Rheumatic Diseases in the Ancient Americas

ORIGINAL ARTICLE
Rheumatic Diseases in the Ancient Americas
The Skeletal Manifestations of Treponematoses
Carlos Pineda, MD,* Josefina Mansilla-Lory, PhD,† Manuel Martínez-Lavín, MD,‡ Ilán Leboreiro, PhD,†
Aldo Izaguirre, MD,* and Carmen Pijoan, PhD†
Introduction: The effect of rheumatic and infectious diseases on skeletal
remains provides an important source of information for knowledge of
contemporary medicine. Few pathologic conditions have attracted so much
interest as treponematoses. One of these, syphilis, was the most feared
venereal disease throughout the civilized world until the introduction of
penicillin in the 20th century.
Objective: To describe paleopathological and ceramic illustrations of treponematoses in ancient Mexico.
Materials and Methods: Paleopathological and ceramic material examples
from the National Institute of Anthropology and History of Mexico were
reviewed.
Results: A unique paleopathologic site for treponemal diseases comprises
the La Candelaria Cave skeletal collection from northern Mexico. The cave
was used as a burial site and contained the bones of at least 83 adults and 33
subadults. Fifty-one percent of the recovered skulls possess erosions of the
vault consistent with treponematoses. Some of these exhibit the impressive
frontal bone lytic changes with irregular borders typical of caries sicca. In
addition, periostosis of the long bones was found in up to 88% of the study
sample, including 6 examples of saber-shin deformity of tibias. Radiocarbon
dating (14⫺C) of a bone retrieved from the cave ranges from 1100 to 1300
A.D. Additionally, a Pre-Hispanic ceramic figurine from the Mexican state of
Nayarit depicting a lame man with multiple nodular skin lesions that suggest
gummatous treponemal infection is described.
Conclusions: These ancient specimens reinforce the notion that treponemal
infection was present on the American Continent before European penetration of the New World. These very advanced paleopathologic lesions and
ceramic representations demonstrate the degree to which these diseases
wrought devastation before the antibiotic era. In ancient times, treponematoses were true rheumatic diseases that produced profound skeletal abnormalities marked by periosteal accretion and bone destruction.
Key Words: treponematoses, paleopathology, syphilis
(J Clin Rheumatol 2009;15: 280 –283)
H
istorical and paleopathological evidence, in addition to antiquity
and disease evolution have undoubtedly played a major role in the
knowledge of contemporary medicine. Modern manifestations of diseases do not necessarily correspond to the ancient lesion expression.
Many rheumatic and infectious diseases leave a distinctive indelible
mark on the skeleton; consequently, paleopathologists are able to track
From the *Biomedical Research Subdirection, Instituto Nacional de Rehabilitación, Mexico City, Mexico; †Department of Physical Anthropology, Instituto
Nacional de Antropología e Historia, Mexico City, Mexico; and ‡Department
of Rheumatology, Instituto Nacional de Cardiología Ignacio Chávez, Mexico
City, Mexico.
Correspondence: Carlos Pineda, MD, Biomedical Research Subdirection, Instituto
Nacional de Rehabilitación, Av. México-Xochimilco 289, Colonia Arenal de
Guadalupe, Tlalpan 14389, Mexico City, México. E-mail: carpineda@yahoo.com
Copyright © 2009 by Lippincott Williams & Wilkins
ISSN: 1076-1608/09/1506-0280
DOI: 10.1097/RHU.0b013e3181b0c848
280
the diseases that leave recognizable marks on human skeletons and
mummies excavated from archaeological sites through time.
Human history is riddled with accounts of epidemics around
the world; nevertheless, few pathologic conditions have attracted
such much interest as treponematoses, especially syphilis. Its identification with prostitution, dissolute morals, and sociocultural embarrassment has added interest to its dissemination.
Treponematoses traditionally refer to the group diseases that
are caused by Treponema species. In humans, the pathogenic treponemata are as follows: Treponema pallidum subspecies pallidum
(the cause of syphilis); Treponema pertenue (yaws); Treponema
endemicum (bejel or endemic syphilis); and Treponema carateum
(pinta). The treponemal diseases, with the exception of pinta, affect
the skeleton and can thus be studied in past civilizations.
The osseous abnormalities of treponemal diseases are discernible by the presence of periosteal reaction, the tibia remodeling
process (saber-shin deformity), and by cranial vault abnormalities,
such as oral/nasal lesions and a crater-like lesion with a central
destructive focus and multinodular bone formation on the margins,
described as caries sicca.1 These morphologic findings do not allow
for making a distinction among types of treponematoses.2 This
article describes paleopathological and ceramic evidence of treponematoses in ancient Mexico.
PALEOPATHOLOGY OF TREPONEMATOSES IN
ANCIENT MEXICO
A unique paleopathologic site for treponemal diseases is the
“La Candelaria Cave” skeletal collection.3 The cave is located in the
semidesert area of the state of Coahuila in northern Mexico. La
Candelaria Cave was explored in 1953 by a group of scientists
headed by Martínez del-Río;4 there are a number of archaeological
and paleopathological descriptions highlighting different ethnographic issues of the cave.5–15 Unfortunately, there were signs that
the cave had been previously desecrated. In ancient times, the cave
was used as burial site and contained the bones of at least 116
individuals (83 adults and 33 subadults). Mortuary bundles, type of
offerings, and stone, wood, shell, and horn tools, along with the
extraordinarily well-preserved textiles and the characteristics of the
burial rites strongly suggest that the people buried in the La Candelaria Cave antedated the Spanish penetration of Mesoamerica.6
Radiocarbon dating (14⫺C) of a bone retrieved from the cave
range from 1100 to 1300 A.D,16 and the skull in Figure 1A was
dated 1020 ⫾ 28 B.P.
The skeletal collection comprises mainly a deposit of mixed
bones and 2 intact infant mortuary bundles. Neither hand nor foot
bones were recovered. Commingling of bones was caused apparently by natural rock falls inside the cave and the destruction of
originally individual mortuary bundles by looters. The incomplete
recovery of skeletal elements is noteworthy.
Examination of skeletal specimens was accomplished by both
morphologic macroscopic analysis and plain radiography. The La
Candelaria Cave skeletal collection is composed of at least 116
individuals (83 adults and 33 subadults). Of the 116 recovered
JCR: Journal of Clinical Rheumatology • Volume 15, Number 6, September 2009
JCR: Journal of Clinical Rheumatology • Volume 15, Number 6, September 2009
FIGURE 1. Caries sicca. Two skulls from the La Candelaria
Cave. A, Shows multiple deep erosions and a large lytic lesion in the frontal and nasal region. B, The areas intervening
between erosions are thickened and nodular from deposition
of new bone giving a moth-eaten appearance (previously
published in References 7–10, and 17) (Photo DAF/INAH).
skulls, 60 (51%) displayed diverse degrees of lytic lesions of the
cranial vault and reactive bone formation on its margins. Of these,
53 (63.8%) were adults and 7 (21.2%) subadults. Seven of the adult
crania displayed impressive frontal bone destruction with irregular
borders together with rhinomaxillary involvement (Fig. 1). The
far-advanced skull erosions typical of caries sicca from the La
Candelaria Cave are unique in the literature of paleopathology.
Of the recovered tibiae (Fig. 2) 134 were complete; of these,
119 (89%) showed diverse degrees of periosteal reaction (109 adults
and 10 subadults). Six tibiae (3 adults and 3 subadults) were curved
outward as a result of periosteal reaction (saber-shin deformity). Of
the 153 femora examined, 35 (23%) were affected (33 adults and 2
subadults). Finally, of the 85 fibulae, 48 (56%) exhibited periosteal
accretion (38 adults and 10 subadults). The 2 mortuary bundles were
studied radiographically, one showed no type of skeletal lesion or
morphologic alteration, while the other displayed several bony
lesions and was submitted for examination by computerized tomography (Fig. 2). Bony involvement of this infant burial bundle was
characterized by diffuse, bilateral periostosis with tibia remodeling
(saber-shin deformities) and osteochondritis.17
CERAMIC REPRESENTATION OF TREPONEMATOSES
FROM ANCIENT MEXICO
Artistic representations in paleopathology are considered
complementary sources of knowledge and additionally as secondhand evidence, although it is considered that only a few examples
possess accurate diagnostic value. Figure 3 shows an example of a
pre-Columbian ceramic human figurine,18 that depicts a man in the
squatting position with drawn-up legs, due to knee and hip flexion;
also, multiple disseminated, nodular skin-surface lesions reminiscent of gummatous treponemal infection are also demonstrated.
DISCUSSION
Attempts to differentiate bony changes of syphilis, yaws, and
bejel based on morphologic analysis of the skeletal remains of single
specimens have failed.19,20 Furthermore, diverse approaches including: imaging,21 laboratory testing, and metabolic, histologic, microbiologic,22 and immunologic techniques23 have not been useful in
© 2009 Lippincott Williams & Wilkins
Rheumatic Diseases in the Ancient Americas
FIGURE 2. Medial view of midportion of an adult tibia from
the La Candelaria cave showing cortical thickening and periosteal reaction (Photo DAF/INAH).
FIGURE 3. Ceramic human figurine from the Mexican state
of Nayarit (200 –900 AD) depicting a lame man seated in a
low position with legs drawn up in front of the body (squatting position), with several papillomatous skin lesions reminiscent of the raspberry-like granuloma, suggesting the presence of a gummatous treponemal infection (previously
published in Reference 18) (Photo: National Museum of Anthropology of Mexico).
distinguishing between nonvenereal treponematoses and syphilis,24
although these approaches may aid in distinguishing treponematoses
as a separate disease category from other infectious diseases, such as
tuberculosis and pyogenic osteomyelitis, or from noninfectious
conditions characterized by hyperostosis or periostosis, such as
infantile cortical hyperostosis, thyroid acropachy, hypertrophic osteoarthropathy, or Paget disease.25,26 Although individuals cannot
be confidently diagnosed solely by morphologic changes, population
prevalences present different treponematosis-dependent patterns.27–32 Recently, an evidence-based approach that combines
morphologic and population-based analyses suggested that distinction among treponemal diseases is feasible.2 Syphilis as a populational phenomenon produces recognizable periosteal reaction in 2%
to 13% of affected adult populations compared with 20% to 40% of
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Pineda et al
individuals with bejel or yaws. In children with syphilis, ⬍5%
displayed osseous abnormalities compared with the 10% to 20%
frequency observed in children with bejel and yaws.33
From population-based analysis, frequency of osseous involvement in the La Candelaria Cave seems to be in excess of that
found in other treponematosis afflicted populations: ⬎50% of the
recovered sample, including ⬎20% of the subadults, was affected.
This high prevalence of bony lesions may be attributable to the
ossuary nature of the La Candelaria Cave skeletal collection and to
incomplete recovery of skeletal elements.
Morphologically-based analysis on affected bones in the La
Candelaria Cave comprise the following: skulls (cranial vaults and
nasopalatine region); femora; tibiae; and fibulae. Cranial vault findings included caries sicca. Periosteal reaction was the main appendicular osseous abnormality, including tibia remodeling (saber-shin
deformity). Bilateral expression of lesions and associated tibia-fibula
involvement in individuals could not be observed because this is an
ossuary sample. There were no hand and foot bony specimens
available for study. Several subadults (children and juvenile) bones
and 1 infant burial bundle were also affected.
The type of bony abnormalities found in the La Candelaria Cave,
along with its very high population-frequency prevalence, as well as the
osseous-involvement age distribution strongly suggest the presence of a
chronic endemic nonvenereal treponematosis in which each individual
came into direct contact with infectious skin lesions in childhood.
Socioecological conditions that could predispose the infection comprise
the following: minimal clothing, and a gatherer-hunter-fisher subsistence way of life in a hot, arid environment.31,34,35
In Colonial Mexico, syphilis was present not only as paleopathologic skeletal cases, such as the child with congenital syphilis referred
by Mansilla and Pijoán36 but also as an art subject. In the Diego Rivera
mural “The History of Mexico” (Fresco, 1929 –1935), a painting that
adorns 3 adjoining walls of the National Palace in Mexico City, Hernán
Cortéz, the Spanish conquistador, is depicted deformed as syphilitic,
malnourished, cachectic, greenish, saddle-nosed, and with markedly
swollen knees, suggesting Clutton joints.37
The origins and antiquity of syphilis have been a matter of
controversy. Recently, Harper et al38 attempted to address the
problem of the origin of treponematoses through a phylogenetic
approach. Employing molecular-genetic analyses, the authors examined a collection of pathogenic Treponema strains. Results were
paired with geographic analysis of strains. They showed that venereal syphilis-causing strains originated most recently and were more
closely related with yaws-causing strains from South America than
other nonvenereal strains. Old-World yaws-causing strains occupied
a baseline position on the phylogenetic tree construct, indicating that
these arose first in human history. This provided support for the
Columbian theory of the origin of syphilis while suggesting that the
nonsexually transmitted subspecies arose earlier in the Old World.
In conclusion, paleopathological and epidemiological evidence found in aboriginal populations from ancient Mexico, as in
those from the La Candelaria Cave, in addition to ancient ceramic
depiction from Nayarit, suggests that various expressions of nonvenereal treponematoses were present on the American Continent
before European penetration of the New World. Paleopathologic and
ceramic evidence of treponemal infection-induced very advanced
lesions demonstrate the degree of devastation wrought before the
antibiotic era. In ancient times, treponematoses comprised true
rheumatic conditions with profound skeletal involvement.
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