
189
154
263
257
296
272
241
81
84
42
178
185
234
211
183
20
43
35
72
79
132
70
51
45
34
39
85
107
129
91
64
1.7
8.2
11.4
11.2
21.6
29.7
41.4
53.0
17.7
24.0
30.7
28.7
33.7
44.6
58.7
65.5
43.9
40.7
39.6
53.6
51.4
65.5
75.0
83.0
42.0
56.0
61.9
67.4
65.4
66.2
77.3
81.4
30.0
48.8
45.7
77.8
73.4
78.8
70.0
76.5
51.1
64.7
64.1
74.1
73.8
82.2
86.8
90.6
0.4
0.6
1.8
1.6
3.8
3.5
3.0
2.7
1.8
6.4
4.0
3.6
6.8
5.5
3.1
1.9
8.6
14.8
18.2
6.8
5.4
3.7
4.8
5.0
6.2
14.3
4.8
9.6
8.6
12.0
9.0
8.7
10.0
14.0
8.6
2.8
6.3
6.1
5.7
9.8
13.3
2.9
10.3
11.8
11.2
9.3
9.9
6.3
caries rates separately for different teeth. Relatively few
studies fit these criteria. Manji et al. (1989, 1991) studied
a full range of adult ages in a sample of 1,131 living people examined during 1985/6 in rural Kenya. They were
divided into five age groups (10 years in each), starting
with 15 years and ending with 64 years. This makes a
good comparison with the present study because the data
were plotted separately for different teeth and different
ages. In addition, as with the people in the Coimbra collection, the Kenyan patients lived in an area with limited
access to dental care. Luan et al. (1989; Manji et al.,
1991) published a similar study of 1,744 Chinese people
from the Beijing area, divided into six age groups (again
with 10 year interval) from 20 years up to 70 or more.
CARIES IN A PORTUGUESE IDENTIFIED SKELETAL SAMPLE
The age groups are closer to those of the present study,
but this study group may be less directly comparable as it
combined people living both in rural and urban conditions.
Manji et al. presented their Kenya study in two ways.
In their original article (1989), they plotted a graph in
which AMTL was included with caries, showing the most
severe lesion (divided into enamel, dentine, pulp, or root)
for each tooth, for each age group. The rationale for
including antemortem loss was that the principal cause
was extraction as a result of caries, except in the case of
lower incisors which were often ritually extracted (Manji
et al., 1988). In a later book chapter (1991) they excluded
AMTL and instead plotted the most severe lesion (divided
into enamel, dentine, pulp, root, filling) for each tooth
and each age group. This type of graph has become the
standard for studies of this kind, and has been used in
presenting the results of the present study.
In Manji et al.’s study in Kenya (1989) the molars
were the most commonly affected teeth, with 60% carious or missing, in all age groups. Premolars, canines
and incisors were little affected in the youngest 15–24
year group, but in older groups progressively larger proportions had lesions or were missing. By the 55–65 year
age group, some 40% of upper premolars had carious
lesions or were missing, and up to 30% of anterior teeth.
Upper premolars, canines and incisors were much more
affected than lower in all age groups. Carious lesions
became progressively larger with increasing age, involving the dentine and pulp as well as enamel, and more
teeth missing. In the oldest age group, up to half of the
teeth in each part of the dentition were missing. Root
caries became more common in older age groups
although enamel caries remained the most common, at
least in cheek teeth. Overall, there was no significant
difference between men and women, although particularly in the oldest age group women tended to be more
affected by caries and tooth loss than men.
When AMTL was excluded from the graph (Manji
et al., 1991) there was an even stronger contrast
between the high proportions of caries affected molars
(40–60% or more) and low proportions of anterior teeth
(mostly 20% or less), with premolars in between. In progressively older age groups, a larger proportion of anterior teeth and premolars were carious, and this was
much more marked in the upper dentition than the
lower. Enamel caries dominated throughout, although
root caries, and more deeply penetrating dentine and
pulp lesions increased with age.
Luan et al.’s (1989; Manji et al., 1991) study in rural
and urban areas of Beijing was presented in same way,
excluding AMTL. It showed very similar patterns of carious lesions, with molars again the main teeth involved.
The age progression was more strongly marked than in
the Kenya study. This was emphasized by the inclusion
of an older 701 year age group. The younger age groups,
under 50 years, had much lower caries rates than for
the Kenya group with less than 40% of molars affected.
This increased to more than 60% in the oldest 701 year
group. The proportion of premolars and anterior teeth
rose steadily with increasing age to 20–40% in the same
oldest group. At all ages, enamel lesions were less common than in the Kenya study. Except in the youngest
20–29 year group, most lesions penetrated the dentine
or pulp, or were root lesions (and thus would also have
penetrated dentine). In the 701 year age group only a
small minority of lesions was confined to the enamel,
77
mainly in the molars. These trends were shown both in
the upper and lower dentitions, but a higher proportion
of upper teeth was carious, particularly the anterior
teeth. Overall, the caries rate in women was slightly
higher than that in men.
Luan et al. (1989) also plotted root surface caries separately for their China study, for each tooth in the dentition and for each age group, with plots for buccal, lingual and interproximal sides of the teeth. On the same
graph, they plotted the proportion of root surfaces which
were exposed and therefore at risk of root caries, and
the proportion of roots surfaces which were both exposed
and had a carious lesion. Once again, this has become
the accepted way to present root caries data. The proportion of exposed root surfaces increased steadily with age
so that, in the oldest 701 year group, 80–100% of buccal
surfaces were exposed in all teeth. Molars were more
strongly affected than premolars and anterior teeth,
although the proportion of the latter teeth with exposed
roots increased strongly with age so that they were more
nearly equal to the molars in the oldest group. For buccal and interproximal root surfaces, the upper teeth
were more strongly affected than lower, particularly in
the younger groups. For lingual surfaces, the opposite
was true. Exposed root surfaces with carious lesions
increased with age, but only a small proportion of
exposed surfaces became carious. In addition, the lesions
were not strongly related to the pattern of root exposure–the teeth with most frequently exposed roots didn’t
show the highest root caries rates.
In general, the pattern of caries through the dentition
and with age is rather similar in the Kenya and China
studies. They are very different parts of the world, with
a contrasting background in climate, foodstuffs and
social conditions. It is supporting evidence for the idea
that caries progresses in a similar pattern (even if the
rate may vary) through the dentition (Thystrup and
Fejerskov, 1994), and with age, in most 20th century
populations with a nutrition based on carbohydrates,
including both starches and sugars. In this context, it is
reasonable to compare the Coimbra study with them.
In the Coimbra study (Figs. 2 and 3, Supporting Information Tables S-2 and S-3), the proportion of teeth missing antemortem at each potential tooth position in the
dentition rose much more sharply with age than in the
Manji et al. (1989) Kenya study. In age Group 5 (60–69
year), approximately 80% of Coimbra molars were missing antemortem, whereas some 40% of the Kenya molars
in the 55–64 year age group were missing. For Coimbra,
as the surviving teeth decreased in number, the proportion of tooth positions occupied by a carious tooth also
fell off more sharply in the older age groups than was
the case for Kenya, although the effect is emphasized by
the inclusion of an older 70–79 year age Group 6 for
Coimbra. Equivalent data were not published for the
China study, so no comparison can be made.
When the surviving teeth are considered without
AMTL for the Coimbra study (Figs. 4 and 5, Supporting
Information Table S-4), the picture is very different. In
the youngest age Group 1 (20–29 year), some 40–80% of
molars had carious lesions, which compares well with
Kenya. Both studies had a higher proportion of affected
molars than the China study in the youngest group. The
Coimbra study, however, showed a much higher proportion of anterior teeth and premolars with carious lesions
in Group 1 than either the Kenya or China studies. As
in the Kenya study, the proportion of the Coimbra
American Journal of Physical Anthropology
78
S.N. WASTERLAIN ET AL.
molars affected by caries remained at a similar level for
older age groups, whereas the proportion of premolars
and anterior teeth affected rose with age up to age
Group 5 (60–69 years), with a slight fall to Group 6 (70–
79 years). Lesions penetrating the dentine were more
common in the Coimbra study than Kenya or China but
it was similar to Kenya in the smaller proportion of
lesions exposing the pulp chamber. The China study
showed a much more marked rise of dentine and pulp
exposing lesions with age.
Exposure of root surfaces showed a similar pattern in
the Coimbra and China studies, with molars slightly
more affected than anterior teeth and a pronounced
increase in older age groups (Table 6, Supporting Information Figs. S-1 and S-2). In both, the proportion of
exposed surfaces with a carious lesion was relatively
small with no clear pattern to the distribution of lesions.
For Coimbra, the proportion of carious surfaces is larger,
approximately double that of the China study.
It is now possible to address the first five research
questions outlined above:
1. The results of the Coimbra study are consistent with
the most appropriate studies available for caries in
living adults, conducted some 60–80 years after the
Coimbra people died. The results are most like those
of the Kenya study and in other respects they fit
between the Kenya and China findings.
2. The pattern of caries around the dentition in the Coimbra study is similar to both Kenya and China, with the
molars most affected, anterior teeth least and premolars in an intermediate position. It departs mainly in
the larger proportion of anterior teeth affected by
caries. In older age groups, this might be related to the
pattern of AMTL (below). There were also more
dentine lesions in all age groups than in the modern
studies. This might possibly reflect the relationship
between poor health and caries, as a death assemblage
is likely to contain individuals with a poorer record of
health than the living populations as a whole.
3. There was a strong progression with age-at-death, following a similar path to that seen in the Kenya and
China studies. Not only did carious lesions become
more common, but they became more deeply penetrating and more anterior teeth were involved. Once again,
the death assemblage results are consistent with studies on the living. The results make it clear that both
age progression and distribution of carious lesions in
the mouth are just as important to consider in archaeological studies as they are in studies of the living.
4. AMTL was more strongly marked in the Coimbra
study than in either the Kenya or the China study. As
with both of these, it affected the molars more than
the premolars or anterior teeth and showed a marked
progression with age. Postmortem tooth loss was not
marked but affected particularly the single-rooted anterior teeth. The pattern of caries through the dentition may have been affected by AMTL, with anterior
teeth surviving preferentially in the older groups and
thus showing higher caries rates simply because they
were the only teeth in the mouth. It might be
expected that the preferential postmortem loss of anterior teeth would reduce this effect, but it is difficult
to unravel the two phenomena.
5. The differences in caries rates between men and
women are small, both in the Coimbra study and in
the Kenya and China studies. There is some variation
American Journal of Physical Anthropology
between different types of lesion and different age
groups, but where there is a significant difference it
is generally the women that have slightly higher
rates. The similarity between the results suggests
that the nature of the death assemblage had little
effect on them.
It would be interesting to compare the figures presented here with caries distribution in modern Portugal.
It is presumed that, given the increasing availability of
dental care over the last decades, there would be some
differences. Unfortunately, this will have to wait until
there are Portuguese epidemiological studies that follow
caries into adult life.
ACKNOWLEDGMENTS
The authors thank the Museum of Anthropology of the
University of Coimbra for permission to study the identified osteological collections. The authors also acknowledge the Editor-in-Chief of the journal, the Associate
Editor and the anonymous reviewers whose valuable
comments and suggestions allowed them to improve the
manuscript.
LITERATURE CITED
Batchelor PA, Sheiham A. 2004. Grouping of tooth surfaces by
susceptibility to caries: a study in 5–16 year-old children.
BMC Oral Health 4:2.
Bocquet-Appel J-P, Morais MHX. 1987. Anthropologie et Histoire. Un essai de reconstrution de la variation biologique de la
population portugaise au XIXe siécle. Paris: Fundação Calouste Gulbenkian.
Boléo JP. 1965. A higiene da boca através dos tempos até à
época presente. Separata de Revista Portuguesa de Estomatologia e Cirurgia Maxilofacial 3–4:1–46.
Capelas M, Pereira A. 1976. As escolas superiores de Medicina
Dentária e a assistõncia odonto-estomatológica em Portugal.
Separata de O Médico 80:238–240.
Corbett ME, Moore WJ. 1976. Distribution of dental caries in
ancient British populations. IV. The 19th century. Caries Res
10:401–414.
Costa FS. 1961. Breves considerações sobre a estomatologia
Portuguesa. Separata de Revista Portuguesa de Estomatologia
1–2:1–12.
Cucina A, Tiesler V. 2003. Dental caries and antemortem tooth
loss in the Northern Peten Area, Mexico: a biocultural perspective on social status differences among the classic maya.
Am J Phys Anthropol 122:1–10.
Cunha E, Wasterlain S. 2007. The Coimbra identified osteological
collections. In: Grupe G, Peters J, editors. Skeletal series and
their socio-economic context. Documenta Archaeobiologiae, Vol.
5. Rahden/Westf: Verlag Marie Leidorf GmbH. p 23–33.
Fejerskov O, Baelum V, Østergaard ES. 1993. Root caries in
Scandinavia in the 1980’s and future trends to be expected in
dental caries experience in adults. Adv Dent Res 7:4–14.
Hillson S. 2000. Dental pathology. In: Katzenberg MA, Saunders
SR, editors. Biological anthropology of the human skeleton.
New York: Alan R. Liss. p 249–286.
Hillson S. 2001. Recording dental caries in archaeological
human remains. Int J Osteoarchaeol 11:249–289.
Hillson S. 2008. The current state of dental decay. In: Irish JD,
Nelson GC, editors. Technique and application in dental anthropology. Cambridge: Cambridge University Press. p 111–
135.
Ismail AI. 1997. Clinical diagnosis of precavitated carious
lesions. Community Dent Oral Epidemiol 25:13–23.
Kerr NW. 1990. The prevalence and pattern of distribution of
root caries in a Scottish medieval population. J Dent Res
69:857–860.
CARIES IN A PORTUGUESE IDENTIFIED SKELETAL SAMPLE
Kerr NW, Bruce MF, Cross JF. 1990. Caries experience in mediaeval Scots. Am J Phys Anthropol 83:69–76.
Lingström P, Borrman H. 1999. Distribution of dental caries in
an early 17th century Swedish population with special reference to diet. Int J Osteoarchaeol 9:395–403.
Luan WM, Baelum V, Chen X, Fejerskov O. 1989. Dental caries
in adult and elderly Chinese. J Dent Res 68:1171–1776.
Lukacs JR. 1995. The ‘caries correction factor’: a new method of
calibrating dental caries rates to compensate for antemortem
loss of teeth. Int J Osteoarchaeol 5:151–156.
Lukacs JR, Thompson LM. 2008. Dental caries prevalence by
sex in prehistory: magnitude and meaning. In: Irish JD, Nelson GC, editors. Technique and application in dental anthropology. Cambridge: Cambridge University Press. p 136–177.
Mack F, Mojon P, Budtz-Jørgensen E, Kocher T, Splieth C,
Schwahn C, Bernhardt O, Gesch D, Korda B, John U, Biffar
R. 2004. Caries and periodontal disease in Pomerania, Germany: results of the study of health in Pomerania. Gerodontology 21:27–36.
Manji F, Baelum V, Fejerskov O. 1988. Tooth mortality in an
adult rural population in Kenya. J Dent Res 67:496–500.
Manji F, Fejerskov O, Baelum V. 1989. Pattern of dental caries
in an adult rural population. Caries Res 23:55–62.
Manji F, Fejerskov O, Baelum V, Luan WM, Chen X. 1991. The
epidemiological features of dental caries in African and Chinese populations: implications for risk assessment. In: Johnson NW, editor. Dental caries. Markers of high and low risk
groups and individuals. Risk markers for oral diseases, Vol. 1.
Cambridge: Cambridge University Press. p 62–99.
Moore WJ, Corbett ME. 1971. The distribution of dental caries
in ancient British populations. 1. Anglo-saxon period. Caries
Res 5:151–168.
Moore WJ, Corbett ME. 1973. The distribution of dental caries
in ancient British populations. II. Iron age, Romano-British
and mediaeval periods. Caries Res 7:139–153.
Moore WJ, Corbett ME. 1975. Distribution of dental caries in
ancient British populations. III. The 17th century. Caries Res
9:163–175.
O’Sullivan EA, Williams SA, Wakefield RC, Cape JE, Curzon
MEJ. 1993. Prevalence and site characteristics of dental
caries in primary molar teeth from prehistoric times to the
18th century in England. Caries Res 27:147–153.
Oxenham MF, Matsumura H. 2008. Oral and physiological paleohealth in cold adapted peoples: Northeast Asia, Hokkaido.
Am J Phys Anthropol 135:64–74.
79
Pinto R, Cristovão E, Vinhas T, Castro MF. 1999. Teor de fluoretos nas águas de abastecimento da rede Pública, nas sedes de
concelho de Portugal Continental. Rev Port Estomatol Cir
Maxilofac 40:125–142.
Ribeiro AS. 1935. Assistõncia Estomatológica em Portugal. A
Saúde. Jornal popular, bi-mensal, de Hygiene e Profilaxia
Sociais.5:5–7.
Roque JL. 1982. Classes populares no Distrito de Coimbra no
séc. XIX (1830–1870). Contributo para o seu estudo, Ph.D.
thesis: University of Coimbra.
Rudney JD, Katz RV, Brand JW. 1983. Interobserver reliability
of methods for paleopathological diagnosis of dental caries.
Am J Phys Anthropol 62:243–248.
Saunders SR, De Vito C, Katzenberg MA. 1997. Dental caries in
nineteenth century upper Canada. Am J Phys Anthropol
104:71–87.
Sheiham A. 1997. Impact of dental treatment on the incidence
of dental caries in children and adults. Community Dent Oral
Epidemiol 25:104–112.
Thylstrup A, Fejerskov O. 1994. Textbook of clinical cariology.
Copenhagen: Munksgaard.
Varrela TM. 1991. Prevalence and distribution of dental caries
in a late medieval population in Finland. Arch Oral Biol
36:553–559.
Vodanovic M, Brkić H, Šlaus M, Demo Ž. 2005. The frequency
and distribution of caries in the mediaeval population of
Bijelo Brdo in Croatia (10th–11th century). Arch Oral Biol
50:669–680.
Waldron T. 1994. Counting the dead: the epidemiology of skeletal populations. Chichester: John Wiley & Sons.
Watt ME, Lunt DA, Gilmour WH. 1997. Caries prevalence in
the permanent dentition of a Mediaeval population from the
South-West of Scotland. Arch Oral Biol 42:601–620.
Whittaker DK. 1993. Oral health. In: Molleson T, Cox M,
editors. The spitalfields project. The Anthropology: the Middling sort, Vol 2. New York: Council for British Archaeology.
p 49–63.
Whittaker DK, Molleson T. 1996. Caries prevalence in the dentition of a late Eighteenth century population. Arch Oral Biol
41:55–61.
Whittaker DK, Molleson T, Bennett RB, Edwards A, Jenkins
PR, Llewelyn JH. 1981. The prevalence and distribution of
dental caries in a Romano-British population. Arch Oral Biol
26:237–245.
American Journal of Physical Anthropology
Документ
Категория
Без категории
Просмотров
3
Размер файла
368 Кб
Теги
identifier, centuries, skeletal, 20th, dental, latex, samples, portuguese, 19th, caries, early
1/--страниц
Пожаловаться на содержимое документа