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External ear canal exostosis and otitis media in temporal bones of prehistoric
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paleoepidemiological study

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External ear canal exostosis and otitis media

in temporal bones of prehistoric and historic
chilean populations. A paleopathological and
paleoepidemiological study

Mario Castro, Marcos Goycoolea & Verónica Silva-Pinto

To cite this article: Mario Castro, Marcos Goycoolea & Verónica Silva-Pinto (2016): External
ear canal exostosis and otitis media in temporal bones of prehistoric and historic chilean
populations. A paleopathological and paleoepidemiological study, Acta Oto-Laryngologica, DOI:
10.1080/00016489.2016.1249949

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ACTA OTO-LARYNGOLOGICA, 2016
http://dx.doi.org/10.1080/00016489.2016.1249949

ORIGINAL ARTICLE

External ear canal exostosis and otitis media in temporal bones of prehistoric
and historic chilean populations. A paleopathological and paleoepidemiological
study
nica Silva-Pintod,e
Mario Castroa,b, Marcos Goycooleac and Vero
a
Department of Morphology, School of Medicine, Clınica-Alemana-Universidad del Desarrollo, Santiago, Chile; bDepartment of Museums,
Dibam, Santiago, Chile; cDepartment of Otolaryngology, Clınica las Condes, Santiago, Chile; dDepartment of Anthropology, National Museum
of National History, Santiago, Chile; eMax Planck Institute for Evolutionary Anthropology, Leipzig, Germany

ABSTRACT ARTICLE HISTORY

Conclusions: External ear canal exostosis is more prevalent in northern coastal groups than in the Received 3 October 2016
highlands, suggesting that ocean activities facilitate the appearance of exostosis. However, southern Accepted 6 October 2016
coastal groups exposed to colder ocean water have a lesser incidence of exostosis, possibly due to less
duration of exposure. There was a high incidence of otitis media in all groups of native population in
KEYWORDS
Chile. One coastal group had a higher incidence, presumably due to racial factors. Exostosis; otitis media; otitis
Background: This is a paleopathological and paleoepidemiological study in temporal bones which media racial factors;
assesses external ear canal exostosis and otitis media in prehistoric and historic native populations in pronicity factors
Chile.
Materials and methods: A total of 460 temporal bones were evaluated for exostosis (ex) and 542 tem-
poral bones were evaluated for otitis media (om). The study involved four groups: (1) Prehistoric
Coastal (400–1000 AD) populations in Northern Chile (Pisagua-Tiwanaku) (22 temporal bones ex; 28
om); (2) Prehistoric Highland (400–1000 AD) populations in Northern Chile (292 temporal bones ex;
334 om); (3) Pisagua-Regional Developments (coastal) in Northern Chile (1000–1450 AD) (66 temporal
bones ex; 82 om); and (4) Historic (1500–1800 AD) coastal populations in Southern Chile (80 temporal
bones ex: 18 Chonos, 62 Fuegians. 98 om: 22 Chonos, 76 Fuegians). Skulls were evaluated visually and
with an operating microscope. In addition, the otitis media group was evaluated with Temporal bone
radiology – -lateral XRays-Schuller view – to assess pneumatization as evidence of previous middle ear
disease.
Results: Prehistoric northern coastal groups had an incidence of exostosis of 15.91%, the northern
highlands group 1.37%, and the southern coastal group 1.25%. There were changes suggestive of otitis
media in: Pisagua/Tiwanaku 53.57%; Pisagua/Regional Developments 70.73%; Northern Highlands
population 47.90%; Chonos 63.64%; and Fuegian tribes 64.47%.

Introduction
External ear canal exostosis is benign bony overgrowths,
usually located in the anteroinferior and posterior bony
walls of the canal. They are attributed to irritation produced
by contact with cold water, with a resulting inflammatory
reaction of the soft tissues that would lead to osteogenic
activity [1–4].
Thus, they are common in individuals who practice water
activities such as surfing, diving, and kayaking in cold
waters [5,6]. These lesions have also been reported in
ancient populations all over the world, and have been con-
sidered a sign of aquatic activities in these societies [1,4].
Another otologic disease that has been recorded since
ancient times [7,8] is otitis media, a multi-factorial inflam-
matory process of high incidence and prevalence. Moreover,
otitis media is a disease that had significant complications –
among them mastoiditis – and a high mortality rate until
the advent of antibiotics [9]. Otitis media has also been
reported in ancient populations all over the world. Since
mastoiditis results in a diminished aereation of the mastoid
cavity, mastoid X-rays have been used to evaluate ancient
skulls in order to determine previous mastoiditis, as an indi-
cator of having had episodes of otitis media [10–12].
The present study was done in skulls of prehistoric and
historic native populations in Chile, in order to evaluate the
presence of external ear canal exostosis and of otitis media
in temporal bones.
Materials and methods
Materials
A total of 460 temporal bones were evaluated for exostosis
(ex), and 542 temporal bones were evaluated for otitis media
(om).

CONTACT Marcos V. Goycoolea mgoycoolea@clinicalascondes.cl Clinica Las Condes, Otorrinolaringologia, Lo Fontecilla 441, Las Condes, Santiago, CL
CP7591046, Chile
ß 2016 Acta Oto-Laryngologica AB (Ltd)
2 M. CASTRO ET AL.

The exostosis study involved four groups: (1) Prehistoric sclerotic) (Figure 1) were considered as secondary to having
Coastal (400–1000 AD) populations in Northern Chile had otitis media episodes (Figure 2).
(Pisagua-Tiwanaku) (22 temporal bones ex; 28 om); (2)
Prehistoric Highland (400–1000 AD) populations in
Northern Chile (292 temporal bones ex; 334 om); (3)
Results
Regional Developments (coastal) in Northern Chile Exostosis of the external ear canal
(1000–1450 AD) (66 temporal bones ex; 82 om); and (4)
Historic (1500–1800) coastal populations in Southern Chile The prehistoric coastal population in Northern Chile had a
(80 temporal bones ex – 18 Chonos, 62 Fuegians – and 98 prevalence of 15.91%, the northern highlands group 1.37%,
om – 22 Chonos, 76 Fuegians). and the southern coastal group 1.25%. Results are described
The coast of Chile is in the Pacific Ocean. Temporal in Tables 1–3.
bones in Groups 1 and 3 were located in Pisagua, on the Of the 88 temporal bones from group 1 (prehistoric
coastal group) only 14 showed exostosis (Figure 3). Most of
coast of northern Chile (19
340 S, 70
140 W). It is a natural
them concentrated in the Late Intermediate Period (AD
bay, and the sea water temperature ranges from 15–19
C.
1000–1450). The 12 exostosis from this period correspond
The area is extremely arid and provides an environment
to two unilateral and five bilateral cases (Table 1). Males
that is ideal for preservation of organic material. These indi-
showed a higher prevalence than females, 30% and 7.69%,
viduals lived in a period which fell in the Tiwanaku period
respectively. When analyzed by topography, the presence of
(400–1000 AD) (mostly agropastoral and maritime) and in
exostosis showed an inverse correlation with altitude and
the so-called Regional Developments Stage (1000–1450 AD)
geographic distance from the coast. The prehistoric highland
(mostly maritime), before the Inca Empire. Culturally,
group had statistically significant differences with both
Pisagua was a transition zone between the agrarian com-
coastal population groups (Pisagua Tiwanaku and Pisagua
munities of the Arica complex in the North and Pica in the
Regional Developments period when combined; p < .05). On
South. Pisagua was influenced and was related with the
the other hand, in the colder water group of southern Chile,
Altiplanic groups from the highlands such as Calama, which
is the origin of the temporal bones of group 2. Calama
(Highlands group) is an inland oasis. The climatic condi-
tions in the area provide an ideal environment for preserva-
tion of organic material. These individuals had agricultural
activities and developed intensive breeding of llamas and
alpacas.
The temporal bones in Group 4 are from the coastal pop-
ulations of southern Chile. They belonged to two groups:
the Chonos and the Fuegian tribes (1500–1800 AD). The
Chonos lived in tortuous channels and deep fiords with a
climate marked by a predominance of damp cloudy days
with very high rainfall throughout the year with strong west-
erly winds and cold temperatures. The sea water tempera- Figure 1. Pneumatized temporal bone.
ture ranges from 9–11
C. They lived in families which
wandered through the channels. Men hunted and women
dived for sea urchins and shellfish. The Fuegians, and
among them the Yamana (Yaghan) and Halakwulup
(Alacaluf), were also tribes that wandered through the West
Patagonian Channel region and had activities and labor divi-
sions like the Chonos. The sea water temperature in these
channels ranges from 7–9
C.

Methods
Skulls were evaluated visually and with an operating micro-
scope. In addition, the otitis media group was evaluated Figure 2. Temporal bone with poor pneumatization.
with temporal bone radiology using lateral X-rays–Schuller
view in order to assess pneumatization as evidence of previ- Table 1. Prevalence of external ear canal exostosis in temporal bones from
ous middle ear disease. In order to compare with similar prehistoric coastal populations of northern Chile.
temporal bone studies [10,11], mastoid findings were classi- External ear canal exostosis
fied according to the criteria of Tremble [13] classified as: Sites Number Male Female %
Pneumatic, diploic, mixed (pneumatic and diploic), and Pisagua/Tiwanaku 22 2/12 0/10 9.09
sclerotic. Pneumatic mastoids were considered normal Pisagua/Reg.Dev. 66 10/40 2/26 18.18
and those with decreased pneumatization (diploic mixed or Total 88 12/52 2/36 15.91
 ACTA OTO-LARYNGOLOGICA 3

Table 2. Prevalence of external ear canal exostosis in temporal bones from agriculturists who have gone through different periods of
prehistoric highland populations of northern Chile.
priority of activities in their economy. There have been pre-
External ear canal exostosis vious reports on populations in Arica; an area which is
Sites Number Male Female % located north of the sites of our study [14,15]. Arica is a
Highlands 292 4/184 0/108 1.37 richer and more fertile land that lends itself to agriculture as
well as for fishing activities. These reported observations
document the presence of exostosis in different periods of
Table 3. Prevalence of external ear canal exostosis in temporal bones from
historic coastal populations of southern Chile. time. In Chinchorro fishers, without agriculture they had a
External ear canal exostosis prevalence of 27.7% of exostosis, while in subsequent agro-
pastoralis societies they had 42.7% and, later, in agropasto-
Sites Number Male Female %
tralis and fishers they had 35.6%. The explanation for this
Chono 18 0/10 1/8 5.56
Fuegian tribes 62 0/30 0/32 0.00 occurrence is that the fisher’s population increased their
Total 80 0/40 1/40 1.25 ocean harvests to gain a surplus in order to trade with the
agricultural non-maritime groups [14,15]. Our Pisagua/
Tiwanaku group with a 9.09% prevalence coincides with a
mixed agropastoral and maritime economy related with the
Calama economy. In this case, fishing was done for con-
sumption and not for trading purposes. In the Pisagua late
intermediate period these societies became more dependent
on marine resources and their frequency increased again to
18.18%. On the other hand, the four exostosis cases found
in Calama might very well be those of coastal immigrants or
traders or the result of intermarriages that were buried in
Calama. This is possible since at that time there was a close
relationship and interchange between coastal and highlands
populations. The association of exostosis and gender is
Figure 3. Exostosis of the external ear canal. related to the northern prehistoric cultures with a division
of labour [14], with men doing most of the ocean harvest.
only one case of exostosis was found in one woman. When Contrary to the above, in our southern coastal groups
compared with the northern coastal group there is a statis- women did most of the marine food gathering through div-
tically significant difference (p < .05). ing [16]. Based solely on the ‘aquatic termal hypothesis’, one
would expect high prevalence of exostosis in these popula-
tions who dive in cold water together with harsh climatic
Otitis media study conditions all year round with strong winds and low tem-
peratures; factors that would provide an ideal stimulus for
Data obtained from the 542 temporal bone X-rays showed
exostosis formation in the ear canals. However, one has to
altered pneumatization in 296 (54.61%) (Table 4). The high-
consider time of exposure since in cold waters without pro-
est frequency of altered pneumatization was found in the
tection prolonged exposure is not feasible. In fact, a direct
Regional Developments group, with 70.7%.
relationship between time of exposure and the appearance of
When the Tiwanaku group is compared with the prehis-
exostoses has been reported [2].
toric highlands group there are no significant differences in
The proposed pathogenesis theory is that of irritation
pneumatization (p > .05). The significant differences occur
produced by the contact with cold water with a resulting
between the Regional Developments group and the inflammatory reaction of the soft tissues that would lead to
Highlands and Tiwanaku groups. osteogenic activity [2–4]. However, there might be a missing
When the combined coastal samples are analyzed by lati- link which could be specific crystals or components found
tude and habitat, Pisagua vs Chono-Fuegian samples and in water that could trigger the periosteal rupture causing a
Chono vs Fuegian samples, no differences in the prevalence localized inflammatory process with new bone formation. In
of pneumatization are observed (p > .05). We did not find histopathological studies of otitis media [17] we have
any sclerotic mastoids. reported and documented periosteal ruptures caused by the
There was one case of a mumified skull which had a cho- infectious process resulting in new bone formation. This
lesteatomatous fistula in the Highlands group. reactivity could also occur in the underlying bone of the
external ear canal. However, a periosteal rupture with subse-
Discussion quent irritation of an exposed underlying bone would be
required for a reaction to occur. Perhaps some water com-
These results confirm that, in Chile’s native populations, the ponents in inflamed skin could be the precipitating factor.
prevalence of external auditory canal exostosis is associated This hypothesis has to be tested experimentally.
with coastal groups and aquatic activities [14,15]. Chile’s Regarding otitis media, our analysis by topography
northern coast has been populated as early as 9000 years revealed a higher percentage of pneumatized temporal bones
ago by hunters, shellfish and fish gatherers, as well as in the prehistoric highlands group (52.1%) compared to the
4 M. CASTRO ET AL.

prehistoric coastal population. However, this great dissimi- Further support of racial factors has been provided by Wiet
larity is explained by the significant difference between the [19], who noted that, among the different groups of
two coastal groups. The group living in the Tiwanaku period American Indians, those with the highest frequencies of oti-
lived in the same period as the Highlands group and were tis media were the modern day Apache and Navajo Indians.
ethnically related to each other. When these two groups are These tribes belonged to the Athapaskans, the last group of
compared there are no significant differences observed in Asians to migrate through the Bering Strait. We evaluated
pneumatization. On the other hand, when the comparison racial factors in Easter Island [20], where we studied three
in prevalence of pneumatization is made between the groups of children who had all factors in common except
Highland group and the coastal Regional Development racial and familial backgrounds. In this study the point
period (who lived in different periods of time and were prevalence of otitis media was higher in children of mixed
unrelated) there are significant differences. When the com- or continental origin than in genetically pure native chil-
bined coastal samples are analyzed by latitude and habitat, dren. The high prevalence of otitis media in children of
northern coastal vs Chono-Fuegian samples and Chono vs mixed parentage and in one particular family of European
Fuegian samples, no differences in the prevalence of pneu- ancestry suggested the presence of intrinsic or pronicity fac-
matization are observed. tors that are seemingly transmissible.
Gregg et al. [10] studied temporal bones in south Dakota Two additional factors have to be mentioned. While the
Indian burials using similar radiological criteria. They populations of the Mogollon Puebloan sites of Arizona were
reported 44% of altered mastoids in Arikara burials and not related to the other groups that were reported, they had
51.8% in middle plains Woodland people (Sioux and others) an additional factor, which was living at 1850 m high. This
(Table 5). is a factor that deserves evaluation, since empiric observa-
On the other hand, using similar radiological criteria, tions are suggestive that people living at high altitudes tend
Titche et al. [11] studied skulls belonging to the late to have less otitis media. There is also a study of pneumati-
Mogollon Puebloan archeological sites in the east-central zation of temporal bones done in Inuit populations by
portion of Arizona. These populations (950–1450 AD) dis- Homoe et al. [12] at different time periods, suggestive that
appeared and are not related to the Indian inhabitants of the pneumatization of temporal bones in older Inuit popula-
the area today. They lived at 1850 m elevation on inter- tions with a lesser influence from caucasians was more pro-
mountain plateaus and surrounded by higher elevations. nounced than in the present population. Whether this
They reported 82.7% of mastoids with normal pneumatiza- reflects otitis media prevalence or higher mortality rate in
tion. These are studies of different populations done in a infancy would have to be determined.
single point in time that show significant differences Cases of cholesteatoma with fistulae have not been previ-
between different populations. It is of interest to note that, ously reported in skulls of our native populations. This case
in the Northern coastal samples, ethnically different popula- will be reported separately, because we have to obtain special
tions living in the same area in different periods of time had permissions for biopsies and CAT scans since this is a
a significantly different prevalence of mastoid disease, as mummified individual.
suggested by X-ray studies. These observations, as well as
Titche et al.’s [11] studies, are suggestive of racial factors in
otitis media. The importance of racial factors has been Disclosure statement
emphasized by Spivey and Hirschhorn [18], who reported The authors report no conflicts of interest. The authors alone are
that the prevalence of otitis media in Apache children responsible for the content and writing of the paper.
did not change when they were adopted into middle class
Foster homes, whereas the prevalence of other illnesses References
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