Palaeopathology and its relevance to understanding health and disease today: The impact of the environment on health, past and present

Abstract

This paper considers the discipline of palaeopathology, how it has developed, how it is studied, and what limitations present challenges to analysis. The study of disease has a long history and has probably most rapidly developed over the last 40-50 years with the development of methods, and particularly ancient pathogen DNA analysis. While emphasizing that palaeopathology has close synergies to evolutionary medicine, it focuses then on three ‘case studies’ that illustrate the close interaction people have had with their environments and how that has impacted their health. Upper and lower respiratory tract disease has affected sinuses and ribs, particularly in urban contexts, and tuberculosis in particular has been an ever present disease throughout thousands of years of our existence. Ancient DNA methods are now allowing us to explore how strains of the bacteria causing TB have changed through time. Vitamin D deficiency and ‘phossy jaw’ are also described, both potentially related to polluted environments, and possibly to working conditions in the industrial period. Access to UV light is emphasized as a preventative factor for rickets and where a person lives is important (latitude). The painful stigmatizing ‘phossy jaw’ appears to be a condition related to the match making industries. Finally, thoughts for the future are outlined, and two key concerns: a close consideration of ethical issues and human remains, especially with destructive analyses, and thinking more about how palaeopathological research can impact people beyond academia.

Full text

Invited Review Article: Received for publication: February 3, 2016
DOI: 10.1515/anre-2016-0001
© 2016 Polish Anthropological Society
AnthropologicAl review • Vol. 79 (1), 1–16 (2016)
Palaeopathology and its relevance
tounderstanding health and disease today:
theimpact of the environment on health,
pastand present
Charlotte Ann Roberts
Department of Archaeology, Durham University, Great Britain
AbstrAct: This paper considers the discipline of palaeopathology, how it has developed, how it is studied,
and what limitations present challenges to analysis. The study of disease has along history and has prob-
ably most rapidly developed over the last 40–50 years with the development of methods, and particularly
ancient pathogen DNA analysis. While emphasizing that palaeopathology has close synergies to evolution-
ary medicine, it focuses then on three ‘case studies’ that illustrate the close interaction people have had
with their environments and how that has impacted their health. Upper and lower respiratory tract disease
has affected sinuses and ribs, particularly in urban contexts, and tuberculosis in particular has been an ever
present disease throughout thousands of years of our existence. Ancient DNA methods are now allowing
us to explore how strains of the bacteria causing TB have changed through time. Vitamin D deciency and
‘phossy jaw’ are also described, both potentially related to polluted environments, and possibly to working
conditions in the industrial period. Access to UV light is emphasized as apreventative factor for rickets and
where aperson lives is important (latitude). The painful stigmatizing ‘phossy jaw’ appears to be acon-
dition related to the match making industries. Finally, thoughts for the future are outlined, and two key
concerns: aclose consideration of ethical issues and human remains, especially with destructive analyses,
and thinking more about how palaeopathological research can impact people beyond academia.
Key words: evolutionary medicine, respiratory disease, ‘phossy jaw’, rickets, tuberculosis, ancient DNA
Introduction
Studying archaeological human remains
(bioarchaeology) forms the primary ev-
idence for past peoples, and is a com-
ponent of the discipline of archaeology
(Roberts 2009). Collecting data from
those remains, whether they are skele-
tons or preserved bodies, provides adi-
rect window on the lives and deaths of
our ancestors; “Human remains are
the most tangible evidence for under-
Palaeopathology and the environment
Charlotte Ann Roberts
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2 Charlotte Ann Roberts
standing how people lived in the past”
(Gowland and Knüsel 2006:ix). Within
bioarchaeology, palaeopathology is akey
sub-discipline that focuses on health and
well being to appreciate how people’s
lives impacted their health (Roberts and
Manchester 2005). Within archaeology,
there is aclear trend to using archaeolo-
gy to inform the present, and bioarchae-
ology can play, and increasingly is play-
ing, a key role in this respect. Indeed,
Kintigh et al. (2014a,b) has highlighted
ve grand challenges for archaeology:
Emergence, communities, and complex-
ity; Resilience, persistence, transforma-
tion, and collapse; Movement, mobility,
and migration; Cognition, behavior, and
identity; and Human-environment inter-
actions. Bioarchaeology, and particularly
palaeopathology, can and increasingly
does contribute to all these ‘challenges’.
As they said, “these challenges show an
increasing concern with relevance to the
modern world” (p. 879). For example,
we look at communities of people via
their remains, and often we may be look-
ing at very large communities (e.g. the
10,000 skeletons excavated from the St
Mary Spital cemetery in London associat-
ed with the priory and hospital – Connell
et al. 2012); we explore resilience (adap-
tation) in the face of adversity (e.g. liv-
ing in urban situations e.g. Roberts and
Cox 2003: chapters on health in late and
post medieval Britain); increasingly we
are tracking the mobility of people in the
past (e.g. Groves et al. 2013), and their
identity (e.g. Roberts in press); nally,
we constantly and particularly consider
the data on health from our ancestors’
remains in relation to the environments
in which they resided (e.g. Roberts and
Cox 2003; Roberts 2010).
This paper specically focuses on the
last ‘challenge’, that of exploring the
interaction of people with their envi-
ronments through the lens of palaeopa-
thology. It rst considers the value of pal-
aeopathology for understanding the past,
the methods of analysis used, including
a focus on ancient biomolecules for in-
tepreting past disease, the limitations of
study, and some past and current ‘big’
projects on past health. It then focuses
on three “case studies” to explore en-
vironmental impacts on health in more
detail. It nishes with some thoughts for
the future of bioarchaeology.
Introduction
Palaeopathology
Today disease affects everybody globally,
and it is without doubt that this was the
case in the past, not least because disease
(or trauma) caused people’s death, even
if they had not suffered poor health dur-
ing their lives. Disease also affects how
we function within our social milieu, and
by extension affects society at large. If we
are ill then our lives are compromised.
Therefore, and thinking about the past,
by exploring the health challenges our
ancestors faced, we can begin to consider
the success or otherwise of past socie-
ties. Current health problems that affect
large sections of society or regions of the
world may lead to considerable ‘damage’
to normal daily life. For example, the
widespread socioeconomic impact of the
Ebola virus disease during 2014 is clear
(World Bank 2015), and ethical issues
associated with its management were
debated (Venkat et al. 2015). Unfortu-
nately, it is usually the poorer sections of
society who are burdened by health prob-
lems in general, but major epidemics in
particular (see Wilkinson and Pickett
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Palaeopathology and the environment 3
2009). They are also the ones who are the
rst to be affected by major catastrophic
‘events’, such as famines. Similarly, in
the past the plague claimed alarge pro-
portion of the English population in the
14
th
century AD, led to particular man-
agement methods, and undermined the
fabric of society (Park 1993). Therefore,
understanding the long history of disease
could be claimed to be essential for un-
derstanding the origin and evolution of
society. Indeed, there is evidence of dis-
ease in remains that stretches back to our
earliest ancestors (e.g. Trinkaus 2005).
Disease has been with us as long as the
human species has been in existence.
It is worth reviewing how our health
has changed over the thousands of years
the human species has been in existence,
but more specically the epidemiological
transitions that have faced the human
population over the last 10,000 years
(Armelagos et al. 2005). These transi-
tions affected the very “fabric” of socie-
ty and changed the way people lived and
died. The rst transition occurred about
10,000 years ago when people started to
farm animals and plants, from aprevious
life as hunter-gatherers (Roberts 2015a).
Diet became less varied, leading to de-
ciency diseases, harvests could fail, with
inevitable starvation and malnutrition,
permanent settlements were essential,
which could lead to challenges for con-
trolling food and water contamination,
population density increased because
a larger population could be supported
(and were needed to farm the land), lead-
ing to density dependent diseases such
as infections. Zoonoses became aprob-
lem for humans because of their closer
association with domesticated animals,
and there was more trade, mobility and
contact between groups, allowing diseas-
es such as infections to be more readi-
ly transmitted (see Cohen 1989 for an
overview). Palaeopathological work has
widely documented a decline in health
with this transition (e.g. Cohen and
Crane-Kramer 2007; chapters in Pinha-
si and Stock 2011; Cohen and Armela-
gos 2014, and many published papers),
although the picture is not consistent.
For example, dental caries in three Thai
populations did not increase with in-
creasing reliance on rice agriculture in
Southeast Asia, unlike in other parts of
the world where rice was not a staple
(Tayles et al. 2000). However, the picture
is complex, as this paper points out. In
a similar study, adecline in caries with
this transition was also seen at asite in
India (Inamgaon, 3700–2700 BP; Lukacs
2007). The second transition occurred with
the onset of the Industrial Revolution in
the 18
th
and 19
th
centuries. There was
dramatic population growth, much mi-
gration, intensied urbanization and in-
dustry, and commercialisation of agricul-
ture. Developments in transport affected
markets and commerce and the distribu-
tion of foodstuffs, the mobility of people,
and the consequent introduction of new
pathogens, leading to exposure of immi-
grants to new diseases (Roberts and Cox
2003: 293–358). There is evidence that
although there was economic growth
during this period, inequalities in wealth
increased, there was much poverty, and
living conditions were often poor. Spe-
cic occupations, the impact of the Little
Ice Age, poor quality housing, low stand-
ards of hygiene, exposure to extremes
of air and water pollution, under-, mal-
and over nutrition all took their toll on
health. In recent years palaeopathology
has provided awindow on the life experi-
ences of people living at that time, espe-
cially as increasing numbers of post-me-
dieval cemeteries have been excavated in
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4 Charlotte Ann Roberts
advance of modern developments. It is
clear that health was frequently compro-
mised (e.g. see Molleson and Cox 1993;
Brickley and Buteux 2006 for England).
The third transition is where the world’s
population now ‘sits’. This is character-
ized by an increase in degenerative con-
ditions such as cancer and heart disease,
and re-emergence of ‘old’ infectious dis-
eases and emergence of new ones. The
rise in infections, often now resistant to
antibiotics, is accelerated by more fre-
quent and rapid travel across the globe
by more people. The human population
has been regularly subjected to change in
their environment that has compromised
their health. Having an understanding
particularly of the impact of these transi-
tions, i.e. from a‘long view’, can help us
to appreciate who we are today and what
might be in store for us in the future. As
such, palaeopathology complements the
increasingly fast emerging discipline of
evolutionary medicine (Nesse and Wil-
liams 1994; Stearns 2012).
Palaeopathology as adiscipline
andits limitations
Palaeopathology concerns documenting
the primary evidence for the origin, evo-
lution and history of disease and trauma;
that is: evidence for health and well-be-
ing as seen in human remains (bones,
teeth and other preserved tissues of the
body), and as preserved parasite eggs. It
takes a biocultural approach and inte-
grates data collected from the remains
with the context from which the re-
mains derive. Thus, to understand why
people in the past suffered health prob-
lems, it is imperative to appreciate how
they lived in the environment (including
their housing and economy, and to what
type of climate they were exposed), what
they ate, what work they did, and who
they interacted with (through trade, for
example). These factors (‘extrinsic’ to
the body) are notwithstanding the effect
of biological sex, age, ethnicity, and ge-
netic inheritance on disease occurrence.
Indeed, many have said, “genes load the
gun and the environment (or lifestyle)
pulls the trigger”. Palaeopathology also
considers the funerary context, which
can provide information that contributes
to understanding of the place of a par-
ticular person in society at the time of
their death.
Palaeopathology also has a long his-
tory, with various parts of the world see-
ing different rates of development of this
discipline within bioarchaeology (see
Buikstra and Roberts 2012 for an over-
view). It takes amulti-disciplinary, mul-
ti-method approach and is question and/
or hypothesis driven. The research that
has been produced incorporates detailed
studies of individual skeletons or mum-
mies (osteobiography), population based
approaches considering larger numbers
of human remains, and studies of spe-
cic diseases. Most research conducted
uses amacroscopic approach where bone
formation and destruction, and dental
and alveolar bone destruction are record-
ed, their distribution pattern document-
ed, and differential diagnostic options
produced (Grauer 2008; Ortner 2012),
based on aclinical understanding (Mays
2012). There is guidance for standards
relating to data recording (Buikstra and
Ubelaker 1994; Brickley and McKinley
2004), an essential consideration if data
are to be reliably compared. Histological
(Turner-Walker and Mays 2008), imaging
(Mays 2008) and biomolecular (Brown
and Brown 2011) methods are also used
to aid diagnosis of disease, the latter –
DNA analysis – particularly developing
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Palaeopathology and the environment 5
in their use at arapid pace (e.g. see Preus
et al. 2011).
The rst report of ancient DNA sur-
vival was reported in 1985 in amummy,
DNA in bones in 1989, and the rst 1
st
pathogen aDNA in 1993 (tuberculosis).
This area of study has seen quite in-
credible developments, supplemented
by sequencing of ancient and modern
genomes, the latter enabling compari-
son with the former. The subject matter
includes conrming disease diagnosis,
helping with differential diagnosis, diag-
nosing disease in skeletons without bone
changes, exploring species or strains of
an organism, detecting carriers of disease
(not necessarily suffering at the time of
death), documenting soft tissue diseases
in skeletons, looking at susceptibility and
resistance genes, and attempting to look
at real frequency rates of disease in pop-
ulations. This method is, however, not
without its challenges (e.g. see Cooper
and Poinar 2000; Roberts and Ingham
2008); these include lack of preservation
of the DNA, contamination with ‘for-
eign’ DNA, the fact that it is adestruc-
tive, costly and time consuming method
needing specialised facilities, that not
everybody uses the same methodology
and processes for extracting DNA and
interpreting it, and nally that there ap-
pears to be many curiosity rather than
question driven studies that raise ethical
issues regarding the destructive nature
of this method using human remains.
Nevertheless, this method is providing
more nuanced data that could never be
accessed using macroscopic analysis.
Alongside all this primary evidence
collected using different methods, and
analysed and interpreted within ‘con-
text’, for some human remains there
may be contemporary documentary and
iconographic evidence that can be used in
tandem (Rawcliffe 2006; Barnett 2014).
This evidence that supplement and en-
hance our understanding of the health
and well being of our ancestors, but may
also provide us with data that is simply
not present via human remains (e.g. soft
tissue diseases such as the plague).
While the progress of palaeopatholo-
gy as a discipline is impressive, it must
not be forgotten that there are limitations
to the study of disease, as seen in human
remains and historical documentation
(Mitchell 2011). Problems with the for-
mer have been well documented in Wood
et al (1992) and will not be fully articu-
lated here. However, some key points in-
clude: is the ‘population’ health as seen
in skeletons representative of the original
living population’s health, postmortem
damage of skeletons can affect effective
recording, there are problems in adult
age and sex estimation (relevant to inter-
pretation of the impact of sex and age on
disease), there will be unidentiable sub-
groups within a population, there is an
inability to assess ‘frailty’ (susceptibility
to disease), the bone changes for disease
are limited (bone formation/destruc-
tion) and many potential diagnoses can
be made, people could die before bone,
affected and, very importantly, skeletons
with chronic (healed) evidence of disease
are, essentially, the healthy ones is rep-
resenting people who survived the acute
stages of adisease and lived long enough
for the disease to manifest itself on the
skeleton. We must be cognizant of these
limitations or our interpretations could
be very awed.
‘Big’ projects on past health
The different types of palaeopathologi-
cal studies have already been considered
above. In this section, some of the ‘big’
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6 Charlotte Ann Roberts
projects on health in the past are consid-
ered. Attempting the synthesis of large
amounts of data on health is challenging
but very rewarding, and technological ad-
vancements, such as for searching pub-
lished and grey literature and database
construction, is allowing some ambitious
projects to be carried out. We are now
moving from a predominance of studying
the individual body or skeleton, through
to more population studies at particular
archaeological sites, and regional studies
of health (e.g. in one country), and nal-
ly to much larger ‘area’ studies, such as
in Europe or the Americas.
In the early years of palaeopathology,
the focus was on studies of disease in in-
dividual skeletons or preserved bodies,
and much of the earliest work was on an-
imal remains (see Buikstra and Roberts
2012; but also Thomas 2012 in particu-
lar). As time passed an increased empha-
sis was placed on hypothesis/question
driven studies of larger populations, on
tracing the history of specic diseases,
and using methods beyond the ‘macro-
scopic’. Afocus was also on integrating
the evidence for disease into its wider
context to understand the patterns seen.
Appreciating how people lived their
lives through archaeological and (where
available) historical evidence was key to
determining why and when diseases ap-
peared in the archaeological record.
Studies in recent years have become
much more interdisciplinary and mul-
ti-method driven, making use of big da-
tasets, statistical analyses, and advanced
analytical methods, such as pathogen
aDNA analysis. People tend to work in
teams, each with a different expertise;
this includes biologists, chemists, his-
torians, archaeologists, clinicians, and
biomolecular scientists. This has en-
sured that it has been possible to do
synthetic regional and wider geograph-
ical studies of health over long time pe-
riods. In addition, the implementation
of standards for recording has helped
make datasets comparable (Buikstra and
Ubelaker 1994; Brickley and McKinley
2004). For example, the Global Histo-
ry of Health Project (European Mod-
ule): http://global.sbs.ohio-state.edu/
european_module.htm) has collected
astandardized health dataset from over
17,000 skeletons from European con-
texts of different time periods in order
to chart the history of health on Europe.
This is the rst time this has been done
for such a large sample size of skele-
tons, requiring each set of data to be
entered onto adatabase where analyses
are carried out to show trends in health.
Other synthetic studies include Benni-
ke’s (1985) study of disease in Danish
skeletons, Roberts and Cox (2003) who
focused on Britain’s health from prehis-
tory to the post-medieval period, and
Cohen and Crane-Kramer (2007) which
brought together authors of chapters on
health from different parts of the world.
This was afollow-up on the well-cited
book by Cohen and Armelagos (2013)
looking at health at the transition to
agriculture. Other studies have seen
a focus on south-east Asia (Oxenham
and Tayles (2006), the Near East (Per-
ry 2012), and the Americas (Steckel and
Rose 2002). Projects are now becoming
much more ambitious and large, and we
are learning much more nuanced infor-
mation about health in the past through
the human remains that are excavated
and analysed. Palaeopathology is also
contributing to evolutionary medicine.
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Palaeopathology and the environment 7
Three “case studies” to explore
environmental impacts on health
inmore detail
We now turn to exploring three specif-
ic examples of how palaeopathology has
helped to show how the environment in
which people resided had an impact on
their health. Upper (sinuses) and lower
(lungs) respiratory tract disease, vita-
min D deciency (rickets), and aspecif-
ic occupationally related disease called
‘phossy jaw’ are discussed.
Respiratory tract disease
(maxillary sinusitis and inammation
of the ribs)
Respiratory health can be affected by
many factors in aperson or population’s
environment, including disease, but in-
door and outdoor ‘pollution’ leading
to poor air quality has been shown to
be akey driver for poor health (http://
www.who.int/respiratory/en/). Indeed,
Hippocrates in the 5
th
century BC talked
about the importance of clean air in his
“Airs, waters and places”. The quality of
air that we breathe can affect health in
many ways. The body cells need energy
and that energy is derived from chemical
reactions for which oxygen is essential.
The respiratory system provides aroute
for oxygen to enter the body and for
carbon dioxide to be excreted (Wilson
1990:123). Particulates that can ‘pollute’
the respiratory system may be inert (car-
bon, diesel exhaust), allergens (house
dust mite, pollen), or living organisms
(bacteria, viruses), alongside gases that
are organic (e.g. sulphur dioxide) or in-
organic (e.g. tobacco smoke). Further-
more, ‘pollution’ may be naturally (e.g.
volcanic eruptions) or human induced
(e.g. car emissions). Detecting respira-
tory disease in skeletal remains relies on
observing inammatory new bone for-
mation in the maxillary sinuses and on
the visceral/internal surfaces of the ribs
(Figs 1 and 2). Of note is the general ina-
bility for the (often) subtle bone changes
in the sinuses and on the ribs to be rec-
ognised by aclinician; even aradiograph
may not detect these bone changes.
Sinusitis is described as an infection
of the paranasal sinuses, which caus-
es headache, facial pain and tenderness
(Holgate and Frew 2002:857). In pal-
aeopathology sinusitis is classied as
anon-specic reaction to poor air qual-
Fig. 1. Maxillary sinusitis in a12th–16th century
person (135) from Fishergate House, York,
England (circled).
Fig. 2. Rib lesions as seen in skeleton 187, Rob-
ert JTerry Collection, Department of Anthro-
pology, National Museum of Natural Histo-
ry, Smithsonian Institution, Washington DC
(lighter new bone formation).
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8 Charlotte Ann Roberts
ity, which may be related to pathogens,
exposure to smoke from biomass fuels
or working in occupations producing
“pollution”, or even dental disease in
the upper molar teeth spreading to the
sinus. Alimited number of studies have
focused on sinusitis in palaeopathology
but the general consensus seems to be
that sinusitis levels are at their highest
in urban populations when compared to
rural and hunter-gatherer groups (see
Roberts 2007; Sundman et al 2013). This
perhaps reects the fact that as societies
become more complex and live in settled
communities with high population den-
sity, the risk factors for sinusitis increase
(e.g. occupations exposing people to poor
air quality such as metalworking, and
living conditions involving open res or
exposure to animals inhabiting the same
space). However, as discussed above, the
causes of sinusitis are many, and focus-
ing on one cause for the changes seen in
the sinuses of skeletons would be adan-
gerous palaeopathological interpretation.
Lower respiratory tract disease may
be recognised by inammatory new
bone formation on the internal rib sur-
faces. While not described clinically, en-
largement of ribs on a radiograph may
suggest new bone formation as aresult
of lung disease (see Eyler et al. 1994).
Again, the causes for these changes are
many and may include not only exposure
to poor air quality due to environmental
“pollution”, but also chronic bronchitis,
pneumonia, lung cancer, emphysema,
and disease caused by specic pathogens
such as tuberculosis (TB). Much work
on this bone change has emanated from
the study of documented skeletal collec-
tions with known causes of death to try
to establish causation (e.g. Roberts et al.
1994; Santos and Roberts 2001). There
have been suggestions that TB more than
any other disease is likely to be the cause
for these lesions in palaeopathology (e.g.
Nicklish et al. 2012), but the lesions are
not pathognomonic (specic) for such
adiagnosis. Perhaps the most likely ex-
planation for their presence is the result
of people living in close contact with
each other at high population density in
an urban environment, and transmitting
their respiratory diseases more readily
than they could in ahunter-gatherer so-
ciety (e.g. see Lambert 2002).
However, TB as arespiratory disease
has been aconsiderable focus of research
in palaeopathology (e.g. see Roberts and
Buikstra 2003). Abacterial infection (or-
ganisms of the Mycobacterium tuberculosis
complex) that is contracted via the lungs
(inhalation) or via the gastrointestinal
tract (ingestion from infected meat and
milk of animals), it has many risk fac-
tors. These include poverty, stress, high
population density, lack of vitamin D,
working with animals and their prod-
ucts, and migration. TB affects the skel-
eton particularly in the spine (Figure 3),
hip and knee joints, but only in 3–5% of
untreated people with TB will develop
this (destructive) damage (Resnick and
Niwayama 1995). TB has a long palae-
opathological history (e.g. see Roberts
and Buikstra 2003; also Roberts 2015b)
stretching back several thousand years in
the Old World, often outdating the his-
torical texts.
This is a disease that has been
re-emerging over the last 20 or so years
(http://www.who.int/topics/tubercu-
losis/en/), and TB strains have become
resistant to antibiotic treatment. Per-
haps this is where palaeopathological
research on this disease may help us
understand this phenomenon. Since
1993 and the rst study of the DNA of
the tuberculous bacteria in an archaeo-
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Palaeopathology and the environment 9
logical skeleton (Spigelman and Lemma
1993), there has been much work on
this disease using this method. As the
method has developed and the questions
posited about the history of TB have be-
come more ambitious, we are beginning
to unravel more about the interaction of
people with environments that are con-
ducive to TB development. Ancient DNA
analysis has focused on identifying the
species (human or animal) that has af-
fected our ancestors, showing that, so
far, the majority of research suggests it
is the human form of the bacteria. How-
ever, it is in the last 10 years, or so, that
technology has been able to show with
which strains of TB people were affect-
ed. This has also been helped by the
availability of modern genomic data on
the bacteria with which to compare the
ancient data (http://genome.tbdb.org/
tbdb_sysbio/MultiHome.html). Indeed,
modern strains have been isolated in
Iron Age England (200BC – Taylor et al
2005) and in 18
th
/19
th
century Hungary
(Fletcher et al. 2003). Most recently, Bos
et al (2014) found 1000 year old Peru-
vians with TB strains closely related to
strains adapted to seals and sea lions. In
the Old World, aNatural Environmental
Research Council funded project has fo-
cused on detecting strains of TB in skele-
tons mainly from English archaeological
sites of different periods. It has become
clear from this research that there were
indeed different strains of TB in England
at varying periods of time. For exam-
ple, at one Roman site (2
nd
–3
rd
century
AD) there were two different strains of
TB, and at contemporary post-medieval
sites (19
th
century AD), there were dif-
ferent strains (Müller et al. 2014a,b).
At another post-medieval site awoman
with TB had contracted astrain that was
not common in England at that time but
was found to be more common in North
America (Bouwman et al. 2012). This
does suggest that there was aconsider-
able relationship between mobility and
the transmission of TB. The differences
in strains in people from any time period
clearly will be affected by environmental
Fig. 3. Tuberculosis in the spine of skeleton 181,
Robert J Terry Collection, Department of An-
thropology, National Museum of Natural His-
tory, Smithsonian Institution, Washington DC
(affected vertebrae circled – destruction of ver-
tebral bodies).
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10 Charlotte Ann Roberts
factors, but this continues to be fasci-
nating research in palaeopathology that
provides a deep time perspective to the
challenge of TB today.
Rickets and osteomalacia
Another environmental factor that can
be detrimental to people’s health is lack
of exposure to ultraviolet light and a con-
sequent deciency in vitamin D. This
vitamin is produced in the skin due to
the action of UV light and its presence
enables calcium and phosphorous to be
absorbed into the bones to make them
strong. Lack of vitamin D leads to rick-
ets (or osteomalacia in adults) and ‘soft’
unmineralised bones (Figures 4 and 5).
Rickets is becoming an increasing prob-
lem today for the world’s children (Hol-
ick 2007; http://www.dailymail.co.uk/
news/article-2543724/Rickets-soar-chil-
dren-stay-indoors-Number-diagnosed-
disease-quadruples-ten-years.html), and
it is exposure to sunlight that is known
to be the main source of vitamin D. Chil-
dren staying indoors for long periods of
time, or being protected excessively from
the sun by sun cream, are risk factors.
While some foods, such as oily sh, have
high levels of this vitamin, they do not
provide the amounts that are comparable
to those derived via exposure to ultravio-
let light. It has also been established that
vitamin D treatments can decrease the
risk of many diseases such as cancers and
infectious diseases (Holick ibid). Other
Fig. 4. Model of aboy with rickets displayed at the
Wellcome Trust Collections, London.
Fig. 5. Rickets in the lower limb long bones of
skeleton 75 (3–4 years old) from Coach Lane,
North Shields, Tyne and Wear, England.
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Palaeopathology and the environment 11
risk factors for this condition include the
wearing of clothing that covers most of
the skin, and staying indoors too much
(for example, in hot countries or in work
environments).
In the past polluted environments and
working long hours in factories were the
most likely risk factors. It is well known
from historical evidence that rickets in
particular increased as environments
became more polluted and populations
worked indoors, as seen in the industri-
al period in England, and skeletons from
archaeological sites have been diagnosed
with rickets (e.g. Mays et al. 2009). Par-
ticularly important, however, is where
in the world a person resides and how
much ultra violet light exposure is avail-
able. Of particular interest in this respect
are data from the History of Health in
Europe, discussed above (Brickley et al.
2009; Fig. 6). Archaeological sites with
evidence of skeletons with rickets were
most often from sites above 45 degrees
latitude where sunlight availability is
reduced.
However, one modern study has
found that allelic frequencies of apoli-
poprotein E (ApoE4) vary substantially
around the world (e.g. Hu et al. 2011).
In Southern Europe they are 10–15% and
in Northern Europe they are 40–50%.
ApoE4 is linked to higher serum vitamin
D levels, and carriers are less likely to de-
velop D deciency. Of course, UV light
exposure is less in the north and conse-
quently we would expect to nd more D
deciency there. What would be interest-
ing to nd out is whether we can nd the
ApoE4 preserved in skeletons to prove
this association.
‘Phossy jaw’
The person whose skeleton is described
here may well have also had rickets and
worked for long hours inside a factory,
and lived in an environment that was
polluted. This person was between 12
and 14 years old when they died and
were buried in aQuaker cemetery in the
north-east of England in North Shields,
next to Newcastle-upon-Tyne in the 18
th
–
19
th
centuries (Roberts et al. 2016). At
this time the region was heavily industri-
alised and historical documentation tells
us that there were a number of pollut-
ing industries operating. This child suf-
fered from many health problems, likely
including rickets, scurvy, and tuberculo-
sis, but the most striking disease evident
seen was damage to the lower jaw (Fig.
7). An inammatory reaction had led to
damage to the left side, and the rib sur-
faces and right elbow joint (Fig. 8) were
also affected. Following a consideration
of differential diagnoses, it was suggest-
ed that this person had been suffering
from ‘phossy jaw’. This was an afiction
common to those working in the white
phosphorus-loaded match making indus-
try at this time, and historical data show
a number of said industries in the re-
gion. Inhalation of phosphorus occurred
through this occupation. It was apainful
disease that affected the person’s identi-
Fig. 6. Rickets in skeletons according to latitude;
Global History of Health Project (courtesy of
Rick Steckel, Ohio State University, USA).
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12 Charlotte Ann Roberts
ty, attracted stigma (facial swelling, oral
discharge), and could lead to septicaemia
and even death. It is possible that phos-
phorus inhalation also caused the rib
lesions evident in this skeleton. Clearly
this is a very specic occupationally re-
lated disease but shows the environmen-
tal effects of the work environment.
These four examples of environment
related conditions affecting people in the
past illustrate how closely related to en-
vironmental risks populations have been
in the past, and continue to be today.
Bioarchaeology (and palaeopathology in
particular) has the potential to show the
long dureé of human-environment inter-
action. Finally we turn to some thoughts
on how palaeopathology may develop in
the future.
Some thoughts for the future
ofpalaeopathology
Palaeopathology potentially has a huge
contribution to make to understanding
health today and planning for the future
health of the world. Its synergies with
evolutionary medicine are clear; evolu-
tionary medicine is dealing with medi-
cal problems using evolutionary biology
insights, and population health today
illustrates that there are mismatches to
modern living that are leading to disease
(biology cannot keep up with cultural
change) – Nesse and Williams 1994. Pal-
aeopathology is relevant to understand-
ing health today (for example, antibiotic
resistance, re-merging/emerging disease,
change in pathogen virulence). It is also
clear that developments in methods will
continue, and more research using an-
cient DNA and other biomolecules to
detect the nuances of the past disease
experience of our ancestors will become
more frequent. It is hoped that more ‘big
picture’ approaches will be taken where
large datasets are synthesized, and am-
bitious questions will be asked of those
data, allowing scholars to think more
‘outside the box’ of the norm for palae-
opathology.
However, it is pertinent at this point
to highlight three areas of concern. One
relates to ethical issues and the increasing
amount of destructive analysis that is be-
ing done using archaeological human re-
mains. In some respects this is inevitable
Fig. 7. Mandible showing bone formation and de-
struction from a 12–14 year old person buried
in apost-medieval cemetery in North Shields,
Tyne and Wear, England, likely illustrating
‘phossy jaw’.
Fig. 8. Elbow joint showing bone formation and de-
struction from a 12–14 year old person buried
in a post-medieval cemetery in North Shields,
Tyne and Wear, England.
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Palaeopathology and the environment 13
as our methods advance and we have the
wherewithal to answer complex ques-
tions about the past. However, destruc-
tive analyses should only ever be under-
taken if the question that is being asked
cannot be answered using anon-destruc-
tive method. Human remains are anite
resource, apart from the fact that they
represent once living people, just like
us. Having access to human remains for
study is aprivilege and not aright, and
if we are to study our ancestors’ remains
we should provide a professional dedi-
cated environment, be respectful of the
remains we curate, and emphasise that
long-term curation benets science. The
second concern relates to making our
palaeopathological research more rele-
vant to the ‘here and now’ so that our
research impacts the living more. Relat-
ed to this, and an area of specic interest
to higher education institutions in the
UK, is that increasingly our research is
being scrutinized not only for its quality,
but for its direct relevance to the needs
of commerce, industry, and to the public
and voluntary sectors (see http://www.
ref.ac.uk). Palaeopathological research
has the potential to create “impact” in
the UK research assessment sense, and
we should promote this opportunity. Fi-
nally, we should try not to call skeletons
or preserved bodies samples, materials,
cases, subjects or specimens. We should
respect that they are the remains of peo-
ple whose identity varied through time
and space. We owe that respect to our
ancestors.
Corresponding author
Charlotte Ann Roberts, Department of
Archaeology, Durham University, South
Road, Durham DH1 3LE Great Britain
e-mail address:
c.a.roberts@durham.ac.uk
References
Armelagos GJ, Brown PJ, Turner B. 2005. Evo-
lutionary, historical and political econom-
ic perspectives on health and disease. Soc
Sci Med 61:755–65.
Barnett R. 2014. The sick rose. Disease and
the art of medical illustration. London:
Thames and Hudson.
Bennike P. 1985. Paleopathology of Danish
skeletons. Copenhagen, Denmark: Akad-
emisk Forlag.
Bos KI. et al. 2014. Pre-Columbian mycobac-
terial genomes reveal seals as asource of
New World human tuberculosis. Nature
514:4–497.
Bouwman AS, Kennedy SL, Muller R, Ste-
phens RH, Holst M, Caffell AC, Roberts
CA, Brown TA. 2012. Genotype of ahis-
toric strain of Mycobacterium tuberculo-
sis. Proceedings of the National Academy
of Sciences of the United States of Ameri-
ca 109(45):18511–6.
Brickley M, Buteux S. 2006. St Martin’s Un-
covered: Investigations in the Churchyard
of St. Martin’s-in-the-Bull Ring, Birming-
ham, 2001. Oxford: Oxbow Books.
Brickley M, McKinley Jeditors. 2004. Guide-
lines to the standards for recording hu-
man remains. Reading: Institute of Field
Archaeologists Paper Number 7.
Brickley M et al. 2009 Socio-culturally me-
diated disease: rickets and scurvy. Poster
presented in the symposium Reconstruct-
ing health and disease in Europe. The
early Middle Ages through the Industrial
Period. American Association of Physical
Anthropologists Annual Meeting, Chica-
go, USA.
Brown TA, Brown K 2011. Biomolecular
archaeology. An introduction. Oxford:
Wiley-Blackwell.
Buikstra JE, Roberts CA. (eds) 2012. The
global history of palaeopathology. Pio-
neers and prospects. Oxford: University
Press.
Unauthenticated
Download Date | 3/20/16 4:12 PM

14 Charlotte Ann Roberts
Buikstra J, Ubelaker D. (eds) 1994. Standards
for data collection from human skeletal
remains. Arkansas: Archeological Survey
Research Seminar Series 44.
Cohen M. 1989. Health and the rise of civili-
sation. Yale, Yale University Press.
Cohen M, Armelagos G. (eds) 2013. Palae-
opathology at the origins of agriculture.
Reprint of 1984 publication). Gainesville,
Florida: University Press of Florida.
Cohen MN, Crane-Kramer GMM. (eds) 2007.
Ancient Health: Skeletal Indicators of Ag-
ricultural and Economic Intensication.
Gainesville, Florida: Florida University
Press.
Connell B, Gray Jones A, Redfern R, Walker
D. 2012. Abioarchaeological study of the
medieval burials on the site of St Mary
Spital. Excavations at Spitalelds Market,
London E1, 1991–2007.London: Museum
of London Archaeology Monograph 60.
Cooper A, Poinar H. 2000. Ancient DNA. Do
it right or not at all. Science 289:1139.
Eyler WR, Monsein LH, Beute GH, Tilley B,
Schultz LR, Schmitt WGH. 1996. Rib en-
largement in patients with chronic pleural
disease. Am JRadiol 167:921–6.
Fletcher HA, Donoghue HD, Holton J, Pap
I, Spigelman M. 2003. Widespread oc-
currence of Mycobacterium tuberculosis
DNA from 18th–19th century Hungari-
ans. Am JPhys Anthropol 120:144–52.
Gowland R, Knüsel C editors. 2006. Social
archaeology of funerary remains. Oxford:
Oxbow Books.
Grauer AL. 2008. Macroscopic analysis and
data collection in palaeopathology. In: R
Pinhasi, S Mays, editors. Advances in hu-
man palaeopathology. Chichester: Wiley.
57–76.
Groves SE, Roberts CA, Lucy S, Pearson G,
Gröcke DR, Nowell G, Macpherson CG,
Young G. 2013. Mobility histories of
7th–9th century AD people buried at Ear-
ly Medieval Bamburgh, Northumberland,
England. Am JPhys Anthropol 151:462–
76.
Holgate ST, Frew A. 2002. Respiratory dis-
ease. In: P Kumar, M Clark editors. Kumar
and Clark Clinical medicine. 5th edition.
Edinburgh: WB Saunders. 833–955.
Holick MF. 2007 .Vitamin D Deciency. New
England JMedicine 357:266–81.
Hu P, Qin YH, Jing CX, Lu L, Hu B, Du PF.
2011. Does the geographical gradient of
ApoE4 allele exist in China? A systemic
comparison among multiple Chinese pop-
ulations. Mol Biol Rep 38:489–94.
Kintigh KW, Altschul JH, Beaudry MC, Dren-
nan RD, Kinzig AP, Kohler TA, Limp WF,
Maschner HDG, Muchener WK, Pauketat
TR, Peregrone P, Sabloff JA, Wilkinson
TJ, Wright HT, Zeder MA. 2014a Grand
challenges for archaeology. Proc National
Academy of Sciences 111:879–80.
Kintigh KW, Altschul JH, Beaudry MC, Dren-
nan RD, Kinzig AP, Kohler TA, Limp WF,
Maschner HDG, Muchener WK, Pauketat
TR, Peregrone P, Sabloff JA, Wilkinson
TJ, Wright HT, Zeder MA. 2014a. Grand
challenges for archaeology. 2014b Grand
challenges for archaeology. American An-
tiquity 79:5–24.
Lambert P. 2002. Rib lesions in aprehistoric
Puebloan sample from Southwestern Col-
orado. Am JPhys Anthropol 117:281–92.
Lukacs JR. 2007. Climate, subsistence and
health in prehistoric India. The biological
impact of a short-term subsistence shift.
In: MN Cohen, GMM Crane-Kramer, ed-
itors. Ancient Health: Skeletal Indicators
of Agricultural and Economic Intensica-
tion. Gainesville, Florida: University Press
of Florida. 237–49.
Mays S. 2008. Radiography and allied tech-
niques in the palaeopathology of skeletal
remains. In R Pinhasi, S Mays, editors.
Advances in human palaeopathology.
Chichester: Wiley. 77–100.
Mays S. 2012. The relationship between pal-
aeopathology and the clinical sciences. In:
AL Grauer, editor. Acompanion to paleo-
pathology. Cambridge: University Press.
285–309.
Mays M, Brickley M, Ives R. 2009. Growth
and vitamin D deciency in apopulation
from 19th century Birmingham, England.
Int JOsteoarchaeol 19:406–15.
Unauthenticated
Download Date | 3/20/16 4:12 PM

Palaeopathology and the environment 15
Mitchell PD. 2011. Retrospective diagnosis
and the use of historical texts for inves-
tigating disease in the past. Int JPaleop-
athol 1:81–8.
Molleson T, Cox M. 1993. The Spitalelds
Project. Volume 2: The Anthropology: The
Middling Sort. York: Council for British
Archaeology Research Report 86.
Müller R, Roberts CA, Brown T. 2014a. Bio-
molecular identication of ancient Myco-
bacterium tuberculosis complex DNA in
human remains from Britain and Con-
tinental Europe. Am J Phys Anthropol
153:178–89.
Müller R, Roberts CA, Brown T. 2014b. Gen-
otyping of ancient Mycobacterium tuber-
culosis strains reveals historic genetic di-
versity. Proceedings of the Royal Society
B: Biological Sciences 281(1781): 2013–
3236.
Nesse RM, Williams GC. 1994. Why we get
sick. The new science of Darwinian medi-
cine. New York: Vintage Books.
Nicklish N, Maixner F, Ganslmeier R, Fried-
erich S, Dresely V, Meller H, Zink A, Alt
KW. 2012. Rib lesions in skeletons from
early Neolithic sites in central Germany:
on the trail of tuberculosis at the on-
set of agriculture. Am J Phys Anthropol
149:391–404.
Oxenham M, Tayles N editors. 2006. Bioar-
chaeology of Southeast Asia. Cambridge:
University Press.
Park K. 1993. Black death. In: K Kiple, editor.
The Cambridge world history of human
disease. Cambridge: University Press.
612–15.
Perry MA. 2012. Bioarchaeology and Behav-
ior: The People of the Ancient Near East
(Bioarchaeological Interpretations of the
Human Past: Local, Regional, and Glob-
al). Gainesville, Florida: University Press
of Florida.
Pinhasi R, Stock JT editors. 2011. Human Bi-
oarchaeology of the transition to agricul-
ture. Chichester: Wiley-Blackwell.
Preus HR, Marvik OJ, Selvig KA, Bennike P.
2011. Ancient bacterial DNA (aDNA) in
dental calculus from archaeological hu-
man remains. JArchaeol Sci 38:1827–31.
Ortner DJ. 2012. Differential diagnosis and
issues in disease classication. In: AL
Grauer, editor. A companion to paleop-
athology. Cambridge: University Press.
250–267.
Rawcliffe C. 2006. Leprosy in medieval Eng-
land. Woodbridge: Boydell Press.
Resnick D, Niwayama G. 1995. Osteomyeli-
tis, septic arthritis and soft tissue infec-
tion: orgnaisms. In: D Resnick, editor.
Diagnosis of bone and joint disorders.
3rd edition. London: WB Saunders. 2448–
558.
Roberts CA, Caffell A, Filipek KL, Gowland
R, Jakob T. 2016. Til Poison Phosphorous
Brought them Death’: Apotentially occu-
pationally-related disease in apost-medi-
eval skeleton from northeast England. Int
JPaleopathol 13:39–48.
Roberts CA. 2007. A bioarcheological study
of maxillary sinusitis. Am J Phys An-
thropol 133:792–807.
Roberts CA. 2010. Adaptation of populations
to changing environments: Bioarchaeo-
logical perspectives on health for the past,
present and future. Bulletins et Mémoires
de la Société d’Anthropologie de Paris
22:38–46.
Roberts CA. 2009. Human remains in archae-
ology: ahandbook. York: Council for Brit-
ish Archaeology.
Roberts CA. 2015a. What did agriculture do
for us? The bioarchaeology of health and
diet. In: G Barker, C Goucher, editors.
The Cambridge World History. Volume 2:
Aworld with agriculture, 12,000 BCE–500
CE. Cambridge: University Press. 93–123.
Roberts CA. 2015b. Old World tuberculosis:
evidence from human remains with are-
view of current research and future pros-
pects. Tuberculosis 95: S117–21.
Roberts CA, Buikstra JE. 2003. The bioar-
cheology of tuberculosis: aglobal view on
are-emerging disease. Gainesville, Flori-
da: University Press of Florida.
Unauthenticated
Download Date | 3/20/16 4:12 PM

16 Charlotte Ann Roberts
Roberts CA, Cox M. 2003. Health and disease
in Britain: prehistory to the present day.
Gloucester; Sutton Publishing.
Roberts C, Manchester K. 2005. The archae-
ology of disease. 3rd edition. Stroud: Sut-
ton Publishing.
Roberts CA, Ingham S. 2008. Using ancient
DNA analysis in palaeopathology: acriti-
cal analysis of published papers with rec-
ommendations for future work. Int JOs-
teoarchaeol 18:600–13.
Roberts C, Lucy D, Manchester K. 1994. In-
ammatory lesions of ribs: an analysis of
the Terry Collection. Am JPhys Anthropol
95:169–82.
Santos AL, Roberts CA. 2001. A picture of
tuberculosis in young Portuguese people
in the early 20th century. Am JPhys An-
thropol 115:38–49.
Spigelman M, Lemma E. 1993. The use of the
polymerase chain reaction (PCR) to detect
Mycobacterium tuberculosis in ancient
skeletons. Int JOsteoarchaeol 3:137–43.
Stearns S. 2012. Evolutionary medicine: its
scope, interest and potential. Proceedings
of the Royal Society B 279:4305–4321.
Steckel RH, Rose JC editors. 2002. The back-
bone of history. Health and nutrition in
the Western Hemisphere. Cambridge:
University Press.
Sundman EA, Kjellström A. 2013. Signs of Si-
nusitis in Times of Urbanization in Viking
Age-Early Medieval Sweden. J Archaeol
Sci 40:4457–65.
Tayles N, Domett K, Nelsen K. 2000. Agricul-
ture and dental caries? The case of rice in
prehistoric Southeast Asia. World Archae-
olology 32:68–83.
Taylor GM, Young DB, Mays S. 2005. Geno-
typic analysis of the earliest known pre-
historic case of tuberculosis in Britain.
JClin Microbiol 43:2236–40.
Thomas R. 2012. Nonhuman paleopathology.
In: JE Buikstra, CA Roberts, editors. The
global history of palaeopathology. Pio-
neers and prospects. Oxford: University
Press. 652–64.
Trinkaus E. 2005. Pathology and the posture
of the La Chapelle-aux-Saints Neandertal.
American J Physical Anthropology 67:19–
41.
Turner-Walker G, Mays S. 2008. Histological
studies of ancient bone. In: R Pinhasi, S
Mays, editors. Advances in human palaeo-
pathology. Chichester: Wiley. 121–46.
Venkat A, Asher SL, Wolf L, Geiderman JM et
al. 2015. Ethical Issues in the Response
to Ebola Virus Disease in United States
Emergency Departments: A Position
Paper of the American College of Emer-
gency Physicians, the Emergency Nurses
Association, and the Society for Academic
Emergency Medicine. Academic Emergen-
cy Medicine 22:605–615.
Wilkinson R, Pickett K. 2009. The spirit level.
Why equality is better for everyone. Lon-
don: Penguin Books.
Wilson KJW. 1990. Ross and Wilson Anatomy
and Physiology in health and illness. Ed-
inburgh: Churchill Livingstone.
Wood JW, Milner GR, Harpending HC, Weiss
KM. 1992. The osteological paradox.
Problems of inferring health from skeletal
samples. Curr Anthropol 33:343–70.
World Bank. 2015. The Socio-Economic Im-
pacts of Ebola in Liberia. Results from
a High Frequency Cell Phone Survey
Round 5. April 15, 2015. World Bank
Group.
Unauthenticated
Download Date | 3/20/16 4:12 PM