Environmental Science and Pollution Research (2022) 29:53382–53394

https://doi.org/10.1007/s11356-022-19561-9

RESEARCH ARTICLE

Thermal paper as a potential source of bisphenol A for humans

and the environment: migration and ecotoxicological impact
Soledad Nasello1 · Érica Beiguel1 · Gretel Fitó‑Friedrichs1 · Carmen Irala1 · Giselle Berenstein1,2 · Silvana Basack1   ·
Javier M. Montserrat1,2 

Received: 30 April 2021 / Accepted: 28 February 2022 / Published online: 14 March 2022
© The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature 2022

Abstract
The objective of this work was to evaluate thermal paper (TP) tickets used in Argentina as a potential source of bisphenol
A (BPA) that could impact humans and the environment. BPA in TP was measured by HPLC ranging from 11.1 to 30.5 mg
­BPAg−1. In order to estimate the impact on humans, dermal BPA estimated daily intake was calculated as being 79.3 ± 19.5
μgd−1 for workers and 1.6 ± 0.4 μgd−1 for the general population. To evaluate TP’s impact on the environment, BPA migra-
tion from TP to water and soil was studied. In the case of water, 99.6% of the BPA tickets content migrated in 30 h, while
78.0% moved into the soil in 96 h. BPA degradation kinetics in soil and water were also carried out; while in soil 61.9% of
BPA degraded in 120 h, no degradation was observed up to 120 h in tap or river water.
Additionally, ecotoxicological effects of BPA on the earthworm Eisenia andrei, a representative terrestrial indicator, were
studied performing bioassays on lethality, avoidance, and reproductive and enzymatic activity. BPA showed to be very
toxic to E. andrei ­(LC50 value in contact paper test of 17 μgcm−2, 95% confidence interval 6–46 μgcm−2, 24 h exposure)
and also caused an increase of total cocoons for earthworms exposed to 10 and 50 mg BPA k­ g−1 soil. Evasion response was
observed at a concentration of 50 mg BPA ­kg−1 soil, while no effect was observed on cholinesterases, carboxylesterases, and
glutathione S-transferases activities (1, 10, and 50 mg BPA k­ g−1 soil). Finally, a simple BPA degradation technology using
water peroxide and radish (Raphanus sativus) tissue as catalyst was explored as a simple and domestic potential treatment
to avoid BPA migration to the environment.

Keywords  Bisphenol A · Thermal paper · Migration · Degradation · Eisenia andrei · Raphanus sativus

Introduction

Bisphenol A (BPA) is an extensively used industrial raw

chemical with a global demand of 7.7 million metric tons in
Silvana Basack and Javier M. Montserrat contributed equally to 2015 (equivalent to US $16.5 billion) and an estimated trade
this work. of 10.6 million metric tons in 2022 (Research and Markets
Responsible Editor: Philippe Garrigues 2016). Its ubiquitous occurrence in different environmental
compartments, like indoor dust (Deng et al. 2018), wastewa-
* Silvana Basack ters (López-Pacheco et al. 2019), surface waters, and sedi-
sbasack@campus.ungs.edu.ar ments (Staples et al. 2018) alerted worldwide environmental
* Javier M. Montserrat protection and regulatory agencies (EPA 2017). BPA safety
jmontser@campus.ungs.edu.ar concern is mainly related to its reported animal and human
1
Instituto de Ciencias, Universidad Nacional de General
toxicological effects as an endocrine disruptor (Molina-
Sarmiento (UNGS), J. M. Gutiérrez 1150, (B1613GSX) Los Molina et al. 2019) and by its genotoxic (Ramos et al. 2019),
Polvorines; Prov. de Buenos Aires, Buenos Aires, Argentina neurotoxic (Rytel et al. 2019), and cytotoxic (Ramos et al.
2
Consejo Nacional de Investigaciones Científicas y Técnicas 2019) activities. This xenobiotic has been recently found
(CONICET), Buenos Aires, Argentina in child and adult human urine in six different continents,

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Environmental Science and Pollution Research (2022) 29:53382–53394
proving the high human exposure to this chemical (Huang
et al. 2018).
BPA’s industrial applications are mainly related to epoxy
resins, polycarbonates, polysulfones, tetrabromobisphenol
preparation, and thermal paper production. In the particular
case of thermal paper (TP), BPA concentration levels are
considerably high compared to other uses, ranging from 0.09
to 1.70 % (g BPA/100 g paper; Mendum et al. 2011). In this
matrix, BPA is used as a proton source for a lactone ring-
opening reaction that develops colour (Björnsdotter et al.
2017). Interestingly, significant BPA amounts have been
found in other varieties of paper, like newspapers, maga-
zines, food cartons, napkins, and toilet paper (Liao and Kan-
nan 2011), perhaps as a consequence of the presence of TP
in recycling practices.
From an environmental and toxicological perspective,
BPA’s impact on soil and water is an important focus of
attention. BPA’s worldwide presence in surface waters
ranged from ca. 0.0005 μgL−1 (Fromme et al. 2002) to 12
μgL−1 (Kolpin et al. 2002), being 0.14 μgL−1 the median
BPA concentration in USA river waters (Kolpin et al. 2002).
BPA’s biodegradation has been reported to occur in the pres-
ence of diverse soil microorganisms (Mtibaà et al. 2018),
as in river sediments (Peng et al. 2015), water (Wu et al.
2015), and in wastewater treatment plants. Environmental
risk assessment of BPA in these compartments fostered
the development of different assays using bioindicators.
Recently, a few studies have focused on the ecotoxicity of
BPA to soil species. Kwak et al. (2018) reported the hazard-
ous concentrations of BPA in soil using a species sensitivity
approach. Verdú et al. (2018) studied the effect of BPA on
life-history parameters (mortality, growth, and reproduction)
on Dendrobaena veneta and Eisenia fetida species. Novo
et al. (2018) studied the impacts of BPA on gene expression
of Eisenia fetida.
Despite the toxicological concern on BPA and the recent
inclusion of BPA structural analogues into the market
(Björnsdotter et al. 2017), TP with BPA is still widely used
in a variety of commercial applications, including point of
sale receipts, luggage tags, bus and taxi tickets, and among
others. TP worldwide production in 2015 was 1.15 × ­106
tons (Frankowski et al. 2020) with a total BPA content of
circa ­104 tons. Regarding other environmentally relevant
sources of BPA, it has been pointed out that polycarbonate
manufacturing is one of them (Fromme et al. 2002), but it is
interesting to remark there is no polycarbonate production
in Argentina (CAIP 2015).
Therefore, a question could be raised on this particular
scenario: What could be the relative contribution of BPA
present in TP to environmental pollution?
Considering this background, the general objective of this
work was to study TP as a BPA source related to soil and
water contamination. The specific objectives were then to
53383
measure BPA content in thermal paper in use in Argentina
and calculate the estimated daily intake for workers and the
general population. In order to evaluate TP as a BPA source
that could affect the environment, BPA migration rates from
thermal paper to soil and water, BPA degradation in these
matrices, and BPA environmental impact on soils using
Eisenia andrei as a bioindicator were performed. Finally,
a BPA in TP simple degradation methodology, potentially
useful domestic treatment, is presented.
Materials and methods
Chemicals and solvents
Chemicals and solvents were of the best analytical grade
(Sintorgan, J. T. Baker). Acetonitrile (ACN) and metha-
nol (MeOH) for chromatographic analysis were HPLC
grade (Merck). Toluene and cyclohexane (Anedra) used
for extractions were analytical grade. Acetylthiocholine
iodide (ATCh), 5,5′-dithiobis-2-nitrobenzoic acid (DTNB),
1-chloro-2,4-dinitrobenzene (CDNB), reduced glutathione
(GSH), phenylthioacetate (PTA), bovine serum albumin
(BSA) for enzyme activities, BPA (4,4′-isopropylidenedi-
phenol, 97%), and N,O-Bis(trimethylsilyl)trifluoroaceta-
mide for GC derivatization (≥ 99%) were purchased from
Sigma-Aldrich.
HPLC quantitation of BPA in thermal paper, soil,
water, and radish tissue
BPA content was measured using a Perkin Elmer HPLC
(Flexar model) with a UV-vis detector set at 278 nm and an
RP-C18 Agilent column (5 μm particle size, 2.1 mm inter-
nal diameter, and 150 mm length). The operating conditions
were as follows: injection volume, 20 μL; aqueous phase
(A), ­H3PO4/H2PO4− buffer 25 mM (pH = 3); organic phase
(B), ACN; flow, 1 ­mLmin−1. The elution programme was t
= 0, min, 70% (A); t = 2 min, 10% (A); and t = 6 min, 70%
(A). Under these conditions, BPA retention time was 3.3
min. HPLC calibration curves (Fig. V-SM, Supplementary
Information) and recovery values are reported at the Sup-
plementary Information.
The different matrices were treated as follows:
– TP: (0.155 ± 0.005) g of TP were extracted with 25 mL
of methanol (10 min sonication) and filtered through a
0.45 μm Teflon membrane. Then, 2 mL of the filtered
solution was transferred to an HPLC vial.
– Soil: 10 g of soil were extracted with 25 mL of methanol
(20 min sonication) and subsequently passed through a
small silica gel column (1 g) before being transferred to
an HPLC vial.
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53384
– Water: 1 mL of the aqueous sample was mixed with 2
mL of ACN and the solution was filtered through a 0.45
μm Teflon membrane. In the case of the aqueous phase of
BPA degradation reaction in water, 1 mL of this solution
was stopped with 1 mL of H ­ 2SO4 (1 M, 70 °C, 3 min,)
and filtered through a 0.45 μm Teflon membrane before
being transferred to an HPLC vial.
– Radish tissue: 10 g of radish tissue were extracted with
2 × 25 mL of hexane by sonication (30 min). Then, the
solvent was rotaevaporated and the residue was dissolved
in 25 mL of acetonitrile (HPLC grade).
Dermal BPA estimated daily intake (EDI)
EDI was calculated according to Adeyemi et al. (2020):
EDI = (k × C × HF × AF × HT) 10−6
where:
k Paper to skin transfer coefficient (21522
μgs−1)
C BPA concentration in thermal paper
(μgg−1)
HF Handling frequency (general popula-
tion: 3; workers: 150 times ­d−1)
Absorption factor 27%
HT Handling time (5 s)
BPA in soil: its migration from thermal paper
and degradation experiments
Soil samples
For all assays, BPA-free (checked by HPLC, see HPLC
quantitation section) natural soil from the university campus
(Argiudoll order) was used. The soil was dried at room tem-
perature and sieved (2 mm maximum particle size) before
use.
BPA migration experiments from thermal paper
To study the BPA migration from thermal paper to the soil,
unused TP (generic, made in Brazil) with a BPA content
of 28.8 mg ­BPAg−1 paper was employed. TP (5.7 cm × 6.0
cm) was cut into small pieces, mixed with 10 g of sterilized
soil (with a water content of 50%), and placed in a 50 mL
glass beaker. Three experimental units were prepared for
each sampling time. All beakers were left in the darkness
at room temperature up to 96 h. BPA content in soil and TP
was determined by HPLC.
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Environmental Science and Pollution Research (2022) 29:53382–53394
BPA degradation experiments
A stock solution of BPA in acetone (5 μL, 60,000 m ­ gL−1)
was added to 6 g of BPA-free soil (checked by HPLC) to
reach a final concentration of 50 mg BPA k­ g−1 dried soil
and placed in a glass beaker. Three experimental units were
prepared for each sampling time (every 24 h). The same
treatment was performed on plain sterile soil to have a nega-
tive control. At predefined times, all the soil content of a
beaker was extracted and analysed as indicated in the section
of HPLC quantitation.
BPA in water: its migration from thermal paper
and degradation experiments
Water samples
Tap and Reconquista River water (sample extracted at
−34.540326 latitude −58.611176 longitude, on July 2019)
were used in BPA degradation assays.
BPA migration from thermal paper experiments
For the study of the BPA migration from thermal paper to
water, unused TP fragments (generic, made in Brazil) with a
BPA content of 28.8 mg BPA g­ −1 paper were employed. TP
(0.155 g) was mixed with 50 mL of sterilized water in a 250
mL glass beaker. Three experimental units were prepared for
each sampling time. All beakers were left in a dark at room
temperature up to the sampling time. BPA content in water
and TP was determined by HPLC.
BPA degradation experiments
A BPA solution of 10 mg BPA ­L−1 water (tap or Recon-
quista River) was prepared. The solutions were kept under
orbital shaking (180 rpm) at room temperature and 2 mL of
aliquots was taken at different times up to 120 h. Then, 2
mL of acetonitrile was added to each sampling; they were
subsequently filtered through a 0.45 μm Teflon filter before
HPLC analysis as described previously.
Eisenia andrei bioassays
Lethality tests
BPA lethal concentration 50 value (­ LC50) was determined
according to the OECD guideline No. 207 (1984) with slight
modifications (contact paper test). Filter papers (Whatman
No. 1, 54 ­cm2) were impregnated with BPA solutions in
acetone. In the case of the control experiment, papers were
impregnated exclusively with acetone. Once the acetone
evaporated, the papers were placed into tubes, lining their
Environmental Science and Pollution Research (2022) 29:53382–53394
inner surface (ten tubes for each concentration) and 2 mL of
distilled water was added to provide humidity. One earth-
worm was introduced into each tube which was then cov-
ered with nylon gauze fastened by a rubber band. The tubes
were kept in darkness for 24 h at 20 ± 2 °C. Earthworms
were considered not alive if they did not respond to a gentle
mechanical stimulus at their front end. As a standard refer-
ence, toxicant 2-chloroacetamide was used to evaluate the
general health of earthworms by assaying ­LC50 (24 h).
Tests to evaluate sublethal effects
For ecotoxicological assays (reproduction, avoidance, and
enzymatic activity), the soil was spiked with a BPA solu-
tion in acetone to reach a final concentration in samples of
0, 1, 10, and 50 mg ­BPAkg−1 of dried soil. In all cases,
acetone to soil ratio was 200 mL of acetone per kg of dried
soil, and the solvent was left to dry at room temperature for
48 h under a laboratory fume hood. BPA concentration in
soil was checked at the beginning of bioassays by HPLC.
Eisenia Andrei earthworms (0.30–0.60 g fresh weighed and
kept in our laboratory) were exposed to samplings prepared
as described above with a 16 h/8 h day/night photoperiod
and at 20 ± 2 °C. Before starting the bioassays, earthworms
were washed with dechlorinated tap water and placed on
moist filter paper for a minimum of 3 h, to let them empty
their guts. OECD/ISO guidelines were used for the tests.
Eisenia andrei avoidance test
ISO 17512-1 (2008) was followed. The spiked soil had a
BPA content of 1, 10, and 50 mg BPA k­ g−1 of dried soil.
BPA non-spiked soil was used as control. Further details are
provided in the Supplementary Information.
Eisenia andrei reproduction test
The spiked soil had a BPA content of 1, 10, and 50 mg
­BPAkg−1 of dried soil, and BPA non-spiked soil was used as
control. The test was performed according to ISO 11268-2
(2012a), with minimal modifications. Six adult earthworms
and 350 g of soil were added to each of four replicate con-
tainers. Dry baby cereal mixture (2 g) was used as food and
added at the beginning of the experiment, and once weekly
afterward. Soil humidity was maintained during the entire
experiment. After 28 days of exposure, earthworms were
removed from the soil and survival rates were recorded.
Each portion of soil (containing cocoons) was returned
to its previous container and incubated for another 28 days
to continue the cocoons’ exposure to soil. At the end of the
assay (56 days), the number of hatched and non-hatched
cocoons and juveniles was recorded.
53385
Enzyme assays in Eisenia andrei
ISO 11268-1 (2012b) recommendations were followed.
Briefly, the soils were treated with BPA in three different
concentrations: 1, 10, and 50 ­mgkg−1. Soil (300 g) and
six adult earthworms were added to each of four replicate
containers. Soil humidity was monitored during the entire
experiment. After 7 days of exposure, earthworms were
removed from the soil and were homogenized using a Pot-
ter-Elvehjem device fitted with a Teflon pestle in Tris-HCl
buffer 100 mM pH 7.5 in 1:3 ratio (tissue weight: buffer vol-
ume). The homogenate was centrifuged at 9000 × g at 4 °C,
and the pellet was discarded. The supernatant fraction was
used for the enzymatic studies. The enzyme activities were
measured on a Perkin Elmer Lambda 25 UV-vis dual-beam
spectrophotometer. Cholinesterases (ChE) and carboxyes-
terases (CaE) activities were determined by the colorimetric
method of Ellman et al. (1961), glutathione S-transferases
(GST) activities were determined by the method of Habig
et al. (1974), and total protein content was determined by the
method of Bradford (1976). Details of the enzyme activity
determination can be found in the Supplementary Informa-
tion section.
Removal of BPA in thermal paper by Raphanus
sativus
Biodegradation of BPA from thermal paper using ­H2O2
and radish tissue
The thermal paper (400 mg) was placed in a domestic glass
jar (500 mL capacity) with 100 mL of tap water for 2 h, to
assure the maximum BPA migration from the TP to water.
Then 10 g of small-diced skinned radish (Raphanus sati-
vus) and 2 mL of ­H2O2 20 vol. (ca. 60 drops) were added.
The mixture was left under these conditions for another 2
h. Blank experiment without the ­H2O2 or Raphanus sati-
vus additions were performed in parallel. BPA content was
determined in all matrices (TP, radish, and water) by HPLC
as described previously.
Phytotoxicity of the remaining waste using Lactuca sativa
seeds
To analyse the phytotoxicity of the resulting BPA degrada-
tion samples, assays employing Lactuca sativa seeds were
carried out (USEPA 1996). The experiments were performed
for 120 h in Petri-dishes, using filter paper with 4 mL of
distilled water (control) or each of both aqueous solutions
coming from biodegradation assays — as already described.
Twenty seeds of Lactuca sativa per replicate were carefully
and neatly placed on the paper, (four replicates, darkness,
22 ± 2 °C). Germinated seeds were harvested (for control
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53386 Environmental Science and Pollution Research (2022) 29:53382–53394

conditions, germination under 90% is unacceptable) and
their root elongation radicle lengths were measured.
Statistical analysis
LC50 value of BPA and its 95% confidence interval was cal-
culated by USEPA Probit Analysis Programme, version 1.5.
Other statistical analyses were performed with GraphPad
InStat 3 (GraphPad Software, San Diego, USA). Data were
first tested for normality (Kolmogorov-Smirnov’s test) and
homogeneity of variances (Bartlett’s test). Depending on
these results, means were compared by one-way ANOVA
(parametric) or non-parametric Kruskal-Wallis tests. When
significance was demonstrated (p < 0.05), Tukey-Kramer or
the non-parametric Dunn’s tests were applied for post hoc
comparison of means. For avoidance experiments, Student
t-test was used (one-tailed test for control-treated experi-
ments; two-tailed test for the dual control tests; Natal Da
Luz et al. 2004).
Results and discussion
It has been reported that 95% of BPA applications are related
to polymeric materials (Verdú et al. 2018) so, as much as
5% remains for other manufactures like thermal paper. In
any case, the environmental impact of a BPA source also
depends on its migration rates from a particular matrix (i.e.
polymeric resin and thermal paper), and the BPA degrada-
tion kinetics in a specific environmental compartment, such
as soil or water. Considering that BPA content in Buenos
Aires periurban rivers is high (see Supplementary Informa-
tion) and that there is no polycarbonate production in Argen-
tina (CAIP 2015), it was expected that most of environmen-
tal BPA would come from thermal paper. With this purpose,
firstly BPA content in TP in use in Argentina was measured,
and the estimated daily intake for workers and the general
population was calculated. Secondly, the BPA migration
rates from TP to water and soil were determined. Thirdly,
the degradation rates of BPA in soil and water were studied.
Fourthly, the impact of BPA on soils, using the earthworms
Eisenia andrei as terrestrial model organisms for ecotoxic-
ity tests, was assessed. Finally, a simple treatment method
for BPA present in TP (BPA/TP) that could be useful in
domestic environments was developed as a proof of concept.
BPA concentration in thermal paper used
in Argentina and human dermal exposure
BPA content on TP of different origins (highway, super-
market, stores, parking, medical appointments, banks, oil
stations, and train tickets), available in Argentina, was deter-
mined by HPLC, finding BPA concentrations in the range
from 11.1 to 30.5 mg ­BPAg−1 paper (Table 1). These values
are in agreement with the previously reported concentra-
tions of BPA in TP used in the USA (Mendum et al. 2011),
Europe (Eckardt et al. 2020), Brazil (Molina-Molina et al.
2019), and Korea (Liao and Kannan 2011). The mean BPA
values found in TP were ca. 90 times higher than the recom-
mended level set by the Europe Commission from January
2020 (Regulation EC No. 1907 2006). This BPA amount
present in TP is worrying, especially considering the ubiq-
uitous presence of BPA in the environment concomitant with
the increased prevalence of endocrine-related cancers, the
estrogenic activity found in cultures of human breast can-
cer MCF-7 cells and human prostate cancer PALM cells,
among other scientific evidence (Molina-Molina et al. 2019).
Indeed, there is a great concern surrounding the impact of
the low-dose BPA effect on living organisms in different
ecosystems, supported by the results of in vitro and in vivo
studies and epidemiological surveys that show the toxic,
endocrine, mutagenic, and carcinogenic actions of BPA
(Michałowicz 2014).

Table 1  BPA content for Ticket origin N BPA in thermal paper EDI(a), (b)(mg ­d−1)
thermal paper tickets in use (mg ­g−1)
in Argentina and calculated
EDI for workers and general Mean Workers General population
population
Highway 4 17.6 ± 1.6 76.7 1.5
Bank 4 14.3 ± 3.1 62.3 1.2
Supermarket 2 16.6 ± 1.4 72.3 1.4
Store 3 21.4 ± 7.9 93.3 1.9
Parking 3 12 ± 2.3 52.3 1.0
Medical appointment 3 15.2 ± 3.4 66.2 1.3
Train 3 25 ± 4.7 109.0 2.2
Oil station 2 24.3 ± 6.0 105.9 2.1
All tickets 24 18.2 5.7 79.3 ± 19.5 1.6 ± 0.4
(a) (b)
 EDI estimated daily intake (dermal). Maximum recommended, 3.0 mg ­d−1 (California regulation)

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Environmental Science and Pollution Research (2022) 29:53382–53394
To compare the BPA content in another relevant poly-
meric matrix, the BPA content in polycarbonate covers was
measured by GC-MS exposed outdoors for at least 10 years,
finding levels ca. the limit of quantitation of the analytical
method (1.2 μg BPA ­g−1 polycarbonate, see Supplementary
Information).
Dermal BPA estimated daily intake
Considering the BPA found in thermal papers in use in
Argentina (Table 1), the BPA estimated daily intake (EDI)
assuming a dermal exposure mechanism was calculated.
For this calculation, the recommendations of Adeyemi
et al. (2020) have been followed. Table 1 shows the EDI
of two different cases: workers (handling frequency = 150
times ­d−1) and the general population (handling frequency
= 3 times ­d−1). It is interesting to observe that for bank-
ing, supermarket, and oil stations (among others) workers,
EDI was between 52.3 and 109.0 μgd−1 (Table 1), which is
considerably higher than the maximum allowable dose level
(MADL) of 3 μgd−1 suggested by the California Code of
Regulations (California 2016). These results are relevant,
especially taking into account data from Vahedi et al. (2016)
correlating polycystic ovary syndrome of women market
sellers with their BPA blood levels.
In our case, the mean EDI for the general population
(considering the mean of all BPA content in thermal paper)
is 1.6 ± 0.4 μgd−1 (Table 1), which is roughly half of the
MADL recommended by the California Code of Regula-
tions (2016).
BPA migration from thermal paper to soil
Regarding the previously mentioned BPA amounts, the fol-
lowing question could be raised. Which proportion of BPA
present in TP is environmentally available? This issue is
particularly important considering that most of the used TP
in Argentina are buried as solid waste. With this purpose, a
microcosmos assay was performed to estimate BPA migra-
tion rates from TP to sterile soil, to avoid biodegradation.
This soil had a water content of 50% and was at room tem-
perature. Figure 1 shows BPA content as a time function, in
TP (black squares, Fig. 1a) and in soil (grey circles, Fig. 1a).
It can be observed that the BPA that migrated from the TP
was mostly found in the soil (in all cases BPA mass balance
was in an 83.1–100% range). After 4 days, ca. 78% of the
BPA originally present in the paper had migrated to the soil.
This fast BPA migration could be explained by the action of
the soil’s water content. Although BPA in thermal paper is
incorporated in a wax layer (Björnsdotter et al. 2017), water
presence is enough to produce migration from the paper sur-
face to the soil.
53387
BPA migration from thermal paper to water
Figure 1b shows the results of BPA migration from TP to
water up to 168 h (black circles, Fig. 1b). It can be observed
that 99.6% of BPA was transferred from the TP to water in
30 h, which means that this process was faster than BPA/TP
migration to soil (Fig. 1a).
As the presence of BPA in solarized polycarbonate (PC)
was found (Supplementary Information), the migration rate
from BPA spiked PC to water (Fig. III-SM, Supplementary
Information) was measured, observing a slower migration
than in the case of TP, behaviour that could be explained
as a consequence of the more hydrophobic nature of PC
compared to paper. The combined results of a much higher
BPA content in TP than in PC and the faster migration rates
prompt the idea that BPA present in TP could have been
underestimated as an environmental contamination source.
BPA degradation in soil and water
It has been discussed that xenobiotic migration to soil is
usually followed by microbial biodegradation as the main
dissipation pathway (Ren et al. 2018). Ying and Kookana
(2005) reported BPA biodegradation in four soils with dif-
ferent physicochemical properties finding a half-life of ca. 7
days under aerobic conditions. Fent et al. (2003) estimated
BPA half-life of less than 3 days in German soils. A similar
trend was found by Jian et al. (2017) with more than 90%
of BPA degradation after 5 days of incubation in the case
of Chinese soils. Therefore, BPA degradation in Argiudoll
soil types of the same kind from the main Buenos Aires
landfill (CEAMSE, Complejo Ambiental Norte III, 2020)
was studied. Figure 2 shows the results in sterilized (black
circles, Fig. 2a) and non-sterilized (grey squares, Fig. 2a)
soils. It can be observed that after 120 h, BPA concentration
in sterilized soil remained constant while only ca. 40% of the
initial BPA could be found in non-sterilized soil, indicating
that the soil’s microbiological activity is responsible for the
BPA degradation.
As BPA can leachate from soil to water, it is environ-
mentally relevant to take into account the half-life BPA in
natural water. Ike et al. (2000) reported a BPA degrada-
tion percentage of 40 to 90% in different microcosmoses
of Japanese river water after a lag period of 3 to 5 days.
Ying and Kookana (2005) also reported the existence
of a lag period of 35 days for the BPA degradation in a
microcosmos of seawater, after which the biodegradation
process was faster. A different behaviour was observed in
water samples from rivers neighbouring BPA chemical
plants. Dorn et al. (1987) reported 90% BPA degradation
in 4 days in water samples, collected 180 m downstream a
BPA plant discharge, and employed under laboratory con-
ditions. Then, the BPA degradation in water microcosmos
13
53388
Fig. 1  BPA migration. A From
thermal paper to soil. B From
thermal paper to water
of the Reconquista River, nearby CEAMSE, Complejo
Ambiental Norte III was studied. Figure 2b shows the BPA
degradation results in natural and sterilized (as negative
control) water. It is interesting to note that after 120 h, no
degradation was observed in the control water or in the
Reconquista River samples.
Taking into consideration that Argentina imports 8.8
tons of PC annually (CAIP 2015) and hypothesizing that
all PC will contain BPA in concentrations similar to BPA
contents described in the Supplementary Information,
the BPA release from this source will be ca. 8 kg y­ ear−1
in total. Unfortunately, data about TP consumption per
13
Environmental Science and Pollution Research (2022) 29:53382–53394
person per year in Argentina was not found. As a sample,
an informal research among our families and colleagues
(100 people) was done, finding a consumption of circa
60 g of TP ­year−1 ­person−1. Taking only into account the
economically active Argentinean population (11.8 mil-
lion) and using the mean BPA concentration in TP found
in the previous section, TP could annually release into
the environment up to 12,600 kg of BPA, which is 1575
times higher than in the case of PC. These BPA figures
could partially explain the high amounts found in Buenos
Aires periurban rivers (Reconquista Basin, Supplementary
Information).
Environmental Science and Pollution Research (2022) 29:53382–53394
Fig. 2  BPA degradation. A In
soil. B In water
Ecotoxicological tests with Eisenia andrei
Lethal toxicity
­(LC50: 10–100 μgcm−2). Since E. andrei and E. fetida are
Acute lethal toxicity tests (contact paper) showed a con-
centration-response to BPA in E. andrei. The calculated
­LC 50 was 17 μgcm −2 for 24 h exposure (95% confidence
interval 6–46 μgcm −2 ). The 2-chloroacetamide was
used as reference for lethality (­ LC 50 , 24 h: 5 μgcm −2 ;
95% confidence interval 2–15 μgcm −2 ). No mortality
was observed in control organisms during L ­ C 50 experi-
ments. Roberts and Dorough (1984) proposed a toxicity
53389
ranking scheme for E. fetida using a contact paper test
for 48 h. In this context, the chemicals were classified
as extremely toxic (­ LC 50 : 1–10 μgcm −2 ) or very toxic
considered representative test organisms for earthworms
and other soil invertebrates, our results demonstrated
the high sensitivity to BPA. E. andrei were exposed to
soils with BPA levels whose effects rise ecotoxicologi-
cal interest since they are within the scope of environ-
mental concentrations reported in soil matrices in the
USA (USEPA 2010), Korea (NIER 2006), and Europe
(Staples et al. 2010).
13
53390 Environmental Science and Pollution Research (2022) 29:53382–53394

Reproduction E. andrei populations in the longer term. If the production

After 28 days of exposure to control and spiked BPA
soils, the survival rate of earthworms was 100%. No sig-
nificant effects on reproduction were observed in earth-
worms exposed to the lowest BPA concentration tested (1
mg ­BPAkg−1). On the other hand, a significant increase in
cocoon production was detected in earthworms exposed
to 10 and 50 mg BPA ­kg−1 when compared to controls
(Table 2). The hatchability percentage was not modified,
and the number of juveniles resulted also significantly
higher than in controls. Consequently, there was no modifi-
cation in the ratio of juveniles/hatched cocoons, indicating
no effect on the viability of the cocoons. Although many
authors pointed out that BPA, or other chemicals, caused a
significant reduction in the number of cocoons and young
worms (Lemos et al. 2010), the positive effect of BPA on
cocoon production at the concentrations tested in this study
could indeed be attributed to its activity as an endocrine
disruptor. Our results could be considered a reproduction
disorder caused by BPA in E. andrei. Perhaps, the hormesis
phenomenon could be taken into account, as it is a biphasic
dose-response process characterized by low-dose stimulation
and high-dose inhibition (Calabrese 2008). Although physi-
ological processes between terrestrial and aquatic organisms
may differ, some reports evidenced the same reproductive
tendency. Exposure of the invertebrate Marisa cornuarietis
to BPA induced an enhancement of mass spawning and egg
production (Oehlmann et al. 2000). Andersen et al. (1999)
informed an increase of egg production in the copepod
Acartia tonsa exposed to either the sex steroid hormone 17
β-estradiol or BPA. Invertebrates and vertebrates are pro-
vided with multiple feedback mechanisms for steroid regula-
tion and BPA can interfere with the normal endocrine func-
tion altering the reproductive process. Despite the evidenced
increase in cocoons and juveniles, further studies involved
in testing multigenerational effects are needed to establish
the deleterious effects that could result in the reduction of
of more cocoons was associated with weaker or infertile
juveniles, then it could be missing the benefic role expected
for the soil ecosystem.
Avoidance behaviour
Figure 3 shows the results of the avoidance behaviour test
after earthworm exposure to soils with BPA. No significant
differences (p > 0.05) were observed in the distribution
of the worms between both chambers of the containers in
dual control tests. Earthworms exposed to soil with BPA
exhibited significant avoidance responses (p < 0.05) at the
­ gkg−1). Though the envi-
highest applied concentration (50 m
ronmental risk is considered a function of the probability of
exposure, avoidance could lead to the disappearance of soil
organisms, with serious ecological consequences. While the
avoidance test is a faster and easier technique than earth-
worm reproduction tests (Casabé et al. 2007), the repro-
ductive chronic assays have proven to be more sensitive in
evidencing effects of BPA on E. andrei (10 mg BPA ­kg−1).
Enzymatic activities
ChE, CaE, and GST of E. andrei were evaluated as potential
biomarkers of BPA in soils. However, these enzymes were
not sensitive at the BPA concentrations exposure assayed
(see Supplementary Information).
BPA degradation using ­H2O2 and Raphanus sativus
It has been estimated that at least 30% of the thermal paper
used as receipts in different points-of-sale is recycled to pro-
duce other paper products, like newspaper and magazines, con-
tainerboard, folding cardboard, and toilet paper and napkins
among other applications (EU 2010). This means that BPA
present in thermal paper can expand its environmental distri-
bution mechanism as a consequence of recycling practices. A

Table 2  Effects of exposure BPA (mg/kg soil)

to BPA treated soils on
reproductive parameters of Parameter 0(a) 1 10 50
Eisenia andrei 
Mortality % (28 days) 0 0 0 0
No. of cocoons (56 days) 17 ± 3 17 ± ­12(b) 30 ± 1 *(c) 30 ± 6 *
No. of hatched cocoons (56 days) 11 ± 4 14 ± 9 24 ± 1 * 23 ± 8 *
No. of unhatched cocoons (56 days) 6±1 3±2 6±1 7±2
Hatchability % (hatched × 100 / total No. 65 ± 26 82 ± 77 80 ± 4 76 ± 30
of cocoons)
No. of juveniles (56 days) 26 ± 4 36 ± 13 50 ± 9 * 47 ± 11 *
No. of juveniles/hatched cocoons 2.4 ± 0.4 2.6 ± 0.7 2.1 ± 0.2 2.0 ± 0.4
(a)
 Control. (b)Mean ± SD (6 replicates). (c) *Significantly different from control (ANOVA and Tukey’s post
test, p < 0.05)

13
Environmental Science and Pollution Research (2022) 29:53382–53394
Fig. 3  Eisenia andrei avoidance
test in soils with BPA
potential solution to this problem could be the development
of an in-house BPA degradation methodology to treat thermal
paper before its recycling. Several methodologies have been
tested for BPA degradation (Li et al. 2020; Liu et al. 2019).
The challenge for an in-house degradation methodology is the
development of a treatment with the lowest possible risk and
with available common supplies. Considering these facts, a
BPA/TP degradation method using ­H2O2 and radish tissue as
a source of peroxidases, with no laboratory glassware, was
assayed (Beiguel et al. 2016). The BPA/TP was left in con-
tact with water in a common glass flask for 2 h to assure the
maximum BPA migration from the TP to water. Then skinless
radish tissue and ­H2O2 were added and the mixture was left
to rest for another 2 h. A blank experiment (without ­H2O2)
was done in parallel as a negative control (Fig. 4). The BPA
content was determined by HPLC in the TP, the radish tissue,
and the remaining solution at the end of the 2 h. While the
BPA content present in the TP in the blank and degradation
experiments was in both cases 0.05 ± 0.04% (of the total BPA
originally present in the TP, Fig. 4), 1.3 ± 0.4% and 0.005 ±
0.004% of BPA were found in the radish tissue for the blank
and degradation experiments. A significant difference was
observed for the BPA present in the remaining water solution.
While 88 ± 8% of BPA was found in the blank experiment, 1.0
±0.4 % remained in the degradation assay. These results indi-
cate that the relative BPA content after the degradation was, at
most, 1.5% of the BPA originally present in the TP. Moreover,
aliquots coming from the degradation assays were ecotoxico-
logically tested with Lactuca sativa seeds. The mean length of
radicles of control seeds exposed to water and seeds exposed
to the supernatant of the recycling process or aqueous extract
of TP was 16.0 ± 2.5 mm (0% inhibition), 14 ± 2 mm (12%
53391
inhibition), and 8.9 ± 3 mm (56% inhibition), respectively. It
can be noted that not only the toxic effect produced by BPA in
the seeds was partially reversed but also no serious deleterious
effect that could come from toxic metabolites was observed in
L. sativa. It is worth noting that the BPA concentration that
inhibited 50% of root seeds elongation ­(IC50) is (1.51 ± 0.05)
× ­10−4 M (see Supplementary Information). The use of veg-
etable tissues of Raphanus sativus as biocatalyst represents a
low-cost technological option with attractive properties such as
low energy requirements, easy handling, and promising results.
Conclusions
BPA presence in one of the more important Argentinean
basins was observed. Thermal paper was proposed as the
main BPA source, finding 11.1–30.5 mg BPA g­ −1 thermal
paper. Considering this value, the estimated daily intake was
79.3 ± 19.5 μg ­d−1 for workers (above recommendations)
and 1.6 ± 0.4 μg d­ −1 for the general population. It was dem-
onstrated that the BPA of thermal paper easily migrates to
soil and water (78.0% and 99.6% of the original BPA on
TP respectively). Additionally, BPA degradation in soil and
natural water was studied, observing that once BPA reaches
natural water it can circulate in the environment.
A set of ecotoxicological assays were done using E.
andrei as bioindicator to evaluate BPA impact on soil. E.
andrei proved to be sensitive to BPA as observed by the low
­LC50 determined (contact paper test) and by its response to
environmentally relevant concentrations in avoidance and
reproduction tests in soils.
13
53392
Fig. 4  BPA/TP degradation using ­H2O2 and Raphanus sativus as a catalyst
Finally, and as a proof of concept, a BPA domestic deg-
radation procedure using H ­ 2O2 and radish tissue (4 h, no
buffers,) yielding 98.5% degradation.
Urgent actions need to be taken in Argentina regarding
BPA use in thermal paper to avoid negative impacts on
humans and on the environment.
Supplementary Information  The online version contains supplemen-
tary material available at https://d​ oi.o​ rg/1​ 0.1​ 007/s​ 11356-0​ 22-1​ 9561-9.
Acknowledgements  SN thanks UNGS for a postgraduate fellowship.
GB and GF thank CONICET for a postdoctoral and doctoral fellowship
respectively. JMM is a CONICET member.
Data availability  All data generated or analysed during this study are
included in this published article (and its supplementary information
files). Any experimental detail needed can be electronically required
to the corresponding authors.
Author contribution  SN: Investigation, field studies, and method
development. EB: Investigation, field studies, and method develop-
ment. GFF: Investigation, field studies, and method development. CI:
Investigation, field studies, and method development. GB: Investiga-
tion, field studies, method development, and paper review. SB: Concep-
tualization, investigation, field studies, original draft writing, editing,
13
Environmental Science and Pollution Research (2022) 29:53382–53394
and general supervision. JMM: Conceptualization, investigation, field
studies, original draft writing, editing, general supervision, and fund-
ing acquisition.
Funding  This work has been financially supported by the Universidad
Nacional de General Sarmiento and CONICET (PIO-UNGS 2015-2016
14420140100012CO).
Declarations 
Ethics approval and consent to participate  Not applicable.
Consent for publication  Not applicable.
Competing interests  The authors declare no competing interests.
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