Received: 20 March 2020
Revised: 15 September 2020
Accepted: 22 September 2020
DOI: 10.1002/oa.2926
RESEARCH ARTICLE
Osteochondritis dissecans and physical activity in skeletal
remains of ancient hunter-gatherers from Southern Patagonia
Rodrigo Zúñiga Thayer1
1
Grupo de Investigación en Bioarqueología,
IMHICIHU-CONICET, Buenos Aires, Argentina
2
Facultad de Ciencias Sociales, Grupo de
Investigación en Bioarqueología, INCUAPACONICET, Universidad Nacional del Centro de
la Provincia de Buenos Aires, Quequén,
Buenos Aires, Argentina
3
Facultad de Filosofía y Letras, Grupo de
Investigación en Bioarqueología, IMHICIHUCONICET, Universidad de Buenos Aires,
Buenos Aires, Argentina
4
Facultad de Ciencias Sociales, Grupo de
Investigación en Bioarqueología, INCUAPACONICET, Universidad Nacional del Centro de
la Provincia de Buenos Aires, Olavarría,
Buenos Aires, Argentina
Correspondence
Lic. Rodrigo Zúñiga Thayer, Grupo de
Investigación en Bioarqueología, IMHICIHUCONICET, Saavedra Street No. 15, C1083ACA
Buenos Aires, Argentina.
Email: rzunigat89@gmail.com
|
Jorge Suby2
|
Leandro Luna3
| Gustavo Flensborg4
Abstract
Osteochondritis dissecans (OCD) is a joint disease characterized by the detachment or
separation of an articular cartilage fragment and subchondral bone in joint epiphyses.
It has been diagnosed in archaeological skeletons worldwide but scarcely studied in
hunter-gatherer skeletal remains. The aim of this paper is to analyse the variation of
OCD in skeletons of past populations that lived in Southern Patagonia during the
Late Holocene, which can be useful to improve our understanding about the effects
of the mechanical demands in hunter-gatherers. The overall prevalence observed in
this sample (40.5%), higher than the data reported for current populations and mostly
located in the shoulder of young and middle adult males of terrestrial and maritime
hunter-gatherers, suggests that physical activity involved in both economic strategies
would have played an important role in the development of OCD. The contact with
European colonizers does not seem to have produced differences in the prevalence
of OCD, although more dated skeletons are needed to test this hypothesis.
KEYWORDS
hunter-gatherers, OCD, paleopathology, Patagonia, physical activity
Funding information
National Agency for Science and Technology,
Argentina, Grant/Award Number: PICT
0191-2016; National Council for Science and
Technology (CONICET-Argentina)
1
|
I N T RO DU CT I O N
pathological joint diseases, also related to mechanical demands, have
been less studied. Consequently, they are rarely included in discus-
The understanding of physical activity in hunter-gatherers' health rep-
sions about stress and disease among these populations.
resents one of the major issues in bioarchaeological and paleopatho-
One of these diseases is Osteochondritis dissecans (OCD), a joint
logical research since at least the 1980s. The results mainly show
defect characterized by the detachment or separation of an articular
higher mechanical loadings, body size and sexual dimorphism in
cartilage fragment and the subchondral bone in joint epiphyses
hunter-gatherers than in agriculturalist and industrial societies,
(Schenck & Goodnight, 1996). The aetiology of the OCD has not
changes that are attributed to differences in social practices and
been completely clarified. Genetic components (Padgett, Mostosky,
mobility (e.g., Larsen & Ruff, 2011; Ruff, 2008). These investigations
Probst, Thomas, & Krecke, 1995) and ischaemia of the articular car-
also suggest that the high mobility of hunter-gatherers strongly
tilage (Carlson, Meuten, & Richardson, 1991) have been stated as
increased the development of joint diseases (Kennedy, 1989; Molnar,
possible causes. However, most authors argued that OCD is mainly
Ahlstrom, & Leden, 2011; Ponce, 2010; Weiss, Corona, &
related to repetitive microtraumas associated with physical activity
Schultz, 2012). Most of the studies to date have been carried out
(Edmonds & Polousky, 2013). Therefore, the study of OCD offers
using markers of occupational stress (MOS), like long-bone shape,
valuable insights about the impact of mechanical demands in ancient
osteoarthrosis
past populations.
(OA)
and
entheseal
Int J Osteoarchaeol. 2021;31:77–87.
changes,
whereas
other
wileyonlinelibrary.com/journal/oa
© 2020 John Wiley & Sons, Ltd.
77
78
TABLE 1
Human remains analysed and summary of joints presence
Present joints
References
Chronology
(years BP)
Sex
Age at death
(years)
Shoulder
Elbow
Wrist
Hip
Diet
R
L
R
L
R
L
R
Knee
Ankle
L
R
L
R
L
Region
Site
Santa Cruz/
Magallanes
N = 10
Rincón del Buque
Suby et al. (2009)
830 ± 42
M
MA
T
P
P
P
P
P
P
P
P
P
P
P
P
Cabo Vírgenes 17
L'Heureux, Guichón, Barberena,
and Borrero (2003)
900 ± 40
M
YA
T
P
P
P
P
P
P
P
P
P
P
P
P
Cerro Johnny
Borrero and Barberena (2006)
390 ± 60
M
YA
T
P
P
P
P
P
P
A
P
A
A
A
A
Juni Aike
Borrero and Barberena (2006)
Contact
a
M
YA
T
P
P
P
P
P
P
P
P
P
P
P
P
Orejas de Burro 1
L'Heureux and Barberena (2008)
3,565 ± 45
M
YA
Mt
P
P
P
P
P
A
A
A
A
A
A
A
Orejas de Burro 2
L'Heureux and Barberena (2008)
3,565 ± 45
M
MA
Mt
P
P
P
P
P
P
P
P
P
P
P
P
Puerto Natales 3
Prieto (1993–1994)
XIX Century
F
YA
NA
P
P
P
P
P
P
P
P
P
P
P
P
Northern Tierra del
Fuego
N = 11
Southern Tierra del
Fuego
N = 16
Punta Daniel
Suby (2014b)
1,118 ± 43
M
YA
Mt
P
P
P
P
P
P
P
P
P
P
A
A
Posesión Olimpia 2
Suby (2014b)
XIX Century
M
YA
T
P
A
P
P
P
P
P
P
P
P
A
A
Cañadón Misionero
Suby et al. (2009)
70 ± 30
M
MA
T
P
P
P
P
P
P
P
P
P
P
P
P
Chorrillos 2
Santiago, Salemme, Suby,
and Guichón (2011)
265 ± 44
M
YA
T
P
P
P
P
A
A
P
P
P
P
P
P
Lengua de Vaca
Suby (2014b)
251 ± 41
F
YA
Mt
P
P
P
P
P
P
P
P
P
P
P
P
Las Mandíbulas
Guichón, Muñoz,
and Borrero (2000)
Contact
M
YA
T
P
P
P
P
P
P
P
P
P
P
P
P
Bahía Gente Grande
Suby (2014b)
Contact
M
YA
T
P
P
P
P
P
P
P
P
P
P
P
P
Bahía Felipe 1
Suby (2014b)
1,608 ± 45
M
MA
Mt
P
P
P
P
P
P
P
P
P
P
P
P
Bahía Felipe 2
Suby (2014b)
1,608 ± 45
F
YA
Mt
A
A
P
P
A
A
A
A
P
P
A
A
La Arcillosa 2
Santiago et al. (2011)
5,208 ± 58
F
YA
T
P
P
P
P
P
P
P
P
P
P
P
P
MFM-2667
This paper
NA
M
MA
NA
P
P
P
P
P
P
P
P
P
P
P
P
Myren 1
Suby (2014b)
640 ± 20
M
YA
Mt
A
P
A
P
A
P
P
P
P
P
P
P
Puesto Pescador
Suby et al. (2009)
335 ± 35
M
YA
T
P
P
P
P
P
P
P
P
P
P
P
P
Santiago et al. (2011)
269 ± 46
M
MA
T
P
A
P
P
A
P
P
P
P
P
P
P
Kochi (2017)
Contact
F
YA
Mar
P
P
P
P
P
P
P
P
P
P
P
P
Harberton Cementerio
Suby, Zangrando,
and Piana (2011)
Contact
M
YA
Mar
P
P
P
P
P
P
P
P
P
P
A
A
Paiashauaia
Suby et al. (2011)
1,504 ± 46
F
MA
Mar
P
P
P
P
P
P
P
P
P
P
P
P
Bahía Tethis
Tessone, Guichón, Suby, and
Kozameh (2011)
NA
M
YA
Mar
P
A
P
A
P
P
P
P
P
P
P
P
Caleta Falsa 8–4
Guichón and Suby (2011)
NA
M
MA
NA
A
A
A
A
A
A
P
P
P
P
P
P
Caleta Falsa 7–2
Guichón and Suby (2011)
NA
F
YA
NA
P
A
A
A
A
A
P
P
P
P
P
P
ZÚÑIGA THAYER ET AL.
Santana 1
Acatushún
OCD was diagnosed in skeletal remains worldwide, but most of
P
A
A
P
P
P
A
P
L
P
79
P
sites (e.g., McWhirr, Viner, & Wells, 1982; Vikatou, 2012; Vikatou,
P
Hoogland, & Waters-Rist, 2017; Wells, 1974). Only a few research
P
A
A
P
P
P
P
P
P
P
P
P
P
P
A
A
P
P
A
A
R
P
P
P
A
P
P
L
R
P
the analyses are case studies of historical European archaeological
P
Knee
Ankle
ZÚÑIGA THAYER ET AL.
described this defect on hunter-gatherer skeletons, most of them
a
small
number
of
samples
P
in
(e.g., Flensborg, Martínez, González, & Bayala, 2011; Scabuzzo, 2013;
P
descriptions
Suby, Guichón, & Zangrando, 2009) or considering OCD as part of
P
P
P
P
P
P
P
P
P
P
P
P
A
A
P
A
A
A
A
P
P
A
P
P
P
L
R
P
P
L
brief
studies on osteoarthritis (e.g., Merbs, 1983). Thus, the prevalence and
Abbreviations: A, absent; F, female; L, left; M, male; MA, middle adult; Mar, maritime; Mt, mixed; NA, not available; P, present; R, right; T, terrestrial; YA, young adult.
Period that considers contact with European colonizers (after 400 years BP).
P
P
P
P
NA
YA
M
NA
This paper
MFM-2403(2)
tion with physical demands, are poorly understood.
a
P
P
P
A
P
P
P
P
A
NA
NA
YA
MA
F
M
NA
NA
This paper
This paper
MFM-796
MFM-2379
P
P
P
P
P
P
A
P
P
P
NA
NA
YA
MA
F
F
NA
NA
This paper
This paper
MFM-2670
MFM-852
P
A
P
A
P
P
P
A
P
P
Mar
Mar
MA
MA
M
F
NA
1,536 ± 46
Suby et al. (2011)
Tessone et al. (2011)
MFM-795
Shamakush Ent. 6
A
P
P
A
A
A
P
P
P
P
NA
NA
MA
MA
F
M
NA
NA
This paper
This paper
Harberton Caja 7
La Anónima
P
P
A
R
P
P
L
P
P
R
Diet
Mar
YA
M
Sex
References
Site
820 ± 40
Age at death
(years)
Chronology
(years BP)
Region
Guichón and Suby (2011)
R
L
causes of OCD in hunter-gatherer societies, and its possible associa-
Caleta Falsa 8–1
Hip
Wrist
Elbow
Shoulder
Present joints
(Continued)
TABLE 1
P
including
Southern Patagonia has been occupied since ca. 11,000 years BP
by terrestrial hunter-gatherers in the southern continental area and
Northern Tierra del Fuego and since ca. 8,000 years BP by maritime
hunter-gatherers in the south and southwest littoral of Tierra del
Fuego until recent times (Prates, Politis, & Steele, 2013). For that reason, these ancient populations offer the opportunity to study the evolution of human diseases in hunter-gatherer societies. Recent studies
suggest a high prevalence of joint diseases in skeletons from this
region, as well as possible differences in physical activity patterns
between individuals with maritime and terrestrial economies
(e.g., D'Angelo del Campo, Suby, García-Laborde, & Guichón, 2017;
Suby, 2014a). However, the impact of different activity patterns and
modes of subsistence on joint diseases, including OCD, is not fully
clarified (Suby, 2020). Therefore, the present paper aims to analyse
the variation of OCD in skeletons of hunter-gatherer populations that
lived in Southern Patagonia during the Late Holocene, which can be
useful to improve our understanding about the effects of the mechanical demands in this particular lifestyle.
2
2.1
|
M A T E R I A L S A N D M ET H O D S
|
Sample
Adult (older than 18 years of age) human skeletons recovered from
Southern Patagonia (South American territory below 50 S latitude)
were selected for this study. Skeletal remains from mission cemeteries
were not included in the present research because important differences in ways of living were suggested compared with a strict huntergatherer lifestyle (D'Angelo del Campo et al., 2017). Only skeletons
with at least 50% of well-preserved shoulder, elbow, wrist, hip, knee
and ankle joints (Table 1) were included. These joints are the most
common sites for OCD.
Sex of the skeletons was estimated recording the dimorphic
structures of the pelvis (Phenice, 1969) and the skull (Acsádi &
Nemeskéri,
1970).
Age
at
death
was
estimated
by
mor-
phological changes of the auricular surface (Lovejoy, Meindl,
Mensforth, & Barton, 1985) and the pubic symphysis (Brooks &
Suchey, 1990; Todd, 1921); the individuals were grouped as young
adults (18–34 years old), middle adults (35–49 years old) and old
adults (50 years of age or over). The sample includes 37 individuals
(Table 1; Figure 1), 25 males (67.6%) and 12 females (32.4%),
ZÚÑIGA THAYER ET AL.
80
F I G U R E 1 Location of the archaeological sites where the skeletons included in this paper were recovered [Colour figure can be viewed at
wileyonlinelibrary.com]
23 (62.2%) young adults and 14 (37.8%) middle adults. No old
absence of the articular cartilage. Therefore, and because the
adults were identified, almost absent in this region (Suby, Luna,
pathological condition does not necessarily imply the development
Aranda, & Flensborg, 2017). Ten of the skeletons are from Santa
of an inflammatory process, the term OCD has recently been con-
Cruz/Magallanes (27%), 11 from Northern Tierra del Fuego (29.7%)
sidered as incorrect in paleopathological diagnosis, and it was
and 16 from Southern Tierra del Fuego (43.3%).
suggested that it must be replaced by osteochondrosis (Thomas &
Human skeletal remains from Southern Patagonia are relatively
Johannsen, 2011; Ytrehus, Carlson, & Ekman, 2007). However,
scarce (Suby et al., 2017), so research commonly studied samples
osteochondrosis is a term also used in other syndromes, such as
assembled by isolated skeletons from different archaeological sites,
Scheuermann's syndrome and Sever's disease (Hendrix, 2005;
grouped under spatial, temporal and/or dietary patterns criteria. Most
Lowe, 1990). Thus, as the term osteochondrosis could be confusing
of the skeletons included in this study were found in simple primary
at least, in this paper we continue using the term osteochondritis
burials, except for Orejas de Burro archaeological site (L'Heureux &
dissecans, but taking into account that it might also include the
Barberena, 2008). The archaeological contextual analyses of each site
phase described as osteochondritis manifesta.
are described in the references cited in Table 1. When no reference is
In this paper, OCD was studied in those elements that correspond
included, no further archaeological data are available. Thus, although
to the joints where it was more diagnosed in current populations
small, the sample studied here includes most of the well-preserved
(i.e., shoulder, elbow, wrist, hip, knee and ankle) (Table 1). However,
skeletons known in the region.
elements of other joints, as the vertebrae and bones of hands and feet
were also studied when possible. OCD was diagnosed when a subchondral circular necrotic area or a crater depression, evidencing an
2.2
|
Methods
osteonecrotic focal area, was identified at any synovial joint
(Ortner, 2003; Vikatou, 2012; Vikatou et al., 2017; Waldron, 2009;
The development of OCD is part of a wider process named
Wells, 1974). The anatomical distribution was recorded and also
osteochondrosis, a deficiency of blood supply in the subchondral bone,
whether the necrotic portion was found in situ or it had been
followed by a necrotic process. Osteochondrosis includes three
detached. The depressions were measured using a digital calliper.
and
The prevalence of OCD was calculated by joint, individual, sex
osteochondritis dissecans. Only the last two phases are recordable in
and age at death. The possible association between OCD and dietary
skeletons, and the distinction between them is not possible due to the
pattern information based on carbon (13C/12C) and nitrogen (15N/14N)
phases:
osteochondritis
latens,
osteochondritis
manifesta
ZÚÑIGA THAYER ET AL.
81
stable isotopes (see references in Table 1) was analysed. The skeletons
soft and rounded edges, without any internal bone fragment
were grouped following three dietary classes: terrestrial, maritime and
(Figure 2). The only lesion that presents the necrotic portion in situ is
mixed. The last one was interpreted as a dietary pattern in which
located at the right scapula glenoid cavity of the skeleton from the
there is no predominance of one kind of consumed resources over the
Harberton Caja 7 site. The average size of the lesions was approxi-
other (Barberena, 2002; Borrero & Barberena, 2006; Borrero, Barbe-
mately 3 mm of diameter and between 2 and 3 mm of depth. None of
rena, Franco, Charlin, & Tykot, 2009). As some of the skeletons lack
the joints with OCD showed evidence of trauma or OA.
paleodietary data, the sample for this particular analysis was reduced
No sign of subchondral cyst or erosive lesions was identified in
to 26 individuals. Moreover, the prevalence of OCD was also
the recorded lesions, compatible with other diseases such as osteoar-
evaluated according to the location of the burial by region, taking
thritis, rheumatoid arthritis, psoriatic arthritis, gout, osteomyelitis and
into account that both terrestrial and mixed economic strategies
tuberculosis, all suggested by Vikatou et al. (2017) as part of the dif-
were mostly identified in human groups that inhabited Santa
ferential diagnosis. There was also no taphonomic evidence
Cruz/Magallanes and Northern Tierra del Fuego, whereas maritime
(i.e., ragged margin and colour contrast) observed in the identified
hunter-gatherers mainly lived in Southern Tierra del Fuego (Santiago,
foramen.
Salemme, Suby, & Guichón, 2011). Thus, in order to evaluate
Thirteen (68.4%) out of the 19 OCD were recorded in scapulae,
differences in economic strategies, skeletons from Santa Cruz/Magallanes
two of them bilateral; three lesions (15.8%) affected the first proximal
and Northern Tierra del Fuego were assumed as a group belonging
phalanx of the foot, two of them bilateral; one (5.3%) was observed in
to terrestrial/mixed hunter-gatherers, while those from Southern Tierra
the lateral condyle of the left femur, one (5.3%) in the proximal epiph-
del Fuego were inferred as maritime hunter-gatherers.
ysis of the right ulna and one (5.3%) in the right joint facet of an axis
Finally, we studied the possible association between the fre-
(Figures 2 and 3a). OCD was diagnosed in 24.2% (15/62) of the
quency of OCD and the chronology of the human remains, classified
studied joints. The shoulder was the most affected joint (Table 2), only
as pre-contact (before 400 years BP) and during contact (after
in the glenoid fossa of the scapula, nine right (69.2%) and four left
400 years BP). The differences of the frequencies related to age, sex,
(30.8%). Moreover, one lesion was recorded in the right elbow (1.6%)
economic strategies, regions and chronology were statistically tested
and another in the left knee (1.5%; Figure 3b). No lesions were
with the Fisher exact test (F; two tales, p = 0.05). Following the aim of
observed in the wrist, hip or ankle (Table 2).
this research, no other type of MOS was evaluated.
Fifteen (40.5%) out of the 37 individuals analysed presented at
least one lesion diagnosed as OCD, three of them bilateral (Table 2).
The OCD affected 14 (56%) males and one (8.3%) female (p = 0.04).
3
|
RESULTS
Concerning the age at death, OCD was diagnosed in nine young
adults (39.1%) and six middle adults (42.9%; p = 1).
OCD was recorded in 19 elements (Table 2). Most of the lesions were
Concerning the paleodietary patterns, OCD was recorded in
identified in the interarticular subchondral surface as a foramen with
seven individuals (58.3%) associated with terrestrial resources, four
TABLE 2
Individuals affected with Osteochondritis dissecans and location of the lesions
Region
Site
No. of lesions
Affected areas
Santa Cruz/Magallanes
Rincón del Buque
1
Proximal epiphysis of the right ulna
Cabo Vírgenes 17
1
Glenoid fossa of the right scapula
Juni Aike
3
First proximal phalanx of the foot (bilateral) and right
articular facet of the axis
Orejas de Burro 1
1
Glenoid fossa of the left scapula
Northern Tierra del Fuego
Southern Tierra del Fuego
Orejas de Burro 2
1
Glenoid fossa of the left scapula
Posesión Olimpia 2
1
Glenoid fossa of the right scapula
Chorrillos 2
1
Glenoid fossa of the right scapula
Lengua de Vaca
1
First proximal phalanx of the right foot
Las Mandíbulas
1
Glenoid fossa of the right scapula
Bahía Felipe 1
2
Glenoid fossa of both scapulae
MFM-2667
1
Lateral condyle of the left femur
Santana 1
1
Glenoid fossa of the right scapula
Caleta Falsa 8-1
2
Glenoid fossa of both scapulae
Harberton Caja 7
1
Glenoid fossa of the right scapula
MFM-2403(2)
1
Glenoid fossa of the right scapula
82
ZÚÑIGA THAYER ET AL.
F I G U R E 2 Osteochondritis dissecans in the skeletal remains analysed. (a) Lateral condyle of the left femur (MFM-2667); (b) glenoid fossa of
the right scapula (MFM-2403-2); (c) proximal epiphysis of the right ulna (Rincón del Buque); (d) right articular facet of the axis (Juni Aike); (e) first
proximal phalanx of the right foot (Lengua de Vaca) [Colour figure can be viewed at wileyonlinelibrary.com]
F I G U R E 3 Prevalence of Osteochondritis dissecans in the sample studied by element (a) and joint (b) [Colour figure can be viewed at
wileyonlinelibrary.com]
(57.1%) linked to a mixed diet and only one (14.3%) with maritime diet
differences. Among the 13 scapulae with OCD, four (30.8%) were
(Table 3). However, no significant differences were found in the prev-
diagnosed in skeletons from Santa Cruz/Magallanes, five (38.5%) from
alence of OCD among individuals with terrestrial and maritime diet
Northern Tierra del Fuego and four (30.8%) from Southern Tierra del
(p = 0.2). When the results are analysed by region, six individuals
Fuego (Table 2). If skeletons from Santa Cruz/Magallanes and Northern
(60%) from Santa Cruz/Magallanes presented OCD, whereas six skel-
Tierra del Fuego are assumed as terrestrial and mixed hunter-gatherers,
etons (54.5%) from Northern Tierra del Fuego and three (18.8%) from
12 of the 21 (57.1%) individuals showed OCD. On the contrary, only
Southern Patagonia were affected (Table 3), with no significant
three out of the 16 (18.8%) skeletons from Southern Tierra del Fuego,
ZÚÑIGA THAYER ET AL.
83
T A B L E 3 Number of individuals with lesions and prevalence of
OCD in the sample of skeletons from Southern Patagonia
Total
elbow (1.6%) is similar to the one recorded in athletes (Aicale,
Tarantino, & Maffulli, 2018; Patel, Yamasaki, & Brown, 2017). For
N studied
n with OCD
%
example, it affects between 2.1% (Matsuura, Suzue, Iwame, Nishio, &
37
15
40.5
Sairyo, 2014) and 3.4% (Kida et al., 2014) of elbows in baseball
players.
Sex
56
The most affected joints recorded in this paper (the shoulder, and
Male
25
14
Female
12
1
8.3
23
9
39.1
14
6
42.9
Santa Cruz/Magallanes
10
6
60
Northern Tierra del Fuego
11
6
54.5
first proximal phalanx of the foot and the axis. Although only
Southern Tierra del Fuego
16
3
18.8
described in a few clinical cases, lesions in the foot were recorded in
Age at death
Young adults (20–35)
Middle adults (35–50)
Subregion
mainly the right scapula) are not coincident with those described for
current populations. Nevertheless, this is one of the most common
bone shoulder lesions in overhead throwing athletes, like tennis
players and archers (Chu et al., 2009; Gogus & Ozturk, 2008; Hamada,
Tamai, Koguchi, Ono, & Saotome, 2005; Ishikawa et al., 1988; Wilk
et al., 2009).
Another non-typical joint for OCD recorded in this paper is the
several archaeological samples (McWhirr et al., 1982; Rodríguez-
Paleodiet
Terrestrial
12
7
58.3
Martín, 2000; Vikatou et al., 2017; Wells, 1974), with prevalence as
Mixed
7
4
57.1
high as 17.9% (McWhirr et al., 1982). Wells (1974) stated that OCD in
Maritime
7
1
14.3
this joint could be caused by both the use of shoes that reduce the
flexion during walking and microtrauma related to physical activities.
Chronology
Pre-contact
12
5
41.7
During-contact
13
6
46.2
Abbreviation: OCD, Osteochondritis dissecans.
In the same way, OCD in the axis was documented only in a few
archaeological samples (McWhirr et al., 1982; Wells, 1974), related to
repetitive microtrauma. As this lesion was scarcely described in current populations, the possible causes remain unknown.
OCD was recorded more frequently in men than in women, in the
same way that it occurs in current populations (Edmonds &
assigned to maritime economy, showed this trait. However, no
Polousky, 2013; Schenck & Goodnight, 1996). This pattern was
statistical difference between these two groups was found (p = 0.2).
suggested for all joints, as stated by many clinical studies in the knee
Finally, from the chronological point of view, five (41.7%) individuals in
(Uematsu et al., 2005), the elbow (Brownlow, O'Connor-Read, &
the pre-contact period and six (46.2%) individuals in the during-contact
Perko, 2006), the ankle (Ming, Jin, & Kanta, 2004) and the shoulder
period had OCD in at least one joint (p = 1) (Table 3).
(Debeer & Brys, 2005). However, as females are less represented, a
possible bias in the structure of the sample could explain part of the
observed differences in the present study.
4
|
DISCUSSION
Concerning age at death, middle adults showed a higher prevalence of OCD than young adults, although this trend is not statistically
OCD is a relatively common finding in skeletal human remains. How-
significant, in contrast with previous research in skeletal remains
ever, data from ancient hunter-gatherers are particularly scarce. This
(Ortner, 2003; Rogers & Waldron, 1995) and clinical samples
paper offers an overview of the prevalence of OCD in past maritime
(Takahara et al., 1999). This difference could be explained considering
and terrestrial hunter-gatherers from Southern Patagonia, useful to
that some of the diagnosed OCD in the middle adults are produced
understand the impact of these economic strategies in physical
during the adolescence and early adulthood, periods when the joints
demands.
may be more affected. The aspect of most of the lesions indicates that
All the recorded lesions are of low extension and with smooth
they could have been produced a short time before the death of the
edges, which suggests that the necrotic area was reduced and was
individuals. Most clinical studies associated OCD with epiphyseal
not recently produced. Only one lesion includes the necrotic portion,
bone growth and development, which can be persistent throughout
whereas the other cases only display the remaining crater-like struc-
adulthood (e.g., Edmonds & Polousky, 2013; Takahara et al., 1999).
tures. In current populations, the knee, the ankle and the elbow are
However, other authors reported that OCD can also begin during
the most frequently affected joints by OCD, whereas it is less com-
adulthood (Garrett, 1991).
mon in the shoulder, the cervical vertebrae and the first proximal pha-
The higher prevalence of OCD in many joints recorded in this
lanx of the foot (Edmonds & Heyworth, 2014; Edmonds &
paper compared with current data suggests that the proliferation of
Polousky, 2013). In the present research, the prevalence of OCD in
these lesions may be related to mechanical demands associated with
the knee (1.5%) is higher than those reported in clinical research
hunter-gatherer economic strategies, mainly the influence of physical
ranged between 0.01% and 0.06% (Petersen, Steinhagen, Catala-
activity involving the upper limbs (e.g., use of hunting tools). Similarly,
Lehnen, & Bruns, 2006). In contrast, the frequency of OCD in the
most of the previous studies in skeletal samples attributed OCD to
ZÚÑIGA THAYER ET AL.
84
intense physical activity (e.g., McWhirr et al., 1982; Ponce, 2010;
need to be the aim of research in large samples, as was recently
Rodríguez-Martín, 2000; Vikatou, 2012; Vikatou et al., 2017;
proposed by Suby (2020). Previous studies were carried out in this
Wells, 1974).
matter, although with small samples, showing some differences in
Lesions diagnosed as OCD were more frequent in Santa Cruz/
skeletal morphology and diseases on samples from Northern and
Magallanes and Northern Tierra del Fuego than in Southern Tierra del
Southern Tierra del Fuego. Zúñiga Thayer (2016) observed high fre-
Fuego. Moreover, OCD was more prevalent in individuals with a ter-
quencies of entheseal changes in the upper limbs on females in a
restrial and mixed diet than in skeletons with a maritime diet, although
preliminary study of a sample of 26 skeletons from Southern Tierra
no statistical differences between regions and among economic strat-
del Fuego, interpreted as evidence of rowing. Moreover, Suby and
egies were found. Anyway, it should be noted that the small size of
Guichón (2009) and Suby and Novellino (2017) identified higher tib-
the sample may have biased the statistical comparisons. On the con-
ial and femoral diaphyseal robusticity in individuals with maritime
trary, OCD similarly affected the shoulder in all regions and economic
economic strategies from Tierra del Fuego than in those with a ter-
strategies. Given that this lesion is commonly diagnosed in contempo-
restrial and mixed diet. On the contrary, Suby (2014b) stated that
rary athletes, it is possible to assume that the individuals analysed
adult individuals from the Santa Cruz/Magallanes region presented a
supported high mechanical loadings in this joint. The results reinforce
higher prevalence of Schmorl's nodes (62.5%) than the skeletons
the hypothesis about the possible influence of physical activities in
from Northern (12.5%) and Southern (0%) Tierra del Fuego.
the development of joint diseases among hunter-gatherers from
D'Angelo del Campo et al. (2017) found high frequencies of
Southern Patagonia proposed in previous research (e.g., D'Angelo del
spondylolysis in skeletons from Southern Patagonia, mostly in terres-
Campo et al., 2017; Suby, 2014a). Nevertheless, developmental
trial hunter-gatherers from the Northern Tierra del Fuego and Santa
defects related to genetic factors cannot be completely rejected as a
Cruz/Magallanes rather than in Southern Tierra del Fuego. Thus, previ-
cause of OCD, at least in some of the skeletons, because biological
ous research suggests that maritime hunter-gatherers were exposed
differences between human populations from Northern and Southern
to high mechanical demands in the limbs, whereas terrestrial hunter-
Tierra del Fuego were suggested based on cranial morphology
gatherers suffered from higher defects of the spine, as Schmorl's
(Cocilovo & Guichón, 1985-1986; González José, García-Moro,
nodes and spondylolysis.
Dahinten, & Hernández, 2002) and DNA analyses (De la Fuente
Finally, the prevalence of OCD does not seem to have changed
et al., 2015; Lalueza Fox, Pérez-Pérez, Prats, Cornudella, &
during the contact period, but as several skeletons affected by OCD
Turbón, 1997).
are not dated, this trend is only preliminary. It will be important to
Ethnographical surveys (e.g., Saletta, 2015) mentioned the fre-
increase the number of dated skeletons in the future, in order to study
quent use of bow and arrow by terrestrial hunter-gatherer men.
the possible impact of the contact on aboriginal populations more
According to the results obtained here, OCD on the shoulder of males
accurately. During-contact sample from missions and farms could
may have been produced by physical activities like archery. Most of
offer different insights about the cultural and biological changes pro-
the recorded OCD affected the right glenoid cavity, so higher loading
duced in these populations in historical times.
demands in the right shoulder could be suspected in the studied skeletons. The OCD in the shoulder of three skeletons from Southern
Tierra del Fuego could also be related to physical activities like rowing
5
|
CONC LU SIONS
and hunting.
As mentioned above, data on large samples of hunter-gatherers
The prevalence of OCD and the affected joint pattern found in
are very scarce, and for that reason, there are only few results to be
this paper suggest that physical activity and mechanical demands
compared with those found in the present research. Merbs (1983)
would have played an important role in the development of this
studied a sample of 91 Inuit skeletons and recorded OA in the glenoid
joint disease, especially in the shoulder of males. Although no
cavity of the shoulder of males (22%) and females (12%), in some
statistical differences were found between economic strategies and
cases associated with OCD in the shoulder. He attributed these high
regions, most of the diagnosed lesions affected individuals with
frequencies
contrast,
terrestrial and mixed hunter-gatherers strategies. However, these
Ponce (2010) only found one skeleton with OCD (0.6% of crude prev-
results need to be considered with caution due to the small sample
alence) in coastal populations from northern Chile, affecting only one
studied.
to
throwing
and
rowing
practices.
In
knee. Nonetheless, she suggested that coastal fishers were more
The contact between local and foreigner populations since
influenced by mechanical demands than inland agriculturalist, based
ca. 400 years BP seems not to have influenced the prevalence of
on OA and other musculoskeletal stress markers.
OCD, although more dated skeletons are needed to test this hypothe-
Previous research in Southern Patagonia (i.e., Suby, 2007; Suby
sis. Studies of OCD have been widely fulfilled in clinical and veterinary
et al., 2009) observed evidence of OA in two of the skeletons with
disciplines. As a result, a wealth of knowledge has been generated
OCD (i.e., Rincón del Buque site and Cabo Vírgenes site). However,
that can be used in the study of bioarchaeological remains. This
a more specific study of OA in these skeletons needs to be further
research could help to understand the impact of OCD in ancient
conducted, as well as studies of other MOS (e.g., entheseal changes,
hunter-gatherers and to evaluate the possible causes that produce
robusticity and bilateral asymmetry in long bones). These issues
this osteochondral defect.
ZÚÑIGA THAYER ET AL.
85
ACKNOWLEDGEMEN TS
We would like to thank Drs Luis Borrero, Mónica Salemme, Fernando
Santiago, Ernesto Piana, Francisco Zangrando, Martín Vazquez and
Ricardo Guichón for allowing access to the human remains recovered
in their archaeological research; to the authorities of Museo del Fin
del Mundo (Ushuaia, Argentina) and Instituto de la Patagonia,
Universidad de Magallanes (Punta Arenas, Chile); to three reviewers
for their comments that improved the manuscript; and to Sandra Baliño for her assistance in language revision. This paper has been
supported by the National Council for Science and Technology
(CONICET-Argentina) and Grant PICT 0191-2016 (National Agency
for Science and Technology, Argentina).
ORCID
Rodrigo Zúñiga Thayer
Jorge Suby
https://orcid.org/0000-0001-9351-2483
https://orcid.org/0000-0002-6066-4031
Leandro Luna
https://orcid.org/0000-0002-5454-5570
Gustavo Flensborg
https://orcid.org/0000-0002-7418-459X
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