Evidence of Tungiasis in Pre-Hispanic America

Ancient parasites of the genus Tunga originated in America and, during the first half of the 19th century, were transported to the Eastern Hemisphere on transatlantic voyages. Although they were first documented by Spanish chroniclers after the arrival of Columbus, little is known about their presence in pre-Hispanic America. To evaluate the antiquity of tungiasis in America, we assessed several kinds of early documentation, including written evidence and pre-Incan earthenware reproductions. We identified 17 written documents and 4 anthropomorphic figures, of which 3 originated from the Chimu culture and 1 from the Maranga culture. Tungiasis has been endemic to Peru for at least 14 centuries. We also identified a pottery fragment during this study. This fragment is the fourth representation of tungiasis in pre-Hispanic America identified and provides explicit evidence of disease endemicity in ancient Peru.

was the most organized civilization in pre-Hispanic America and was characterized by substantial technologic advances in agriculture, architecture, and pottery, which were inherited from their ancestors and conquered tribes (9). Most pre-Hispanic anthropologic evidence originates from Inca predecessors, ancient cultures of Peru that were technologically advanced and developed pottery many centuries before the collapse of the Incan civilization (10).
Although tungiasis was recognized and documented by Spanish chroniclers shortly after the arrival of Columbus in Central America in 1492 (11), the South American ancestors of the Incas distinguished this affliction from others and depicted it on clay jars, pottery, and ceramics, called huacos in Peru (12)(13)(14). Many other autochthonous diseases of ancient Peruvians have also been portrayed on anthropomorphic vessels, thus providing indirect evidence of their presence in this part of the continent (15). Most of this pottery was initially discarded by the Spanish invaders, who looted sacred places, temples, and tombs in their search for gold in the mid-16th century. However, at the turn of the century, interest in pre-Incan cultures and their legacy increased, and these anthropologic pieces represented a cornerstone for understanding the dynamics of cultures that antedated the Incas.
Our objective was to evaluate the antiquity of tungiasis in pre-Hispanic America through the assessment of different kinds of early documentation from 1 of the most advanced civilizations of pre-Hispanic America, which was in Peru. Because documentation of the tungiasis presence in Peru is scarce, we conducted an extensive retrospective search that Page 3 of 16 involved the critical appraisal and inspection of 2 main classes of materials: written evidence and earthenware representations.
During our studies, a pottery fragment was newly identified in a collection storage facility at the Amano Museum Foundation in Lima, Peru. This unique polychromic fragment is the fourth earthenware representation of early tungiasis in Peru identified to date and the only one that represents the different stages of Tunga spp. infection, which distinguishes it from previously described pre-Incan pottery.

The Search
To critically inspect written evidence and cover all available information relating to the presence of Tunga spp. in Peru, we searched for all documented names ascribed to this parasite over the past 4 centuries (16)(17)(18)(19)

Search Results
We found written evidence of tungiasis in pre-Incan or Incan times in 17 documents (7 in English, 4 in French, and 6 in Spanish) ( Table 1). The documents were 1 unique 17th-century manuscript written by the indigenous Peruvian chronicler Guaman Poma de Ayala (finalized during 1615-1616), 1 monograph, 1 bulletin, 2 doctoral theses, 5 books, and 7 journals. The timeframe in which these documents were written extends from 1615 through 1990.
As for the earthenware representations, we identified 4 anthropomorphic figures representing pre-Incan tungiasis ( Table 2). Of these 4 figures, 3 were reproduced in the written materials surveyed (1 from an unknown location and 2 from the American Museum of Natural History), and 1 was a piece of polychromic ceramic, located in the Amano Museum Foundation, which had not been previously described.
The anthropomorphic pottery shown in Figure  The anthropomorphic piece shown in Figure 4 originated from the Maranga culture (c. AD 150-650). It is a fragment that portrays a person whose right arm, upper torso, and head are broken off. The left arm and leg are decorated with black, triangle-shaped tattoos arranged in a linear distribution. Cream-colored tweezers hang from the person's chest. The person is using a stick to extract foreign bodies from a cluster of elevated lesions with central holes in the heel of the left foot. There are also 8 holes in the posterior external aspect of the sole, which are clustered and highlighted by a brick-red background. This piece was located in a storage room at the Amano Museum Foundation and, to our knowledge, has not been previously described or reproduced. It was originally found in Las Pampas, Surquillo, Lima (Figure 1, panel B).

Discussion
Tungiasis is an old disease that has been endemic to Peru for centuries and has been  (22). Unlike Tello, Ashmead documented the site at which this huaco was originally found, the Chicama Valley (this information was probably provided by the archeologist who discovered the piece). Nevertheless, Ashmead did not associate these lesions with tungiasis and instead thought they were a product of syphilis. In a letter addressed to Ashmead, Tello uses the word piquinosis to describe to the tungiasis depicted on huaco 1; unfortunately, Ashmead did not recognize this regional term (piquinosis = pique infection) used to designate tungiasis (22).  (33). Because he was interested in prehistoric syphilis and Peruvian earthenware representing diseases, Ashmead maintained correspondence with several renowned physicians from Lima, including Tello. However, Ashmead never associated these 2 huacos with tungiasis, arguing that the holes in the feet were too prominent to represent tungiasis (32). It was paleopathologist Roy L. Moodie (1880Moodie ( -1934 and then Americanist Raoul d'Harcourt (1879-1971) who later reevaluated the significance of these vessels, both concurring that the holes on the feet of these 2 huacos represent residual lesions left by nigua infections (12,23,24,26). Pachacamac, the site at which these 2 jars were located, was not part of the Chimu culture's territory (Figure 1, panel B). Because the Old Sanctuary of Pachacamac was the major place of worship of the pre-Hispanic Peruvian coast for >1,500 years (31), its temples were Page 7 of 16 visited by masses of pilgrims from the entire Andean world, who carried with them diverse offerings, including huacos, during religious rituals and ceremonies. Thus, archeological pieces from the coastal, highland and Amazon regions of Peru can be found in Pachacamac.
During our visit to the Amano Museum Foundation in 2009, we found the fragment of a huaco from Las Palmas (Figure 4) in a private collection storage room. It had originally been excavated by Yoshitaro Amano (1898-1982), a prosperous Japanese businessman who arrived in Peru in 1951 and was captivated by its history. He excavated and rescued innumerable pieces from sacked and abandoned archeological sites. Pedro Weiss (1893-1985), a Peruvian pathologist who dedicated part of his life to the study of these potteries, mentioned that there were representations of niguas in this museum in his 1980 article La Enfermedad en las Creencias de los Primitivos Americanos; however, he neither photographed nor described any huacos (29). In contrast to the evidence we have for the previously described huacos, we do not have strong evidence proving that this fragment was the one described by Weiss in his abovementioned work. Together with the first 3 vessels described here, which were also cited by Hoeppli in 1959 as early documentation of parasites in the Western Hemisphere (28), to our knowledge, this fragment is the fourth representation of Tunga spp. infection identified in pre-Hispanic American art. Furthermore, it is the only vessel that depicts different stages of tungiasis, thus representing explicit evidence of its endemicity in ancient Peru.
Along with these 4 huacos, additional evidence suggests the presence of tungiasis in pre-Incan Peru. The 2 most common names attributed to the sand flea in Peru and other countries of South America-nigua and pique-come from the Arawak and Quechua languages, respectively. Indeed, Quechua was the official language of the Incan Empire and is currently the second most commonly spoken language in Peru, after Spanish. Furthermore, the Incas named it seccec from the verb seccen, a Quechua word that means itching (16,17). Currently, it is called huchuy piqui (or huchhuy piqui, according to Lavoveria [20]) or ushtuchi piki by Amerindian communities in the Highlands.
Another aspect of pre-Incan tungiasis is documentation of the therapeutic approaches by historians, anthropologists, and physicians. For example, in his book La Médecine dans l'Ancien Pérou, d'Harcourt mentioned that Peruvian natives used a stick to remove fleas from their feet (26), similar to what is observed on our fragment. In addition, Lastres, in his compendious Page 8 of 16 Historia de la Medicina Peruana, mentioned nigua as being endemic to Peru and described the application of sweet potatoes leaves to the feet to treat infections (27).
Until now, numerous factors have impeded our understanding of the history of tungiasis in Peru. First, the sand flea has been given multiple names by populations living in parasiteendemic areas, making literature searches difficult. Nigua, pique, jigger, chigoe, puce-chique, and tchique are only a few of the many names that have been given to this burrowing flea.
Second, it has been taxonomically reclassified multiple times with different names by entomologists over the past 3 centuries (16)(17)(18)(19)34). Finally, the high rates of endemicity, along with a relatively uncomplicated clinical course, have made it a disease that is underreported and neglected among physicians in Peru (8).
Our search had some limitations. The dispersed distribution of these Peruvian anthropomorphic pieces in art museums throughout the world made it difficult to document the exact number of pottery pieces that depict tungiasis (35). An unknown number of diseaseillustrating huacos remain to be located and investigated. At the beginning of the Spanish Conquest, the conquerors looted religious places in their quest for gold, leaving behind innumerable pieces of pottery made by the Incas and their predecessors. Later, at the beginning of the 20th century, theories about the people of the Americas were propounded along with the study of pre-Hispanic cultures. As a result, sacred places, ceremonial paraphernalia, and other anthropologic pieces in the coast and the Andes were unearthed. These clay pottery pieces were deemed rarities and were highly prized by antiquity collectors. In fact, Ashmead and Tello clearly stated that a large number of Peruvian archeological pieces were highly prized on the black market in their time (36,37). Even today, substantial illicit traffic of ceramics from ancient Peru continues, which has forced the International Council of Museums to include Mochica vessels in the Red List of Latin American Cultural Objects at Risk (38).
Our photograph of the newly identified fragment depicting tungiasis provides additional evidence of tungiasis among ancient Peruvians. The knowledge of this disease in pre-Incan cultures is a valuable legacy that gives a historical insight into the endemicity of this arthropod in South America. These anthropological pieces are now dispersed among numerous museums worldwide. Their identification and analytic evaluation is critical for enhancing our Page 9 of 16 understanding of the history and effects of this flea that continues to affect Peruvians today as it did in pre-Incan times.