Evidence of Hypertrophic Osteoarthropathy in Human Skeletal Remains from Pre-Hispanic Mesoamerica

  1. Manuel Martinez-Lavin;
  2. Josefina Mansilla;
  3. Carlos Pineda;
  4. Carmen Pijoan; and
  5. Patricia Ochoa
  1. From Instituto Nacional de Cardiologa Ignacio Chavez and Institituto Nacional de Antropologa e Historia, Mexico City, Mexico. Requests for Reprints: Manuel Martnez-Lavn, MD, Rheumatology Department, Instituto Nacional de Cardiologa Ignacio Chavez, Juan Badiano #1, 14080 Mexico D.F., Mexico.

    Abstract

    Hypertrophic osteoarthropathy is one of the earliest recognized disease entities in the history of medicine. It has a peculiar periosteal proliferation distinctive from other bone diseases. In its advanced stage, it leaves an indelible mark on the skeleton. It has been recently shown that digital clubbing is accompanied by a bone remodeling process of the underlying phalanges. Thus, theoretically, this entity can be recognized in ancient human skeletal remains.

    We studied part of the collection of skeletal remains from pre-Hispanic Mesoamerica preserved at the National Museum of Anthropology of Mexico City. We examined 1000 specimens and found 2 skeletons with widespread, bilateral, symmetric periosteal proliferation of the tubular bones in addition to the bone remodeling changes of the distal phalanges. One of the specimens was from the Formative period (2000 B.C. to 100 A.D.).

    We conclude that hypertrophic osteoarthropathy can be recognized in ancient human skeletal remains and that this disease was present in Mesoamerica near the time of the original description of clubbing by Hippocrates about 2500 years ago.

    Hypertrophic osteoarthropathy is a disease entity characterized by a peculiar bulbous deformity of the digits conventionally described as “clubbing” and by periosteal proliferation of the tubular bones. Its presence usually indicates a serious internal illness, such as cyanotic heart disease, cystic fibrosis, lung cancer, or liver cirrhosis. Nevertheless, instances occur in which the syndrome is manifested without any underlying illness; these patients are classified as having primary hypertrophic osteoarthropathy [1].

    Clubbing is one of the earliest recognized abnormalities in the history of medicine; it was originally described by Hippocrates (about 450 B.C.). When roentgen rays became available as a diagnostic tool at the end of the 19th century, periostosis of the tubular bones was identified as the other key characteristic of the syndrome. Synovial effusion of the large joints is a frequent finding in such patients [1].

    The periostosis of hypertrophic osteoarthropathy has peculiar aspects that allow its differentiation from other bone diseases [2, 3]. It is a progressive process that affects mainly the tubular bones, principally the tibia and fibula. It is bilateral and symmetric. There is no involvement of the medullary cavity, the axial skeleton, or the skull. In mild cases of the disease, the periosteal apposition is limited to the diaphysis and has a monolayer configuration; in advanced stages, it thickens the cortex of the bones, imprinting a “tree bark” configuration, and thus leaves an indelible mark [4].

    Another distinctive aspect of the syndrome, which has been recently defined, is that clubbing is accompanied by remodeling changes of the underlying distal phalanges [1, 5]. These peculiar features of hypertrophic osteoarthropathy, in addition to the fact that the skeleton is the only part of the body able to withstand the passage of time, provide a unique opportunity to identify this illness in human skeletal remains.

    In pre-Hispanic Mesoamerica, death was considered a transition; therefore, persons were buried with different types of offerings, such as food, utensils, and figurines, to assist them in their journey. During exploration of the diverse ceremonial centers of Mesoamerica, a careful study of the burial sites with their skeletal remains and offerings was also done. These specimens are classified and preserved at the National Museum of Anthropology of Mexico City. This collection is an excellent source of information for the study of Mesoamerican osteopaleopathology. We examined human skeletal remains from pre-Hispanic Mesoamerica for evidence of hypertrophic osteoarthropathy.

    Methods

    The skeletal remains preserved at the physical anthropology department of the National Museum of Anthropology of Mexico City were studied. A total of 1000 specimens originating from diverse pre-Hispanic sites were examined for the following features: 1) adequate state of preservation; 2) bilateral symmetric periostosis of tubular bones that was evident on visual examination; 3) lack of involvement of the axial skeleton and the skull; and 4) remodeling of the distal phalanges. Those specimens that fulfilled such criteria had a radiographic survey including anteroposterior views of the tubular bones. The charts describing the findings during excavation of the burial sites were reviewed. For comparison, skeletons matched for gender, age range, chronology, and burial site were also studied.

    One of the specimens that had hypertrophic osteoarthropathy originated from Jaina Island. Jaina is a Mayan necropolis from the Classic period (300 to 900 A.D.) and is famous for its figurines of persons doing typical daily activities or having signs of diverse illnesses [6]. The museum's collection of figurines from Jaina was studied for evidence of digital clubbing or for any of the illnesses known to be associated with hypertrophic osteoarthropathy [1].

    Results

    Two specimens fulfilled criteria that were consistent with the diagnosis of hypertrophic osteoarthropathy.

    Specimen 1

    The bones belonged to a young woman found in burial site 23 during the 1974 exploration of Jaina. A conspicuous thickening of the tibias and fibulas with a “tree bark” configuration of their cortex was evident. A lesser degree of periostosis was found in the femora, radii, and ulnae. Only one distal phalanx was preserved; it was truncated. No alteration of the axial skeleton was noted. Radiographs showed thickening of the cortex of tubular bones due to a multilayered type of periosteal apposition (Figure 1, top). No abnormalities of the medullary cavity were noted. The periosteal changes clearly differed from the condition of the skeletons used for comparison.

    Figure 1. Radiographic periostosis. Anteroposterior views of tibias and fibulas of specimen 1 show a conspicuous thickening of the tibias with disappearance of their normal biconcave shape. Arrowheads point to the multilayered periosteal apposition. Middle. Advanced periostosis. A detailed view of the distal part of the left fibular of specimen 2 show an irregular shaggy cortex resembling tree bark (arrows). Bone changes of digital clubbing. The first distal phalanx of the foot of specimen 2 ( ) with osteolysis and with remodeling of the tuft compared with the uniform contour of the first phalanx of a foot from the same archeologic source ( ).
    View larger version:
    Figure 1. Radiographic periostosis. Anteroposterior views of tibias and fibulas of specimen 1 show a conspicuous thickening of the tibias with disappearance of their normal biconcave shape. Arrowheads point to the multilayered periosteal apposition. Middle. Advanced periostosis. A detailed view of the distal part of the left fibular of specimen 2 show an irregular shaggy cortex resembling tree bark (arrows). Bone changes of digital clubbing. The first distal phalanx of the foot of specimen 2 ( ) with osteolysis and with remodeling of the tuft compared with the uniform contour of the first phalanx of a foot from the same archeologic source ( ). Top.Bottom.rightleft

    Specimen 2

    The skeleton of a young man was found in burial site 17 of Ticoman in the central part of Mexico. It belonged to the Formative period (2000 B.C. to 100 A.D.). It had a widespread shaggy periostosis involving tibias, fibulas (Figure 1, middle), femora, radii, ulnae, and metatarsal bones. Two distal phalanges of the feet were preserved. Figure 1, bottom, shows the prominent remodeling changes consistent with digital clubbing, clearly different from the skeletons used for comparison. No alteration of the axial skeleton or the skull was noted. Radiographs showed widespread periosteal proliferation of the tubular bones, without involvement of the marrow.

    Review of the Jaina figurines did not indicate any example of digital clubbing; however, these figurines had a crude modeling of the hands. A sculpture of a man depicted massive ascites Figure 2, a gross abdominal deformity usually associated with chronic liver disease, which is a well-known cause of hypertrophic osteoarthropathy [1, 7].

    Figure 2. Figurine from Jaina depicting a man with massive ascites and with eversion of the umbilicus. Chronic liver disease is a well-known cause of hypertrophic osteoarthropathy.
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    Figure 2. Figurine from Jaina depicting a man with massive ascites and with eversion of the umbilicus. Chronic liver disease is a well-known cause of hypertrophic osteoarthropathy. Ancient Mesoamerican illness.

    Discussion

    The widespread, bilateral, symmetric periostosis of these specimens from two persons strongly suggests hypertrophic osteoarthropathy. Other causes of hyperostosis and periostitis can be ruled out [3]. An infectious disease, such as treponematosis, is unlikely on the basis of the diffuse symmetric involvement and the lack of concomitant destructive lesions of the underlying medullary bone. Melorheostosis is asymmetric and also involves the pelvis and the skull. Osteopoikilosis and osteopathia striata are accompanied by disseminated radio-opaque changes. Hypervitaminosis A and fluorosis also affect the axial skeleton. Chronic venous stasis is found in older persons, and the bone changes are limited to the lower extremities [3]. More unequivocal evidence for the diagnosis of hypertrophic osteoarthropathy was found in specimen 2, which also showed the bone remodeling process of the distal phalanges that is typical of clubbing [5]. The only preserved phalanx of specimen 1 had bone dissolution, an alteration also reported in clubbing [5]; it is not possible to ascertain whether this finding was due to postmortem decay.

    With the information gathered, we cannot define which underlying illness caused the hypertrophic osteoarthropathy in these two specimens. It has been recently determined that the shape of the periosteal apposition is not dependent on the underlying disease but rather on its duration. Moreover, primary and secondary hypertrophic osteoarthropathy may feature similar periostosis [2]. The advanced changes seen in our two specimens suggest that the persons had had the disease for a long time. Of additional interest was the Jaina figurine depicting ascites. To recognize most of the illnesses associated with hypertrophic osteoarthropathy, modern diagnostic tools are required. However, ascites is a gross abdominal deformity recognizable by visual examination.

    We are aware of no previous studies attempting to identify hypertrophic osteoarthropathy in ancient skeletal remains from any part of the world. A report exists of a prominent hyperostosis occurring in a left femur from the Huari civilization of Peru (about 1000 A.D.) [8]; unfortunately, the femur was the only tubular bone recovered so no further inferences could be made.

    Our report shows that hypertrophic osteoarthropathy can be recognized in ancient human skeletal remains and suggests that the disease was present in Mesoamerica near the time of its original description by Hippocrates.

    References

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