Adaptive function of soil consumption: an in vitro study modeling the human stomach and small intestine

SUMMARY Despite occurring in a wide variety of taxa, deliberate soil consumption (geophagy) is a poorly understood behavior. In humans, geophagy is sometimes considered aberrant or a sign of metabolic dysfunction. However, geophagy is normally assigned an adaptive function in nonhuman primates and various other organisms. One hypothesis submits that clay-rich soil adsorbs intestinal insults, namely plant metabolites or diarrhoea-causing enterotoxins. Here we test the capacity of kaolin, a commonly ingested clay, to adsorb quinine (an alkaloid) and two types of tannin (digestion-inhibitors). Trials were conducted in vitro using the TNO Intestinal Model, a device that closely simulates digestion by the human stomach and small intestine. Kaolin reduced the bioavailability of each compound by ≤30%. However, because we could not replicate clay-epithelial adhesion and reduced motility, these results may underestimate adsorption in vivo. We also show that kaolin fails to render calcium oxalate soluble. We conclude that gastrointestinal adsorption is the most plausible function of human geophagy. Adaptive advantages include greater exploitation of marginal plant foods and reduced energetic costs of diarrhoea, factors that could account for the high frequency of geophagy in children and pregnant women across the tropics.

[1]  Brouillard My,et al.  [Adsorption potency of 2 clays, smectite and kaolin on bacterial enterotoxins. In vitro study in cell culture and in the intestine of newborn mice]. , 1989 .

[2]  D. Vermeer,et al.  Nigerian geophagical clay: a traditional antidiarrheal pharmaceutical. , 1985, Science.

[3]  R. Sodhi,et al.  The Adaptive Significance of Geophagy for Japanese Macaques (Macaca fuscata) at Arashiyama, Japan , 2001, International Journal of Primatology.

[4]  D. Cooney,et al.  Charcoal Consumption by Zanzibar Red Colobus Monkeys: Its Function and Its Ecological and Demographic Consequences , 1997, International Journal of Primatology.

[5]  R. Havenaar,et al.  A computer-controlled system to simulate conditions of the large intestine with peristaltic mixing, water absorption and absorption of fermentation products , 1999, Applied Microbiology and Biotechnology.

[6]  S. Lightman,et al.  Quinine toxicity. , 1986, Adverse drug reactions and acute poisoning reviews.

[7]  W. Parry‐Jones,et al.  Pica: Symptom or Eating Disorder? A Historical Assessment , 1992, British Journal of Psychiatry.

[8]  A. Wiley,et al.  Geophagy in Pregnancy: A Test of a Hypothesis , 1998, Current Anthropology.

[9]  J. Kvalsvig,et al.  Geophagy and its association with geohelminth infection in rural schoolchildren from northern KwaZulu-Natal, South Africa. , 2002, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[10]  D. Kreulen Lick use by large herbivores: a review of benefits and banes of soil consumption , 1985 .

[11]  H. Friis,et al.  Geophagy among school children in Western Kenya , 1997, Tropical medicine & international health : TM & IH.

[12]  M. Laskey,et al.  Dual-Energy X-Ray Absorptiometry: A New Insight Into Geophagy , 2001, Journal of pediatric gastroenterology and nutrition.

[13]  L. Greco,et al.  Smectite in the Treatment of Acute Diarrhea: A Nationwide Randomized Controlled Study of the Italian Society of Pediatric Gastroenterology and Hepatology (SIGEP) in Collaboration With Primary Care Pediatricians , 2001, Journal of pediatric gastroenterology and nutrition.

[14]  W. Mahaney,et al.  Mineral and chemical analyses of soils eaten by humans in Indonesia , 2000 .

[15]  J. Rateau,et al.  A histological, enzymatic and water-electrolyte study of the action of smectite, a mucoprotective clay, on experimental infectious diarrhoea in the rabbit. , 1982, Current medical research and opinion.

[16]  R. Urbaschek,et al.  Ability of various adsorbents to bind endotoxins in vitro and to prevent orally induced endotoxemia in mice. , 1983, Gastroenterology.

[17]  H. Severance,et al.  Profound muscle weakness and hypokalemia due to clay ingestion. , 1988, Southern medical journal.

[18]  Philippe Marteau,et al.  A Multicompartmental Dynamic Computer-controlled Model Simulating the Stomach and Small Intestine , 1995 .

[19]  A. Shibl,et al.  Influence of various agents on adsorption capacity of kaolin for Pseudomonas aeruginosa toxin. , 1980, Journal of pharmaceutical sciences.

[20]  D. Cooney,et al.  Adsorptive Capacity of Charcoals Eaten by Zanzibar Red Colobus Monkeys: Implications for Reducing Dietary Toxins , 1997, International Journal of Primatology.

[21]  I. Beck,et al.  Methods for the study of antidiarrheal agents. Study of commonly used protective and adsorbent agents. , 1977, Journal of medicine.

[22]  W. Mahaney,et al.  Geophagy among primates: adaptive significance and ecological consequences , 2000, Animal Behaviour.

[23]  P. Abrahams,et al.  Geophagy in the Tropics: a literature review , 1996 .

[24]  T. Sauerbruch,et al.  Reference range for gastrointestinal oxalate absorption measured with a standardized [13C2]oxalate absorption test. , 2003, The Journal of urology.

[25]  D. Finley Patterns of calcium oxalate crystals in young tropical leaves: a possible role as an anti-herbivory defense , 1969 .

[26]  R. Derache,et al.  Tannic acid and oxidized tannic acid on the functional state of rat intestinal epithelium. , 1977, The Journal of nutrition.

[27]  Robert L. Jones,et al.  Mineral Licks, Geophagy, and Biogeochemistry of North American Ungulates , 1984 .

[28]  V. Reynolds,et al.  Condensed tannins and sugars in the diet of chimpanzees (Pan troglodytes schweinfurthii) in the Budongo Forest, Uganda , 1998, Oecologia.

[29]  M. Duquette,et al.  Traditional detoxification of acorn bread with clay , 1991 .

[30]  R. Holdo,et al.  GEOPHAGY IN THE AFRICAN ELEPHANT IN RELATION TO AVAILABILITY OF DIETARY SODIUM , 2002 .

[31]  J. Fioramonti,et al.  Effects of treatment with smectite on gastric and intestinal glycoproteins in the rat: A histochemical study , 1987, The Histochemical Journal.

[32]  I. Johnson,et al.  Interactions between hemolytic saponins, bile salts and small intestinal mucosa in the rat. , 1988, The Journal of nutrition.

[33]  A. Zarate,et al.  Geophagia. A cause of life-threatening hyperkalemia in patients with chronic renal failure. , 1975, JAMA.

[34]  I CASTILLO ODENA,et al.  [Social organization]. , 1956, Prensa medica argentina.

[35]  Luciane L. de Souza,et al.  Geophagy as a Correlate of Folivory in Red-Handed Howler Monkeys (Alouatta belzebul) from Eastern Brazilian Amazonia , 2002, Journal of Chemical Ecology.

[36]  G. Hartmann,et al.  Geophagy in moustached tamarins,Saguinus mystax (platyrrhini: Callitrichidae), at the Río Blanco, Peruvian Amazonia , 1991, Primates.

[37]  R. Berton,et al.  Geophagy in the golden-faced saki monkey ( Pithecia pithecia chrysocephala ) in the Central Amazon , 1999 .

[38]  D. Macdonald,et al.  Social Organization of the Babirusa (Babyrousa babyrussa) and Their Use of Salt Licks in Sulawesi, Indonesia , 1999 .

[39]  J. Lambert Primate digestion: Interactions among anatomy, physiology, and feeding ecology , 1998 .

[40]  B. Schmid,et al.  Geophagy by large mammals at natural licks in the rain forest of the Dzanga National Park, Central African Republic , 1998, Journal of Tropical Ecology.

[41]  K. Izawa Soil-eating byAlouatta andAteles , 1993, International Journal of Primatology.

[42]  P. Rudall,et al.  Calcium Oxalate Crystals in Monocotyledons: A Review of their Structure and Systematics , 1999 .

[43]  S. Simon,et al.  Soil ingestion by humans: a review of history, data, and etiology with application to risk assessment of radioactively contaminated soil. , 1998, Health physics.

[44]  W. Leber A new suspension form of smectite (Liquid 'Diasorb') for the treatment of acute diarrhoea: a randomized comparative study. , 1988, Pharmatherapeutica.

[45]  M. Knezevich,et al.  Geophagy as a therapeutic mediator of endoparasitism in a free‐ranging group of rhesus macaques (Macaca mulatta) , 1998, American journal of primatology.

[46]  W. Mahaney,et al.  Geochemistry and mineralogy of soils eaten by humans , 1997 .

[47]  T. Johns Detoxification function of geophagy and domestication of the potato , 1986, Journal of Chemical Ecology.

[48]  M. Duquette,et al.  Detoxification and mineral supplementation as functions of geophagy. , 1991, The American journal of clinical nutrition.

[49]  L. Cosmides,et al.  The Adapted mind : evolutionary psychology and the generation of culture , 1992 .

[50]  C. Hladik,et al.  [Geophagia and mineral nutrition in wild primates]. , 1974, Comptes rendus hebdomadaires des seances de l'Academie des sciences. Serie D: Sciences naturelles.

[51]  R. Wrangham,et al.  Analysis of geophagy soils in Kibale Forest, Uganda , 1997, Primates.

[52]  R. Reid,et al.  Cultural and medical perspectives on geophagia. , 1992, Medical anthropology.

[53]  P. Abrahams The Chemistry and Mineralogy of Three Savanna Lick Soils , 1999, Journal of Chemical Ecology.

[54]  D. Danford Pica and nutrition. , 1982, Annual review of nutrition.

[55]  E J Calabrese,et al.  Daily estimates of soil ingestion in children. , 1995, Environmental health perspectives.

[56]  C. Munn,et al.  Biochemical Functions of Geophagy in Parrots: Detoxification of Dietary Toxins and Cytoprotective Effects , 1999, Journal of Chemical Ecology.

[57]  G. Klaus,et al.  GEOPHAGY AT NATURAL LICKS AND MAMMAL ECOLOGY: A REVIEW , 1998 .

[58]  C. Hladik 16 – Chimpanzees of Gabon and Chimpanzees of Gombe: some Comparative Data on the Diet , 1977 .

[59]  P. Abrahams Geophagy (soil consumption) and iron supplementation in Uganda , 1997, Tropical medicine & international health : TM & IH.

[60]  B. N. Narasinga Rao,et al.  Tannin content of foods commonly consumed in India and its influence on ionisable iron. , 1982, Journal of the science of food and agriculture.

[61]  P. Feeny,et al.  Sodium: Stimulus for Puddling Behavior by Tiger Swallowtail Butterflies, Papilio glaucus , 1974, Science.

[62]  G Levy,et al.  Gastrointestinal clearance of drugs with activated charcoal. , 1982, The New England journal of medicine.

[63]  M. Wilson,et al.  Clay Mineralogical and Related Characteristics of Geophagic Materials , 2003, Journal of Chemical Ecology.

[64]  M. Profet Pregnancy sickness as adaptation : A deterrent to maternal ingestion of teratogens , 1992 .

[65]  F. Burton,et al.  Chemical Analysis of Soils of Kowloon (Hong Kong) Eaten by Hybrid Macaques , 1998, Journal of Chemical Ecology.

[66]  M. Grynpas,et al.  Geophagy amongst rhesus macaques on Cayo Santiago, Puerto Rico , 1995, Primates.

[67]  K. Müller,et al.  Geophagy in masked titi monkeys (Callicebus personatus melanochir) in sBrazil , 2006, Primates.

[68]  J. Halsted,et al.  Geophagia in man: its nature and nutritional effects. , 1968, The American journal of clinical nutrition.