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Back to the roots: dental calculus analysis of the first documented case of coeliac disease

Abstract

Dental calculus of a Roman woman (late first century–early second century CE), supposed to be the first historical evidence of coeliac disease (CD), was subjected to archaeobotanical investigations for reconstructing diet and phytotherapeutic practices. Light microscopy provided the proof she came in contact with gluten-rich cereals (i.e. Triticeae, Aveninae), which, maybe, were deleterious for a CD genetic predisposed individual like her. Gas-chromatography mass-spectrometry revealed that the young woman ingested, at least once in lifetime, plant foods and several herbs (e.g. Brassicaceae, Mentha sp., Valeriana sp., Apiaceae, Asteraceae, grapes or wine, honeydew or manna). About the latter, surprisingly, markers of Curcuma sp. and Panax sp. were detected. The consumption of these rhizomes, already used in the ancient Oriental medicine, supported the existence of cultural contact and exchange with the Eastern Asia. Encouraged by modern knowledge, we hypothesised that the inhumate used these roots as natural remedies to soothe her pathological condition. Our data provided information about the key role of the ethnobotany in Roman Imperial age.

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Abbreviations

LM:

Light microscopy

GC-MS:

Gas-chromatography mass-spectrometry

CD:

Coeliac disease

EPA:

Eicosapentaenoic acid

DHA:

Docosahexaenoic acid

References

  1. Abd El-Aty AM, Kim IK, Kim MR, Lee C, Shim JH (2008) Determination of volatile organic compounds generated from fresh, white and red Panax ginseng (CA Meyer) using a direct sample injection technique. Biomed Chromatogr 22:556–562

    Google Scholar 

  2. Adams RP (2013) Comparison of the volatile leaf and wood oils of the subspecies of Pinus torreyana: two isolated, narrow endemics in California. Phytologia 95:188–191

    Google Scholar 

  3. Agricoli G, Chilleri F, Pacciani E (2012) Una tomba alla cappuccina da Ansedonia. Notiziario della Soprintendenza per i Beni Archeologici della Toscana 8:285–290

    Google Scholar 

  4. Ahmed S, Khatri MS, Hasan MM (2017) Plants of family Lamiaceae: a promising hand for new antiurolithiatic drug development. World J Pharm Pharm Sci 6:90–96

    Google Scholar 

  5. Amarapurkar DN, Somani VS, Shah AS, Kankonkar SR (2016) HLA–DQ genotyping in celiac disease in western India. Trop Gastroenterol 36:174–178

    Google Scholar 

  6. Arranz-Otaegui A, Gonzalez Carretero L, Ramsey MN, Fuller DQ, Richter T (2018) Archaeobotanical evidence reveals the origins of bread 14,400 years ago in northeastern Jordan. Proc Natl Acad Sci U S A 115:7925–7930

  7. Badler VR, McGovern PE, Michel RH (1990) Drink and be merry! Infrared spectroscopy and ancient near eastern wine. MASCA Res Pap Sci 7:25–36

    Google Scholar 

  8. Baldoni M, Scorrano G, Gismondi A, D’Agostino A, Alexander M, Gaspari L, Vallelonga F, Canini A, Rickards O, Martìnez-Labarga C (2018) Who were the miners of Allumiere? A multidisciplinary approach to reconstruct the osteobiography of an Italian worker community. PLoS One 13:e0205362

    Google Scholar 

  9. Bell L, Wagstaff C (2017) Enhancement of glucosinolate and isothiocyanate profiles in Brassicaceae crops: addressing challenges in breding for cultivation, storage, and consumer-related traits. J Agric Food Chem 65:9379–9403

    Google Scholar 

  10. Bellini C, Mariotti-Lippi M, Mori Secci M, Aranguren B, Perazzi P (2008) Plant gathering and cultivation in prehistoric Tuscany (Italy). Veg Hist Archaeobotany 17:103–112

    Google Scholar 

  11. Boi M (2012) The ethnocultural significance for the use of plants in ancient funerary rituals and its possible implications with pollens found on the Shroud of Turin. Valencia, 2012; http://www.shroud.com/pdfs/boiveng.pdf; https://doi.org/10.13140/2.1.3690.3682

  12. Borstad CM, Garvie-Lok S, Katsonopoulou D (2018) Diet at ancient Helike, Achaea, Greece based on stable isotope analysis: from the Hellenistic to the Roman and Byzantine periods. J Archaeol Sci Rep 18:1–10

    Google Scholar 

  13. Bratanic N, Smigoc Schweiger D, Mendez A, Bratina N, Battelino T, Vidan-Jeras B (2010) An influence of HLA-A, B, DR, DQ, and MICA on the occurrence of celiac disease in patients with type 1 diabetes. Tissue Antigens 76:208–215

    Google Scholar 

  14. Bucchi A, Burguet-Coca A, Expósito I, Bocanera FJA, Lozano M (2019) Comparisons between methods for analyzing dental calculus samples from El Mirador cave (Sierra de Atapuerca, Spain). Archaeol Anthropol Sci:1–10

  15. Buckley SA, Stott AW, Evershed RP (1999) Studies of organic residues from ancient Egyptian mummies using high temperature-gas chromatography-mass spectrometry and sequential thermal desorption-gas chromatography-mass spectrometry and pyrolysis-gas chromatography-mass spectrometry. Analyst 124:443–452

    Google Scholar 

  16. Buckley S, Usai D, Jakob T, Radini A, Hardy K (2014) Dental calculus reveals unique insights into food items, cooking and plant processing in prehistoric Central Sudan. PLoS One 9:e100808

    Google Scholar 

  17. Cervino G, Fiorillo L, Laino L, Herford AS, Lauritano F, Giudice GL, Famà F, Santoro R, Troiano G, Iannello G, Cicciù M (2018) Oral health impact profile in celiac patients: analysis of recent findings in a literature review. Gastroenterol Res Pract. https://doi.org/10.1155/2018/7848735

  18. Choi KT (2008) Botanical characteristics, pharmacological effects and medicinal components of Korean Panax ginseng CA Meyer. Acta Pharmacol Sin 29:1109–1118

    Google Scholar 

  19. Christaki E, Bonos E, Giannenas I, Florou-Paneri P (2012) Aromatic plants as a source of bioactive compounds. Agriculture 2:228–243

    Google Scholar 

  20. Chung IM, Lim JJ, Ahn MS, Jeong HN, An TJ, Kim SH (2016) Comparative phenolic compound profiles and antioxidative activity of the fruit, leaves, and roots of Korean ginseng (Panax ginseng Meyer) according to cultivation years. J Ginseng Res 40:68–75

    Google Scholar 

  21. Copeland L, Hardy K (2018) Archaeological starch. Agronomy 8:4

    Google Scholar 

  22. Cristiani E, Radini A, Edinborough M, Borić D (2016) Dental calculus reveals Mesolithic foragers in the Balkans consumed domesticated plant foods. Proc Natl Acad Sci U S A 113:10298–10303

    Google Scholar 

  23. Cristiani E, Radini A, Borić D, Robson HK, Caricola I, Carra M, Mutri G, Oxilia G, Zupancich A, Šlaus M, Vujević D (2018) Dental calculus and isotopes provide direct evidence of fish and plant consumption in Mesolithic Mediterranean. Sci Rep 8:8147

    Google Scholar 

  24. Crowther A, Haslam M, Oakden N, Walde D, Mercader J (2014) Documenting contamination in ancient starch laboratories. J Archaeol Sci 49:90–104

    Google Scholar 

  25. Cummings LS, Yost C, Sołtysiak A (2018) Plant microfossils in human dental calculus from Nemrik 9, a pre-pottery Neolithic site in northern Iraq. Archaeol Anthropol Sci 10:883–891

    Google Scholar 

  26. Deng C, Liu N, Gao M, Zhang X (2007) Recent developments in sample preparation techniques for chromatography analysis of traditional Chinese medicines. J Chromatogr A 1153:90–96

    Google Scholar 

  27. Di Marco G, Manfredini A, Leonardi D, Canuti L, Impei S, Gismondi A, Canini A (2017) Geographical, botanical and chemical profile of monofloral Italian honeys as food quality guarantee and territory brand. Plant Biosyst: An International Journal Dealing with all Aspects of Plant Biology 151:450–463

  28. Di Sabatino A, Corazza GR (2009) Coeliac disease. Lancet 373:1480–1493

    Google Scholar 

  29. Dikshit SS, Rai S, Sharma MM (2016) Saga of ethnobotanical genesis from ancient to present scenario with special reference to the Darjeeling Himalayas. J Med Plants Stud 4:108–116

  30. Donkin RA (2013) Manna: an historical geography. In: Biogeographical. Springer, The Hague, Boston and London, Vol. 17. https://doi.org/10.1007/978-94-017-6117-8.

  31. Eerkens JW, Tushingham S, Brownstein KJ, Garibay R, Perez K, Murga E, Kaijankoski P, Rosenthal JS, Gang DR (2018) Dental calculus as a source of ancient alkaloids: detection of nicotine by LC-MS in calculus samples from the Americas. J Archaeol Sci Rep 18:509–515

    Google Scholar 

  32. Eglinton G, Hamilton RJ, Raphael RA, Gonzalez AG (1962) Hydrocarbon constituents of the wax coatings of plant leaves: a taxonomic survey. Phytochemistry 1:89–102

    Google Scholar 

  33. Ehsani-Ardakani MJ, Rostami Nejad M, Villanacci V, Volta U, Manenti S, Caio G, Giovenali P, Becheanu G, Diculescu M, Pellegrino S, Magazzù G, Casella G, Di Bella C, Decarli N, Biancalani M, Bassotti G, Hogg-Kollars S, Zali MR, Rostami K (2013) Gastrointestinal and non-gastrointestinal presentation in patients with celiac disease. Arch Iran Med 16:78

    Google Scholar 

  34. Ermolli ER, Romano P, Ruello MR, Lumaga MRB (2014) The natural and cultural landscape of Naples (southern Italy) during the Graeco-Roman and Late Antique periods. J Archaeol Sci 42:399–411

    Google Scholar 

  35. Evergetis E, Haroutounian SA (2015) The Umbelliferae (Apiaceae) of Dioscorides annotated in codex Neapolitanus Graecus. J Ethnopharmacol 175:549–566

    Google Scholar 

  36. FoodDB (2013) version 1.0. http://fooddb.ca/. Accessed July 2018

  37. Gasbarrini G (2008) Malabsorption syndrome. Introduction. Dig Dis 26:91

  38. Gasbarrini G, Miele L, Corazza GR, Gasbarrini A (2010) When was celiac disease born?: the Italian case from the archeologic site of Cosa. J Clin Gastroenterol 44:502–503

    Google Scholar 

  39. Gasbarrini G, Rickards O, Martínez-Labarga C, Pacciani E, Chilleri F, Laterza L, Marangi G, Scaldaferri F, Gasbarrini A (2012) Origin of celiac disease: how old are predisposing haplotypes? World J Gastroenterol 18:5300

    Google Scholar 

  40. Gismondi A, Di Marco G, Martini F, Sarti L, Crespan M, Martínez-Labarga C, Rickards O, Canini A (2016) Grapevine carpological remains revealed the existence of a Neolithic domesticated Vitis vinifera L. specimen containing ancient DNA partially preserved in modern ecotypes. J Archaeol Sci 69:75–84

    Google Scholar 

  41. Gismondi A, De Rossi S, Canuti L, Novelli S, Di Marco G, Fattorini L, Canini A (2018a) From Robinia pseudoacacia L. nectar to Acacia monofloral honey: biochemical changes and variation of biological properties. J Sci Food Agric 98:4312–4322

    Google Scholar 

  42. Gismondi A, Canuti L, Rocco G, Pisani M, Ghelli A, Bonanno M, Canini A (2018b) GC–MS detection of plant pigments and metabolites in Roman Julio-Claudian wall paintings. Phytochem Lett 25:47–51

    Google Scholar 

  43. Gismondi A, D'Agostino A, Canuti L, Di Marco G, Martínez-Labarga C, Angle M, Rickards O, Canini A (2018c) Dental calculus reveals diet habits and medicinal plant use in the Early Medieval Italian population of Colonna. J Archaeol Sci Rep 20:556–564

    Google Scholar 

  44. Gismondi A, D’Agostino A, Canuti L, Di Marco G, Basoli F, Canini A (2019) Starch granules: a data collection of 40 food species. Plant Biosyst 153:273–279

    Google Scholar 

  45. Golparvar AR, Hadipanah A, Mehrabi AM (2015) Diversity in chemical composition from two ecotypes of (Mentha longifolia L.) and (Mentha spicata L.) in Iran climatic conditions. J Biodivers Environ Sci (JBES) 6:26–33

  46. Green PH, Cellier C (2007) Celiac disease. N Engl J Med 357:1731–1743

    Google Scholar 

  47. Gruber JW, DerMarderosian A (2015) Back to the future: traditional medicinals revisited: the use of plants in medicine. Lab Med 27:100–108

    Google Scholar 

  48. Guarrera PM, Savo V (2016) Wild food plants used in traditional vegetable mixtures in Italy. J Ethnopharmacol 185:202–234

    Google Scholar 

  49. Guasch-Jané MR, Ibern-Gómez M, Andrés-Lacueva C, Jáuregui O, Lamuela-Raventós RM (2004) Liquid chromatography with mass spectrometry in tandem mode applied for the identification of wine markers in residues from ancient Egyptian vessels. Anal Chem 76:1672–1677

    Google Scholar 

  50. Guimarães R, Barros L, Carvalho AM, Sousa MJ, Morais JS, Ferreira IC (2009) Aromatic plants as a source of important phytochemicals: vitamins, sugars and fatty acids in Cistus ladanifer, Cupressus lusitanica and Eucalyptus gunnii leaves. Ind Crop Prod 30:427–430

    Google Scholar 

  51. Gurib-Fakim A (2006) Medicinal plants: traditions of yesterday and drugs of tomorrow. Mol Asp Med 27:1–93

    Google Scholar 

  52. Harrison SG (1950) Manna and its sources. Kew Bull 5:407–417

    Google Scholar 

  53. Hendy J, Warinner C, Bouwman A, Collins MJ, Fiddyment S, Fischer R, Hagan R, Hofman CA, Holst M, Chaves E, Klaus L, Larson G, Mackie M, McGrath K, Mundorff AZ, Radini A, Rao H, Trachsel C, Velsko IM, Speller CF (2018) Proteomic evidence of dietary sources in ancient dental calculus. Proc R Soc B 285:20180977

    Google Scholar 

  54. ICSN (2011) The international code for starch nomenclature. http://fossilfarm.Org/ICSN/Code.html. Accessed 22 April 2018

  55. Inoue M, Hayashi S, Craker LE (2017) Culture, history and applications of medicinal and aromatic plants in Japan. In: Hany A. El-Shemy (Eds.), Aromatic and medicinal plants-back to nature. InTech. https://doi.org/10.5772/66505

  56. Iskandar J, Iskandar BS (2017) Various plants of traditional rituals: ethnobotanical research among the Baduy community. Biosaintifika 9:114–125

    Google Scholar 

  57. Kanthilatha N, Boyd W, Dowell A, Mann A, Chang N, Wohlmuth H, Parr J (2014) Identification of preserved fatty acids in archaeological floor sediments from prehistoric sites at Ban Non Wat and Nong Hua Raet in northeast Thailand using gas chromatography. J Archaeol Sci 46:353–362

    Google Scholar 

  58. Keenleyside A, Schwarcz H, Stirling L, Lazreg NB (2009) Stable isotopic evidence for diet in a Roman and Late Roman population from Leptiminus, Tunisia. J Archaeol Sci 36:51–63

    Google Scholar 

  59. Kelly K (2009) The history of medicine. Facts on file, New York, pp 29–50

    Google Scholar 

  60. Kim JK, Tabassum N, Uddin MR, Park SU (2016) Ginseng: a miracle sources of herbal and pharmacological uses. Orient Pharm Exp Med 16:243–250

    Google Scholar 

  61. Kocaadam B, Şanlier N (2017) Curcumin, an active component of turmeric (Curcuma longa), and its effects on health. Crit Rev Food Sci Nutr 57:2889–2895

    Google Scholar 

  62. Kumar A, Dora J, Singh AA (2011) Review on spice of life Curcuma longa (turmeric). Int J Appl Biol Pharm Technol 2:371–379

    Google Scholar 

  63. Leonard C, Vashro L, O'Connell JF, Henry AG (2015) Plant microremains in dental calculus as a record of plant consumption: a test with Twe forager-horticulturalists. J Archaeol Sci Rep 2:449–457

    Google Scholar 

  64. Liang Y, Zhao S, Zhang X (2009) Antisense suppression of cycloartenol synthase results in elevated ginsenoside levels in Panax ginseng hairy roots. Plant Mol Biol Report 27:298–304

    Google Scholar 

  65. Lieverse AR (1999) Diet and the aetiology of dental calculus. Int J Osteoarchaeol 9:219–232

    Google Scholar 

  66. Lindhe J (1984) Parodontologia. Edi Ermes, Milano, pp 110–117

    Google Scholar 

  67. Liu F, Bai X, Yang FQ, Zhang XJ, Hu Y, Li P, Wan JB (2016) Discriminating from species of Curcumae radix (Yujin) by a UHPLC/Q-TOFMS-based metabolomics approach. Chin Med 11:21

    Google Scholar 

  68. Losowsky MSA (2008) History of coeliac disease. Dig Dis 26:112–120

    Google Scholar 

  69. Martin AC, Harvey WJ (2017) The Global Pollen Project: a new tool for pollen identification and the dissemination of physical reference collections. Methods Ecol Evol 8:892–897

    Google Scholar 

  70. Nagara ZZ, Saour KY (2015) Phytochemical and pharmacological study of Valepotriates in Valeriana officinalis L. F. Valerianeceae cultivated in Iraq. Iraqi J Pharm Sci (IJPS) 24:1–10

  71. Norrie PA (2003) The history of wine as a medicine. In: Sandler M, Pinder R (eds) Wine: a scientific exploration. Taylor and Francis, London, pp 21–55

    Google Scholar 

  72. Petrovska BB (2012) Historical review of medicinal plants’ usage. Pharmacogn Rev 6:1–5

    Google Scholar 

  73. Pinto-Sánchez MI, Bercik P, Verdu EF, Bai JC (2015) Extraintestinal manifestations of celiac disease. Dig Dis 33:147–154

    Google Scholar 

  74. Power RC, Salazar-García DC, Wittig RM, Freiberg M, Henry AG (2015) Dental calculus evidence of Taï Forest chimpanzee plant consumption and life history transitions. Sci Rep 5:15161

    Google Scholar 

  75. Power RC, Salazar-García DC, Rubini M, Darlas A, Havarti K, Walker M, Hublin JJ, Henry AG (2018) Dental calculus indicates widespread plant use within the stable Neanderthal dietary niche. J Hum Evol 119:27–41

    Google Scholar 

  76. Radini A, Nikita E, Buckley S, Copeland L, Hardy K (2017) Beyond food: the multiple pathways for inclusion of materials into ancient dental calculus. Am J Phys Anthropol 162:71–83

    Google Scholar 

  77. Rawal G, Yadav S, Shokeen P, Nagayach S (2015) Turmeric: the ancient elixir. IJHSR 5:380–383

  78. Richter R, Basar S, Koch A, König WA (2005) Three sesquiterpene hydrocarbons from the roots of Panax ginseng CA Meyer (Araliaceae). Phytochemistry 66:2708–2713

    Google Scholar 

  79. Riddle JM (1986) Dioscorides on pharmacy and medicine. University of Texas Press, Austin

    Google Scholar 

  80. Rostami K, Malekzadeh R, Shahbazkhani B, Akbari MR, Catassi C (2004) Coeliac disease in Middle Eastern countries: a challenge for the evolutionary history of this complex disorder? Dig Liver Dis 36:694–697

    Google Scholar 

  81. Salvini L, Pecci A, Giorgi G (2008) Cooking activities during the Middle Ages: organic residues in ceramic vessels from the Sant'Antimo Church (Piombino–Central Italy). J Mass Spectrom 43:108–115

    Google Scholar 

  82. Scorrano G, Brilli M, Martínez-Labarga C, Giustini F, Pacciani E, Chilleri F, Scaldaferri F, Gasbarrini A, Gasbarrini G, Rickards O (2014) Palaeodiet reconstruction in a woman with probable celiac disease: a stable isotope analysis of bone remains from the archaeological site of Cosa (Italy). Am J Phys Anthropol 154:349–356

    Google Scholar 

  83. Soto M, Inwood J, Clarke S, Crowther A, Covelli D, Favreau J (2019) Structural characterization and decontamination of dental calculus for ancient starch research. Archaeol Anthrop Sci 11:4847–4872. https://doi.org/10.1007/s12520-019-00830-7

  84. Staub PO, Casu L, Leonti M (2016) Back to the roots: a quantitative survey of herbal drugs in Dioscorides’ De Materia Medica (ex Matthioli, 1568). Phytomedicine 23:1043–1052

    Google Scholar 

  85. Swanson D, Block R, Mousa SA (2012) Omega-3 fatty acids EPA and DHA: health benefits throughout life. Adv Nutr 3:1–7

    Google Scholar 

  86. TGSC (2015) The Good Scents Company. http://www.thegoodscentscompany.com/. Accessed July 2018

  87. Touwaide A, Appetiti E (2013) Knowledge of Eastern materia medica (Indian and Chinese) in pre-modern Mediterranean medical traditions: a study in comparative historical ethnopharmacology. J Ethnopharmacol 148:361–378

    Google Scholar 

  88. Touwaide A, Pollio A, Aliotta G, Piomelli D, De Santo NG (1977) Medicinal plants for the treatment of urogenital tract pathologies according to Dioscorides’ De Materia Medica. Am J Nephrol 17:241–247

    Google Scholar 

  89. Travaglini A, Arsieni A, Brighetti MA, Vinciguerra F (2014) Atlante Del Polline Delle Principali Specie Allergeniche d'Italia. Il Raggio Verde, Lecce

    Google Scholar 

  90. Tursi A, Giorgetti G, Brandimarte G, Rubino E, Lombardi D, Gasbarrini G (2001) Prevalence and clinical presentation of subclinical/silent celiac disease in adults: an analysis on a 12-year observation. Hepatogastroenterology 48:462–464

    Google Scholar 

  91. Volta U, Villanacci V (2011) Celiac disease: diagnostic criteria in progress. Cell Mol Immunol 8:96–102

    Google Scholar 

  92. Warinner C, Speller C, Collins MJ (2015) A new era in palaeomicrobiology: prospects for ancient dental calculus as a long-term record of the human oral microbiome. Philos Trans R Soc B 370:20130376

    Google Scholar 

  93. Zanchetta MB, Longobardi V, Bai JC (2016) Bone and celiac disease. Curr Osteoporos Rep 14:43–48

    Google Scholar 

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Acknowledgements

The authors want to thank Prof. Giovanni Gasbarrini and Dr. Elsa Pacciani who promoted the first research activity on this case-study, “Ministero per i Beni e le Attività Culturali – Polo Museale Regionale della Toscana” and “Museo Archeologico Nazionale e Area Archeologica di Cosa” which kindly give us the possibility to collect dental calculus and, finally, Miss Sophie Gart who revised the English form of this manuscript.

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AG, AC and CML designed research; VL authorised the sampling; GDM, ADA and CML carried out the sampling; ADA, AG and GDM performed research; ADA, AG and GDM analysed data; AG and ADA wrote the paper; AC and OR provided financial support; all authors edited, revised and provided comments to the manuscript.

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Correspondence to Antonella Canini.

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Gismondi, A., D’Agostino, A., Di Marco, G. et al. Back to the roots: dental calculus analysis of the first documented case of coeliac disease. Archaeol Anthropol Sci 12, 6 (2020). https://doi.org/10.1007/s12520-019-00962-w

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Keywords

  • Gas-chromatography mass-spectrometry
  • Light microscopy
  • Starch granules
  • Plant drugs
  • Secondary metabolites
  • Exotic rhizomes