Detection of microplastics in human colectomy specimens

Abstract

Background and Aim
While dietary exposure to microplastics is increasingly recognized, it is unknown if ingested plastics remain within the digestive tract. We aimed to examine human colectomy specimens for microplastics and to report the characteristics as well as polymer composition of the particles.

Methods
Colectomy samples were obtained from 11 adults (mean age 45.7, six males) who were residents of Northeastern Peninsular Malaysia. Microplastics were identified following chemical digestion of specimens and subsequent filtration. The samples were then examined for characteristics (abundance, length, shape, and color) and composition of three common polymer types using stereo‐ and Fourier Transform InfraRed (FTIR) microscopes.

Results
Microplastics were detected in all 11 specimens with an average of 331 particles/individual specimen or 28.1 ± 15.4 particles/g tissue. Filaments or fibers accounted for 96.1% of particles, and 73.1% of all filaments were transparent. Out of 40 random filaments from 10 specimens (one had indeterminate spectra patterns), 90% were polycarbonate, 50% were polyamide, and 40% were polypropylene.

Conclusion
Our study suggests that microplastics are ubiquitously present in the human colon.

Full text

ORIGINAL ARTICLE
Detection of microplastics in human colectomy specimens
Yusof Shuaib Ibrahim,*Sabiqah Tuan Anuar,*Alyza A Azmi,*Wan Mohd Afiq Wan Mohd Khalik,*
Shumpei Lehata,*Siti Rabaah Hamzah,*Dzulkiflee Ismail,
†
Zheng Feei Ma,
‡,§
Andee Dzulkarnaen,
‡
Zaidi Zakaria,
‡
Nazri Mustaffa,
‡
Sharifah Emilia Tuan Sharif
‡
and Yeong Yeh Lee
‡,¶,∥
*Microplastic Research Interest Group, Faculty of Science and Marine Environment, Universiti Malaysia Terengganu, Kuala Nerus, School of
†
Health Sciences,
‡
Medical Sciences, Universiti Sains Malaysia, Kota Bharu,
¶
Gut Research Group, Faculty of Medicine, National University of Malaysia, Kuala Lumpur, Malaysia,
§
Department of Health and Environmental Sciences, Xi’an Jiaotong-Liverpool University, Suzhou, China and
∥
St George and Sutherland Clinical School,
University of New South Wales, Sydney, Australia
Key words
cancer, colectomy, human, microplastic.
Accepted for publication 2 November 2020.
Correspondence
Yeong Yeh Lee, School of Medical Sciences,
Health Campus, Universiti Sains Malaysia, Jalan
Raja Perempuan Zainab II, 16150, Kota Bharu,
Kelantan, Malaysia.
Email: justnleeyy@gmail.com
Declaration of conflict of interest: None.
Author contribution: Yusof Shuaib Ibrahim and
Yeong Yeh Lee were responsible for the
conception and design of the work. Andee
Dzulkarnaen, Zaidi Zakaria, Nazri Mustaffa, and
Sharifah Emilia Tuan Sharif were involved in
sample acquisition and processing. All authors
performed the data analysis and interpretation.
Yusof Shuaib Ibrahim, Nazri Mustaffa, and Yeong
Yeh Lee wrote the manuscript and all authors
approved the final version.
Funding support: Ministry of Higher Education
(MOHE) of MalaysiaFRGS 203.
PPSP.6171192FRGS 59457
Abstract
Background and Aim: While dietary exposure to microplastics is increasingly recog-
nized, it is unknown if ingested plastics remain within the digestive tract. We aimed
to examine human colectomy specimens for microplastics and to report the character-
istics as well as polymer composition of the particles.
Methods: Colectomy samples were obtained from 11 adults (mean age 45.7, six
males) who were residents of Northeastern Peninsular Malaysia. Microplastics were
identified following chemical digestion of specimens and subsequent filtration. The
samples were then examined for characteristics (abundance, length, shape, and color)
and composition of three common polymer types using stereo- and Fourier Transform
InfraRed (FTIR) microscopes.
Results: Microplastics were detected in all 11 specimens with an average of 331 parti-
cles/individual specimen or 28.1 15.4 particles/g tissue. Filaments or fibers
accounted for 96.1% of particles, and 73.1% of all filaments were transparent. Out of
40 random filaments from 10 specimens (one had indeterminate spectra patterns),
90% were polycarbonate, 50% were polyamide, and 40% were polypropylene.
Conclusion: Our study suggests that microplastics are ubiquitously present in the
human colon.
Introduction
Since the 1950s, billions of tons of plastic waste have been indis-
criminately disposed in the environment, ending up in remote
locations and oceans.
1,2
Over time, some of these disposed plas-
tics are degraded into microplastics (broadly defined as size
<5 mm).
1
Microplastics pollution is a significant environmental
issue in the Southeast Asia region.
2,3
For example, a recent study
showed that microplastics were detected in abundance at the
marine shores of Kuala Nerus and Kuantan, which are located on
the east coast of Peninsular Malaysia.
4
There were also abundant
microplastics found in local marine species; this included key-
stone species that are crucial in maintaining water quality.
5
Microplastics were also identified in cage-cultured Asian sea
bass.
6
Microplastics exist within the human food chain not only
as a result of ingesting contaminated cetaceans and fish
7
; micro-
plastics are also disseminated through atmospheric transport from
inland trash (e.g. landfills or indiscriminate waste), or even from
everyday plastic materials (e.g. food packaging) and clothes.
8–10
There are increasing reports on potential human exposure
to plastics in the food chain,
11–13
and a recently published study
detected microplastics in eight human stool samples which was
presumed to be due to ingestion of plastics from different
sources.
14
Ingested microplastics have been shown to cause
adverse bowel consequences in marine organisms.
15
For instance,
in zebrafish, microplastics were found to cause inflammation and
oxidative stress within gut tissue.
16
However, it is unknown if
microplastics remain within the human digestive tract for pro-
longed periods after dietary exposure; and if so, the potential
doi:10.1002/jgh3.12457
JGH Open: An open access journal of gastroenterology and hepatology (2020) 1–6
© 2020 The Authors. JGH Open published by Journal of Gastroenterology and Hepatology Foundation and John Wiley & Sons Australia, Ltd.
This is an open access article under the terms of the Creative Commons Attribution-NonCommercial License, which permits use, distribution and reproduction in any
medium, provided the original work is properly cited and is not used for commercial purposes.
1

health impacts these microplastics may cause, including the pos-
sibility of malignancies.
17
Hence, in the present study, we aimed to examine human
colectomy specimens for the presence of microplastics, particle
characteristics, and polymer composition. These samples were
readily available for research as colectomies are routinely per-
formed in patients with colorectal malignancies.
Methods
Participants were recruited from Hospital Universiti Sains Malay-
sia (USM), a tertiary care center situated in the northeastern
coastal region of Peninsular Malaysia (Fig. 1). Patients
(≥18 years) who were scheduled for colectomy were recruited
sequentially for this study. Clinical indications for colectomy
included colorectal cancer and non-cancer (e.g. bleeding arterio-
venous malformation, colonic perforation, and trauma) diagno-
ses. Prior to colectomy, potential subjects were counseled, and
informed consent was obtained. Colectomy was performed as per
standard surgical practice. A portion of the colectomy specimen
was then harvested for study analysis, the remaining sample was
then sent for routine histopathological processing. Cautionary
measures were taken during specimen harvesting by investigators
to avoid possible contact with common plastics in the operation
theater, which included sutures, mesh, and containers. All tissue
samples were placed in formalin except for one tissue sample
(stored on filter paper enclosed in a glass petri dish) during labo-
ratory transport. The formalin and filter paper were thoroughly
checked for microplastic contamination before use.
Sample preparation as well as techniques to quantify and
identify polymers in microplastics were adapted from previously
described methods which were used for marine organisms.
18
Weighed tissue were chemically digested with 10% potassium
hydroxide at 60C for 7–10 h. The digested samples were then
diluted with deionized water to prevent clogging during filtration,
filtered using 0.45 μm cellulose membrane paper (Whatman,
Merck KGaA, Darmstadt, Germany) and subsequently dried in a
glass desiccator with silica gel at room temperature over 2 days.
Following this, using a stereo dissecting microscope with a 7:1
zoom ratio and a magnification of 0.8–5.6×(model SZX7, Olym-
pus Corp., Tokyo, Japan), the abundance and characteristics
(length, shape, and colors) of the microplastic particles that had
the longest average length were determined. Micrographs of the
microplastic particles were captured using microscope cameras
(STEMI2000-c, Zeiss, Oberkochen, Germany) and ScopePad-
500 (Yenway Microscopes, United Kingdom) at magnifications
of 0.6-5×. Using a scanning electron microscope with energy-
dispersive X-ray (SEM/EDX) analysis (JOEL JSM-6360LA,
JEOL Ltd., Japan), the surface morphology and elemental com-
position (carbon counts) of the samples were also studied.
Finally, the composition of three common polymers that is, poly-
carbonate (PC), polypropylene (PP), and polyamide (PA) in
microplastics were identified for each specimen. These polymers
were chosen not only because they are found abundantly in water
and marine organisms but also because of their potential effects
on human health.
19,20
To distinguish plastic from natural parti-
cles, especially smaller microplastics, a representative random
subset of samples (10–30% of the total microplastic count) were
subjected to a hot needle test which were then validated by
micro-FTIR spectroscopy.
4,21–25
In addition, to determine the
presence of three common polymers that is, PA, PC, and PP, at
least four representative filaments were chosen randomly from
each specimen. In brief, plastic (but not natural) particles will
melt when subjected to a hot needle test. A standalone micro-
Fourier Transform InfraRed (FTIR) microscope (model LUMOS,
Bruker Optics Inc., MA, USA) in Attenuated Total Reflectance
mode was used to identify the polymer types by recording the
spectra in the mid-IR range of 4000–400 cm
−1
(60 scans per
analysis). The recorded images and spectra were processed using
the OPUS/IR Package Version 8.0 software, which identifies
characteristic wavelengths and compares the recorded spectra
against those from a reference library.
As potential airborne contamination was a significant con-
cern, the following preventive steps were rigorously undertaken
during laboratory experiments: (i) cotton lab gowns and latex
gloves were worn during laboratory work, (ii) all liquid reagents
and media were filtered before use, (iii) when not in use, samples
were covered with a lid or aluminum foil, (iv) each test apparatus
would be cleaned with distilled or deionized water before the
experiment, (v) sorting of samples were performed inside
Figure 1 Map of Peninsular Malaysia. Sites of microplastics research
in the pristine northeastern coast that include ( ) Kota Bharu (current
study), ( ) Setiu wetlands, ( ) Kuala Nerus and ( ) Kuantan Port.
Microplastics in human colectomy YS Ibrahim et al.
2JGH Open: An open access journal of gastroenterology and hepatology (2020) 1–6
© 2020 The Authors. JGH Open published by Journal of Gastroenterology and Hepatology Foundation and John Wiley & Sons Australia, Ltd.

contamination chambers, and (vi) use of plastic-containing
apparatus was kept to a bare minimum. In addition, during
microscopic analysis, dampened and exposed filter papers adja-
cent to the sample dishes as well as systematic blanks were
used for quality control.
All data were entered into and analyzed using SPSS ver-
sion 22 (SPSS Inc., Chicago, IL, USA). Numerical data were
presented as mean and SD unless otherwise stated.
Approval was obtained from the Human Research Ethics
Committee of Universiti Sains Malaysia (USM) (reference:
USM/JEPeM/19010050).
Results
Samples were obtained from 11 participants (mean age
45.7 17.9 years, age range 34–88 years, six males); nine sub-
jects had colorectal cancer while two had a normal colon
(Table 1). All systematic blanks were negative. The mean
weight of colectomy samples was 13.4 4.5 g. All samples
had evidence of microplastics with an average count of 331 per
individual or 28.1 15.4 particles per g of colon tissue. The
filament form accounted for 96.1% of all samples. The filamen-
tous particles came in different colors including transparent,
black, red, green, blue, brown, purple, and yellow (Fig. 2a).
Overall, transparent filaments accounted for 73.1% of all colors.
The longest dimension of particles ranged from 0.8 to 1.6 mm
with an average of 1.1 0.3 mm. Figure 2b shows the typical
morphology and the high carbon counts of polymeric micro-
plastics observed under SEM/EDX. Polymers were identified in
a subset of samples, except for one sample because of an inde-
terminate spectra pattern. Of the subset of 40 randomly chosen
filaments from 10 specimens (eight cancer and two normal sub-
jects), 90% were PCs, 50% were PAs 50%, and 40% were PPs
(Fig. 2c).
Discussion
Our study detected microplastics in colectomy specimens; this
indicates the ubiquitous nature of microplastics in our digestive
tract and corroborates recent findings from a study on human
stool samples.
14
On average, we detected 331 particles per indi-
vidual specimen or 28 particles per g of colon tissue. Our study
provides evidence supporting the ingestion (and or inhalation)
of plastics by humans.
7,11
As ours is the first human study
using colectomy samples, there are no similar data for compari-
son; however, recent estimates of human exposure to micro-
plastics might provide some clues.
11,12,26
For instance, based
on 15% of an American citizen’s caloric intake, Cox et al. have
estimated an annual microplastics ingestion of 39 000 to
52 000 particles, this estimate increases from 74 000 to
121 000 when the inhalation route is included.
11
Zhang et al.
have also estimated human microplastics burden through the
use of table salt and drinking water as well as inhaled air of
(0–7.3) ×10
4
,(0–4.7) ×10
3
and (0–3.0) ×10
7
items per per-
son per year, respectively.
26
In a prospective study of 2000
individuals from Iran, there were 650 microplastics or an aver-
age of 0.33 particles per individual which were identified from
saliva samples.
12
Moreover, existing literature reveals that the
abundance of microplastics in the digestive tract seems to vary
across different marine organisms; for example, one study states
Table 1 Characteristics of study participants
Age
(years) Sex Colectomy diagnosis
Weight of
sample
(g)
Microplastic
abundance
Transparent
filaments
abundance
%of
transparent
filaments Polymer content
34 Female Moderately differentiated adenocarcinoma 17.0 35 20 57.1 Polycarbonate
88 Female Moderately differentiated adenocarcinoma 17.3 214 115 54.0 Polycarbonate,
polypropylene
35 Male Poorly differentiated adenocarcinoma with mucinous and
signet-ring component
15.8 450 407 91.5 Polycarbonate, polyamide
63 Female Moderately differentiated adenocarcinoma 15.9 563 528 95.1 Polycarbonate, polyamide
63 Female Moderately differentiated adenocarcinoma 4.7 202 104 55.0 Polycarbonate
34 Male Moderately differentiated adenocarcinoma 14.8 615 285 66.3 Polycarbonate, polyamide
48 Female Poorly differentiated neuroendocrine carcinoma 6.4 331 192 58.0 Not available
41 Male Mucinous adenocarcinoma with carcinomatous peritonei 11.0 375 317 84.5 Polycarbonate, polyamide
36 Male Signet ring carcinoma 17.0 145 87 60.0 Polyamide, polypropylene
67 Male Bleeding arteriovenous malformation 16.7 430 385 93.0 Polypropylene
34 Male Normal perforated colon with background history of
inflammatory bowel disease
10.7 278 250 89.9 Polycarbonate,
polypropylene
YS Ibrahim et al. Microplastics in human colectomy
JGH Open: An open access journal of gastroenterology and hepatology (2020) 1–6
© 2020 The Authors. JGH Open published by Journal of Gastroenterology and Hepatology Foundation and John Wiley & Sons Australia, Ltd.
3

that there were 5.5 particles per marine mammal
27
while another
study found 2 particles per fish.
28
In human stool, however, there
was a median of 20 pieces of microplastic per 10 g of stool.
14
Subjects included in our study were long-time coastal resi-
dents where seafood and fish sauce are the dietary norm.
29,30
Pre-
vious studies have shown that even at pristine shores,
microplastics could be found in abundance
4,31
which was proba-
bly associated with the use of fishing nets, plastic fishing gear,
food packaging, and also the likelihood of airborne particles.
5,32
Subsequent ingestion of these microplastics by zooplankton and
other marine organisms for example, Scapharca cornea would
then introduce plastics into the food web of nearby residents.
5,32
Therefore, the plastic particles found in the colonic samples of
our subjects could be explained by exposure to microplastics
contained in contaminated seafood or similarly sourced foods.
However, it is important to note that even though bivalve con-
sumption may be a major exposure pathway, inhalation of micro-
plastics should also be considered as a significant contributing
factor. Contamination from the operation theater environment,
during transportation or within the laboratory cannot be totally
excluded. However, the negative procedural blanks does provide
assurance on the quality of this study.
Filament or fiber was the most common shape found in
our study. This observation is similar to studies on the environ-
ment and other studies on cetaceans, fish, and mammals
15
which
further support the validity of our findings. In contrast, fragments
and films were more common than fibers in the study on human
stools.
14
We cannot explain this disparity; we did not collect
stool samples from our subjects for comparison. Instead of col-
ored filaments commonly found in marine organisms,
33
our
human samples had more transparent filaments. We hypothesized
that ingested colored microplastics may be later “bleached”by
digestive enzymes during prolonged colonic transit within
humans. While we are unsure of the actual bleaching agent(s) or
processes in-vivo, we postulate that bile salts could be involved.
Future in-vitro tests with microplastics exposed to bile aspirated
during endoscopy could help determine if bleaching of colors
occurs over time.
In humans, toxicity from microplastics exposure is still
unclear due to limited data. Based on ecotoxicology studies in
marine species, microplastics could elicit gut inflammation
through changes in intestinal permeability and dysbiosis.
16
From
studies in human cell lines, including a recent report on polysty-
rene, some degree of cytotoxicity by microplastics have been
documented especially at high concentration and with smaller
particles.
20,34,35
Furthermore, evidence from occupational risk
studies indicate that exposure to plastics might be a potential
cause of colorectal cancer.
36,37
Although our study reported the
presence of microplastics in human colon, the relationship
between microplastics exposure and colon cancer in humans
remains speculative. However, individuals with increased intesti-
nal permeability for example, in those with inflammatory bowel
Figure 2 Filament form in various colors detected in (A1) normal colon and (A2) colon cancer; (B1) SEM/DX image of morphology and (B2) carbon
counts of a representative plastic sample confirming its polymeric nature. (C1) chemical imaging using micro-FTIR of the three polymers in filament
particles and (C2) respective spectroscopy wavelengths.
Microplastics in human colectomy YS Ibrahim et al.
4JGH Open: An open access journal of gastroenterology and hepatology (2020) 1–6
© 2020 The Authors. JGH Open published by Journal of Gastroenterology and Hepatology Foundation and John Wiley & Sons Australia, Ltd.

diseases might have a higher risk of microplastic particle translo-
cation, especially into deeper tissue and blood vessels which
could potentially result in systemic adverse effects.
38
We would like to highlight several physical characteristics
of the polymers that were identified in this study. PC is a durable
and robust thermoplastic polymer commonly found in electronic
components and construction materials, but also individual drink-
ing bottles and food containers. Bisphenol-A, a by-product
of PC, is a known endocrine disruptor that may cause colon
cancer.
39
PA is a component of nylon, commonly found in fish-
nets, and may cause direct inflammatory responses in the colon
and indirectly from chemical additives.
40
PP is a thermoplastic
polymer and because of its inert character, PP is commonly used
in medical applications which include sutures and meshes. In this
present study, we are not able to explain the differences in the
relative abundance of these various polymers. It is postulated that
differential degradation of polymers by gastric and intestinal
secretions may be a factor; however, further studies are needed
to prove this.
We acknowledge that there are limitations to our study.
Colectomy specimens were only obtained as part of the subject’s
clinical management, which explains the small sample size in our
study. While stool analysis is not absolutely necessary, if avail-
able this may assist in explaining the possible discrepancy in
polymer characteristics found in stool versus those from colonic
mucosal samples. For example, PC was most abundant in our
colonic specimens; however, stool studies from Schwabl et al.
found that PP was the most frequent polymer detected.
14
We also
did not attempt to determine the dietary sources of microplastics;
this could have involved seafood, food packaging, or even air-
borne particles. In view of this, having a food diary which lists
down what the subjects consumed may be helpful for future stud-
ies. Only a subset of filaments and limited number of polymer
types were investigated due to the time-consuming nature of
processing the samples; there were also financial constraints. Due
to the exploratory nature of our study and the limitations listed
above, further confirmatory analysis is needed using specimens
from a larger human cohort. Future research should include con-
centrations of colonic microplastics in normal and colorectal car-
cinoma subjects, or even in those with other bowel ailments to
elucidate the cut-off points of these plastic particles and their
relation to colonic diseases.
In conclusion, our preliminary study provides evidence
that microplastics exist in human colonic tissue samples.
Acknowledgments
The work was supported by the Ministry of Higher Education
(MOHE) of Malaysia through the following research grants;
FRGS 59457 and FRGS 203.PPSP.6171192. We wish to
acknowledge UMT (Centre Lab & INOS) and USM for provid-
ing research facilities, and UNESCO/IOC WESTPAC for train-
ing as well as related technical support.
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