Environmental Science and Pollution Research

https://doi.org/10.1007/s11356-020-08197-2

RESEARCH ARTICLE

Relationship between butyrylcholinesterase activity and lipid

parameters in workers occupationally exposed to pesticides
Iris Betzaida Molina-Pintor 1,2 & Aurora Elizabeth Rojas-García 1 & Yael Yvette Bernal-Hernández 1 &
Irma Martha Medina-Díaz 1 & Cyndia Azucena González-Arias 1 & Briscia Socorro Barrón-Vivanco 1

Received: 9 July 2019 / Accepted: 21 February 2020

# Springer-Verlag GmbH Germany, part of Springer Nature 2020

Abstract
Exposure to organophosphate pesticides (OP) has been associated with the inhibition of cholinesterase enzymatic activity, such
as butyrylcholinesterase (BuChE). Changes in BuChE activity have been associated with obesity, diabetes, hyperthyroidism, and
metabolic syndrome. However, few studies have evaluated the effects of pesticides on both BuChE and lipid parameters. The aim
of this study was to evaluate lipid parameters in urban sprayers and their association with BuChE activity. An analytical cross-
sectional study was conducted in workers exposed to pesticides. The pesticide exposures were evaluated by the measurement of
urinary dialkylphosphates. BuChE activity was determined spectrophotometrically in serum, and biochemical parameters were
determined at a certified laboratory. Information regarding general characteristics, lifestyle, and other aspects was obtained from a
structured questionnaire. The results showed variations in glucose, cholesterol, albumin, atherogenic index, creatinine, LDL,
VLDL, triglycerides, and total lipids according to the level of exposure to pesticides in individuals with overweight and obesity.
Furthermore, positive correlations between BuChE activity and lipid parameters were observed; these effects were associated
with the body mass index. More studies are needed in human population to better elucidate the role of BuChE in lipid
metabolism.

Keywords Butyrylcholinesterase . Lipids . Biochemical parameters . Pesticide . Occupational exposure . Urban sprayers . Body
mass index

Introduction

Butyrylcholinesterase (BuChE; EC 3.1.1.8) is an α-

Highlights
• Biochemical parameters vary according to the exposure degree to
pesticides.
• Correlations between BuChE activity and biochemical and lipid
parameters were observed according to BMI.
• Data suggest a relationship between BuChE activity and biochemical
parameters in workers exposed to pesticides.
Responsible editor: Philippe Garrigues
* Briscia Socorro Barrón-Vivanco
bbarron@uan.edu.mx
1
Laboratorio de Contaminación y Toxicología Ambiental, Secretaría
de Investigación y Posgrado, Universidad Autónoma de Nayarit,
Ciudad de la Cultura s/n. Col. Los Fresnos, 63190 Tepic, Nayarit,
Mexico
2
Posgrado en Ciencias Biológico Agropecuarias, Unidad Académica
de Agricultura, Km. 9 Carretera Tepic–Compostela,
Xalisco, Nayarit, Mexico
glycoprotein found in the central and peripheral nervous sys-
tem, as well as in the majority of the tissues (Santarpia et al.
2013) with the exception of erythrocytes (Lejus et al. 1998).
Its principal form is a homotetramer; each monomer contains
574 amino acids, with nine glycosidic chains bound to aspar-
agine residues, and its plasma half-life ranges from 8 to
12 days (Lejus et al. 1998). The BuChE gene is located on
the long arm of chromosome 3 at 3q26.1–q26.2. BuChE also
is denominated serum cholinesterase, plasma cholinesterase,
nonspecific cholinesterase, pseudocholinesterase, and
acylcholine acylhydrolase (Lockridge 2015).
The BuChE plasmatic form is synthesized by the liver. It is
capable of hydrolyzing choline and aliphatic esters including
butyrylthiocholine, butyrylcholine, propionylthiocholine,
propionylcholine (Dietz et al. 1973), and compounds with
physiological, pharmacological, and toxicological relevance
(Stewart et al. 1977; Casida and Quistad 2004; Duysen et al.
2009).

The physiological function of BuChE is not completely
known, but it has been described as a scavenger of xenobiotic
compounds, including carbamates and organophosphate pes-
ticides (OP) by forming a covalent bond with them. Both OP
and BuChE are inactivated during the process (Raveh et al.
1993; Masson and Lockridge 2010), probably due to the
BuChE geometrics of active-site gorges. BuChE inhibition
is a more sensitive marker of exposure by carbamates and
OP including chlorpyrifos, diazinon, and malathion than other
cholinesterases such as acetylcholinesterase (USEPA 2000;
Lotti 2001; Masson and Lockridge 2010; Bernal-Hernández
et al. 2014).
Several reports have associated BuChE activity with obe-
sity, coronary artery disease, adiposity, type 2 diabetes
mellitus, and hepatic fat content (Kutty et al. 1981; Abbott
et al. 1993; Alcântara et al. 2002; Calderon-Margalit et al.
2006; Santarpia et al. 2013). In this regard, BuChE has been
related with lipid metabolism, as well as with the content of
cholesterol, triglycerides, low-density lipoproteins (LDL),
very-low-density lipoproteins (VLDL), and total lipids
(Cucuianu et al. 2002; Valle et al. 2006; Sridhar et al. 2010).
Indeed, in Mexico, in a child population, a significant associ-
ation between BuChE and serum triglyceride levels has been
observed (Ramírez-Jiménez et al. 2018).
The proposed mechanism through which BuChE affects
lipid metabolism involves the hydrolysis of ghrelin in
humans (Schopfer et al. 2015). Serum BuChE converts the
ghrelin hormone into deacyl ghrelin (inactive form); this
hormone stimulates food intake, carbohydrate utilization,
and adiposity; regulates insulin secretion; and controls blood
glucose levels (Marzullo et al. 2004; Chen et al. 2015;
Schopfer et al. 2015; Brimijoin et al. 2016). It has been sug-
gested that the modification of BuChE activity might be the
first sign of altered lipid metabolism (Krnić et al. 2008). In
addition, there is evidence that suggesting that fatty acids
activate nuclear receptors and alter the expression of some
genes, such as the polyunsaturated fatty acids involved in
immune function regulation through eicosanoid synthesis
and nuclear receptor activation (Stulnig 2003; Vanden
Heuvel et al. 2006). In this regard, Gok et al. (2016) ob-
served, in HepG2 cells treated with fatty acids, a significant
increase of functional BuChE levels.
Taking into account that BuChE might play a pivotal role
in lipid metabolism and that lipids might regulate BuChE
levels, it is expected that compounds capable of inhibiting
BuChE activity, such as OP and carbamate, might be related
to modification in lipid metabolism. In this regard, Kutty et al.
(1975) observed a marked reduction in BuChE activity and
LDL concentration in a patient poisoned with the pesticide
parathion; enzyme and lipoprotein levels returned to normal
on the patient’s clinical recovery. In vivo studies also suggest
the role of BuChE in lipid and lipoprotein metabolism in rats
treated with the OP dichlorvos (Lucić et al. 2002).
Environ Sci Pollut Res
Therefore, the aim of this study was to evaluate the rela-
tionship between BuChE activity and lipid parameters in
workers occupationally exposed to pesticides.
Methods
Study design
An analytical cross-sectional study was conducted in 208 ur-
ban sprayers in Nayarit, Mexico. An open invitation was is-
sued to the general population engaged in fumigation services
and to the population with similar socioeconomic and anthro-
pometric characteristics without occupational exposure. The
sample size was convenient, and participants who met the
inclusion criteria and also agreed to participate were included
in the study. The participants were informed of the objectives
of the study and signed a letter of informed consent.
Information regarding anthropometric characteristics, life-
style, symptoms related to pesticide exposure, frequency of
exposure, and the use of personal protective equipment was
obtained from a structured questionnaire. The study was ap-
proved by the Bioethics Commission of Nayarit State, Mexico
(CEBN/0112017). The population was categorized, according
to their pesticide exposure, into three groups: reference, mod-
erate exposure, and high exposure, as described previously
Zepeda-Arce et al. (2017).
Sample collection
Blood samples were collected without anticoagulant for
BuChE activity and lipid parameters. Serum was prepared
by centrifugation at 3500 rpm and aliquots were stored at −
20 °C until analysis. Glucose, urea, blood-urea-nitrogen
(BUN), creatinine, uric acid, cholesterol, triglycerides, LDL,
VLDL, total lipids, atherogenic index, HDL, and albumin
tests were performed in a certified clinical laboratory.
The first urine of the morning was collected for 7 days from
each participant in sterile wide-mouth plastic bottles and
transported to the laboratory at 4 °C, where a compound sam-
ple was made for each participant everyone and then stored at
− 20 °C. In total, 98 participants donated multiple daily urine
samples, as described by Herrera-Moreno et al. (2019).
Determination of dialkylphosphate metabolites
Dialkylphosphate metabolites (DAP) were determined in
compound urine samples according to the method described
by Valcke et al. (2006), with some modifications (Ramírez-
Jiménez et al. 2014). The analytes were derivatized using
pentafluorobenzyl bromide and potassium carbonate at
70 °C for 2 h. The esters obtained were extracted with a
hexane/dichloromethane mixture and concentrated under a
Environ Sci Pollut Res
stream of nitrogen to a volume of 50 μL. As internal standard,
DETP-d10 was used at a final concentration of 12.5 ppb in the
initial sample. The metabolites included dimethylphosphate
(DMP), dimethylthiophosphate (DMTP),
dimethyldithiophosphate (DMDTP), diethylphosphate
(DEP), diethylthiophosphate (DETP), and
diethyldithiophosphate (DEDTP). DAP quantification was
performed in a gas chromatograph (GC System, model
7820A; Agilent Technologies) coupled to a mass spectrome-
ter (Agilent model 5975 MSD), through selective ion moni-
toring (SIM). DAP urinary concentrations were corrected by
urinary specific gravity following the method of Sokoloff
et al. (2016) and were expressed in ng/mL.
Determination of BuChE activity
BuChE activity determination was performed according to the
method of Ellman et al. (1961) with modifications. The reac-
tion mixture consisted of 0.010 mL of serum, 3 mL of phos-
phate buffer (0.1 M, pH 7.4), and 0.100 mL of DTNB
(10 mM). The mixture was incubated at 37 °C for 10 min
and 0.050 mL of S-butyrylthiocholine iodide (63.2 mM) was
added. Absorbance was monitored at 405 nm for 4 min.
BuChE activity was reported in U/L. Analysis repeatability
was assessed based on analysis triplicate. In each case, the
coefficient of variation calculated was 5% or less.
Statistical analysis
The Kolmogorov–Smirnov test was applied to assess the nor-
mal distribution of dependent variables in general sample pop-
ulation and groups by exposure levels and BMI. One-way
analysis of variance (ANOVA) was used when data followed
normal distribution, and the Mann–Whitney U and Kruskal–
Wallis tests were employed for comparing two or more
groups, respectively, when data were non-normally distribut-
ed. Categorical variables were analyzed using the Ji−2 test.
Pearson and Spearman correlation coefficients were calculat-
ed to examine the correlation between BuChE and serum lipid
parameters and albumin. Statistical significance was set as
p < 0.05. Stata ver. 11 software (Stata Corp., LP, College
Station, TX, USA) was utilized for statistical analyses.
Results
Population characteristics
Two hundred and eight urban sprayers participated in this
study; 66.8% were male and 33.2%, female. The geometric
mean (GM) of the age of participants was 36.3 years.
Regarding body mass index (BMI), 18.3% of the participants
were of normal weight, 34.6% were overweight, and 47.1%
were obese. The participants worked 7.4 h per day on average
and 6 days a week. The workers were divided into three
groups according to the degree of exposure: reference, mod-
erately exposed, and highly exposed. Only 19.8% of the mod-
erately exposed group and 28.3% of the highly exposed group
reported the use of personal protective equipment, and hats
and caps were those most commonly utilized. A higher edu-
cation level was observed in the group of reference with re-
spect to the remaining groups. Overall, 21.6% were active
smokers and 79.31% were passive smokers. A total of
86.5% of participants regularly consumed alcohol and 5.8%
reported consuming some type of drug (Table 1).
The most commonly used pesticides were OP (63.3%),
pyrethroids (29.8%), and carbamates (3.9%).
Dialkylphosphate metabolites
The results of the total urinary dialkylphosphate (DAP) con-
centrations revealed a GM of 33.45 ng/mL (range: 24.58–
41.32 ng/mL) in the reference group, 58.50 ng/mL (range:
24.45–353.32 ng/mL) in the moderate-exposure group, and
122.54 ng/mL in the high-exposure group (range: 25.62–
488.40 ng/mL); these values comprised significant differences
among the groups (p < 0.05, obtained by the Kruskal–Wallis
test). No differences in DAP among BMI groups were ob-
served. However, a correlation between total urinary DAP
concentrations and BMI was observed only in the group with
obesity (rho = 0.4894, p = 0.0012, obtained by the Spearman
test).
Biochemical parameters
Higher cholesterol, LDL, and albumin concentrations were
observed in the reference group, and these were lower in the
highly exposed group with regard to the other groups
(Table 2). Analysis of biochemical parameters by pesticide
exposure level and BMI demonstrated differences in creati-
nine, cholesterol, LDL, and the atherogenic index in the group
with overweight (Fig. 1), as well as in glucose, creatinine, and
albumin in the group with obesity (Fig. 2).
BuChE activity and lipid parameters
The study population exhibited BuChE activities within the
normal range (5400–13,200 U/L) (Randox Laboratories-
Antrim, UK). The mean value of BuChE activity was
5550.8 U/L (range, 5334.3–5767.3 95% confidence intervals
[95% CI differences were observed for exposure levels in both
males and females (Table 3)]), but no differences were ob-
served by age and BMI (data not shown). A positive correla-
tion between BuChE activity and albumin concentrations in
individuals with normal weight and with overweight was ob-
served (Table 4). Also, positive correlations were observed
 Environ Sci Pollut Res

Table 1 General characteristics of study population

Characteristic Reference group n = 22 Moderately exposed n = 126 Highly exposed n = 60 p value

Gender n (%)
Female 5 (23.7) 49 (38.9) 15 (25.0) 0.09
Male 17 (77.3) 77 (61.1) 45 (75.0)
Age (GM/range) 34.91 (20–68) 37.31 (20–67) 34.69 (20–27) 0.16
BMI (GM/range) 28.24 (20.1–39.9) 29.50 (19.0–45.5) 28.87 (20.4–54.4) 0.23
Normal weight n (%) 5 (22.7) 18 (14.3) 15 (25.0) 0.60
Overweight n (%) 8 (36.6) 43 (34.1) 21 (35.0) 0.83
Obesity n (%) 9 (40.9) 65 (51.6) 24 (40.0) 0.85
Hours working per day (GM/range) 7.5 (3.2–17.5) 7.2 (6.9–7.5) 7.3 (6.8–7.8) 0.60
Use equipment protection n (%) – 25 (25.5) 17 (28.81) 0.93
Education (GM/range) 14.77(9–19) 11.49(5–19) 11.50(8–19) < 0.001
Active smokers n (%) 8 (36.3) 18 (15.1) 19 (31.7) 0.01
Passive smokers n (%) 21 (95.5) 90 (73.8) 50 (84.8) 0.03
Alcohol consumption n (%) 20 (90.9) 105 (83.3) 55 (91.7) 0.22
Drug consumption n (%) 7 (5.6) 5 (8.3) 0.35

Age, BMI, education, and hours working per day p values were obtained by the Kruskal–Wallis test. Gender, active smokers, passive smokers, alcohol
consumption, drug consumption, and use equipment protection p values were obtained by Ji−2 test, p<0.05 was considered statistically significant. BMI:
normal weight 18.50–24.99 kg/m2 , overweight 25.00–29.99 kg/m2 , and obesity ≥ 30 kg/m2
GM geometric mean

between BuChE activity and glucose concentration in individ- Discussion

uals with overweight (Table 4) (Fig. 3).
Correlations between BuChE activity and lipid parameters
by BMI were evaluated (Fig. 4). In this regard, positive cor-
relations were observed with triglycerides, VLDL, and total
lipids in the normal-weight group (Table 4). In the overweight
group, positive correlations were observed with cholesterol,
atherogenic index, triglycerides, LDL, VLDL, and total lipids
(Table 4). In the obese group, only a marginal correlation with
VLDL concentration was observed (Table 4).
Biochemical parameters and BuChE activity
In this study, significantly lower cholesterol and LDL and
albumin concentration in individuals with high pesticide ex-
posure were observed; this effect is in agreement with other
studies, such as that of Kutty et al. (1975). These authors
reported a decrease in BuChE activity in individuals poisoned
with parathion, and this was correlated with a decrease in

Table 2 Biochemical parameters of study population

Characteristic Reference groupa n = 22 Moderately exposedb n = 126 Highly exposedc n = 60 p value

Glucose (mg/dL) 80.5 (74.7–86.9) 90.3 (85.6–95.4) 84.9 (79.7–90.4) 0.14

Urea (mg/dL) 23.0 (20.7–25.5) 22.3 (21.0–23.6) 22.3 (20.8–24.1) 0.84
Bun (mg/dL) 10.7 (9.7–11.9) 10.4 (9.8–11.0) 10.9 (9.8–12.0) 0.77
Creatinine (mg/dL) 0.8 (0.7–0.9) 0.7 (0.7–0.8) 0.8 (0.7–0.8) 0.08
*Uric acid (mg/dL) 6.1 (5.4–6.8) 5.8 (5.5–6.1) 6.1 (5.6–6.6) 0.50
Cholesterol (mg/dL) 209.6 (190.3–230.9) 196.7 (190.3–203.4) 185.2 (176.2–194.6)a,b 0.01
HDL (mg/dL) 45.0 (39.8–50.9) 44.7 (42.5–47.0) 44.7 (41.9–47.7) 0.99
Atherogenic index (mg/dL) 4.7 (4.0–5.5) 4.5 (4.2–4.8) 4.1 (3.9–4.4) 0.29
Triglycerides (mg/dL) 140.1 (107.5–182.6) 147.1 (130.8–165.3) 123.2 (108.5–140.4) 0.23
*LDL (mg/dL) 137.2 (120.4–153.9) 122.0 (116.7–127.3) 114.0 (105.6–122.5)a 0.015
VLDL (mg/dL) 27.1 (21.8–33.6) 28.0 (25.3–30.9) 23.9 (21.3–26.8) 0.17
Total lipids (mg/dL) 538.4 (457.1–634.2) 459.4 (391.1–539.7) 472.1 (438.3–508.5) 0.27
Albumin (g/dL) 4.9 (4.8–5.1) 4.8 (4.7–4.8)a 4.8 (4.7–4.9) 0.03

LDL and uric acid are shown in arithmetic mean and p values were obtained by the ANOVA test. Albumin, cholesterol, triglycerides, VLDL, LDL,
HDL, atherogenic index, creatinine, bun, urea, glucose, and total lipids were reported in geometric mean and p values were obtained by the Kruskal–
Wallis test, p<0.05 was considered statistically significant
Environ Sci Pollut Res

Fig. 1 Biochemical parameters

evaluated by exposure level in
overweight group. The p value
was determined using the
Kruskal–Wallis test to creatinine
and atherogenic index, and cho-
lesterol and LDL parameters were
evaluated using the ANOVA test.
RE-reference group, ME-
moderate exposure, HE-high
exposure

cholesterol and LDL content. Similar results were obtained by
Patil et al. (2009), who observed a decrease in the concentra-
tion of cholesterol and albumin in sprayers of vineyards. In
addition, the lowering of cholesterol and LDL could comprise
an effect of BuChE inhibition according to Darvesh et al.
(2004) and Pytel et al. (2017), who suggested a close relation-
ship between the two.
Our data showed a positive correlation between BuChE
activity and glucose in individuals with overweight. Similar
results were reported in a population aged 18–65 years
(Stojanov et al. 2011) and Japanese males aged 40–55 years
(Sato et al. 2014). This correlation might be due to a possible
role of BuChE in insulin resistance. In this regard, Abbott
et al. (1993) suggested that when the insulin secretion is inad-
equate, serum BuChE activity increased and adversely influ-
enced lipid and glucose metabolism. Studies in vivo and
in vitro have shown that OP could cause hyperglycemia and
deregulate glucose uptake in adipose tissue and, in the Islets of
Langerhans, decreased uptake and an effect on secretions of
insulin (Pakzad et al. 2013; Nili-Ahmadabadi et al. 2013;
Pournourmohammadi et al. 2007; Abdollahi et al. 2004;
Lasram et al. 2008; Nili-Ahmadabadi et al. 2019).
In addition, a positive correlation between BuChE activity
and albumin in individuals with normal weight and over-
weight was observed. These results are in agreement with
those described by Lampón et al. (2012), who observed a
positive correlation between BuChE activity and albumin in
humans, and in those of Calderon-Margalit et al. (2006), who
described a positive correlation between BuChE activity and
albumin in persons aged > 50 years who were residents of
West Jerusalem. In 1989, Masson suggested that plasma
BuChE is found in heteromeric forms produced in
association with other proteins, such as albumin and Kumar
et al. (2018) hypothesized that the pseudoesterase activity of
human serum albumin is a contributing factor to lipid metab-
olism, including cholesterol biosynthesis. Thus, this associa-
tion might explain the correlation observed between BuChE
and albumin.
On the other hand, we observed differences in creatinine
levels by exposure levels in overweight and obese groups. In

p=0.05 p=0.02
400 6 p=0.08 6.0

5
5.5
Creatinine (mg/dL)
Glucose (mg/dL)

300 2.0
Albumin (g/dL)

5.0
1.5
200
4.5

1.0
4.0
100
0.5
RE ME HE RE ME HE RE ME RE

Fig. 2 Biochemical parameters evaluated by level exposure in obese group. The p value was determined using the Kruskal–Wallis test to glucose,
creatinine, and albumin parameters. RE-reference group, ME-moderate exposure, HE-high exposure
 Environ Sci Pollut Res

Table 3 BuChE activity stratification by gender and exposure level in study population

Gender M (CI 95%) p value Reference group n = 22 Moderately exposed n = 126 Highly exposed n = 60 p value

Female 5654.8 (5383.3–5926.3) 0.51 6104 (5780.8–6427.2) 5892.7 (5580.5–6205.0) 4743.7 (4199.9–5287.6) 0.001
Male 5499.2 (5202.7–5795.6) 6840.7 (6283.2–7398.3) 5976.8 (5569.8–6383.7) 4196.4 (3894.6–4498.1) < 0.001

p values were obtained by the ANOVA analysis of variance, p<0.05 was considered statistically significant
M mean, CI confidence interval

this respect, although obesity has been associated with glo-
merular hyperfiltration, visceral adiposity has been suggested
to be associated with reduced glomerular filtration (Gerchman
et al. 2009). More studies are needed to know the mechanism
by which obesity is associated with an increase in creatinine
levels in populations exposed to pesticides.
BuChE activity, lipid parameters, and BMI
It has been suggested that BuChE may be involved in lipid
metabolism, in that elevated serum BuChE activity has been
found in several pathologies associated with lipid metabolism
(Kutty et al. 1981; Kutty and Payne 1994; Vallianou et al.
2014). Although the nature of this interaction is not well
established, results in animal models indicate that BuChE
may possess a role in the regulation of lipoprotein metabolism
(Vallianou et al. 2014).
In this study, correlations between BuChE activity and lip-
id parameters were observed according to BMI (Table 4, Fig.
4). According to Kálmán et al. (2004), high serum lipid con-
centrations may induce alteration in the enzymatic configura-
tion that modifies BuChE activity or that alters the expression
of the enzyme-encoding BuChE gene.
In this regard, different studies have demonstrated correla-
tions between BuChE activity and lipid parameters and BMI.
Stojanov et al. (2011) described a positive correlation between
BuChE activity and BMI, cholesterol, triglycerides, and LDL
in young and healthy males. Likewise, Vallianou et al. (2014)
described a positive association between BuChE and BMI,
LDL, cholesterol, and triglycerides in apparently healthy
adults.
In contrast with our data, some studies have reported a
significant association between BuChE and triglycerides,
VLDL, and LDL in human populations with obesity (Kutty
et al. 1981; Jain et al. 1983; Kutty and Payne 1994; Alcântara
et al. 2002). These studies are in agreement with the possible
involvement of BuChE in alterations in lipid metabolism. In
particular, the marginal correlation in the obese group with
VLDL might be the result of an effect of insulin resistance
on obesity. This hypothesis was supported by Packard and
Shepherd (1997), who described a hepatic overproduction of
VLDL as the principal fault of the condition of insulin resis-
tance in obesity. Other studies described that insulin acts on
VLDL in two key factors: regulating the initiation of VLDL
assembly and the maturation of VLDL particles (Brown and
Gibbons 2001; Carpentier et al. 2002; Au et al. 2003).
According to data observed in the present study, an
association is suggested between serum BuChE activity
and lipid parameters. In this regard, it has been proposed
that BuChE could interact with lipoproteins through the
phosphorylcholine polar group (Kutty and Payne 1994)
and that BuChE might play a role in lipid metabolism
directly (Van Lith and Beynen 1993; Rustemeijer et al.
2001), or through a synergistic action with cholesterol
esterase (Finer et al. 2004). In regard, De Vriese et al.
(2004) described that BuChE is capable of hydrolyzing
the acylated peptide known as ghrelin, which stimulates
hunger and food intake. Li et al. (2008) reported that
BuChE−/− S129 mice exhibited an excessive weight gain
on a high-fat diet under parameters that did not promote
obesity in their wild-type littermates. Brimijoin et al.
(2016) demonstrated, in mice of the BuChE −/− mouse
strain (C57BL/6) with a high-fat diet, that the BuChE
gene transfer can restore resistance to obesity, and the
authors concluded that BuChE could be a key regulator
of ghrelin in peripheral circulation.

Table 4 BuChE activity correlations with biological parameters in BMI groups

BuChE Glucose Cholesterol Triglycerides VLDL Atherogenic index LDL Total lipids Albumin
(U/L) (mg/dL) (mg/dL) (mg/dL) (mg/dL) (mg/dL) (mg/dL) (mg/dL) (g/dL)

Normal − 0.15 0.21 0.47** 0.32* 0.27 0.16 0.38** 0.42**

weight
Overweight 0.35** 0.48** 0.39** 0.49** 0.38** 0.35** 0.31** 0.21*
Obesity 0.02 0.13 0.14 0.18* 0.15 0.09 0.15 0.13

Urea, bun, creatinine, uric acid, and HDL presented no correlation with BuChE
p values were obtained by the Pearson correlation test (*0.05 < p < 0.1; **p < 0.05)
Environ Sci Pollut Res

p=0.01
Glucose (mg/dL)

Albumin (g/dL)
p=0.08
p=0.22

p=0.004
p=0.38
p=0.84

0 2000 4000 6000 8000 10000 0 2000 4000 6000 8000 10000

BuChE (U/L) BuChE (U/L)

Normal weight Overweight Obesity

Fig. 3 Correlation analysis between BuChE activity and biochemical parameters. The p value was determined using the Pearson correlation test

In addition, Nili-Ahmadabadi et al. (2019) reported that in adipocytes, and may be accompanied by a decrease in BuChE
rats exposed to diazinon, dyslipidemia may be caused by a activity. These observations suggest that the BuChE contribu-
significant increase of ghrelin serum levels, TNF-α, size of tion is through the deacylate of ghrelin and lipid metabolism.

Fig. 4 Correlation analysis between BuChE activity and lipid parameters. The p value was determined using the Pearson correlation test

Our data suggest that biochemical parameters and BMI
might be influenced by exposure to OP with an impact on
BuChE activity. Therefore, repeated exposure to OP could
disrupt feeding behavior and consequently, lipid metabolism,
bringing about alterations in lipid parameters and possibly
weight gain, in turn giving rise to overweight and obesity.
More studies are needed in human population to better eluci-
date the role of BuChE in lipid metabolism.
Acknowledgments We thank all the workers that participate in the study.
The authors also thank Leticia Yáñez-Estrada Ph. D. and her team at the
Autonomous University of San Luis Potosí, Mexico, for measurements of
DAP.
Funding information This work was supported by CONACyT grants:
SALUD-2014-1-#233803 and Red Temática de Toxicología de
Plaguicidas #271775.
Compliance with ethical standards
Conflict of interest The authors declare that they have no conflict of
interest.
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