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ISSN: 2161-0525

Krüger et al., J Environ Anal Toxicol 2014, 4:2
DOI: 10.4172/2161-0525.1000210

Research Article
Research
ArticleOpenAccess
AccessOpen

Detection of Glyphosate Residues in Animals and Humans
Monika Krüger1, Philipp Schledorn1, Wieland Schrödl1, Hans-Wolfgang Hoppe2, Walburga Lutz3 and Awad A. Shehata1,4*
Institute of Bacteriology and Mycology of Veterinary Faculty, University of Leipzig, Germany
Medizinisches Labor Bremen Haferwende 12, 28357 Bremen, Germany
3
Wildlife Research Institute, Bonn, Germany
4
Avian and Rabbit Diseases Department, Faculty of Veterinary Medicine, Sadat City University, Egypt
1
2

Abstract
In the present study glyphosate residues were tested in urine and different organs of dairy cows as well as in urineof hares, rabbits and humans using ELISA and Gas Chromatography-Mass Spectroscopy (GC-MS). The correlation
coefficients between ELISA and GC-MS were 0.96, 0.87, 0.97and 0.96 for cattle, human, and rabbit urine and organs,respectively. The recovery rate of glyphosate in spiked meat using ELISA was 91%. Glyphosate excretion in German
dairy cows was significantly lower than Danish cows. Cows kept in genetically modified free area had significantly
lower glyphosate concentrations in urine than conventional husbandry cows. Also glyphosate was detected in different
organs of slaughtered cows as intestine, liver, muscles, spleen and kidney. Fattening rabbits showed significantly
higher glyphosate residues in urine than hares. Moreover, glyphosate was significantly higher in urine of humans withconventional feeding. Furthermore, chronically ill humans showed significantly higher glyphosate residues in urine thanhealthy population. The presence of glyphosate residues in both humans and animals could haul the entire population
towards numerous health hazards, studying the impact of glyphosate residues on health is warranted and the global
regulations for the use of glyphosate may have to be re-evaluated.

Keywords: Glyphosate; Animals; Husbandry cows; Health hazards;
Gas Chromatography Mass Spectroscopy (GC-MS); ELISA

Introduction
Glyphosate (N-phosphonomethyl glycine) is registered as herbicide
for many food and non-food crops as well as non-crop areas where total
vegetation control is desired. The predominating uses of glyphosate, indescending order, are stubble management, pre-sowing applicationand pre-harvest application (desiccation). Glyphosate is also used toprevent weeds in fields with glyphosate resistant genetically modified(GM) crops like soybean, rapeseed, corn, etc. Since 1996 the amountand the number of genetically engineered crops dramatically increased
worldwide. It is estimated that 90% of the transgenic crops grownworldwide are glyphosate resistant [1]. The rapidly growing problem
of glyphosate-resistant weeds is reflected in steady increases in theuse of glyphosate on crops. Steams, leaves and beans of glyphosate
resistant soy are contaminated with glyphosate. Moreover, due to theintensive use of glyphosate it was frequently detected in water, rain
and air. Chang and coworkers [2] detected glyphosate concentrations
in air and rain up to 2.5 μg/L in agricultural areas in Mississippi and
Iowa. In Europe GM soybean for food and feed was admitted in
1996. All animals and humans eating this soy chronically incorporate
unknown amounts of this herbicide. Residues of glyphosate in tissues
and organs of food animals fed with GM feed (soybean, corn, etc.) are
not considered or neglected in legislation. The influence of glyphosate
residues on the quality of animal Products intended for human foodis almost unknown. The incorporation of GM soybean meal in broiler
feed significantly affects the color parameter for breast muscles [3]. In
contrast Erickson and coworkers [4] did not find any effects on theperformance and carcass characteristics of feedlot steers. Furthermore,glyphosate is a potent chelator fixing trace and macro elements [5-7].
The mode of action of glyphosate is through specific inhibition of
5-enolpyruvyl shikimate 3-phosphate synthase (EPSPS), an enzyme ofthe shikimate pathway that governs the synthesis of aromatic amino
compounds in higher plants, algae, bacteria and fungi [8]. As thisenzyme is absent in mammals it is often assumed that glyphosate is notharmful for mammalians. Even so, there is an ongoing debate about
J Environ Anal Toxicol
ISSN: 2161-0525 JEAT, an open access journal

the safety of this herbicide. Firstly, long-term toxicology of the low
glyphosate residues has not been investigated in vertebrates. Secondly
although EPSPS is absent, glyphosate has been reported to inhibit otherenzymes, e.g., enzymes of the cytochrome P450 (Cyp450) family [8].
Other inhibition pathways are reported. Richard et al. [9] reported thatsuch as glyphosate inhibits Cyp450 aromatase inhibition, indicatedcrucial for sex steroid hormone synthesis.
Glyphosate also interferes with cytochrome P450 enzymes which
include numerous proteins able to metabolize xenobiotics [10]. This
may also act synergistically with disruption of the biosynthesis ofaromatic amino acids by gut bacteria, as well as impairment in serum
sulfate transport. Recently, it was suggested that gastrointestinal
disorders, obesity, diabetes, heart disease, depression, autism,
infertility, cancer and Alzheimer’s disease are associated with Western
diet [11]. Furthermore, genotoxic activity [12], teratogenic activity[13], and disturbance of the normal gut bacterial community [14,15]
due to glyphosate are reported. Glyphosate showed cytotoxic effects
on different cells in vitro [16-18], and Barbosa et al. [19], proposedthat glyphosate may have contributed to the Parkinsonism due to its
chemical similarity with glycine, a co-factor required for activation of
the N-methyl-d-aspartase (NMDA) receptor, which controls excitatory
actions in the central nervous system and is also involved in memory
and learning. However, in clinical studies has not shown NMDA
activity in relation to glyphosate poisoning [20].

*Corresponding author: Dr. Awad A Shehata, Institute of Bacteriology andMycology of Veterinary Faculty, University of Leipzig, Germany, Tel: 004903419738183; Fax: 0049-03419738199; E-mail: shehata@vetmed.uni-leipzig.deReceived January 04, 2014; Accepted January 28, 2014; Published January
31, 2014
Citation: Krüger M, Schledorn P, Schrödl W, Hoppe HW, Lutz W, et al. (2014)
Detection of Glyphosate Residues in Animals and Humans. J Environ Anal Toxicol
4: 210. doi: 10.4172/2161-0525.1000210
Copyright: © 2014 Krüger M, et al. This is an open-access article distributed under
the terms of the Creative Commons Attribution License, which permits unrestricted
use, distribution, and reproduction in any medium, provided the original author andsource are credited.

Volume 4 • Issue 2 • 1000210

Citation: Krüger M, Schledorn P, Schrödl W, Hoppe HW, Lutz W, et al. (2014) Detection of Glyphosate Residues in Animals and Humans. J Environ
Anal Toxicol 4: 210. doi: 10.4172/2161-0525.1000210

Page 2 of 5
The aim of the present study was to investigate if glyphosate residues
in different biological samples from humans and animals can be used togain insight in the exposure situation.

Material and Methods

The samples were measured using a GC-MSMS system. This system
was composed of a gas chromatograph 7890 A equipped with a split/
split less injector connected to 7000 Triple-Quad mass spectrometer
operating in the chemical ionization (NCI) -Mode (both instrumentsfrom Agilent Technologies, Waldbronn, Germany).

Samples

Statistical analysis

Samples from German dairy cows were collected as follow: urine
from conventional husbandry (N=343), urine from cows kept in GM
free areas (N=32), organs from slaughtered cows from conventional
husbandry (gut wall [(N=32]), liver [N=41], kidney [N=26], lung
[N=23] and muscles [N=6]. Urine samples also were collected from
Danish cows (N=242). A total of 193 and 77 urine samples were collectedfrom hares and fattening rabbits, respectively. In addition, a total of 99
and 41 urine samples were collected from humans with conventionalor organic diet, respectively. Furthermore, a total of 102 and 199 urine
samples were collected of healthy and chronically diseased humans. All
samples were frozen at -20°C until analyzed.

The statistical analysis was carried out with GraphPad Prism 4(GaphPad Software, La Jolla, USA). Two-way analysis of variancefollowed by unpaired Student t-test was used to identify significant
differences between means.

Sample preparations
Tissue samples were minced to small pieces (~ 0.25 cm). In relation
to the ability to retain water, samples were diluted with distilled water(Braun, Germany) at the rate of 1:1 (low water retention), 1:5 or 1:10
(high water retention). The specimens were heated at 100°C for 10 min,homogenized and frozen at -80°C for 8 h. Samples were carefully thawed
at 40°C and centrifuged at 10.000 x g for 10 min. The supernatant was
filtered with an ultra-centrifugal filter with a cut off of 3000 Da toremove proteins and peptides. Filtrates were centrifuged (10.000 x g)
again at 20°C for 10 min and the supernatant was tested for glyphosate
using ELISA and Gas Chromatography-Mass Spectroscopy (GC-MS).
Urine samples were diluted with distilled water (Braun, Germany) at
the rate of 1:20.

ELISA
Prepared samples were tested for glyphosate concentration by
ELISA using glyphosate ELISA kits (Abraxis, USA) according to
the manufacturer´s protocol. Test validation of ELISA was done incomparison with GC-MS and the Spearman rank order correlation
analysis was calculated for human urine (N=14), cows urine (N=21),
cow tissues (N=16), and rabbit urine (N=13). To study the recovery rateof glyphosate, meat samples were spiked with 100 μg of glyphosate which
was carefully distributed in the meat and processed as mentioned above
then the glyphosate was measured in the supernatant using ELISA.

Gas chromatography-mass spectroscopy
Glyphosate in urine and tissue samples was measured according
to the procedure of Alferness and coworkers [21] with somemodifications. Briefly, all chemicals used were of analytical grade unlessstated otherwise. Urine samples and prepared tissue samples were
thawed and equilibrated to room temperature. Samples were vortex
mixed prior to transferring 100 μl aliquots to 10 ml screw-capped
glass tubes containing 1 ml of acetonitrile. To each sample internal
standard solution containing 13C215N-Glyphosate was added. Afterevaporation to dryness in a vacuum centrifuge, for derivatization 0.5
ml of 2,2,2-trifluoroethanol and cautiously 1 ml of freezing cold (-40°C)
trifluoroacetic anhydride were added to the residue. The mixture wasvortex mixed briefly and sonicated for 10 min and heated to 85°C
for 1 h. After cooling the tube was uncapped and the solution was
cautiously evaporated at 80-85°C without a stream of air or nitrogen.
After cooling, the oily residue was dissolved in 200 μl of acetonitrile.
J Environ Anal Toxicol
ISSN: 2161-0525 JEAT, an open access journal

Results
Validation of analytical method
The correlation coefficients between ELISA and GC-MSMS were
0.96, 0.87, 0.97, and 0.96 for cattle urines, human urines, rabbit urines
and tissues, respectively, (Table 1). The recovery rate of glyphosate inspiked meat was 91% (Table 2).

CattleGlyphosate excretion in German dairy cows was significantly(P<0.0001) higher than Danish cows (Figure 1A). Surprisingly, cows
kept in GM free region had significantly (p<0.001) lower glyphosate
concentrations in their urine compared with cows under conventional
husbandry (Figure 1B). Also glyphosate was detected in different organsof slaughtered cows including intestine, liver, muscles, spleen andkidney (Figure 1C). There were no significant differences of glyphosate
residues in these organs.

Hares and rabbits
Hares showed significantly lower (P<0.0001) glyphosate residues inurine than fattening rabbit (Figure 2).

HumansGlyphosate was significantly higher (P<0.0002) in humans feed
conventional feed compared with predominantly organic feed humans(Figure 3). Also the glyphosate residues in urine were grouped
Glyphosate (µg/ml or µg/g)
ELISA

GC-MS

Mean ±
Minimum Maximum
Minimum MaximumSD

Mean ±
SD

R2

Human
urine
(N=14)

0.1

71.3

9± 15

01

40

5.4± 11.5 0.87

Cows
urine
(N=21)

0.46

164

27± 420164

35± 50

Rabbiturine(N=16)

2.3770

17.9±193.17

4212.5±12.1 0.97

Organs(N=13)

1.3680

14.7± 21

4.7

108

20±26

0.96

0.96

Table 1: Spearman rank order correlation analysis between ELISA and GC-MS.
spikedstandard recovery
glyphosate sample minimum maximum mean median
deviation
rate
concentration number (µg/g)(µg/g)(µg/g) (µg/g)(µg/g)%(µg/g)
100

8

75.25

164.56109.26 103.02

30.13

91

Table 2: Recovery rate of glyphosate in spiked meat ELISA.

Volume 4 • Issue 2 • 1000210

Citation: Krüger M, Schledorn P, Schrödl W, Hoppe HW, Lutz W, et al. (2014) Detection of Glyphosate Residues in Animals and Humans. J Environ
Anal Toxicol 4: 210. doi: 10.4172/2161-0525.1000210

Page 3 of 5

Figure 1: Glyphosate excretion in urine of cows. A) Comparison of glyphosate excretion in urine of German (343) and Danish (N=242) cows. B) Glyphosate in urineof conventional (N=343) and organic (N=32) livestock husbandry in Germany. C: Glyphosate accumulation in different organs.

according to the human health status. Chronically ill humans had
significantly higher (P=0.03) glyphosate residues in urine than healthy
humans (Figure 2).

Discussion

Figure 2: Glyphosate excretion in urine hares (N=193) and fattening rabbits(N=77).

J Environ Anal Toxicol
ISSN: 2161-0525 JEAT, an open access journal

Glyphosate-containing herbicides are applied in large amounts tocrops 2 to 3 times per season to remove weeds and dry out grain in aprocess called ‘desiccation’ [22]. Once applied, glyphosate accumulates
in leaves, grains or fruit. Glyphosate residues cannot be removed bywashing and they are not broken down by cooking [23]. Glyphosate
residues can remain stable in foods for a year or more, even if the foods
are frozen, dried or processed. Recently, many studies have proposedthat glyphosate could impact the health of animals and humans. Despite
glyphosate’s global dominance as an herbicide, there is little testing ofglyphosate residues in animals and humans. Previously, we recorded thepresence of glyphosate residues in Danish dairy cows [7]. Glyphosate
residues could differ from country to country (in some countries
glyphosateis not regulated) and even within a country depending on
the quantity, frequency and time of glyphosate application. The present
study compared glyphosate residues in urine and different organs ofVolume 4 • Issue 2 • 1000210

Citation: Krüger M, Schledorn P, Schrödl W, Hoppe HW, Lutz W, et al. (2014) Detection of Glyphosate Residues in Animals and Humans. J Environ
Anal Toxicol 4: 210. doi: 10.4172/2161-0525.1000210

Page 4 of 5

Figure 3: Glyphosate in humans. A) Comparison of glyphosate excretion with urine of humans with conventional (N=99) and predominantly organic (N=41) feeding.
B) Glyphosate in healthy (N=102) and chronically (N=199) diseased humans.

German cows compared with Danish cows using ELISA and GC-MS.
Other investigations were carried out to shed light on the presenceof glyphosate in hares, rabbits and humans. The ELISA technique forthese studies was validated by comparing paired samples with GC-MS(Tables 1 and 2).
Excreted glyphosate in urine of Danish cows was significantly
higher than from German cows and represents a higher intake fromfeed. Interestingly, the glyphosate concentration in German dairy
cows kept in a GM free region excreted much less glyphosate thanconventionallymanaged cows. Thus, the prohibition of GM grains andsoy prevent these animals from consuming glyphosate with their feed.
Since organic farmers don`t live in an isolated area, the presence of lowlevels of glyphosate could be attributed to contamination by air and rain[2]. The presence of glyphosate residues in organs and meat of cattle
is not a surprise since cows excretesignificant amounts of glyphosate
in urine. An animal study with Sprague-Dawley rats reported thatapproximately 35-40% of the administered glyphosate dose wasabsorbed from the gastrointestinal tract so that urine and feces wereequally important routes for elimination after one oral application[24]. These authors also found that glyphosate accumulated in bones.
Considering the strong chelating stability of glyphosate for calcium,
accumulation in bones is not surprising. Our own results showed thatglyphosate is detectable in intestine, liver, muscle, spleen and kidney
tissue.
Hares are among the first animals to enter fields after glyphosate
is applied before sowing, in no-till cropping, and with pre harvest
desiccation. Surprisingly,the many fold higher glyphosate excretionof domesticated rabbits than of hares (Figure 2) or Danish dairy cows
was not anticipated, but probably reflects the high levels of glyphosate
in their feed Tedesco et al. [25] evaluated the possible effects of GM
soya bean on cell metabolism of rabbits. Although no differences inenzyme levels were detected in serum, a significant increase of lactic
dehydrogenase, mainly the LDH1 iso-enzyme, was found especially inthe kidney and heart.
In the present study, the median glyphosate concentration in urine(around 1 ppb) of people consuming predominantly organic food was

J Environ Anal Toxicol
ISSN: 2161-0525 JEAT, an open access journalsignificantly lower than in urine of people consuming conventional
food. Thus, the prohibition of herbicide use in organic agriculture
greatly reduces the intake of glyphosate. Glyphosate in urine of agenerally healthy population was significantly lower than in urine froma chronically diseased population. Curwin et al. [18] mentioned that it
is important to determine if glyphosate is consumed in conventional
foods. Glyphosate in urine of humans (non-suicidal or accidental
overdose cases) was measured in different populations. The presenceof glyphosate in humans was previously reported [20] by monitoring48 farmers, their spouses and 79 children (4-18 years) for glyphosate inurine the day before, as well as 1 and 3 days after glyphosate application.
They reported detectable levels of glyphosate were found in urine on
the day of application in sixty percent of the farmers (geometric mean
was 3 ppb, the maximum value was 233 ppb, and the highest estimatedsystemic dose was 0.004 mg/kg). Farmers who did not use rubber
gloves had five times more glyphosate in their urine. Mesnage et al.
[26] detected 9.5 ppb glyphosate in urine of a farmer 7h after beginningpesticide handling. Moreover, the excretion of glyphosate in urine is
not limited to farmers [18] and glyphosate has been described as a newenvironmental neurotoxin.
Exposure of mammals to glyphosate may cause loss of
mitochondrial transmembrane potential and result in oxidative stressto liver and brain [27, 28]. Both apoptosis and autophagy are involved
in glyphosate toxicity mechanisms [29] Case reports indicated that
exposure to glyphosate was related to Parkinsonism [19, 30].

Conclusions
Glyphosate residue could reach humans and animals throughfeed and excreted in urine. Presence of glyphosate in urine and its
accumulation in animal tissues is alarming even at low concentrations.
Unknown impacts of glyphosate on human and animal health warrants
further investigations of glyphosate residues in vertebrates and other
non-target organisms.
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Citation: Krüger M, Schledorn P, Schrödl W, Hoppe HW, Lutz W, et al. (2014) Detection of Glyphosate Residues in Animals and Humans. J Environ
Anal Toxicol 4: 210. doi: 10.4172/2161-0525.1000210

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