Mahoney, P., Johns, S.E., (due 2012). Tooth enamel defects and infant stress. In: ParkerPearson, M., Richards, M., Chamberlain, A. (Ed’s), The Beaker People: isotopes, mobility and
diet in prehistoric Britain. Prehistoric Society Monograph. Oxford: Oxbow.
TOOTH ENAMEL DEFECTS AND INFANT STRESS
Mahoney P1, Johns S1.
School of Anthropology and Conservation, University of Kent.
Disruptions to enamel forming cells during childhood development can produce hypoplastic
defects that are visible on the outer tooth surface as a localized thinning of enamel (e.g., Boyde,
1989; Goodman & Rose, 1990). These developmental defects are caused by dietary deficiencies,
infectious disease (e.g., Sarnat and Schour, 1941; Sweeney et al., 1971; May et al., 1993;
Guatelli-Steinberg, 2001 for a review), and psychological trauma (Schwartz et al., 2006). Thus,
aspects of systemic stress are often inferred from the prevalence of enamel hypoplasia in
archaeological samples of modern humans and fossil hominoids (e.g., Lacruz et al., 2001;
Guatelli-Steinberg et al., 2004).
Studies of enamel defects usually assess the outer tooth surface. Yet, developmental
defects can also be contained within enamel. These ‘sub-surface’ defects are called accentuated
growth lines. The first one, the neonatal line, marks a period of enamel disruption at birth
(Rushton, 1933) that lasts for 3 to 8 days (Mahoney, 2011). Approximately one year after birth
accentuated lines start to emerge on the outermost enamel surface of permanent first molars as a
type of hypoplasia (e.g., Mahoney, 2008). Before then, the lines in this tooth type are contained
within the enamel and are not normally visible to the naked eye. They become visible in thin
sections when viewed at magnification under a polarizing microscope where they appear as dark
bands. Because enamel also contains other markings that represent daily and near weekly
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growth increments (e.g., Risnes, 1990; Bromage, 1991) the timing of accentuated lines can be
accurately calculated. Thus, chronological patterns of infant stress can be reconstructed from
adult permanent enamel.
Previous histological studies have examined accentuated growth lines in human
deciduous (e.g., FitzGerald and Saunders, 2005) and non-human fossil and extant primate teeth
(e.g., Macho et al., 1996; Dirks et al., 2002, 2010). The aim of this study is to calculate the
timing of accentuated lines in a sample of permanent human teeth to reconstruct the chronology
of stress events in the first postnatal year. The timing and the cause of the lines will be
discussed.
Materials
Twelve erupted but unworn permanent lower first mandibular molars were selected from
human juvenile skeletons recovered from previously excavated archaeological sites in England
and Scotland. First molars rather than canines (e.g., Rose et al., 1978) were chosen because of
the permanent teeth, only first molar enamel initiates before birth and thus contains a neonatal
line. These samples are from the Beaker People project database, skeletal numbers 11, 14, 31,
36, 57, 59, 60, 75, 80, 82, 100, 105. For database skeletal numbers 60, 75, 80, and 82, the cuspal
enamel was complete before the end of the first postnatal year, thus accentuated lines were
recorded in the cuspal continuing into the lateral enamel (Fig.1).
2
Methods
The molars were previously sectioned for a study of modern human molar enamel growth
rates (Mahoney, 2008). Each molar was embedded in polyester resin to reduce the risk of
splintering while sectioning. Using a diamond-wafering blade (Buehler® IsoMet 1000) buccallingual sections were taken through the tip of the protoconid cusp enamel and tip of the enameldentin junction (EDJ).
Section obliquity was minimized following methods discussed by
Mahoney (2010). Each section was mounted on a microscope slide, lapped using a graded series
of grinding pads (Buehler®IsoMet 1000) to reveal the accentuated and other incremental lines,
polished with a 0.3mm aluminum oxide powder, placed in an ultrasonic bath to remove surface
debris, dehydrated through a series of alcohol baths, cleared (Histoclear®), and mounted with a
cover slip using a xylene-based mounting medium (DPX®). Sections were examined under a
high powered microscope (Olympus BX51) using transmitted and polarized light. Images were
captured (Olympus DP25) and analyzed (Olympus Cell D).
The distance between the neonatal line in cuspal enamel and the next accentuated line
(also called Wilson bands and accentuated Retzius lines in the literature) was measured along the
long axis of a prism (see Fig. 2; and see FitzGerald et al., 2006 for a discussion of accentuated
marking identification). This distance was divided by a local daily enamel secretion rate (DSR)
to give the amount of time elapsed in days from birth.
The procedure was repeated on
subsequent markings to establish a chronology of stress events (e.g., Macho et al., 1996). Daily
enamel secretion rates were calculated by measuring a distance corresponding to five days of
enamel secretion along a prism, which was then divided by five to yield a mean daily rate (e.g.,
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Mahoney, 2008: Fig 3-4). The procedure was repeated a minimum of six times, which allowed a
mean DSR value to be calculated. Prism lengths divided by DSRs were used to estimate the time
elapsed between accentuated markings in lateral enamel (see Mahoney et al., 2007 for a
description). The frequency of accentuated markings from birth was recalculated into monthly
intervals. The prevalence of the markings was recalculated following Waldron (1994):
Prevalence =
number of individuals with condition
x x 100 (expressed as a percentage)
total population
Results
The greatest frequency and prevalence of accentuated markings occurred in the ninth and
tenth post natal month. Table 1 shows the timing of the first accentuated line after birth. Table 2
shows the frequency of accentuated lines in months through the first postnatal year. Figure 2
shows accentuated lines in Beaker People project database skeletal number 14. Figures 3-4 show
frequency and prevalence bar charts.
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Discussion
The timing of accentuated lines was calculated in first molar enamel, thus reconstructing
the age at which stress events occurred during the first postnatal year in an archaeological sample
of modern human infants from England and Scotland.
This has provided a record of infant
health from adult permanent tooth enamel that is not normally visible to the naked eye. Thus
histological examination of permanent first molars provides an alternative methodological
approach when deciduous teeth are either not present or the enamel is too worn for this type of
analysis.
The timing of the stress events reported here differ compared to FitzGerald and coauthor
(2006), who examined accentuated markings in a sample of human deciduous teeth from an
Imperial Roman Necropolis. They reported a period of high prevalence in the second through to
the fifth postnatal month, and another period of greater prevalence beginning in the sixth
continuing through to the ninth month. In the present study, line prevalence gradually increased
from the second through to the fifth month, but the overall frequency in each month was low. In
contrast to the infants from the Necropolis, the greatest prevalence of stress events occurred in
the ninth and tenth post-natal month. Differences in the age-at-death profiles between these
studies suggest one factor that may have contributed to the difference in the timing of the stress
events. In the study by FitzGerald and coauthors (2006) most of the children died in their second
year. Here, the juveniles survived into at least their third year because permanent first molar
cervical enamel was complete (Mahoney, 2008).
Therefore, differences in life-expectancy
between the two infant populations may reflect differences in the stresses experienced during
their first year.
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The cause of the developmental defects is difficult to determine with certainty because
accentuated markings form in response to multiple stressors. With this in mind, high frequencies
of accentuated lines in non-human primate tooth enamel can correlate with a life history event,
weaning (Dirks et al., 2010), the age at which food other than breast milk is introduced into the
diet (mixed feeding) or breast feeding eventually ceases. A shift from exclusive suckling to a
mixed feeding strategy is potentially beneficial for infant brain development and growth as it
allows access to foods that are higher in protein and calories than maternal milk (Kennedy 2005)
as well as the inclusion of specific key micronutrients in the diet (Davies 2004). However, as
breast milk intake is reduced in favour of other foods there is an increased risk of exposure to
food borne pathogens and intestinal parasites (Black et al. 1981; Motarjemi et al. 1993), being
unable to digest adult food efficiently (Kennedy 2005), tooth wear (Ayers et al. 2002),
kawashiorkor (Walker 1990), and conditions related to vitamin deficiency (West et al. 1986).
This tradeoff is known as ‘the weanling’s dilema’ (Rowland et al. 1978). If the transition to a
mixed feeding strategy is poorly regulated and weaning food preparation is unhygienic, the costs
of including solid food in the diet will outweigh the benefits, and will only serve to increase
infant nutritional stress, sickness, and mortality.
In addition to high frequencies of accentuated lines, weaning age can correlate with other
dental defects. For example, increased frequencies of surface hypoplastic defects have been
associated with the age at which infant mixed feeding commences in living human populations
(Alcorn and Goodman, 1985; Goodman et al., 1987), and to textual evidence of weaning in
archaeological samples of modern humans dating to the historic periods (e.g., Moggi-Cecchi et
al., 1994) though this latter association is not always consistent (e.g., Wood, 1996). Other
6
animals show a similar relationship between surface hypoplasia and weaning (Franz-Odendaal,
2004; Dobney et al., 2005).
For the infant sample studied here, none of the children displayed indicators of stress in
the month after birth, but this was followed by a gradual increase in stress until it peaked at 10
months of age. This suggests that the timing of these tooth enamel defects might reflect, in part, a
gradual weaning process in this population starting at approximately 6-7 months, with weaning
stress peaking at 10 month. Some traditional societies begin to supplement milk feeds with
weaning foods in the second half of the first year (Kennedy 2005), and there are developmental
changes of the mandible and teeth that occur at a similar time (Humphrey 2009) making a mixed
feeding strategy possible. Stable isotope findings for Iron Age Yorkshire also suggest a weaning
strategy (Jay et al., 2008) that is comparable to the one proposed here. Infant milk intake at this
site may have been supplemented by animal and / or plant foods from a very early age because
δ15N values through the first year were not elevated to the extent expected for exclusive
breastfeeding (Jay et al., 2008: see their Fig.4; also see Herring et al., 1998 for a similar example
from the historic periods).
Thus, while we cannot exclude the possibility that the tooth enamel defects reported here
formed in response to trauma or infectious disease unrelated to diet, the timing of the accentuated
lines in this sample are consistent with a gradual process of weaning that led to dietary
deficiencies and increased illness and disease.
7
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