A human dietary risk assessment associated with glycoalkaloid responses of potato to Colorado potato beetle defoliation

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Food and Chemical Toxicology
j o u r n a l h o m e p a g e : w w w . e l s e v i e r . c o m / l o c a t e / f o o d c h e m t o x
A human dietary risk assessment associated with glycoalkaloid responses
of potato to Colorado potato beetle defoliation
Courtney L. Pariera Dinkins, Robert K.D. Peterson *
Department of Land Resources and Environmental Sciences, Montana State University, Bozeman, Montana 59717-3120, USA
a r t i c l e
i n f o
a b s t r a c t
Article history:
A quantitative human dietary risk assessment was conducted using the glycoalkaloid concentrations
Received 15 May 2007
measured from tubers of plants defoliated by Colorado potato beetles and undefoliated (control). There
Accepted 21 May 2008
was a signi?cantly greater production of glycoalkaloids for defoliated plants compared to control plants
for both skin and inner tissue of tubers. The dietary risk posed to different human subgroups associated
with the consumption of potatoes was estimated for the 50th, 95th, and 99.9th percentile US national
Keywords:
consumption values. Exposures were compared to a toxic threshold of 1.0 mg/kg body weight. Defoliation
Solanum tuberosum
by Colorado potato beetles increased dietary risk by approximately 48%. Glycoalkaloid concentrations
Alkaloid
within the inner tissue of tubers, including undefoliated controls, exceeded the toxic threshold for all
Herbivory
Food safety
human subgroups at less than the 99.9th percentile of exposure, but not the 95th percentile.
Food toxicity
Ó 2008 Elsevier Ltd. All rights reserved.
Dietary exposure
1. Introduction
higher glycoalkaloid concentrations than tubers from undefoliated
plants.
Many secondary metabolites serve as natural pesticides within
Although there are many glycoalkaloids present in potatoes, a-
plants. At certain concentrations, these compounds can be toxic to
chaconine and a-solanine make up 95% of the total glycoalkaloids
humans and other animals (Theis and Lerdau, 2003). There are
present (Friedman and McDonald, 1997); a-solanine is found in
three types of secondary metabolites: terpenes, phenolics, and
greater concentrations than a-chaconine, and a-solanine has only
nitrogen-containing alkaloids. Although terpenes are the largest
half as much speci?c toxic activity as a-chaconine (Lachman
class of secondary metabolites (Theis and Lerdau, 2003), glycoalka-
et al., 2001). Tubers typically have about 75 mg/kg fresh weight
loids are thought to be the most highly consumed natural toxin in
(FW) or 500 mg/kg dry weight (DW) total of a-chaconine and a-
North America (Hall, 1992). However, little is known about the hu-
solanine (Zeiger, 1998). Neither a-solanine nor a-chaconine is reg-
man dietary risks associated with the consumption of these chem-
ulated in the US. However, the US Department of Agriculture
icals or how the dietary risks change in response to herbivory of
(USDA) has recommended a food-safety level for glycoalkaloids
crop plants.
of 200 mg/kg FW or 1000 mg/kg DW (Zeiger, 1998; Bejarano
In potato (Solanum tuberosum L.), glycoalkaloids serve as natural
et al., 2000). Levels of a-solanine greater than 140 mg/kg FW or
defense mechanisms against pathogens and insects (Lachman
933 mg/kg DW taste bitter, and levels greater than 200 mg/kg
et al., 2001). Because naturally occurring pesticides are synthesized
FW or 1000 mg/kg DW cause a burning sensation in the throat
when plants are under stress, it is expected that injury to plant tis-
and mouth (Lachman et al., 2001).
sue would instigate synthesis of higher concentrations of these
Although the potential hazard associated with human con-
compounds in the injured versus uninjured plant tissue. Hlywka
sumption of potatoes injured by insects has been recognized
et al. (1994) found that tubers from plants subjected to Colorado
(Hlywka et al., 1994), there has not been an analytical consider-
potato beetle (Leptinotarsa decemlineata Say) defoliation contained
ation of the potential human dietary risks associated with
increased production of glycoalkaloids as a result of Colorado pota-
to beetle injury. In Pariera Dinkins et al. (2008), we quanti?ed the
Abbreviations: BW, body weight; DW, dry weight; EPA, Environmental Protec-
concentrations of glycoalkaloids in response to Colorado potato
tion Agency; FCID, food commodity ingredient data; FW, fresh weight; LOAEL,
beetle and manual defoliation. The objective of this study was to
lowest-observed-adverse-effect-level; NOAEL, no-observed-adverse-effect-level;
estimate the potential human dietary risk associated with con-
USDA, US Department of Agriculture.
sumption of potatoes with elevated glycoalkaloid levels from
* Corresponding author. Tel.: +1 406 994 7927; fax: +1 406 994 3933.
E-mail address: bpeterson@montana.edu (R.K.D. Peterson).
plants defoliated by Colorado potato beetles.
0278-6915/$ - see front matter Ó 2008 Elsevier Ltd. All rights reserved.
doi:10.1016/j.fct.2008.05.022

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C.L. Pariera Dinkins, R.K.D. Peterson / Food and Chemical Toxicology 46 (2008) 2837–2840
2. Materials and methods
2.5. Exposure assessment
2.1. Quanti?cation of glycoalkaloid concentrations
Because peeling potatoes reduces the quantity of glycoalkaloids in potatoes
approximately 30–80% (Zeiger, 1998), and because the glycoalkaloid values we ob-
All experimental methods for injuring potato plants and quantifying glycoalka-
tained from skins were very high compared to typical store-bought potatoes, only
loid responses in tubers can be found in Pariera Dinkins et al. (2008).
the risks for consuming the inner tissue of potatoes were assessed. Alpha-chaconine
and a-solanine are found within the tuber, are heat stable, and are not degraded
from cooking or frying as they begin to degrade between 230 and 280 °C (Bejarano
2.2. Problem formulation
et al., 2000). Therefore, risks associated with different types of preparation were not
assessed. Concentrations of glycoalkaloids from control and Colorado potato beetle
Our human dietary risk assessment focused on the human acute oral exposure
defoliation treatments were from Pariera Dinkins et al. (2008).
to the glycoalkaloids, a-solanine and a-chaconine, in the inner tissue of tubers from
The human subgroups included the entire US population, all infants, children 1–
plants with no defoliation (control) and Colorado potato beetle defoliation. The ini-
6 years, children 7–12 years, youth 13–19 years, women 13 years and older who
tial symptoms of glycoalkaloid toxicity occur within 30 min of consumption and
were pregnant, but not nursing, women 20 years and older not pregnant nor nurs-
last for approximately 7 h (Friedman and McDonald, 1997). Therefore, in our
ing, and men 20 years and older. All exposure and risk estimates were determined
assessment acute exposure was de?ned as a single-day total exposure after con-
using the Dietary Exposure Evaluation ModelTM (DEEM-FCIDTM, Ver. 2.03, Durango
sumption of skinless tubers. To account for the potential age group and size differ-
Software, Exponent, Inc., Washington, DC) based on the USDA’s Continuing Surveys
ences related to exposure, we estimated the risk to different population subgroups
of Food Intakes by Individuals (CSFII) food consumption data for 1994–1996, 1998.
in the US (e.g., infants, children 7–12 years, and women 13 years and older who are
Food translations within the program to convert foods-as-eaten to commodities
pregnant).
were based on EPA, USDA Food Commodity Ingredient Data (FCID) recipe set as
of August, 2002.
The acute (one day) food consumption patterns for each of the subgroups listed
2.3. Hazard identi?cation and dose-response relationships
above were evaluated using the 50th, 95th, and 99.9th percentile US national con-
sumption values for skinless potatoes only. DEEM calculates the acute oral expo-
Most commercial tubers contain 20–130 mg/kg FW (Zeiger, 1998) or 133–
sure, the risk quotient (see below), and exposure as a percentage of the toxic
867 mg/kg DW glycoalkaloids. The USDA has recommended a food-safety level
threshold at different percentiles of US national consumption.
for glycoalkaloids of 200 mg/kg FW or 1000 mg/kg DW (Bejarano et al., 2000; Zei-
ger, 1998). Levels of a-solanine greater than 140 mg/kg FW or 933 mg/kg DW taste
2.6. Risk characterization
bitter, and levels greater than 200 mg/kg FW or 1000 mg/kg DW cause a burning
sensation in the throat and mouth (Lachman et al., 2001).
The assumptions associated with the dietary risk assessment of glycoalkaloid
Hellenäs et al. (1992) used seven volunteers who abstained from eating pota-
consumption to all the different human subgroups were: (1) only skinless potatoes
toes for two days and were then given potatoes containing glycoalkaloids at a dose
were consumed, (2) the only route of exposure was orally through ingestion of skin-
of 1 mg/kg body weight (BW) per individual. Six out of the seven subjects experi-
less tubers, (3) the toxic threshold for a human was 1 mg/kg BW, and (4) the toxic
enced burning sensation of the mouth and light to severe nausea and one of the
threshold was the same for all ages and sizes within the different human population
six experienced diarrhea; the initial symptoms were observed 30 min after con-
subgroups.
sumption and lasted for approximately 4 h. Animal studies have shown that in
To determine the risk posed to a subgroup in a population, the estimated gly-
mouse, rat, and hamster tissue, a-chaconine and a-solanine reached their highest
coalkaloid exposure level was divided by the toxic threshold. The resulting ratio
concentrations within 6–14 h after ingestion and in less than 35 h, peak concentra-
is known as the risk quotient (RQ) and serves as an index of relative risk.
tions in the blood were reached (Zeiger, 1998).
The symptoms of ‘‘solanine” poisoning include nausea, vomiting, diarrhea,
stomach and abdominal cramps, headache, fever, rapid and weak pulse, rapid
3. Results and discussion
breathing, hallucinations, delirium, and coma (Friedman and McDonald, 1997).
Effects on the nervous system include increased heart, pulse, and respiratory
rates, sedation, and coma (Zeiger, 1998). Effects from cell membrane disruption
Means and standard errors for glycoalkaloid concentrations in
include internal hemorrhaging, edema, diarrhea, constriction of the abdominal
inner tissue of tubers were 174.5 ± 8.59 mg/kg DW for the control
muscles, and lesions in the stomach and duodenum of the large intestines. Tera-
and 258.8 ± 23.3 mg/kg DW for Colorado potato beetle defoliation
togenic effects were observed mainly in the central nervous system and included
exencephaly, cranial bleb, encephalocele, and anophthalmia (Zeiger, 1998). Alpha-
(Pariera Dinkins et al., in 2008). A typical store-bought potato
chaconine exerts teratogenic effects at lower concentrations than a-solanine (Zei-
has a mean inner tissue glycoalkaloid concentration of 206 mg/kg
ger, 1998).
DW (Zeiger, 1998). The difference between control and Colorado
Tissues that were observed to accumulate a-chaconine and a-solanine were
potato beetle defoliation treatments was statistically signi?cant,
abdominal fat, adrenal glands, blood, brain, heart, kidney, liver, lungs, muscle, pan-
and defoliation represented a 48.3% increase in glycoalkaloid
creas, spleen, testis, thymus, and thyroid. Alpha-chaconine and a-solanine re-
mained unchanged or as solanidine when excreted in urine and feces (Zeiger, 1998).
concentrations.
Peeling reduces the quantity of glycoalkaloids in tubers approximately 30–80%
The acute oral exposures for the eight population subgroups ex-
(Zeiger, 1998). Alpha-chaconine and a-solanine are not broken down from cooking
posed to glycoalkaloid concentrations in the inner tissue of tubers
or frying because they are heat stable and only begin to break down between 230
from control plants at the 50th percentile of exposure ranged from
and 280 °C (Bejarano et al., 2000).
In humans, the toxic dose for glycoalkaloids is 2–5 mg/kg BW and the fatal dose
0.19 to 0.58 mg/kg BW/day, and the risks ranged from 19% to 58.3%
is approximately 3–6 mg/kg BW (Morris and Lee, 1984). According to Friedman and
of the toxic threshold (Table 1). The acute oral exposures for the
McDonald (1997), the minimal acute toxic effect level most likely is closer to
eight population subgroups exposed to glycoalkaloid concentra-
1.0 mg/kg BW or less, but there are few human toxicity studies to determine what
tions in the inner tissue of tubers from plants defoliated by Colo-
a toxic or fatal dose would be. An oral LD50 for mice is greater than 1000 mg/kg BW
rado potato beetles at the 50th percentile ranged from 0.28 to
(Nishie et al., 1971) and is approximately 590 mg/kg BW in rats (Gull et al., 1970).
Although animal studies have shown similar effects when ingesting a-solanine, a-
0.86 mg/kg BW/day, and the risk ranged from 28.2% to 86.5% of
chaconine, and plant material containing these two glycoalkaloids, a-solanine and
the toxic threshold (Table 2).
a-chaconine have been shown to be poorly absorbed (Zeiger, 1998), and to elicit a
Table 3 compares the RQ’s for all eight population subgroups at
similar response as observed in humans requires a much greater concentration to
the 50th, 95th, and 99.9th consumption percentiles for tubers from
be administered.
control plants and Colorado potato beetle defoliated plants. At the
50th percentile, the RQ’s were greatest for all infants and least for
2.4. Selection of toxic threshold
women 13 and older who were pregnant but not nursing. At the
Many synthetic chemicals have an acute and/or chronic regulatory threshold
95th percentile, the RQ’s were greatest for children between the
(acceptable daily intake) that is typically based on a no-observed-adverse-effect-le-
ages of 1–6 years and least for women 13 and older who were
vel (NOAEL) from the required toxicity study that generates the lowest dosage nec-
pregnant but not nursing. At the 99.9th percentile, the RQ’s were
essary to produce the lowest-observed-adverse-effect-level (LOAEL). The data
greatest for all infants and least for women 20 and older who were
available indicate that humans are more sensitive to a-chaconine and a-solanine
neither pregnant nor nursing. At the 50th, 95th, and 99.9th percen-
than test animals, and because no human oral LD50’s or NOAEL’s are available for
a-solanine and a-chaconine, the human toxic threshold of 1 mg/kg BW was used
tiles, RQ’s were greatest for all human subgroups exposed to tubers
based on Friedman and McDonald (1997).
from Colorado potato beetle defoliated plants.

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Table 1
Exposure, percentage of toxic dose, and risk quotient for the acute exposure of human subgroups to glycoalkaloids in the inner tissue of tubers from control plants
Control (No defoliation)
Demographic
50th percentile
95th percentile
99.9th percentile
Exposure
% Toxic dose
RQ*
Exposure
% Toxic dose
RQ
Exposure
% Toxic dose
RQ
(mg/kg BW/day)
(mg/kg BW/day)
(mg/kg BW/day)
US population
0.239
23.9
0.24
0.551
55.1
0.55
2.488
248.8
2.49
All infants
0
0
0
0.553
55.3
0.55
4.812
481.2
4.81
Children 1–6
0.515
51.5
0.51
1.131
113.1
1.13
3.753
375.3
3.75
Children 7–12
0.33
33
0.33
0.731
73.1
0.73
2.597
259.7
2.6
Youth 13–19
0.245
24.5
0.25
0.526
52.6
0.53
2.407
240.7
2.41
Women 13+ (pregnant/not nursing)
0.19
19
0.19
0.406
40.6
0.41
1.147
114.7
1.15
Women 20+ (not preg./not nursing)
0.206
20.6
0.21
0.428
42.8
0.43
1.07
106.9
1.07
Males 20+
0.216
21.6
0.22
0.488
48.8
0.49
1.422
142.2
1.42
* RQ = risk quotient.
Table 2
Exposure, percentage of toxic dose, and risk quotient for the acute exposure of human subgroups to glycoalkaloids in the inner tissue of tubers from Colorado potato beetle
defoliated plants
Colorado potato beetle defoliation
Demographic
50th percentile
95th percentile
99.9th percentile
Exposure
% Toxic dose
RQ*
Exposure
% Toxic dose
RQ
Exposure
% Toxic dose
RQ
(mg/kg BW/day)
(mg/kg BW/day)
(mg/kg BW/day)
US population
0.354
35.4
0.35
0.817
81.7
0.82
3.69
369
3.69
All infants
0
0
0
0.82
82
0.82
7.135
713.5
7.13
Children 1–6
0.763
76.4
0.76
1.676
167.6
1.68
5.565
556.5
5.57
Children 7–12
0.489
48.9
0.49
1.085
108.5
1.08
3.85
385
3.85
Youth 13–19
0.363
36.3
0.35
0.78
78
0.78
3.569
356.9
3.57
Women 13+ (pregnant/not nursing)
0.282
28.2
0.28
0.603
60.3
0.6
1.7
170
1.7
Women 20+ (not preg./not nursing)
0.305
30.5
0.31
0.635
63.5
0.64
1.586
158.6
1.59
Males 20+
0.32
32.1
0.32
0.723
72.3
0.72
2.108
210.8
2.11
* RQ = risk quotient.
3.1. Estimates of dietary risk
3.2. Uncertainty
Hlywka et al. (1994) observed a 37.5% increase in glycoalkaloids
The primary uncertainty associated with our human dietary risk
after defoliation by the same insect (we observed a 48.3% increase).
assessment is the toxic threshold. Toxic thresholds (e.g., acute LD50
To get a conservative idea of what this means in terms of potato
and acute, subchronic, and chronic NOAEL’s or LOAEL’s) for glycoal-
consumption, by taking the average tuber glycoalkaloid concentra-
kaloids either are not available or are not suf?ciently robust to set
tion (including both inner and skin tissue), 500 mg/kg DW, a per-
threshold levels. It is unlikely that the 1 mg/kg BW threshold used
son weighing 60 kg would need to consume 120 g DW of
here is suf?ciently conservative because the value has not been
potatoes to reach the 1 mg/kg BW toxic threshold. Because an aver-
established experimentally and is an acute dose known to cause
age bagged potato weighs approximately 193 g FW (85% moisture),
clinical signs of mild toxicity in humans. Indeed, Friedman and
this translates to 4.1 potatoes. If the glycoalkaloid concentrations
McDonald (1997) and Essers et al. (1998) argue that the current
within the average tuber were to increase 48.3%, a person weighing
60 kg would need to eat only 81 g DW, which would be 2.8
potatoes.
Table 3
Acute risk quotients (RQ) for human subgroups exposed to glycoalkaloids in tubers
The US EPA uses the 99.9th population exposure percentile to
determine and regulate risk from dietary exposure to pesticides.
Acute risk quotients for human subgroups
At this percentile, RQ’s for glycoalkaloids in our control tubers
Demographic
50th percentile
95th percentile
99.9th percentile
(or typical store-bought tubers) would exceed 1.0, and these levels
Control CPB
Control CPB
Control CPB
are for the inner tissue only; they do not include the levels mea-
defoliated
defoliated
defoliated
sured in the skins of tubers.
US population
0.24
0.35
0.55
0.82
2.49
3.69
Using the exposure levels for adult males 20 years or older, a
All infants
0
0
0.55
0.82
4.81
7.14
male weighing 70 kg would need to consume approximately 7
Children 1–6
0.51
0.76
1.13
1.68
3.75
5.57
and 20 skinless potatoes to equal the RQ’s determined by DEEM
Children 7–12
0.33
0.49
0.73
1.08
2.6
3.85
at the 95th and 99.9th percentiles, respectively. Approximately
Youth 13–19
0.25
0.35
0.53
0.78
2.41
3.57
Women 13+
0.19
0.28
0.41
0.6
1.15
1.7
14 skinless tubers of typical store-bought size from uninjured
(pregnant/
plants would need to be consumed for the exposure of glycoalka-
not nursing)
loids to reach an RQ of 1.0. Nine skinless tubers from plants defo-
Women 20+
0.21
0.31
0.43
0.64
1.07
1.59
liated by Colorado potato beetle would need to be consumed to
(not pregnant/
not nursing)
reach an RQ of 1.0. Again, this re?ects the increase in dietary risk
Males 20+
0.22
0.32
0.49
0.72
1.42
2.11
from the injury to the plants.

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USDA recommended food-safety levels are not suf?ciently protec-
standard for such substances is that the food be ‘‘ordinarily injuri-
tive of public health. It is likely, therefore, that an acute NOAEL
ous” which may be contrasted with ‘‘may render injurious” for hu-
would be much lower, and a chronic NOAEL (which typically forms
man-made substances. Because tubers typically can be eaten
the basis for the acceptable daily intake of pesticides) would be
without harm, they are considered safe within the meaning of
even lower than an acute NOAEL. Consequently, it is possible that
the law. This increases the importance of information leading to
the toxic threshold could be orders of magnitude less than the va-
a reduction of risk through proper handling, proper storage, and
lue used here, especially given that safety factors of as much as
the use of insecticides to prevent insect damage.
1000-fold are typically applied to the NOAEL to establish the
Our work shows that the deleterious consequences of injury by
acceptable daily intake for pesticides.
insect pests are not limited solely to considerations of yield and
A complicating factor associated with the uncertainty in toxic
physical appearance. Insect injury to crops also may increase the
thresholds is that animal models (which are used to determine
health risks to humans, livestock, and wildlife through alterations
most human toxic thresholds) may not be useful for glycoalkaloids.
in phytotoxin production. Risk-bene?t evaluations of pest manage-
Both mice and rats are much less sensitive to these toxins than
ment should be expanded to include these poorly understood ef-
humans.
fects of pest activity.
3.3. Comparative risk
Con?ict of interest statement
Our results and those of Hlywka et al. (1994) suggest that high
The authors declare that there are no con?icts of interest.
levels of Colorado potato beetle defoliation result in an appreciable
increase in dietary risk. To manage this risk, growers can use insec-
Acknowledgements
ticides approved for use on Colorado potato beetles on potato.
However, what if the insecticides increase dietary risk greater than
We thank D. Weaver (Montana State University) for technical
that posed by increased glycoalkaloid concentrations? Of the 17
support. This work was supported by the Montana Agricultural
insecticides currently approved in the US for use on potatoes, only
Experiment Station and Montana State University.
four (diazinon, methamidophos, endosulfan, and aldicarb) have
been found in quanti?able concentrations in potato tubers in re-
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65% of the US population would exceed an RQ of 1.0. Clearly, this
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Our results demonstrate differences in regulatory approaches to
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er risk for natural food ingredients that may be toxic. The legal
Research Triangle Park, North Carolina, 120 pp.

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