Graphene-based contrast agents for photoacoustic and
Gaurav Lalwania,1, Xin Caib,1, Liming Nieb, Lihong V. Wangb,2,*, Balaji Sitharamana,3,**
aDepartment of Biomedical Engineering, Stony Brook University, Stony Brook, NY 11794-5281, USA
bOptical Imaging Laboratory, Department of Biomedical Engineering, Washington University in St. Louis, Campus Box 1097, One Brookings Drive, St. Louis,
MO 63130, USA
Hybrid imaging modalities, such as photoacoustic (PA) tomog-
raphy (PAT)  and thermoacoustic (TA) tomography (TAT) ,
have been developed for different applications. PAT/TAT combines
advantages of pure ultrasound and pure optical imaging/radio
frequency (rf), providing good spatial resolution, great penetration
depth, and high soft-tissue contrast. These imaging modalities are
based on detection of acoustic waves from an object that absorbs
electromagnetic (EM) energy (laser in PAT and microwave in TAT).
Endogenous molecules, such as hemoglobin, melanin, and water/
ion, can absorb EM energy, producing acoustic waves. High
resolution PAT and/or TAT enable functional brain imaging ,
breast cancer detection , melanoma detection , tumor
angiogenesis , and functional molecular imaging . However,
in cases when endogenous molecules are insufficient, exogenous
contrast agents (CAs) are developed and administered. Contrast-
enhanced PAT has been applied in lymph node mapping ,
multiscale imaging of tissue engineering scaffolds [8,9], and
molecular, cellular, and functional imaging [10,11]. A variety of CAs
for PAT have been reported, such as, carbon nanoparticles [7,12–
14], metallic nanoparticles [11,15–17], and organic dyes . In
comparison to PAT, fewer reports have focused on development of
CAs for TAT. Superparamagnetic iron oxide nanoparticles, single-
and multi-walled carbon nanotubes (SWCNT and MWCNT), and
air-filled microbubbles have been investigated as CAs for TAT
In this work, we investigate efficacy of graphene nanoparticles,
prepared by two widely used methods ((1): longitudinal unzipping
method , (2): modified Hummer’s method of oxidation ) as
CAs for PAT and TAT. We compare PA and TA signal amplitudes of
oxidized single- and multi-walled graphene oxide nanoribbons (O-
SWGNRs and O-MWGNRs), and oxidized graphene nanoplatelets
(O-GNPs) to pristine SWCNTs, pristine MWCNTs, pristine graphite
microparticles (GMPs), and oxidized graphite microparticles (O-
2. Results and discussions
O-SWGNRs, O-MWGNRs, and O-GNPs were synthesized as
reported previously [22,23]. Pristine SWCNTs, MWCNTs, and GMPs
Photoacoustics 1 (2013) 62–67
A R T I C L E
I N F O
Received 14 July 2013
Received in revised form 18 September 2013
Accepted 8 October 2013
A B S T R A C T
In this work, graphene nanoribbons and nanoplatelets were investigated as contrast agents for
photoacoustic and thermoacoustic tomography (PAT and TAT). We show that oxidized single- and multi-
walled graphene oxide nanoribbons (O-SWGNRs, O-MWGNRs) exhibit approximately 5–10 fold signal
enhancement for PAT in comparison to blood at the wavelength of 755 nm, and approximately 10–28%
signal enhancement for TAT in comparison to deionized (DI) water at 3 GHz. Oxidized graphite
microparticles (O-GMPs) and exfoliated graphene oxide nanoplatelets (O-GNPs) show no significant
signal enhancement for PAT, and approximately 12–29% signal enhancement for TAT. These results
indicate that O-GNRs show promise as multi-modal PAT and TAT contrast agents, and that O-GNPs are
suitable contrast agents for TAT.
? 2013 The Authors. Published by Elsevier GmbH. All rights reserved.
§This is an open-access article distributed under the terms of the Creative
Commons Attribution-NonCommercial-No Derivative Works License, which
permits non-commercial use, distribution, and reproduction in any medium,
provided the original author and source are credited.
* Corresponding author at: Department of Biomedical Engineering, Washington
University in St. Louis, Campus Box 1097, One Brookings Drive, St. Louis, MO 63130,
** Corresponding author at: Department of Biomedical Engineering, Bioengineer-
ing Building Room 115, Stony Brook University, Stony Brook, NY 11794-5281, USA.
Tel.: +1 631 632 1810; fax: +1 631 632 8577.
E-mail addresses: firstname.lastname@example.org (L.V. Wang),
email@example.com, firstname.lastname@example.org (B. Sitharaman).
1These authors contributed equally to the work.
2PAT and TAT.
3Graphene contrast agents.
Contents lists available at ScienceDirect
jo ur n al ho m epag e: ww w.els evier .c om /lo cat e/pac s
2213-5979/$ – see front matter ? 2013 The Authors. Published by Elsevier GmbH. All rights reserved.
were used as starting materials in the preparation of O-SWGNRs,
O-MWGNRs, and O-GNPs, respectively. O-GMPs are intermediate
product formed during the synthesis of O-GNPs. These nanoma-
terials were characterized by Raman spectroscopy and electron
SWCNTs, MWCNTs, O-SWGNRs, O-MWGNRs, GMPs, O-GMPs,
and O-GNPs has been reported previously [22,24–26]. Table 1
lists the size distribution of various nanomaterials. Fig. 1 shows
representative transmission EM (TEM) images of all nanomaterials
used in the study (scanning EM (SEM) for GMPs). SWCNTs (Fig. 1A)
and MWCNTs (Fig. 1B) were nanotubes of lengths ?3–30 mm and
0.5–200 mm, and diameters ?1–2 nm and ?20–30 nm, respec-
tively. O-SWGNRs (Fig. 1C) and O-MWGNRs (Fig. 1D) possessed
lengths ?0.5–1 mm and 0.5–1.5 mm, and diameters of ?3–6 nm
and ?60–90 nm, respectively, confirming complete unzipping of
SWCNTs and MWCNTs (p*diameter). Pristine GMPs were <45 mm
in size (Fig. 1E). O-GMPs (Fig. 1F) were loosely arranged sheets of a
few layered graphene (?8 sheets, size >1 mm) whereas O-GNPs
(Fig. 1G) had ?2–4 graphene sheets and diameters of ?5–15 nm.
We have estimated that future in vivo preclinical safety (acute
toxicity) studies to establish the therapeutic dosages of graphene
would require their administration at a range of dosages; from
50 mg/kg upto possibly ?500 mg/kg body weight of the small
animal . If the graphene formulations are injected at a dose of
50 or 500 mg/kg body weight of a 250 g rat (total circulating blood
volume 12–13 ml), its steady state blood concentration after the
first pass would be ?1 or 10 mg/ml, respectively. Thus, a median
concentration of 5 mg/ml was chosen for this study. Since
Fig. 1. Representative transmission electron microscopy images of (A) single-walled carbon nanotubes (SWCNTs), (B) multi-walled carbon nanotubes (MWCNTs), (C) oxidized
single-walled graphene nanoribbons (O-SWGNRs), (D) oxidized multi-walled graphene nanoribbons (O-MWGNRs), (F) oxidized graphite microparticles (O-GMP), and (G)
exfoliated graphene nanoplatelets (O-GNP). Image (E) is a scanning electron micrograph of pristine GMPs.
G. Lalwani et al. / Photoacoustics 1 (2013) 62–67
hemoglobin is a dominant optical absorber producing strong PA
signal in human tissue, efficacy of these nanomaterials was
compared with blood in the NIR wavelength window. Fig. 2A
shows PA signal amplitudes obtained from a tygon tube (I.D.
250 mm, O.D. 500 mm) filled with SWCNT, MWCNT, O-SWGNR, O-
MWGNR, micro-graphite flakes, O-GMP, O-GNP and lysed bovine
blood (905–250, Quad Five), respectively. The signals were
normalized to that for blood at 740 nm. At 755 nm excitation
wavelength, peak-to-peak PA signal amplitudes obtained from
micro-graphite flakes, O-GMPs, and O-GNPs were comparable to
that from blood alone. In contrast, those from SWCNTs, MWCNTs,
O-SWGNRs and O-MWGNRs were more than 5 times stronger than
that from blood, in which, O-SWGNRs showed ?14 times stronger
signal. At 5 mg/ml concentration, PA signal intensities obtained
from gold nanoparticles were 3 times greater, and methylene blue
dye were similar, compared to blood [28,29]. We detected a very
high signal-to-noise ratio (SNR; ratio of the average signal to the
standard deviation of the background) of O-SWGNRs at 5 mg/ml.
The SNR was >170 and suggested that the concentration of the O-
SWGNRs can be as low as 0.03 mg/ml using PAT. At this low O-
SWGNR concentration, a 2-fold increase in PA signal was measured
compared to background (1.2 mg/ml DSPE-PEG in DI water)
(Fig. 2B). These results suggest that minimum detectable
concentration of O-SWGNRs will be comparable to other PA
contrast agents such as gold nanoparticles [17,30]. Furthermore,
the results showed that PA signal obtained from these nanoma-
terials exceeded inherent blood signal over the investigated NIR
bandwidth, suggesting their utility for in vivo imaging.
Water and ions are two well-known sources of microwave
absorbers in human tissue, and they generate strong TA signals.
Therefore, to show that nanomaterials can function as CAs for TAT,
we compared TA signal of nanomaterials to that of DI water. Fig. 3B
shows TA signals obtained from a low-density polyethylene (LDPE)
vial (I.D. = 6 mm and 1.5 cc volume) filled with DI water, SWCNTs,
Fig. 2. (A) Photoacoustic spectral amplitudes of blood, single-walled carbon nanotubes (SWCNTs), multi-walled carbon nanotubes (MWCNTs), oxidized single-walled
graphene nanoribbons (O-SWGNRs), oxidized multi-walled graphene nanoribbons (O-MWGNRs), micro-graphite flakes (GMPs), oxidized graphite microparticles (O-GMPs),
and exfoliated graphene nanoplatelets (O-GNPs). PA signal amplitudes are normalized to that of blood at 740 nm. (B) PA signal amplitude of O-SWGONRs at 0.03 mg/ml
concentration compared to background (1.2 mg/ml of DSPE-PEG solution).
Size distribution of various nanomaterials.
Single-walled carbon nanotubes (SWCNTs)
Multi-walled carbon nanotubes (MWCNTs)
Oxidized single-walled graphene nanoribbons (O-SWGNRs)
Oxidized multi-walled graphene nanoribbons (O-MWGNRs)
Pristine graphite microparticles (GMPs)
Oxidized graphite microparticles (O-GMPs)
Oxidized graphene nanoplatelets (O-GNP)
G. Lalwani et al. / Photoacoustics 1 (2013) 62–67
MWCNTs, O-SWGNRs, O-MWGNRs, GMPs, O-GMPs, and O-GNPs,
respectively. The signal amplitudes were normalized to DI water.
Additionally, TA signal amplitude of DSPE-PEG was comparable to
DI water (Fig. 3C), and LDPE vial does not generate any measurable
TA signal . At 3 GHz, the SNR of the nanomaterials was >170,
and the nanomaterials exhibited ?10–28% TA signal enhancement
compared to DI water.
To the best of our knowledge, this is the first study exploring
and comparing efficacy of graphene nanoparticles prepared via
longitudinal ‘‘unzipping’’ method and Hummer’s method as CAs
for multimodal PAT and TAT. These results indicate that O-GNRs
could be used for multimodal PAT and TAT applications, and O-
GNPs are suitable CAs for TAT. Bulk of the work performed towards
developing CAs for PAT has been focused on metallic nanoparticles,
Fig. 3. (A) Schematic depiction of the experimental setup for thermoacoustic signal measurements. (B) Thermoacoustic signal amplitudes of water, single-walled carbon
nanotubes (SWCNTs), multi-walled carbon nanotubes (MWCNTs), oxidized single-walled graphene nanoribbons (O-SWGNRs), oxidized multi-walled graphene nanoribbons
(O-MWGNRs), micro-graphite flakes (GMPs), oxidized graphite microparticles (O-GMP), and exfoliated graphene nanoplatelets (O-GNP) at 3 GHz. TA signals are normalized
to that of water at 3 GHz. (C) TA signal amplitude of DSPE-PEG compared to DI water.
G. Lalwani et al. / Photoacoustics 1 (2013) 62–67
organic dye molecules, and carbon nanotubes. In comparison to
those CAs, graphene possesses several benefits: (1) Compared to
carbon nanotubes, graphene possesses larger surface area, lower
aspect ratio, and better dispersibility in most biological media.
These properties are important, for most in vivo applications.
Furthermore, colloidal dispersions (with high stability and less
aggregation) of graphene sheets can be achieved without
impurities that may be harmful in biological systems [31,32].
(2) The sp2bonded carbon sheets of graphene can be directly
functionalized for targeting and drug delivery . For other PAT/
TAT CAs, such as gold nanoparticles and organic dye molecules, to
disperse and stabilize gold nanoparticles in solution or embed
organic dye molecules, functionalization is performed on the
biocompatible coating/capping agent. (3) O-GNPs and O-GNRs
have been reported as CAs for other whole-body imaging
applications such as magnetic resonance imaging  and nuclear
imaging . Therefore, they can be developed as multimodal CAs
that provide complementary information at micro- to macro-
scopic length scales. (4) Graphene can be developed as ther-
agnostic (simultaneous therapy and diagnostics) agent combining
PAT/TAT molecular imaging and NIR-induced hyperthermia .
Due to these unique features, graphene may serve as a platform for
approaches. Indeed, several in vitro and in vivo safety and efficacy
studies on these graphene nanoparticles have been reported for
various biomedical applications [23,35].
3. Materials and methods
3.1. Synthesis and characterization of nanomaterials
SWCNTs (Cheap Tubes Inc., VT, USA) and MWCNTs (Sigma
Aldrich, NY, USA) were used as received. O-SWGNRs, O-MWGNRs,
O-GMPs, and O-GNPs were synthesized and characterized as
reported previously [22–24]. All nanomaterials were dispersed at
5 mg/ml in DSPE-PEG for PA and TA measurements.
3.2. Photoacoustic (PA) imaging
A deep reflection-mode PA imaging system was used (Scheme 1
in Ref. ) for PA tests of graphene samples. A tunable Ti:sapphire
laser (LT-2211A; Lotis TII, Minsk, Belarus) pumped by a Q-switched
Nd:YAG (LS-2137; Lotis TII) laser was used for PA excitation (pulse
width: 5 ns, pulse repetition rate: 10 Hz). A 5-MHz central
frequency, spherically focused ultrasonic transducer (V308;
Panametrics-NDT, Waltham, MA, USA), low-noise amplifier
(5072PR; Panametrics-NDT), a digital oscilloscope (TDS 5054;
Tektronix, Beaverton, OR, USA) were used to acquire, amplify, and
record signals. The reported PA signal amplitudes have been
normalized for laser fluence at their corresponding wavelengths.
3.3. Thermoacoustic (TA) imaging
Fig. 3A is a schematic depiction of the experimental setup for TA
measurements. TA results were obtained from a TAT system with a
3.0-GHz microwave generator (pulse width = 0.6 ms, repetition
rate = 10 Hz) and a 20 dB amplifier. The pulses (average power
density = 4.5 mW/cm2, within safety standard) were guided
toward the target through a horn antenna (11 cm ? 7 cm) .
A 1-MHz spherically focused transducer with a bandwidth of 70%
(V314, Panametrics, Olympus) was used to receive TA signals from
samples placed in a plastic tank filled with mineral oil for
ultrasound coupling. The received TA signals were amplified and
stored by a data-acquisition (DAQ) card (CS 14200; Gage Applied,
IL) . The microwave generator simultaneously triggered data
Conflict of interest statement
The authors declare no conflict of interest.
We are grateful to Sandra Matteucci for proof reading of the
manuscript. Our work was sponsored by NIH Director’s New
Innovator Award 1DP2OD007394-01 (to S.B.), Wallace H. Coulter
Foundation (S.B.), and NIH grants R01 EB008085, R01 CA140220,
R01 CA157277, R01 CA159959, U54 CA136398, and DP1 EB016986
– NIH Director’s Pioneer Award (to L.V.W.). L.V.W. has a financial
interest in Microphotoacoustics, Inc. and Endra, Inc., which,
however, did not support this work.
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Gaurav Lalwani received his B.Tech. in Biotechnology
from SRM University, Chennai, India, in 2010, and M.S.
in Biomedical Engineering from Stony Brook University,
New York, in 2012. He is currently working towards a
Ph.D. in Biomedical Engineering at Stony Brook University
under the guidance of Dr. Balaji Sitharaman. His research
areas include biomaterials and regenerative medicine.
He is working on the design of nanoparticle-reinforced
biodegradable polymeric nanocomposites and multi-
functional three-dimensional macroscopic all-carbon
graphene-based nanostructures as multimodal contrast
agents for medical diagnostics.
Xin Cai earned his M.S. degree at Huazhong University of
Science and Technology, Wuhan, China, in 2008. He is
currently a research associate in the Optical Imaging
Laboratory, Department of Biomedical Engineering,
Washington University in St. Louis. His research inter-
ests are the developments of non-ionizing and non-
invasive novel biomedical imaging techniques, includ-
ing photoacoustic imaging, fluorescence imaging, and
ultrasonic imaging. He has published 22 papers in peer-
Dr. Liming Nie earned his B.S. in 2005 and Ph.D. in 2010,
both in Optics, from South China Normal University. His
Ph.D project was focused on microwave-induced ther-
moacoustic tomography and its biomedical application.
In August 2010, he joined Optical Imaging Lab at
Washington University in St. Louis under the mentor-
ship of Dr. Lihong V. Wang. His project involved nonin-
vasive photoacoustic imaging of the primate brain and
reconstruction correction for imaging distortion. In Oc-
tober 2012, he joined Dr. Shawn Chen’s Laboratory of
Molecular and Nanomedicine (LOMIN), NIBIB, NIH. His
current research is focused on developing photoacous-
tic/ultrasound imaging system, image processing, and
Lihong V. Wang earned his Ph.D. degree at Rice University,
Houston, Texas under the tutelage of Robert Curl, Richard
Smalley, and Frank Tittel. He is Gene Beare Distinguished
Professor at Washington Univ. His laboratory invented
functional photoacoustic tomography, 3D photoacoustic
microscopy, and time-reversed ultrasonically encoded
(TRUE) optical focusing. He has published 342 journal
articles and delivered 357 invited talks. His Google Schol-
ar h-index and citations have reached 80 and 25,500,
respectively. He has received 34 grants as PI with a budget
of $41M. He is the Editor-in-Chief of the Journal of Bio-
medical Optics. He co-founded two companies to com-
mercialize photoacoustic tomography. He is a Fellow of
the AIMBE, OSA, IEEE, and SPIE. His book entitled ‘‘Biomedical Optics: Principles and
Imaging’’ won the Goodman Award. He was awarded OSA’s C.E.K. Mees Medal and
IEEE’s Technical Achievement Award for ‘‘seminal contributions to photoacoustic
tomography and Monte Carlo modeling of photon transport in biological tissues and
for leadership in the international biophotonics community’’.
Balaji Sitharaman is an Assistant Professor of Biomedical
Engineering at Stony Brook University. He received his
B.S. (2000) from the Indian Institute of Technology at
Kharagpur. He received his M.A and Ph.D. (2005) from
Rice University, where he also completed his postdoc-
toral research (2005–2007) as the J. Evan Attwell-Welch
Postdoctoral Fellow at the Richard E. Smalley Institute
for Nanoscale Science and Technology. Sitharaman’s
research program is at the interface of nanotechnology,
regenerative and molecular medicine and synergizes
the advancements in each of these fields to tackle
problems related to diagnosis/treatment of disease
and tissue regeneration. He is the author of over 40
peer-reviewed publications. He has received several
awards for his research including NIH Director’s New Innovator Award from the
National Institute of Health, the Idea Award from the Department of Defense, the
Carol M. Baldwin Breast Cancer Research Award from the Carol Baldwin Foundation
and the George Kozmetsky Award from the Nanotechnology Foundation of Texas.
G. Lalwani et al. / Photoacoustics 1 (2013) 62–67