This article appeared in a journal published by Elsevier. The attached
copy is furnished to the author for internal non-commercial research
and education use, including for instruction at the authors institution
and sharing with colleagues.
Other uses, including reproduction and distribution, or selling or
licensing copies, or posting to personal, institutional or third party
websites are prohibited.
In most cases authors are permitted to post their version of the
article (e.g. in Word or Tex form) to their personal website or
institutional repository. Authors requiring further information
regarding Elsevier’s archiving and manuscript policies are
encouraged to visit:
http://www.elsevier.com/copyright
Author's personal copy
Transactions of the Royal Society of Tropical Medicine and Hygiene 104 (2010) 787–795
Contents lists available at ScienceDirect
Transactions of the Royal Society of
Tropical Medicine and Hygiene
journal homepage: http://www.elsevier.com/locate/trstmh
Geophagy and potential health implications: geohelminths, microbes
and heavy metals
Ruth Kutalek a,∗ , Guenther Wewalka b , Claudia Gundacker c,d , Herbert Auer e , Jeff Wilson f ,
Daniela Haluza g , Steliana Huhulescu b , Stephen Hillier f , Manfred Sager h , Armin Prinz a
a
Medical University of Vienna, Center for Public Health, Department of General Practice and Family Medicine, Unit Ethnomedicine and International Health,
Waehringerstrasse 25, 1090 Vienna, Austria
b
Austrian Agency for Health and Food Safety AGES, Institute for Medical Microbiology and Hygiene, Vienna, Waehringerstrasse 25A, 1090 Vienna, Austria
c
Medical University of Vienna, Center for Public Health, Department of Ecotoxicology, Waehringerstrasse 10, 1090 Vienna, Austria
d
Medical University of Vienna, Department for Medical Genetics, Waehringerstrasse 10, 1090 Vienna, Austria
e
Medical University of Vienna, Center for Pathophysiology, Infectiology and Immunology, Department of Medical Parasitology, Institute of Specific
Prophylaxis and Tropical Medicine, Kinderspitalgasse 15, 1090 Vienna, Austria
f
Macaulay Land Use Research Institute, Craigiebuckler, Aberdeen AB15 8QH, United Kingdom
g
Medical University of Vienna, Center for Public Health, Institute of Environmental Health, Kinderspitalgasse 15, 1090 Vienna, Austria
h
Austrian Agency for Health and Food Safety AGES, Competence Centre Elements, Spargelfeldstrasse 191, 1226 Vienna, Austria
a r t i c l e
i n f o
Article history:
Received 4 February 2010
Received in revised form 1 September 2010
Accepted 1 September 2010
Keywords:
geophagy
soil
microbes
parasites
heavy metals
Africa
a b s t r a c t
The practice of geophagy (soil-eating) is widespread among pregnant and breast-feeding
women in sub-Saharan Africa. To assess some of the potential risks accompanying the
consumption of geophagic material, we analysed contamination with bacteria, fungi, and
geohelminths as well as heavy metals (lead, mercury and cadmium) in 88 African geophagic
soil samples, which were purchased in Central, West and East Africa, Europe and the United
States. Median microbial viable counts of positive samples were 440 cfu/g (maximum
120 000 cfu/g). The median metal concentrations were 40 mg/kg lead (up to 148 mg/kg),
0.05 mg/kg mercury (up to 0.64 mg/kg), and 0.055 mg/kg cadmium (maximum 0.57 mg/kg).
No geohelminth eggs were found in these samples. Our results suggest that geophagic soil
samples can be highly contaminated with microbes and may contain high levels of lead.
Geophagy, however, is not a cause of adult helminth infection. The periodic consumption of
geophagic materials at high dosages might be problematic particularly during pregnancy.
© 2010 Royal Society of Tropical Medicine and Hygiene. Published by Elsevier Ltd.
All rights reserved.
1. Introduction
Geophagy, ‘the habit of eating earth including clay and
other types of soil’,1 has been observed in many parts of
the world,2–4 but is especially widespread in sub-Saharan
Africa (Supplementary Figure 1). Soil or clay is mostly
consumed by pregnant or breast-feeding women and also
∗ Corresponding author. Tel.: +43 1 4277 63436; fax: +43 1 4277 9634.
E-mail address: ruth.kutalek@meduniwien.ac.at (R. Kutalek).
by children.5–8 Little data is available on the percentage
of women consuming clay or on the amount consumed.
Several studies, however, suggest that in African regions
where geophagy occurs, between 46% and 73% of pregnant or breast-feeding women consume soil regularly. The
amounts differ considerably, with average values from 1100 g/day (and more) being reported.5,9–11 The practice of
geophagy is deeply embedded in cultural traditions, and
in many cultural contexts earth eating is seen as normal.
Geophagy clearly also has biological components. A great
deal of misunderstanding surrounds this issue because
0035-9203/$ – see front matter © 2010 Royal Society of Tropical Medicine and Hygiene. Published by Elsevier Ltd. All rights reserved.
doi:10.1016/j.trstmh.2010.09.002
Author's personal copy
788
R. Kutalek et al. / Transactions of the Royal Society of Tropical Medicine and Hygiene 104 (2010) 787–795
Figure 1. Geophagic samples were collected in Tanzania, Kenya, Uganda, Rwanda, Swaziland, Democratic Republic of Congo, Sudan, Burkina Faso and
Senegal, and from ethnic shops in Austria, Belgium, the United Kingdom, and the United States.
the assumption is that it is pathological and because
it is largely practiced in disadvantaged populations or
countries.12
Various hypotheses on geophagy have been forwarded
and there are conflicting views as to whether soil eating is
beneficial to health or not. Several studies point to positive
effects: geophagic material is a source of mineral nutrients – especially of iron13,14 – helps against gestational
nausea15 and detoxifies foods, for example, by adsorption
of various plant secondary compounds.16 The consumption
of clay increases food efficiency,17 which might be important in poor countries. Furthermore, smectite and other
clays have long been used in pharmaceutical preparations
and to treat acute gastroenteritis.18 Other studies report
negative effects, e.g., an association of geophagy with iron
and other mineral nutrient deficiencies,19 anaemia20,21 and
geohelminth infections6,8,9 . Moreover, geophagic materials
can contain toxic heavy metals, especially lead.22–25 The
heavy metals lead, mercury and cadmium are ubiquitous
and persistent environmental pollutants that primarily
affect the kidneys and the brain. Exposure to these metals
during pregnancy and early childhood can impact children’s renal systems and brain development. This implies
the need to control and regulate the potential sources of
lead, mercury and cadmium contamination.
Geophagic earth may vary widely in its physical, mineralogical, and chemical properties.26 In Africa, it is either
procured from local sources, such as termite mounds,
house walls and from natural exposures or it is purchased
in local markets where it has often been traded over long
distances.15 It is ingested as a drink or powder, gnawed or
crushed.
Through international migration, geophagy is also
present in typical immigrant countries. Here, the clay is
mostly imported from African and Asian countries and sold
in ethnic stores and markets in urban areas.13,22 Therefore,
the consumption of soil is increasingly seen as an international public health issue especially regarding pregnant
and breast-feeding women.23–25,27,28
We collected African geophagic soil samples from a
wide geographical range and analysed their contamination
with geohelminths, bacteria and fungi, as well as their content of toxic heavy metals (lead, mercury and cadmium).
To our knowledge, no studies are available on the microbial contamination of geophagic soil. Only a few studies
deal with their heavy metal contents (usually analysing low
sample numbers)22,23,25 or the presence of geohelminths
in geophagic soils consumed by adults.29 Our study is
unique for its combined focus on geohelminths, potentially
pathogenic microorganisms and heavy metals. The broad
interdisciplinary approach and the variety and amount of
African geophagic clays analysed are also a first.
2. Materials and methods
2.1. Sample collection
Geophagic material was purchased from markets or
local shops in Tanzania (Arusha, Moshi, Njombe, Zanzibar),
Uganda (districts Migi, Mubende, Mukono, Wakiso), Kenya,
Rwanda, Swaziland (Nhlangano), Democratic Republic of
Congo (Isiro, Kinshasa, Kisangani), Sudan (Tuok Nyekok),
Burkina Faso and Senegal (Fimla, Joual, Dakar) and from
ethnic shops in the United Kingdom (London), United
States (New York), Belgium (Brussels) and Austria (Vienna)
(Figure 1). All 88 samples originated from Africa, although
specific information on the physical geographical sources
was lacking. Shopkeepers were asked to wrap the substances in materials (mostly paper and plastic bags) they
use for their customers. All samples were numbered and
put into polyethylene bags.
2.2. Mineralogy
The bulk mineralogy and clay mineral composition of
29 samples of geophagic materials were assessed by X-ray
powder diffraction analysis. These samples were considered to be representative of the samples set as a whole
based on their physical appearance and their geographical
location.
2.3. Helminths
As geophagic samples are stored in shops or on markets for an unknown period of time, fresh soil material was
not available. To detect geohelminths about 3 g of each of
Author's personal copy
R. Kutalek et al. / Transactions of the Royal Society of Tropical Medicine and Hygiene 104 (2010) 787–795
the 88 geophagic samples were dispersed in 10 ml sodium
acetate-acetic acid-formalin (SAF) solution according to
Marti and Escher.30 The SAF supernatant was removed and
the sediment was examined microscopically (100-400x
magnification). This method has been successfully used
when analysing palaeo-parasitological material.31
789
(n = 12). The limit of detection (LOD) was determined by
the concentration equivalent to the threefold standard
deviation of the signal of the blank solution and was
0.27 g/kg lead, 0.02 g/kg cadmium, and 0.20 g/kg mercury. Recoveries of reference material were 104% (lead),
84% (cadmium), and 95% (mercury). In six samples, mercury concentrations were below LOD.
2.4. Microbiology
2.6. Statistical analysis
From newly broken surfaces of 88 geophagic samples
material was scraped with sterilised knives and pulverised in sterilised mortars. Then, 0.3 g powder of each
sample was suspended in 2.7 ml buffered pepton water
(bioMérieux, Marcy-l‘Etoile, France) and suspensions were
plated in volumes of 1 ml and 0.1 ml onto different agar
media. The cut off for viable counts of bacteria and fungi
was 10 colony forming units (cfu) per g. For investigation of total viable counts of aerobic bacteria, especially
potentially pathogenic bacteria, Columbia-agar with 5%
sheep blood (bioMérieux) was used.32 Colimycin-nalidixicacid-agar was used for aerobic growth of gram-positive
bacteria,32 and bromthymol-blue-lactose-agar for aerobic
growth of gram-negative bacteria.33 Plates were incubated
aerobically at 35 ◦ C for 24 h and thereafter at 22 ◦ C for an
additional 48–72 h.
Fungi were investigated by plating 1 ml and 0.1 ml
of suspensions onto sabouraud-glucose-gentamycinchoramphenicol-agar (bioMérieux)34 and incubating
aerobically at 30 ◦ C for up to 10 days. Quantitative and qualitative analysis involved counting cfu of morphologically
different bacteria and fungi.
Bacteria were determined to genus level by means
of gram stain, oxidase reaction, catalase reaction and, if
necessary, by API identification system (bioMérieux). The
identification was done mostly to genus level by macroscopic attributes, e.g., speed of growth, pigmentation and
texture of air mycel, and microscopic attributes, e.g., types
of conidia, size, colour and septation of fungal filaments,
and by lactophenol-cotton-blue stained preparations.
2.5. Lead, mercury and cadmium analyses
Between 100 and150 mg of the 88 geophagic samples
and reference materials (light sandy soil [trace elements]
BCR 142R, Institute for Reference Materials and Measurements, Geel, Belgium) were digested with a mixture of
2 ml 65 vol% HNO3 suprapur (Merck, Darmstadt, Germany)
and 0.75 mL 30% H2 O2 (Merck) in a microwave oven (MLS,
mls 1200 mega, Leutkirch, Germany). The sample solutions were volumetrically filled up to 10 ml with deionised
water. Metal concentrations were analysed by AAS using a
Hitachi Z 8200 Polarized Zeeman Atomic Absorption Spectrophotometer (Hitachi, Tokyo, Japan). Lead and cadmium
concentrations were determined by graphite furnace AAS
(GF-AAS). Mercury contents were analysed by cold vapour
AAS (CV-AAS) in combination with an amalgamation unit
(Uwe Binninger Analytik, Schwaebisch Gmuend, Germany)
and a hydride generation system (Hitachi; HFS-3). All samples were measured in duplicate (RSD<10%) by the working
curve method. Quality assurance was achieved by measuring blank test solutions (n = 12) and reference material
The data were analysed statistically, using the SPSS
(Statistic Package for Social Science, SPSS Inc., Chicago, IL,
USA) 17.0 software. Histograms of microbial counts were
checked for normality. Based on the spread of the data, a
log transformation was performed. Log transformation was
used to improve interpretability and visualisation of the
data. All reported P-values were two-sided, and all associations were considered significant when P-values were
< 0.05. Because metal levels were not normally distributed
(Lilliefors test P<0.001), the non-parametric Mann Whitney
U test was applied.
3. Results
3.1. Mineralogy
Many of the soils showed some rudimentary manufacturing. Some samples were mixed with herbs (especially
the Ugandan samples), shaped in certain forms, or made
into a powder. They were mostly air dried and occasionally
baked, smoked or salted. Most samples consisted of the raw
material which can usually be described as a weakly bedded, fine grained mudstone or shale. Both manufactured
and raw materials showed a variety of colours, ranging
from white to light red as assessed by the Munsell Color
chart for soils. The bulk samples were usually dominated
by quartz or by a kaolin-type mineral, which was also dominant in most clay (<2 m) fractions. Some clay fractions,
however, were dominated by a mica-type mineral and others by a swelling smectitic clay mineral (Supplementary
Table 1).
3.2. Helminths
Neither helminth eggs nor larvae were detected in any
of the samples. In one sample (No. 63), an unidentified fragment of an arthropod, probably the larva of an insect (ca.
500 m long), was found.
3.3. Microbiological contamination
All but three of the 88 geophagic samples contained aerobic bacteria. Total viable counts of positive samples ranged
between 10 and 120 000 cfu per gram with a median of
440 cfu/g. The total viable counts were highest in samples
from East Africa (median: 2050 cfu/g) followed by samples from Central Africa (median: 700 cfu/g), West Africa
(median: 130 cfu/g) and imported specimens (median: 65
cfu/g), but the differences were not significant (Figure 2A).
Spore-forming bacteria of the genus Bacillus were most frequent and occurred in all of the 85 geophagic samples with
Author's personal copy
790
R. Kutalek et al. / Transactions of the Royal Society of Tropical Medicine and Hygiene 104 (2010) 787–795
bacterial contamination (Table 1). The Enterobacteriaceae
occurring in two samples in viable counts of 1600 to 26
000 cfu/g belonged to the genera Enterobacter, Klebsiella
and Pantoea which can be summarised as coliform bacteria.
Contamination with fungi was found in 65 of the 88
samples. Total viable counts ranged between 10 and 100 00
cfu/g, with a median for all samples of 30 cfu/g. Values were
highest in specimens from East Africa (median: 60 cfu/g)
followed by imported specimens (median: 50 cfu/g), specimens from West Africa (median: 40 cfu/g) and specimens
from Central Africa (median: 30 cfu/g) (Figure 2B). Moulds
of the genus Penicillium were found most frequently (in 58
samples) (Table 2). Aspergillus flavus which potentially produces aflatoxins occurred in five samples in low numbers.
About one fourth of the samples (all of them from
Congo) were reportedly baked. When differentiating
between baked (n = 21) and unbaked samples (n = 65),
fewer viable counts were found in baked material (mean
value: 1463.8 cfu/g, SD: 3618.2) than in unbaked material
(mean value: 13 788 cfu/g, SD: 28 521.5).
Bacteria
35
(A)
<10 cfu/g
30
10-99 cfu/g
100-999 cfu/g
25
1000-9999 cfu/g
10 000-99 999 cfu/g
20
>100 000 cfu/g
15
10
5
0
Total
Central Africa
East Africa
West Africa
imported
Fungi
40
(B)
35
1-9 cfu/g
30
10-99 cfu/g
25
100-999 cfu/g
3.4. Lead, mercury and cadmium in the geophagic
samples
1000-9999 cfu/g
20
15
The median lead concentration was 40 mg/kg (range:
3–148 mg/kg), the median mercury content 0.053 mg/kg
(range: 0.001–0.637 mg/kg), and the median cadmium concentration 0.055 mg/kg (range: 0.007 and 0.573 mg/kg)
(Table 3). When we tested for region-specific differences,
the levels of all three metals were higher in samples from
Central Africa than in samples from West Africa and East
Africa, respectively (P < 0.05).
The exposure assessment in Tables 4 and 5 is based on
median, minimum and maximum concentrations, respectively. We assumed a daily consumption of 1, 10, 30 and
100 g of geophagic materials, variable bioavailability of
10
5
0
Total
Central Africa
East Africa
West Africa
imported
Figure 2A. Total viable counts of aerobic bacteria in 88 geophagic samples
from different regions ranged between 10 and 120 000 colony forming
units (cfu) per gram with a median of 440 cfu/g. Total viable counts were
highest in samples from East Africa.
Figure 2B. Total viable counts of fungi in 88 geophagic samples from different regions ranged between 10 and 10 000 colony forming units (cfu)
per gram with a median of 30 cfu/g. Values were highest in samples from
East Africa.
Table 1
Groups of bacteria found in geophagic samples from different regions (n = number of samples collected in each region).
Groups of bacteria
Central Africa n = 34
East Africa n = 31
West Africa n = 17
Imported specimens n = 6
Total n = 88
Bacillus spp.
Corynebacterium spp.
Coagulase negative Staphylococci
Micrococcus spp.
Acinetobacter spp.
Enterobacteriaceae
Pseudomonas spp.
32
1
4
1
2
0
0
31
9
5
1
4
1
0
17
8
4
10
2
1
1
5
1
0
2
0
0
0
85
19
13
13
6
2
1
Table 2
Groups of fungi found in geophagic samples from different regions (n = number of samples collected in each region).
Groups of fungi
Central Africa n = 34
East Africa n = 31
West Africa n = 17
Imported specimens n = 6
Total n = 88
Penicillium spp.
Aspergillus spp.
Alternaria spp
Cladosporium spp.
Streptomyces spp.
Acremonium spp.
Paecilomyces spp.
Rhizopus spp.
Chrysonilia spp.
Nigrospora spp.
Scedosporium spp.
Candida spp.
28
7
3
4
1
1
1
0
0
0
0
0
13
10
5
3
3
2
1
1
0
1
1
0
14
6
4
3
0
0
0
1
2
0
0
1
3
1
1
0
0
0
0
0
0
1
0
0
58
24
13
10
4
3
2
2
2
2
1
1
Author's personal copy
R. Kutalek et al. / Transactions of the Royal Society of Tropical Medicine and Hygiene 104 (2010) 787–795
791
Table 3
Lead, mercury and cadmium contents of geophagic samples
n
All
Mean ± SD
88
Median
Range
Central Africa
Mean ± SD
34
Median
Range
West Africa
Mean ± SD
17
Median
Range
East Africa
Mean ± SD
31
Median
Range
Imported (Europe, UK, USA)
Mean ± SD
6
Median
Range
Lead (mg/kg)
n
Mercury (mg/kg)
n
Cadmium (mg/kg)
47 ± 35
40
3–148
82
0.20 ± 0.24
0.050
0.001–0.637
88
0.073 ± 0.078
0.055
0.007–0.573
57 ± 37
59
3–137
34
0.42 ± 0.21
0.53
0.002–0.637
34
0.097 ± 0.093
0.093
0.014–0.573
39 ± 24
34
6–114
15
0.006 ± 0.004
0.005
0.002–0.014
17
0.051 ± 0.094
0.027
0.017–0.413
32 ± 23
29
6–105
28
0.048 ± 0.045
0.035
0.001–0.230
31
0.065 ± 0.046
0.056
0.007–0.206
92 ± 50
89
20–148
5
0.048 ± 0.026
0.0047
0.017–0.074
6
0.044 ± 0.024
0.0051
0.008–0.068
metals (3%, 10%, 30%), body weight of 60 kg for adult
women (Table 4), body weight of 3 kg for newborns
(Table 5), and 100% placentar transfer (see Discussion).
These exposure scenarios were selected because geophagic
material consumption varies substantially in a range
from 1–100 g/day (and more) being reported.5,11 Also,
the amount of bioaccessible (the amount of a contaminant that is released from the matrix [e.g. soil] during
the digestion in the gastrointestinal tract) or bioavailable
(the fraction of an orally administered dose that reaches
the systemic circulation) lead, mercury, and cadmium in
geophagic samples is highly variable depending on the
sample matrix, chemical form of the metal, soil pH, stomach and intestinal pH, soil-to-solution ratio, and fasting
conditions.35–39
4. Discussion
Microbial contamination of geophagic material was
unexpectedly high, especially in unbaked material. The
median lead content was very high, that of cadmium and
mercury relatively low. We found no contamination of
geophagic material with helminths.
4.1. Helminths
Our findings that geophagic materials purchased on
markets are not contaminated with helminths support
the studies by Vermeer and Frate40 and Young et al.29
Geophagy has long been speculated to be a risk factor for
soil-transmitted helminth infection,9,20 especially among
children.6,8 Children, however, are less choosy and are
more likely to use unsafe soil which might contain a higher
helminth density. Past studies differ greatly in their sampling and methods. The only study that determined the
parasite content of earth consumed by adults found no
helminths.29 Even though Toxocara canis and T. cati infection is sometimes associated with geophagy and Toxocara
contamination in soil is quite widespread,41 we found no
eggs or larvae. Furthermore, our study showed a wide geographic distribution of uncontaminated clay.
4.2. Microbial contamination
Microbial contamination of geophagic material was
unexpectedly high, especially in unbaked material. This can
be explained mainly by the long survival time of spores of
the bacteria genus Bacillus under dry conditions. The European Pharmacopoeia42 sets a limit of 1000 aerobic cfu for
clays used for ingestion in pharmaceutical preparations.
Current FAO standards43 for dry foodstuff, which does not
undergo germ-reducing procedures before consumption,
require total viable counts of aerobic mesophilic bacteria
to be below 100 000 cfu/g, and four out of five samples
should have viable counts below 10 000 cfu/g. In our study,
two out of 88 samples exceeded values of 100 000 cfu/g;
10 samples reached counts between 10 000 and 99 999
cfu/g. In addition, a second criterion in FAO standards limits
the amount of coliform bacteria to 100 cfu/g. Both samples
containing coliform bacteria exceeded this amount and had
total viable counts >10 000 cfu/g.
The microbiological investigation of the samples
showed that two of 88 samples exceeded limits for total
viable counts of aerobic mesophilic bacteria of the genus
Bacillus and two further samples contained high numbers
of coliform bacteria; accordingly, four samples would be
rejected if examined as foodstuff. Some of the most frequently found aerobic spore-forming bacteria of the genus
Bacillus could potentially cause gastrointestinal irritation
when germinating in the upper gastrointestinal tract by
producing toxins. The presence of coliform bacteria indicates faecal contamination and the potential presence of
diarrhoeal pathogens.
Limits for fungal contamination, especially moulds, are
not included in the FAO standards. According to the German
Society for Hygiene and Microbiology (DGHM)44 standards,
however, mould contamination is allowable up to 10 000
cfu/g for instant products. None of the geophagic clay
792
Table 4
Daily lead, mercury and cadmium intake through ingestion of geophagic materials for a person weighing 60 kg in various exposure scenarios.
Daily ingestion: 1 g
3% BA
MED
MIN
MAX
Pb intake (mg/kg body weight/day)
0.000020
0.000067
0.000200
0.000002
0.000005
0.000015
0.000074
0.000247
0.000740
Hg intake (g/kg body weight/day)
0.000000
0.000000
0.000000
0.000000
0.000000
0.000000
0.000000
0.000001
0.000003
Cd intake (g/kg body weight/day)
0.000000
0.000000
0.000000
0.000000
0.000000
0.000000
0.000000
0.000001
0.000003
Daily ingestion: 100 g
3% BA
10% BA
30% BA
3% BA
10% BA
30% BA
3% BA
10% BA
30% BA
0.000200
0.000015
0.000740
0.000667
0.000050
0.002467
0.002000
0.000150
0.007400
0.00060
0.00005
0.00222
0.00200
0.00015
0.00740
0.00600
0.00045
0.02220
0.00200
0.00015
0.00740
0.00667
0.00050
0.02467
0.02000
0.00150
0.07400
0.000000
0.000000
0.000003
0.000001
0.000000
0.000011
0.000003
0.000000
0.000032
0.00000
0.00000
0.00001
0.00000
0.00000
0.00003
0.00001
0.00000
0.00010
0.00000
0.00000
0.00003
0.00001
0.00000
0.00011
0.00003
0.00000
0.00032
0.000000
0.000000
0.000003
0.000001
0.000000
0.000010
0.000003
0.000000
0.000029
0.00000
0.00000
0.00001
0.00000
0.00000
0.00003
0.00001
0.00000
0.00009
0.00000
0.00000
0.00003
0.00001
0.00000
0.00010
0.00003
0.00000
0.00029
Pb: lead; Hg: mercury; Cd: cadmium
BA: Bioavailability; MED: Median; MIN: Minimum; MAX: Maximum; mg: milligrams; g: micrograms
Metal intakes exceeding the provisional tolerable daily intake (PTDI) are marked in bold. The PTDI was calculated from the provisional tolerable weekly intake (PTWI) (i.e., 0.025 mg/kg body weight/week (Pb),
5 g/kg body weight/week (Hg), 7 g/kg body weight/week (Cd)), which is defined as the estimate of the amount of a substance that can be ingested over a lifetime without appreciable risk to health.
Table 5
Daily lead, mercury, and cadmium intake through ingestion of geophagic materials for a newborn weighing 3 kg in various exposure scenarios.
Daily ingestion: 1 g
3% BA
MED
MIN
MAX
MED
MIN
MAX
MED
MIN
MAX
Pb (mg/kg) in soil
40
3
148
Hg (g/kg) in soil
0.050
0.001
0.637
Cd (g/kg) in soil
0.055
0.007
0.573
10% BA
Daily ingestion: 10 g
30% BA
Pb intake (mg/kg body weight/day)
0.000400
0.001333
0.004000
0.000030
0.000100
0.000300
0.001480
0.004933
0.014800
Hg intake (g/kg body weight/day)
0.000001
0.000002
0.000005
0.000000
0.000000
0.000000
0.000006
0.000021
0.000064
Cd intake (g/kg body weight/day)
0.000001
0.000002
0.000006
0.000000
0.000000
0.000001
0.000006
0.000019
0.000057
Daily ingestion: 30 g
Daily ingestion: 100 g
3% BA
10% BA
30% BA
3% BA
10% BA
30% BA
3% BA
10% BA
30% BA
0.004000
0.000300
0.014800
0.013333
0.001000
0.049333
0.040000
0.003000
0.148000
0.01200
0.00090
0.04440
0.04000
0.00300
0.14800
0.12000
0.00900
0.44400
0.04000
0.00300
0.14800
0.13333
0.01000
0.49333
0.40000
0.03000
1.48000
0.000005
0.000000
0.000064
0.000017
0.000000
0.000212
0.000050
0.000001
0.000637
0.00002
0.00000
0.00019
0.00005
0.00000
0.00064
0.00015
0.00000
0.00191
0.00005
0.00000
0.00064
0.00017
0.00000
0.00212
0.00050
0.00001
0.00637
0.000006
0.000001
0.000057
0.000018
0.000002
0.000191
0.000055
0.000007
0.000573
0.00002
0.00000
0.00017
0.00006
0.00001
0.00057
0.00017
0.00002
0.00172
0.00006
0.00001
0.00057
0.00018
0.00002
0.00191
0.00055
0.00007
0.00573
Pb: lead; Hg: mercury; Cd: cadmium
BA: Bioavailability; MED: Median; MIN: Minimum; MAX: Maximum; mg: milligrams; g: micrograms
Metal intakes exceeding the provisional tolerable daily intake (PTDI) are marked in bold. The PTDI was calculated from the provisional tolerable weekly intake (PTWI) (i.e., 0.025 mg/kg body weight/week (Pb),
5 g/kg body weight/week (Hg), 7 g/kg body weight/week (Cd)), which is defined as the estimate of the amount of a substance that can be ingested over a lifetime without appreciable risk to health.
Author's personal copy
MED
MIN
MAX
Pb (mg/kg) in soil
40
3
148
Hg (g/kg) in soil
0.050
0.001
0.637
Cd (g/kg) in soil
0.055
0.007
0.573
30% BA
Daily ingestion: 30 g
R. Kutalek et al. / Transactions of the Royal Society of Tropical Medicine and Hygiene 104 (2010) 787–795
MED
MIN
MAX
10% BA
Daily ingestion: 10 g
Author's personal copy
R. Kutalek et al. / Transactions of the Royal Society of Tropical Medicine and Hygiene 104 (2010) 787–795
samples exceeded this limit. The low counts of the potentially aflatoxin-producing Aspergillus flavus in the samples
indicate a low threat for human health.
These microbiological results indicate no concrete
health hazard following the consumption of the geophagic
clay products. They do, however, give cause for concern
because, contrary to most food purchased on markets
(which is either cooked or peeled before consumption),
geophagic material is typically consumed uncooked.
4.3. Levels of lead, mercury and cadmium
Lead and cadmium are less bioavailable than mercury.35
Bioaccessibility of lead in various soil types amount to
3–83%,38,45 with the value being 3% in geophagic soils.13
Mercury bioaccessibility ranges between 5% and 100%
depending on its chemical form (mercuric sulfide: 1%, total
mercury: 5%, mercuric chloride: 100%),36 and that of cadmium is certainly beyond 30%.39
Lead intake through geophagic soil consumption by a
person weighing 60 kg exceeds the PTDI of 0.0036 mg/kg
body weight when more than 10 g are consumed per day
and when bioavailability of lead is relatively high (>10%)
(Table 4). The exposure assessment shows that newborns
(3 kg body weight) are at a higher risk of exceeding the PTDI
of lead (Table 5). Nonetheless, the PTDI of 0.714 g/kg body
weight (mercury) and 1.0 g/kg body weight (cadmium) is
not exceeded by any of the exposure scenarios assumed
here. The daily ingestion of geophagic clay does not contribute to unsafe mercury and cadmium intakes, neither
in adults nor newborns. The risk of prenatal cadmium
exposure is even lower than estimated here: this metal is
trapped by placenta tissues, with very little reaching the
fetus.46 In the case of lead, however, adults and particularly
newborns are at risk to exceed critical levels. Lead exposure of pregnant and breast-feeding women gives cause
for concern. This metal easily crosses the placenta and is
excreted into breast milk. The fetus is particularly sensitive to lead, which is a potent neurotoxin. Adverse effects
on child neurodevelopment and physical growth may occur
even at relatively low exposure levels.47 Children are also
known to consume geophagic clays.6–8,25
Two factors should be considered when interpreting our
exposure assessment. First, consumption habits are known
to vary substantially: thus, we might have overestimated
the risk by assuming daily consumption. Nonetheless,
representative data on consumption habits are not yet
available. Second, the percentage of lead that is bioavailable
to humans in the soils analyzed here is highly speculative. In one scenario the metal is embedded within the
structure of the constituent minerals. If such, host minerals are insoluble, then the metal would probably not be
bioavailable and would simply pass through the body. If,
however, the metal results from the external environment,
then it will probably be adsorbed at the surfaces of the
fine-grained minerals in the geophagic materials. In this
scenario, bioavailability will depend, amongst other things,
on the adsorption mechanism involved. Again, metals such
as lead potentially precipitate in forms that are so insoluble as to render them completely non-available. Finally, the
pH and particle size distribution of the geophagic materi-
793
als, as well as age, nutritional status, dietary composition
and body weight of the exposed individual needs to be
taken into account.26,48 These issues would require further
detailed research.
Our exposure assessment refers to the provisional tolerable weekly intake (PTWI) levels set by the Joint FAO/WHO
Expert Committee on Food Additives (JECFA), which are
appropriate guideline values with regard to metal toxicity. To date, there is no consensus on which regulatory
guidelines should be applied to geophagic soil samples.
The UK Food Standards Agency23 and other authors13,22
find the application of food quality standards for geophagic
material appropriate because it is consumed in large
quantities.27 According to EC Commission Regulation (No.
466/2001)49 the highest concentration of lead, cadmium
and mercury permitted in specific foodstuffs should not
exceed 1 mg/kg. The European Pharmacopoeia43 has set a
maximum level of 25 mg/kg lead for clays for internal use.
These clays, however, are used in much lower quantity than
geophagic material.
Metal levels in geophagic samples differed greatly
according to sampling site. The regional differences in
the lead, mercury, and cadmium levels between samples
collected, but, as already mentioned, not necessarily originating, from Central Africa and samples collected from
West Africa and East Africa are significant. They show that
pregnant women consuming geophagic soils in Central
Africa are at higher risk than pregnant women consuming geophagic soil in other regions. Many of the samples
we examined are clearly rock samples, not soils, and have
presumably been sampled mainly from natural outcrop
exposures (Supplementary Table 1). This calls for consideration of the mean lead, mercury, and cadmium contents
that such materials (clays and shales) contain in their natural state. The mean cadmium content of shales is 1 ppm,
that of mercury ∼0.4 ppm. The levels of these two metals
in our samples were much lower. For lead, however, the
mean content in clays and shales is ∼22 ppm.50 The levels
in our samples are therefore twice as high as those occurring naturally in shales and clays. It is not known at present
whether this enrichment is natural or due to contaminating
sources from the atmosphere or from surface waters.
5. Conclusions
Geophagic soil samples can be contaminated with
pathogenic microbes. This gives cause for concern because
these materials are usually consumed uncooked. Furthermore, the high lead contents of some soil samples are
problematic. When pregnant females regularly consume
highly contaminated soils, the vulnerable fetus might be
exposed to undesirably high lead levels. Note, however,
that lead is one of the least bioavailable metals and probably only a fraction will become bioaccessible. This calls for
cautiously interpreting the risk. We found cadmium and
mercury in low to very low concentrations in geophagic
materials. Thus, it is unlikely that geophagy contributes to
toxic cadmium and mercury exposure levels.
To date, we cannot satisfactorily estimate the health
risks associated with geophagy. Most of the exposure factors and individual risk factors are poorly known. Data are
Author's personal copy
794
R. Kutalek et al. / Transactions of the Royal Society of Tropical Medicine and Hygiene 104 (2010) 787–795
required with regard to: (1) consumption habits, particularly of pregnant and lactating women, and children, (2)
nature and provenance of the geophagic materials and the
ways in which they are prepared or manufactured and
consumed, (3) bioaccessibility and bioavailability of lead,
cadmium, and mercury (including the particularly neurotoxic compound methyl mercury) in geophagic soils and
(4) prenatal metal exposures of children born to mothers
who practice geophagy.
Because of the frequency and nearly worldwide distribution of earth consumption, as well as the perceived
benefits of geophagy (e.g., reduced nausea during pregnancy), it is unlikely that consumers will refrain from
the practice. Regulations will be difficult to apply because
geophagic materials are often not sold openly, especially in
Europe.27
Overall, our current knowledge suggests that the
periodic consumption of geophagic materials should be
discouraged, particularly during pregnancy.
Authors’ contributions: RK and AP designed the study,
oversaw sample collection and drafted the article; GW
and SH examined the samples, wrote the microbiology
methods, and interpreted the results on microbiology; CG
examined the samples, wrote the methods on heavy metal
analyses, and interpreted the results on heavy metals; HA
examined the samples, wrote the methods on helminth
analyses and interpreted the results on geohelminths. JW
and SHi examined the samples, wrote the methods on mineralogy and interpreted the results; DH wrote the methods
on statistical data and interpreted the results statistically;
MS helped with the interpretation of results and critically
revised the article. All of the authors revised the manuscript
critically for important intellectual content and approved
the final version submitted for publication. AP is guarantor
of the paper.
Acknowledgements: We thank all the persons who
helped in obtaining geophagic samples and with laboratory
work, especially Ingrid Gruener. SH acknowledges support
from the Scottish Executive Environment and Rural Affairs
Department (SEERAD). We thank Manfred Maier, Sera L.
Young and Horst Aspöck for valuable comments on a previous draft of the manuscript.
Funding: Medical University of Vienna, the Austrian
Agency for Health and Food Safety AGES, and the Macaulay
Land Use Research Institute, Aberdeen, United Kingdom.
Conflicts of interest: None declared.
Ethical approval: Not required.
Appendix A. Supplementary data
Supplementary data associated with this article can be found, in the online version, at
doi:10.1016/j.trstmh.2010.09.002.
References
1. Halsted JA. Geophagia in man: its nature and nutritional effects. Am
J Clin Nutr 1968;21:1384–93.
2. Laufer B. Geophagy. Chicago: Field Museum of Natural History; 1930.
3. Anell B, Lagercrantz S. Geophagical customs. Studia Ethnographica
Upsaliensia 17. Uppsala: Almqvist and Wiksell Boktryckeri AB; 1958.
4. Abrahams PW, Parsons JA. Geophagy in the tropics. A literature
review. Geogr J 1996;162:63–72.
5. Luoba AI, Geissler PW, Estambale B, Ouma JH, Magnussen P, Alusala
D, et al. Geophagy among pregnant and lactating women in Bondo
District, western Kenya. Trans R Soc Trop Med Hyg 2004;98:734–41.
6. Saathoff E, Olsen A, Kvalsvig JD, Geissler PW. Geophagy and its
association with geohelminth infection in rural schoolchildren from
northern KwaZulu-Natal, South Africa. Trans R Soc Trop Med Hyg
2002;96:485–90.
7. Geissler PW. The significance of earth-eating: social and cultural
aspects of geophagy among Luo children. Africa 2000;70:653–82.
8. Glickman LT, Camara AO, Glickman NW, McCabe GP. Nematode
intestinal parasites of children in rural Guinea, Africa: prevalence
and relationship to geophagia. Int J Epidemiol 1999;28:169–74.
9. Luoba AI, Geissler PW, Estambale B, Ouma JH, Alusala D, Ayah R, et al.
Earth-eating and reinfection with intestinal helminths among pregnant and lactating women in western Kenya. Trop Med Int Health
2005;10:220–7.
10. Prince RJ, Luoba AI, Adhiambo P, Ng’uono J, Geissler PW. Geophagy is
common among Luo women in western Kenya. Trans R Soc Trop Med
Hyg 1999;93:515–6.
11. Hunter JM. Insect clay geophagy in Sierra Leone. J Cult Geogr
1984;4:2–13.
12. Reid RM. Cultural and medical perspectives on geophagia. Med Anth
1992;13:337–51.
13. Abrahams PW, Follansbee MH, Hunt A, Smith B, Wragg J. Iron
nutrition and possible lead toxicity: an appraisal of geophagy undertaken by pregnant women of UK Asian communities. Appl Geochem
2006;21:98–108.
14. Yanai J, Noguchi J, Yamada H, Sugihara S, Kilasara M, Kosaki T. Function of geophagy as supplementation of micronutrients in Tanzania.
Soil Sci Plant Nutr 2009;55:215–23.
15. Vermeer DE, Ferrell RE. Nigerian geophagical clay: A traditional
antidiarrheal pharmaceutical. Science 1985;227:634–6.
16. Johns T, Duquette M. Detoxification and mineral supplementation as
functions of geophagy. Am J Clin Nutr 1991;53:448–56.
17. Habold C, Reichardt F, Le Maho Y, Angel F, Liewig N, Lignot JH, et
al. Clay ingestion enhances intestinal triacylglycerol hydrolysis and
non-esterified fatty acid absorption. Br J Nutr 2009;102:249–57.
18. Szajewska H, Dziechciarz P, Mrukowicz J. Meta-analysis: Smectite
in the treatment of acute infectious diarrhoea in children. Aliment
Pharmacol Ther 2006;23:217–27.
19. Hooda P, Henry J, Seyoum TA, Armstrong LDM, Fowler MB.
The potential impact of geophagia on the bioavailability of iron,
zinc and calcium in human nutrition. Environ Geochem Health
2002;24:305–19.
20. Kawai K, Saathoff E, Antelman G, Msamanga G, Fawzi WW. Geophagy
(soil-eating) in relation to anemia and helminth infection among
HIV infected pregnant women in Tanzania. Am J Trop Med Hyg
2009;80:36–43.
21. Geissler PW, Shulman CE, Prince RJ, Mutemi W, Mnazi C, Friis H, et
al. Geophagy, iron status and anaemia among pregnant women on
the coast of Kenya. Trans R Soc Trop Med Hyg 1998;92:549–53.
22. Dean JR, Deary ME, Gbefa BK, Scott WC. Characterisation and analysis
of persistent organic pollutants and major, minor and trace elements
in Calabash chalk. Chemosphere 2004;57:21–5.
23. Food Standards Agency. Lead contamination of calabash chalk.
2002; London: Food Standards Agency; www.food.gov.uk/
enforcement/alerts/2002/oct/94151. [accessed 29 July 2008].
24. U.S. Food and Drug Administration. Nzu, traditional remedy for
morning sickness. 2009; http://www.fda.gov/Safety/MedWatch/
SafetyInformation/SafetyAlertsforHumanMedicalProducts/ucm
196045.htm. [accessed 14 July 2010].
25. RIVM-RIKILT Front Office Food Safety. Risk assessment concerning
dioxins and heavy metals in clay products for human consumption.
2009; http://www.vwa.nl/txmpub/files/?p file id=42303. [accessed
14 July 2010].
26. Wilson MJ. Clay mineralogical and related characteristics of
geophagic materials. J Chem Ecol 2003;29:1525–47.
27. Middleton J. Sikor consumption by Asian ethnic groups: an unquantified health hazard. Fac Med Dent Bull (Univ Birmingham) 1989;77:
4–5.
Author's personal copy
R. Kutalek et al. / Transactions of the Royal Society of Tropical Medicine and Hygiene 104 (2010) 787–795
28. WHO. Calabash chalk may pose health risk for pregnant and breastfeeding women. WHO Pharm Newsl 2007, 5: 6.
29. Young SL, Goodman D, Farag TH, Ali SM, Khatib MR, Khalfan SS,
et al. Geophagia is not associated with Trichuris or hookworm
transmission in Zanzibar, Tanzania. Trans R Soc Trop Med Hyg
2007;101:766–72.
30. Marti H, Escher E. SAF – an alternative fixation solution for parasitological stool specimens. Schweiz Med Wochenschr 1990;120:1473–6.
31. Aspöck H, Auer H, Picher O. Trichuris trichiura eggs in the neolothic
glacier mummy from the Alps. Parasitol Today 1996;12:255–6.
32. Murray PR, Barron EJ, Pfaller MA, Tenover FC, Yolken RH. Manual of
clinical microbiology. 6th ed. Herndon, USA: ASM Press; 1995.
33. Dupeyron CM, Guillermin GA, Leluan GJ. Rapid diagnosis of gram
negative urinary infections: identification and antimicrobial susceptibility testing in 24 hours. J Clin Pathol 1986;39:208–11.
34. De Hoog GS, Guatto J, Gené J, Figueras MJ. Atlas of clinical fungi. 2nd
ed. Utrecht: Centraalbureau voor Schimmelcultures; 2000.
35. Sheppard SC, Evenden WG, Schwartz WJ. Ingested soil: bioavailability of sorbed lead, cadmium, cesium, iodine, and mercury. J Environ
Qual 1995;24:498–505.
36. Barnett MO, Turner RR. Bioaccessibility of mercury in soils. Soil Sediment Contam 2001;10:301–16.
37. Yang J-K, Barnett MO, Jardine PM, Brooks SC. Factors controlling the
bioaccessibility of arsenic(V) and lead(II) in soil. Soil Sediment Contam
2003;12:165–79.
38. Marschner B, Welge P, Hack A, Wittsiepe J, Wilhelm M. Comparison of soil Pb in vitro bioaccessibility and in vivo bioavailability
with Pb pools from a sequential soil extraction. Environ Sci Technol
2006;40:2812–8.
39. Juhasz AL, Weber J, Naidu R, Gancarz D, Rofe A, Todor D, et al. Determination of cadmium relative bioavailability in contaminated soils
and its prediction using in vitro methodologies. Environ Sci Technol
2010;44:5240–7.
795
40. Vermeer DE, Frate DA. Geophagia in rural Mississippi: environmental and cultural contexts and nutritional implications. Am J Clin Nutr
1979;32:2129–35.
41. Auer H, Aspöck H. The diagnosis of Toxocara infestations and of
human toxocarosis [German]. J Lab Med 2006;30:1–12.
42. European Pharmacopoeia (Europäisches Arzneibuch) (official Austrian version). 6th ed. Vienna: Verlag Oesterreich; 2008.
43. FAO. Manual of food quality control, 4 Rev. 1. Microbiological analysis. Rome: Food and Agriculture Organisation of the United Nations;
1992.
44. DGHM (German Society of Hygiene and Microbiology). Guidance levels and critical limits for the assessment of food: A recommendation
of the working group of the Commission Food Microbiology and
Hygiene of the German Society of Hygiene and Microbiology (DGHM)
[in German]. Bundesgesundheitsblatt 1988, 31: 93–4.
45. Ruby MV, Davis A, Schoof R, Eberle S, Sellstone CM. Estimation of lead
and arsenic bioavailability using a physiologically based extraction
test. Environ Sci Technol 1996;30:422–30.
46. Lee CK, Lee JT, Yu SJ, Kang SG, Moon CS, Choi YH, et al. Effects of cadmium on the expression of placental lactogens and Pit-1 genes in the
rat placental trophoblast cells. Mol Cell Endocrinol 2009;298:11–8.
47. Wigle DT, Arbuckle TE, Walker M, Wade MG, Liu S, Krewski D. Environmental hazards: evidence for effects on child health. J Toxicol
Environ Health B Crit Rev 2007;10:3–39.
48. ATSDR. Summary report for the ATSDR soil-pica workshop, June
2000, Atlanta, Georgia. Atlanta: Agency for Toxic Substances
and Disease Registry; 2001. www.atsdr.cdc.gov/NEWS/soilpica.html.
[accessed 10 December 2009].
49. EU Commission. Commission Regulation (EC) No 466/2001 of 8
March 2001 setting maximum levels for certain contaminants in
foodstuffs. Brussels: European Commission; 2001.
50. Wedepohl, KH. Handbook of Geochemistry. Volume II-5: Elements
La(57)-U(92). Lead 82. Berlin: Springer Verlag; 1978 p. K2–K3.