Assessing the Parasitic Burden in a Late Antique Florentine Emergency Burial Site.

Excavation (2008-2014) carried out under the Uffizi Gallery (Florence, Italy) led to the discovery of 75 individuals, mostly buried in multiple graves. Based on Roman minted coins, the graves were preliminarily dated between the second half of the 4th and the beginning of the 5th centuries CE. Taphonomy showed that this was an emergency burial site associated with a catastrophic event, possibly an epidemic of unknown etiology with high mortality rates. In this perspective, paleoparasitological investigations were performed on 18 individuals exhumed from 9 multiple graves to assess the burden of gastrointestinal parasitism. Five out of eighteen individuals (27.7%) tested positive for ascarid-type remains; these are considered as "decorticated" Ascaris eggs, which have lost their outer mammillated coat. Roundworms (genus Ascaris) commonly infest human populations under dire sanitary conditions. Archaeological and historical evidence indicates that Florentia suffered a period of economic crisis between the end of 4th and the beginning of the 5th centuries CE, and that the aqueduct was severely damaged at the beginning of the 4th century CE, possibly during the siege of the Goths (406 CE). It is more than plausible that the epidemic, possibly coupled with the disruption of the aqueduct, deeply affected the living conditions of these individuals. A 27.7% frequency suggests that ascariasis was widespread in this population. This investigation exemplifies how paleoparasitological information can be retrieved from the analysis of sediments sampled in cemeteries, thus allowing a better assessment of the varying frequency of parasitic infections among ancient populations.

Intestinal Parasites in an Ottoman Period Latrine from Acre (Israel) Dating to the Early 1800s CE.

The aim of this study is to determine the species of parasites that affected the inhabitants of the city of Acre on the coast of the eastern Mediterranean during the Ottoman Period. This is the first archaeological study of parasites in the Ottoman Empire. We analysed sediment from a latrine dating to the early 1800s for the presence of helminth eggs and protozoan parasites which caused dysentery. The samples were examined using light microscopy and enzyme-linked immunosorbent assay (ELISA) kits. We found evidence for roundworm (Ascaris lumbricoides), whipworm (Trichuris trichiura), fish tapeworm (Dibothriocephalus sp.), Taenia tapeworm (Taenia sp.), lancet liver fluke (Dicrocoelium dendriticum), and the protozoa Giardia duodenalis and Entamoeba histolytica. The parasite taxa recovered demonstrate the breadth of species present in this coastal city. We consider the effect of Ottoman Period diet, culture, trade and sanitation upon risk of parasitism in this community living 200 years ago.

Parasitic diversity found in coprolites of camelids during the Holocene.

Knowledge of parasitic infections to which fauna was exposed in the past provides information on the geographical origin of some parasites, on the possible dispersal routes and for archaeological fauna on the potential zoonotic risk that human and animal populations could be exposed. The aim of the present study was to examine the gastrointestinal parasite present in camelid coprolites collected from the archaeological site Cerro Casa de Piedra, cave 7 (CCP7), Patagonia, Argentina. Coprolites were collected from different stratified sequences dating from the Pleistocene-Holocene transition to the late Holocene. Paleoparasitological examination revealed the presence of eggs of Trichostrongylidae attributed to Lamanema chavezi or Nematodirus lamae, eggs of three unidentified capillariids, Strongylus-type eggs and oocysts of Eimeria macusaniensis. These parasites affected camelids living in the studied area since the Pleistocene-Holocene transition, about 10,000 years ago. Gastrointestinal parasite fauna of patagonian camelids did not vary significatively from Pleistocene-Holocene transition to late Holocene, although environmental conditions fluctuated greatly throughout this period, as indicative of the strength and the stability of these associations over time. In this study, the zoonotic and biogeography importance of parasites of camelids are also discussed.

An unexpected life in nutrition.

In this biographical article, I describe the evolution of my career in nutrition from an early period as an animal nutritionist interested in amino acid metabolism and genetic variation in nutrient requirements to an involvement in human nutrition and international public health. The career changes were in some respects a mirror of the evolution of nutritional science in my lifetime. I spent my entire career at Cornell University in what I think of as three distinct phases. As a researcher and teacher in the Poultry Science Department, I was able to do research in animal nutrition and witness the rapid industrialization of the production of poultry meat and eggs, helped by the findings of the era of nutrient discovery in nutritional science. Later I had the opportunity to lead the reorganization of human nutrition at Cornell during a period when research in nutritional science turned away from identifying new nutrients and became increasingly concerned with the roles of diet and chronic disease. During this period my research focus evolved as I became interested in aspects of international nutrition problems, particularly the influence of parasitic infections on child health and nutrition. I also became involved nationally in nutrition issues through participation in organizations such as the National Nutrition Consortium, the Food and Nutrition Board, and National Institutes of Health study sections at a time of great ferment in nutrition about the relationship of dietary patterns to health. Finally, I became provost of Cornell University and involved in the administration of a major research university. I describe my career in the context of my origins and early education springing from life on a sustainable family farm in rural Illinois.

Continuity in intestinal parasite infection in Aalst (Belgium) from the medieval to the early modern period (12th-17th centuries).

OBJECTIVE: To characterize patterns in the taxonomic diversity of parasites infecting the population of Aalst, Belgium, between the 12th and 17th centuries. MATERIALS: 14 sediment samples from seven cesspits dated 1100-1700 CE. METHODS: Digital light microscopy and Enzyme-linked immunosorbent assay (ELISA). RESULTS: We identified eggs of four species of helminths: whipworm (Trichuris trichiura), roundworm (Ascaris lumbricoides), Echinostoma fluke and Dicrocoelium fluke. ELISA results for protozoal parasites were negative. CONCLUSIONS: Taxonomic diversity of parasite infections remained constant from the 12th to the 17th centuries. Roundworm and whipworm, spread by poor sanitation, were dominant. Two species of zoonotic parasites were also identified, including for the first time ever in the Low Countries the Echinostoma fluke, which may have been spread by eating uncooked freshwater animal foods. SIGNIFICANCE: Analysis of sediment samples spanning such a broad chronology (six centuries) from a single city offers the opportunity to track diachronic change, which is rare in paleoparasitological studies. LIMITATIONS: We were unable to acquire samples from cesspits dating to the 14th century. SUGGESTIONS FOR FURTHER RESEARCH: Additional data from other Low Countries towns may strengthen the patterns identified in this paper. A similar approach can be used to investigate towns in different regions of the world.

Mid-7th century BC human parasite remains from Jerusalem.

OBJECTIVE: To determine the species of intestinal parasites present in 7th century BC high-status residents of Jerusalem and to expose the history of regional health and sanitary conditions. MATERIALS: Fifteen sediment samples were collected from the cesspit below a stone toilet seat found at the site of Armon Hanatziv, southern Jerusalem. The toilet installation was located in a garden adjacent to a monumental structure with extraordinary architectural elements. METHODS: A light microscope was used to identify and measure the eggs. RESULTS: The presence of four intestinal parasite egg taxa was detected: Trichuris trichiura (whipworm), Taenia sp. (beef/pork tapeworm), Ascaris lumbricoides (roundworm), and Enterobius vermicularis (pinworm). This is the earliest appearance of roundworm and pinworm in the ancient Israel parasitological record. CONCLUSIONS: Findings reveal that intestinal parasitic diseases most likely caused by poor sanitary conditions were a human problem in the Late Iron Age of Israel, affecting even high-status groups. SIGNIFICANCE: The study demonstrates the potential of archaeoparasitological investigations to expand our knowledge of the origin and history of regional infections. Moreover, parasitological evidence enabled us to determine the purpose of the cubical perforated stone artifacts (stone toilet seats rather than cultic objects as currently debated). LIMITATIONS: The eggs of some parasite taxa are less durable, so may theoretically be absent due to selective preservation. SUGGESTIONS FOR FURTHER RESEARCH: Future excavations of ancient Israel should include archaeoparasitological studies of rare toilet installations to prevent information loss of regional history of diseases and to better understand their archaeological context.

Gastrointestinal parasite burden in 4th-5th c. CE Florence highlighted by microscopy and paleogenetics.

The study of ancient parasites, named paleoparasitology, traditionally focused on microscopic eggs disseminated in past environments and archaeological structures by humans and other animals infested by gastrointestinal parasites. Since the development of paleogenetics in the early 1980s, few paleoparasitological studies have been based on the ancient DNA (aDNA) of parasites, although such studies have clearly proven their utility and reliability. In this paper, we describe our integrative approach for the paleoparasitological study of an ancient population from Florence in Italy, dated to the 4th-5th c. CE. The first stage consisted in the study of sediment samples from the pelvic area of 18 individuals under light microscopy. This allowed us to detect Ascarid-type eggs belonging very probably to the human-infesting roundworm Ascaris lumbricoides. Ten subsamples were selected corresponding to five individuals, and we extracted their whole DNA following sediment aDNA protocols. A targeted approach allowed us to detect two nematodes and one trematode aDNA fragments, namely Ascaris sp., Trichuris trichiura, and Dicrocoelium dendriticum. Among the five individuals tested for microscopic eggs and aDNA, three of them showed the remains of eggs (only Ascarid-type), but all of them tested positive to the presence of at least one parasite aDNA. Microscopic diagnosis first guided our research for the selection of promising samples while the targeted aDNA approach significantly improved our knowledge in terms of parasitic diversity and frequency in this population subgroup. These results enabled us to discuss the possible impact of latent parasitism in this past population at the time of an epidemic, as suggested in Florence. In particular, the singular case of D. dendriticum detection is discussed in light of the present-day scarcity of genuine human infections. Nevertheless, actual infections are known in the paleoparasitological record, and food habits may have led to false parasitism in this historical context. aDNA leaching from overlying strata may also explain this detection. This study strongly pleads for a systematic integrative approach combining microscopy and aDNA in paleoparasitology.

Intestinal helminths as a biomolecular complex in archaeological research.

Enteric helminths are common parasites in many parts of the world and in the past were much more widespread both geographically and socially. Many enteric helminths are relatively long-lived in the human host, often benign or of low pathogenicity while producing large numbers of environmentally resistant eggs voided in the faeces or found associated with individual remains (skeletons and mummies). The combination of helminth characters offers opportunities to the field of historical pathogen research that are quite different to that of some of the more intensively studied high impact pathogens. Historically, a wealth of studies has employed microscopic techniques to diagnose infection using the morphology of the helminth eggs. More recently, various ancient DNA (aDNA) approaches have been applied in the archaeoparasitological context and these are revolutionizing the field, allowing much more specific diagnosis as well as interrogating the epidemiology of helminths. These advances have enhanced the potential for the field to provide unique information on past populations including using diseases to consider many aspects of life (e.g. sanitation, hygiene, diet, culinary practices and other aspects of society). Here, we consider the impact of helminth archaeoparasitology and more specifically the impact and potential for application of aDNA technologies as a part of the archaeologists' toolkit. This article is part of the theme issue 'Insights into health and disease from ancient biomolecules'.

First report in pre-Columbian mummies from Bolivia of Enterobius vermicularis infection and capillariid eggs: A contribution to Paleoparasitology studies.

OBJECTIVE: This study was designed to search for ancient parasites in abdominal content and coprolites from Bolivian mummies. MATERIALS: Twelve mummified individuals from the Andean highlands, housed at the National Museum of Archaeology (MUNARQ) in La Paz, Bolivia. METHODS: Microscopic analysis of rehydrated samples (coprolites and abdominal content), following Lutz's spontaneous sedimentation technique. RESULTS: Eggs of Enterobius vermicularis were identified in coprolites from one mummy, and capillariid eggs in the organic abdominal content from another individual. CONCLUSIONS: This is the first evidence of ancient intestinal parasites in Bolivian mummies. SIGNIFICANCE: This pioneering study focused on the search of ancient intestinal parasites in human remains of the Bolivian Andes and contributes to greater knowledge of paleoparasitology in South America. LIMITATIONS: All mummies in the MUNARQ belonged to the Andean Bolivian highlands (post-Tiwanaku era or Late Intermediate Period), although the exact provenance of the material and the associated contexts are not well recorded. SUGGESTIONS FOR FURTHER RESEARCH: Considering the great number of well-known archaeological sites and other unexplored sites in Bolivia, in addition to large collections in museums, further paleopathological and paleoparasitological molecular studies in mummies and skeletons are called for.

Metagenomics and microscope revealed T. trichiura and other intestinal parasites in a cesspit of an Italian nineteenth century aristocratic palace.

This study evidenced the presence of parasites in a cesspit of an aristocratic palace of nineteenth century in Sardinia (Italy) by the use of classical paleoparasitological techniques coupled with next-generation sequencing. Parasite eggs identified by microscopy included helminth genera pathogenic for humans and animals: the whipworm Trichuris sp., the roundworm Ascaris sp., the flatworm Dicrocoelium sp. and the fish tapeworm Diphyllobothrium sp. In addition, 18S rRNA metabarcoding and metagenomic sequencing analysis allowed the first description in Sardinia of aDNA of the human specific T. trichiura species and Ascaris genus. Their presence is important for understanding the health conditions, hygiene habits, agricultural practices and the diet of the local inhabitants in the period under study.

Intestinal parasites in six Islamic medieval period latrines from 10th-11th century Córdoba (Spain) and 12th-13th century Mértola (Portugal).

OBJECTIVE: To investigate the types of intestinal parasites that infected people living in Islamic period southern Iberia (al-Andalus), and compare with other regions of Europe. MATERIALS: Four cesspits from 10th-11th century CE Córdoba (Spain), and two from 12th-13th century Mértola (Portugal). METHODS: Sediment from each cesspit was analyzed using digital light microscopy and enzyme-linked immunosorbent assay (ELISA). RESULTS: Analysis revealed eggs of roundworm (Ascaris lumbricoides) in every cesspit analyzed, but no evidence of other species of helminth or protozoal parasites. CONCLUSION: Differences were noted between parasite species found in Mediterranean Europe and northern Europe, where a range of zoonotic parasites were endemic alongside sanitation-related parasites. We suggest that the scarcity of zoonotic parasites in southern Europe in the medieval period may reflect contrasts in climate between northern and southern Europe. SIGNIFICANCE: The repeated identification of roundworm eggs suggests that al-Andalus was less hygienic than historically depicted. We did not note a difference between parasites found in Muslim and Christian regions of Iberia, and the predominance of parasites spread by fecal contamination of food is consistent with past research. LIMITATIONS: The eggs of some species of parasite are fragile, so may theoretically have been present in the population but did not survive for us to identify them. SUGGESTIONS FOR FURTHER RESEARCH: To further investigate the role of climate upon the parasites that affected past human populations.

Development and application of anthelminthic drugs in China.

China was once a country plagued by parasitic diseases. At the beginning of the founding of the People's Republic of China, nearly 80% of the population suffered from parasitic diseases because of poverty and poor sanitary conditions. After nearly 70 years of development, China has made remarkable achievements in the prevention and control of parasitic diseases, and the prevalence of parasitic diseases has been greatly reduced. In addition to organizational leadership from the government and various preventive measures, drug treatment and drug research & development are important and irreplaceable links in prevention and control work. Since the 1950s, China has begun to introduce, produce and imitate antiparasitic drugs from abroad, such as santonin, benzimidazole, and praziquantel. Chinese scientists have also contributed to the optimization of production techniques, improvements in drug formulation, the application in the clinic and the mechanisms of actions of generic drugs. At the same time, China has independently developed tribendimidine (TrBD, a broad spectrum anthelminthic), and its anthelminthic spectrum has been comprehensively studied. It is active against almost 20 parasites, is especially superior to benzimidazoles against Necator americanus, and surpasses the effectiveness of praziquantel against Clonorchis sinensis. In the treatment of tapeworm disease, the traditional Chinese medicines pumpkin seeds and betel nuts have good curative effects for taeniasis. Chinese scientists have explored the action modes and clinical administration methods of pumpkin seeds and betel nuts, which is still the main clinical regimen for the disease. This paper reviews the history and progress of the study of anthelmintics in intestinal helminth infections since the founding of the People's Republic of China and aiming to support clinicians and drug researchers in China and other countries.

Caelius Aurelianus (5th century AD) study on worms.

Caelius Aurelianus (5th century AD) translated in Latin the work of Soranus of Ephesus (2nd half of 1st century - 1st quarter of 2nd century AD) On Acute and on Chronic Diseases. In this Latin translation, the 8th chapter of the fourth book of chronic diseases is devoted in worm's infection in children and in adults. This study is the most complete and comprehensive analysis of this special infection of the Greek and Roman antiquity. In this chapter, the physician examined in great detail the semiology, differential diagnosis and treatment of such an infection. In addition, there are saved the views of many other ancient Greek physicians whose original text now are lost. Although the study of Caelius Aurelianus was based on the original Greek text of Soranus of Ephesus it should not be denied that Caelius Aurelianus made his own additions and arranged the text in a more accurate and organized manner.

New paleoparasitological investigations from the pre-inca to hispanic contact period in northern Chile.

Paleoparasitological studies have demonstrated that changes in environment or culture are reflected in the patterns of parasitic infection diseases in populations worldwide. The advent of agriculture and animal domestication, with its accompanying reduction in human mobility and expanding population involves changes in or emergence of, parasites, the so-called first epidemiological transition. Cultural processes related to territory occupation contribute to both loss and acquisition of parasites. The archaeological site Lluta 57 in the Lluta Valley, Chile, provides a chronology of the transition from the pre-Inca or Late Intermediate Period (LIP), through the Late or Inca Period (LP), to the Hispanic Contact Period (HCP), providing the possibility of evaluating this epidemiological transition. The aim of this study was to conduct a paleoparasitological investigation of to gain insight into the dynamics of parasitism in Lluta people throughout the Inca expansion. Fourteen human coprolites from the three periods were rehydrated, submitted to spontaneous sedimentation, and examined by light microscopy for the presence of intestinal parasite eggs, pollen grains, and micro-remains. Eggs of four parasites: Enterobius vermicularis, Trichostrongylus sp., Trichuris sp., and Eimeria macusaniensis were recovered. Frequency, diversity, and number of parasite eggs per sample increased over the studied time period. Trichostrongylus sp. and E. macusaniensis were recorded in the region for the first time. Enterobius vermicularis eggs, absent in the LIP, were present as a hyper-infection in LP. The presence of E. macusaniensis is likely related to exploitation of llamas, which were used for food and transport and as sacrificial offerings. The paleobotanical analysis revealed ten families of pollen grains, as well as phytoliths and floral remains. In contrast to parasitological results, a diachronic pattern was not detected. Evolution of the settlements, with the advent of larger, more densely populated, villages, could have influenced the emergence and intensification of transmission of parasites in the region. The study showed that the Inca expansion influenced host-parasite-environment relationships in the Lluta Valley.

[Original procreation or generational change? The investigation of cysticercus and tapeworms]. / Urzeugung oder Generationswechsel? Zur Erforschung der Blasen- und Bandwürmer.

The doctrine of the abiogenesis postulated the origin of human and animal intestinal worms from "not complete digested ingesta". Indeed Peter Simon Pallas (1741-1811) defined already 1760 in his dissertation that endoparasitic worms reproduce themselves by eggs. But he characterised the nature of cysticercus as "pathologically degenerated tail bladder". In 1856 Rudolf Leuckart (1822-1898) paraphrased the alternation of generation with "marvellous metamorphoses and peculiar form of development". The Dane Johannes Japetus Smith Steenstrup (1813-1897) recognised finally the principle of the alternation of generation and Gottlob Friedrich Heinrich Küchenmeister (1821-1890), a physician at the Saxon city Zittau realised the special correlation between the alternate and end host of tapeworms. Both, Leuckart and Küchenmeister proved their insights by animal and human experimentations.

Intestinal parasites from the 2nd-5th century AD latrine in the Roman Baths at Sagalassos (Turkey).

The aim of this research was to determine the species of intestinal parasite present in a Roman Imperial period population in Asia Minor, and to use this information to improve our understanding of health in the eastern Mediterranean region in Roman times. We analyzed five samples from the latrines of the Roman bath complex at Sagalassos, Turkey. Fecal biomarker analysis using 5ß-stanols has indicated the feces were of human origin. The eggs of roundworm (Ascaris) were identified in all five samples using microscopy, and the cysts of the protozoan Giardia duodenalis (which causes dysentery) were identified multiple times in one sample using ELISA. The positive G. duodenalis result at Sagalassos is particularly important as it represents the earliest reliable evidence for this parasite in the Old World (i.e. outside the Americas). As both these species of parasite are spread through the contamination of food and water by fecal material, their presence implies that Roman sanitation technologies such as latrines and public baths did not break the cycle of reinfection in this population. We then discuss the evidence for roundworm in the writings of the Roman physician Galen, who came from Pergamon, another town in western Asia Minor.

Short report: cysticercosis in an Egyptian mummy of the late Ptolemaic period.

We describe here an ancient case of cysticercosis that was discovered in an Egyptian mummy of a young woman of about 20 years of age who lived in the late Ptolemaic period (second to first centuries b.c.). On removal of the stomach and its rehydration, a cystic lesion in the stomach wall was observed by naked eye. Microscopical examination of sections of this lesion revealed a cystic structure, with a wall, with numerous projecting eversions, a characteristic feature of the larval stage (cysticercus) of the human tapeworm Taenia solium (or "pig tapeworm"). Immunohistochemical testing with serum from a T. solium-infected human confirmed the identity of the cyst. This finding is the oldest on record of the antiquity of this zoonotic parasite. This observation also confirms that, in Hellenistic Egypt, the farming of swine, along with man an intermediate host of this parasite, was present, and supports other archeological evidence.