Adaptive function of soil consumption: an in vitro study modeling the human stomach and small intestine
1 Department of Ecology and Evolution, University of Chicago, 1101 East 57th
Street, Chicago, IL 60637, USA
2 Université d'Auvergne, 28 place Henri Dunant, 63300
Clermont-Ferrand, France
3 TNO Nutrition and Food Research Institute, PO Box 360, NL-3700 AJ Zeist,
The Netherlands
* Author for correspondence (e-mail: njdominy{at}uchicago.edu)
Accepted 16 October 2003
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Summary |
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Key words: geophagy, pica, diet, tannin, alkaloid, human
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Introduction |
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Mineral nutrient supplementation is the historical and intuitive basis for
geophagy (Jones and Hanson,
1985; Kreulen,
1985
). Indeed, sodium acquisition reportedly explains the
phenomenon in organisms ranging from butterflies to babirusas
(Arms et al., 1974
;
Clayton and MacDonald, 1999
).
In humans, however, investigators have largely discounted the hypothesis that
geophagy is a physiological response to a need for nutrients, such as iron.
The tendency to infer that anemia elicits soil consumption
(Abrahams, 1997
) is confounded
by the fact that geophagy often leads to, rather than corrects, iron, zinc, or
potassium deficiencies (Severance et al.,
1988
; Reid, 1992
).
The phenomenon is exacerbated when clays with high cation-exchange capacities
are ingested. Moreover, mineral nutrients are usually sufficient in an
animal's routine diet (Hladik and Gueguen,
1974
; Gilardi et al.,
1999
); and, among primates, elements are similar between
unconsumed soils and those consumed selectively and repeatedly
(Izawa, 1993
;
Mahaney et al., 1995
;
Müller et al., 1997
;
Bolton et al., 1998
).
Furthermore, in soils consumed by chimpanzees, only Fe was present in high
concentrations (range 6-17%; Mahaney et
al., 1997
). However, available Fe was only partially soluble in
conditions modeling the chimpanzee stomach (oxalic acid at pH 2.0), indicating
it was an improbable cue. Finally, it is notable that dissolved salts in some
soils may render calcium oxalate soluble
(Kreulen, 1985
). To our
knowledge, this hypothesis has never been tested despite the importance of Ca
to vertebrate reproduction. In plants, Ca exists principally as oxalate
crystals (Finley, 1999
;
Prychid and Rudall, 1999
),
which readily cross intestinal epithelia
(Hatch and Freel, 1995
). It is
perhaps significant that primates incurring high reproductive costs consume
soil despite considerable risk of predation
(Heymann and Hartmann,
1991
).
The clay fraction of ingested soils could also protect the gastrointestinal
epithelium by cross-linking with glycoproteins in the intestinal mucosa
(Rateau et al., 1982;
Moré et al., 1987
).
Because toxins and tannins cross or afflict the epithelium
(Mitjavila et al., 1977
;
Gee and Johnson, 1988
), the
adsorption of such dietary compounds is the leading hypothesis for geophagy in
some animals (Gilardi et al.,
1999
; Setz et al.,
1999
; Wakibara et al.,
2001
). Clays with high cation-exchange properties also adsorb
diarrhoea-causing enterotoxins (Said et
al., 1980
; Brouillard and
Rateau, 1989
). Accordingly, Kaopectate® and Smecta® are
common commercial products featuring, respectively, kaolinite and smectite,
clays that assuage diarrhoea in monkeys and humans
(Beck et al., 1977
;
Leber, 1988
;
Guarino et al., 2002
).
Compellingly, humans report consuming soil expressly to relieve diarrhoea, and
kaolinite is usually, but not always, the principle clay fraction ingested by
humans and nonhuman primates (Vermeer and
Ferrell, 1985
; Aufreiter et
al., 1997
; Mahaney et al.,
1997
,
2000
;
Knezevich, 1998
). Of course,
both adsorptive functions are not mutually exclusive. Indeed, they may be
linked. Practitioners of geophagy are often socially disadvantaged cultural
and ethnic groups living in the tropics
(Abrahams and Parsons, 1996
;
Simon, 1998
). Under such
conditions, geophagy may facilitate exploitation of marginal plant foods and
concomitantly reduce the energetic costs of diarrhoea. Given the selective
benefits to pregnant women and children, it is unsurprising that they are the
principal consumers of soil (Wiley and
Katz, 1998
). In fact, humans use clay explicitly to render
tanniniferous acorns and alkaloid-rich potatoes edible
(Johns, 1986
; Johns and
Duquette,
1991a
,b
).
Although the incidence of geophagy is decreasing
(Parry-Jones and Parry-Jones,
1992), the practice remains common in many cultures. For example,
a single Nigerian village produces 500 tons of soil yearly for consumption
across West Africa (Vermeer and Ferrell,
1985
). Moreover, children consume considerable quantities of soil
regardless of geography and socio-economic status. Ingestion varies from the
incidental to the incredible, ranging from 75 mg day-1 in Amherst,
USA (Stanek and Calabrese, 1995) to 650 g reported in vivo in a
single Gambian boy (Collinson et al.,
2001
). Accordingly, understanding and quantifying the adsorptive
capacity of clay continues to be important. To date, modeling of dietary
compound adsorption by clays has been investigated only in Amazonian parrots
(Gilardi et al., 1999
). Here
we model the human gastrointestinal system and test the capacity of kaolin to
adsorb a toxin (quinine) and tannins, both condensed (quebracho) and soluble
(tannic acid). Furthermore, we evaluate the solubility of calcium oxalate in
the presence of kaolin.
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Materials and methods |
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Gastric environment
Before introducing the substance to be digested, 10 ml of gastric
electrolyte solution (CaCl2 0.22 g l-1, KCl 2.2 g
l-1, NaCl 5 g l-1 and NaHCO3 1.5 g
l-1 adjusted to 500 ml with water) with 500 kU l-1
pepsinogen (Sigma) and rhizopus lipase (Amano, Nagoya, Japan) were introduced
into the gastric compartment and adjusted to pH 1.5 with 1 mol l-1
HCl. Gastric solutions were secreted at 0.5 ml min-1 and pH was
controlled according to a pre-set profile by secreting 1 mol l-1
HCl or water.
Small intestine environment
Secretions of NaHCO3 or water at 0.25 ml-1
min-1 maintained pH in the small intestine at 6.5. Pancreatic
output was simulated by secreting 10% pancreatin in small intestinal
electrolyte solution (CaCl2 0.22 g l-1, KCl 2.2 g
l-1, NaCl 5 g l-1) at 0.25 ml min-1. Biliary
output was simulated by secreting 4% bile solution at 0.5 ml min-1.
Before the experiment, the duodenal compartment was filled with 1 gtrypsin
(Bovine Pancreas Type III; Sigma), 15 ml of 4% bile solution, and 7 ml 10%
pancreatin solution. Jejunal and ileal compartments were filled with 100 ml of
small intestinal electrolyte solution and pumped through the hollow fiber at a
rate of 10 ml min-1.
Digestion trials
We used kaolin (Sigma) and four test compounds: calcium oxalate (Farco,
Beijing, China), crude quebracho (a condensed tannin from the bark of
Schinopsis balansae; gift of Dr A. E. Hagerman), tannic acid (a
soluble tannin; Riedel de Haën, Seelze, Germany), and quinine (an
alkaloid, Sigma). Digestion trials and control trials (without kaolin) were
executed in duplicate with a meal volume of 300 ml. Forexperimental trails we
chose 10 g kaolin. Although this amount exceeds the US Environmental
Protection Agency's 200 mg day-1 risk-assessment level for
involuntary soil ingestion (Stanek and Calabrese, 1995), it is within the
daily range of human consumption reported by Simon
(1998). For example, children
in western Kenya consume an average of 28 g of soil daily, ranging from 8 to
108 g (Geissler et al.,
1997
).
Because humans and chimpanzees share a similar gastrointestinal system
(Lambert, 1998), we chose 1 g
tannic acid and 3.3 g quebracho (40% of which is condensed tannin; A. E.
Hagerman, personal communication) to approximate a dietary intake of 1% tannin
in both humans and chimpanzees (Hladik,
1977
; Narasinga Rao and
Prabhavathi, 1982
; Reynolds et
al., 1998
). We chose 1 g calcium oxalate to simulate a modest meal
of 100 g spinach (US Department of Agriculture, Agricultural Research Service
2001, USDA Nutrient Database for Standard Reference, Release 14.
http://www.nal.usda.gov/fnic/foodcomp).
Finally, we chose 1 g quinine as a dosage toxic enough to induce human
cinchonism (Bateman and Dyson,
1986
).
Sampling and analyses
Digestion was simulated during duplicate 5 h experiments. Ileal delivery
was collected after 2, 4 and 5 h. The mass of the samples was measured to
determine fresh matter emptying. Samples were stored at 4°C. Similarly,
the bottles with dialysis fluid were replaced every 2 h and samples were
collected and stored at 4°C. At the end of the experiment the contents of
the gastric and intestinal compartments were collected and stored at
4°C.
We measured levels of absorbed calcium directly using a Ca2+-selective electrode (Orion; Beverly, USA). Levels of condensed tannin (crude quebracho) were measured with the Folin-Denis assay (200 µl sample + 100 µl NaHCO3 + 100 µl Folin-Denis reagent + 1.6 ml H2O) at 790 nm on an LKB spectrophotometer (Pharmacia LKB Biotechnology, Uppsala, Sweden) after 30 min. For tannic acid, the assay was adjusted (200 µl sample + 200 µl Folin-Denis Reagent + 1.6 mlNaHCO3) and absorption measured at 760 nm. Quinine was measured by adding 100 µl of sample with 1900 µl Dragendorff's reagent and measuring absorption at 595 nm. All measurements were referenced to 5-point standard curves.
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Results |
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Discussion |
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Furthermore, we show that calcium oxalate is insoluble in the presence of
ingested kaolin; however, dissolved salts in natural clay licks may improve
solubility to some extent (Kreulen,
1985). This possibility deserves further study. Moreover, the
causal link between increased Ca precipitation and kaolin is unclear, although
the range reported here is consistent with the results of von Unruh et al.
(2003
), in which calcium
oxalate precipitated 2.2-18.5% (±4.0-7.9%) of ingested Ca.
Our results support hypotheses advocating an adsorptive function of
ingested clay. For pregnant women the advantages of reduced toxicity and
digestion-inhibition are clear. By adhering to gastrointestinal epithelia,
clays may not only improve digestive efficiency, but also reduce fetal
exposure to toxins tolerated by the mother
(Profet, 1992). Similarly,
economically disadvantaged children living in the tropics are also frequent
consumers of soil. They are particularly susceptible to undernourishment and
diarrhoeal dehydration, conditions that may be exacerbated by a reliance on
marginal plant foods rich in tannins and toxins
(Johns, 1990
). It is notable
that howling monkeys are geophagous when they consume foliage, which is often
toxic (De Souza et al., 2002
).
Both adsorption and cytoprotection mechanisms offer adaptive advantages.
Similar effects are attributed to charcoal, which is prescribed commonly in
cases of child poisoning (Levy,
1982). In fact, murine models indicate that charcoal is more
effective than kaolin at adsorbing endotoxins
(Ditter et al., 1983
), which
could explain why some primates consume charcoal regularly
(Cooney and Struhsaker, 1997
;
Struhsaker et al., 1997). However, the adsorptive properties of clay or
charcoal can also produce negative effects. For example, Tsakala et al.
(1990
) reported that a
traditional anti-diarrhoeal soil from the Republic of Congo (mouboumou)
adsorbed
60% of bioavailable chloroquine. The compromising effect of
antidiarrhoeal soils on common antimalarial treatments deserves further study.
Furthermore, we show that consuming kaolin-rich soils together with calcium
oxalate-rich leaves could precipitate
30% of available Ca. Nevertheless,
given its prominence in human history, the adaptive benefits of geophagy would
appear to surpass these potential costs, as well as those of ingesting
geohelminths, lead and other potentially harmful elements (e.g.
Gelfand et al., 1975
).
Finally, although we did not study the importance of mineral
supplementation, it is an unlikely cause of geophagy in parrots, humans and
nonhuman primates (Reid, 1992;
Mahaney et al., 1997
;
Gilardi et al., 1999
;
Krishnamani and Mahaney,
2000
). However, for large herbivores, mineral supplementation
could be an important factor (Klaus et
al., 1998
; Abrahams,
1999
; Milewski,
2000
; Holdo et al.,
2002
). Accordingly, the adaptive function of soil consumption
could be multifactorial, with none of the mechanisms being mutually exclusive
(Wilson, 2003
). We conclude
that human geophagy is a likely mechanism for maintaining gastrointestinal
health. Our results are consistent with this view as kaolin reduced the
bioavailability of three dietary compounds by
30%. Thus, the tendency of
the medical literature to view geophagy as aberrant behavior or a symptom of
metabolic dysfunction is probably unwarranted in most cases.
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Acknowledgments |
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Footnotes |
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