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 Imaging in
Photodynamic Therapy
Series in Cellular and Clinical Imaging
Series Editor
Ammasi Periasamy

PUBLISHED
Coherent Raman Scattering Microscopy
edited by Ji-Xin Cheng and Xiaoliang Sunney Xie

Imaging in Cellular and Tissue Engineering

edited by Hanry Yu and Nur Aida Abdul Rahim

Second Harmonic Generation Imaging

edited by Francesco S. Pavone and Paul J. Campagnola

The Fluorescent Protein Revolution

edited by Richard N. Day and Michael W. Davidson

Natural Biomarkers for Cellular Metabolism:

Biology, Techniques, and Applications
edited by Vladimir V. Gukasyan and Ahmed A. Heikal

Optical Probes in Biology

edited by Jin Zhang, Sohum Mehta, and Carsten Schultz

Super-Resolution Imaging in Biomedicine

edited by Alberto Diaspro and Marc A. M. J. van Zandvoort

Imaging in Photodynamic Therapy

edited by Michael R. Hamblin and Yingying Huang
SERIES IN CELLULAR AND CLINICAL IMAGING
Ammasi Periasamy, series editor

Imaging in
Photodynamic Therapy

Edited by
Michael R. Hamblin, PhD
Yingying Huang, MD
CRC Press
Taylor & Francis Group
6000 Broken Sound Parkway NW, Suite 300
Boca Raton, FL 33487-2742

© 2017 by Taylor & Francis Group, LLC

CRC Press is an imprint of Taylor & Francis Group, an Informa business

No claim to original U.S. Government works

Printed on acid-free paper

Version Date: 20160830

International Standard Book Number-13: 978-1-4987-4145-3 (Hardback)

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Library of Congress Cataloging-in-Publication Data

Names: Hamblin, Michael R., editor. | Huang, Ying-Ying, editor.

Title: Imaging in photodynamic therapy / [edited by] Michael R. Hamblin,
Ying-Ying Huang.
Description: Boca Raton: Taylor & Francis, 2017. | Includes bibliographical
references and index.
Identifiers: LCCN 2016032241 | ISBN 9781498741453 (hardback: alk. paper)
Subjects: | MESH: Photochemotherapy--methods | Photosensitizing
Agents--therapeutic use
Classification: LCC RC271.P43 | NLM WB 480 | DDC 615.8/31--dc23
LC record available at https://lccn.loc.gov/2016032241

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“To the love of my life, my beautiful wife Angela, to whom I have been devoted for thirty-four years”.
Michael R Hamblin
Contents

Series preface ix
Preface xi
Acknowledgment xiii
Editors xv
Contributors xvii

Part 1 INTRODUCTION 1

1 Looking out the optical window: Physical principles and instrumentation of imaging
in photodynamic therapy 3
Hui Liu and Jonathan P. Celli
2 Photochemistry and photophysics of PDT and photosensitizers 29
Marcin Ptaszek

Part 2 IN VITRO MICROSCOPY FOR PHOTOSENSITIZER LOCALIZATION IN CELLS 49

3 Phthalocyanines in photodynamic therapy 51

Heidi Abrahamse
4 Singlet oxygen luminescence imaging: A prospective tool in bioscience? 67
Michael Pfitzner, Jan C. Schlothauer, Lisheng Lin, Buhong Li, and Beate Röder
5 Microbial biofilms and antimicrobial photodynamic therapy 89
Anil Kishen
6 High-content imaging for photosensitizer screening 103
Gisela M.F. Vaz, Mathias O. Senge, Sarah-Louise Ryan, and Anthony Davies

Part 3 IN VITRO MICROSCOPY OF CELL DAMAGE AND DEATH PROCESSES

AFTER PDT 117
7 Enhanced efficacy of photodynamic therapy via an iron–lysosome–mitochondria
connection: Studies with phthalocyanine 4 119
Anna-Liisa Nieminen, Hsin-I Hung, and John J. Lemasters
8 Role of cell death pathways in response to photodynamic therapy in gliomas 131
Leonardo Barcelos de Paula, Fernando Lucas Primo, and Antonio Claudio Tedesco
9 In search of specific PDT photosensitizers: Subcellular localization and cell death
pathways 149
Tayana M. Tsubone, Christiane Pavani, Isabel O.L. Bacellar, and Maurício S. Baptista

vii
viii Contents

Part 4 THERANOSTIC AGENTS AND NANOTECHNOLOGY 183

10 Quantum dots in PDT 185

Ričardas Rotomskis and Giedre Streckyte
11 Tetrapyrrole-based theranostic combinations of photodynamic action and magnetic
resonance imaging 211
Duygu Aydın Tekdaş, Devrim Atilla, Vefa Ahsen, and Ayşe Gül Gürek
12 Theranostic applications of photodynamic molecular beacons 249
Wentao Song, Yang Zhou, and Jonathan F. Lovell
13 Tumor-specific imaging and photodynamic therapy targeting the urokinase receptor 259
Zafar Iqbal, Longguang Jiang, Zhuo Chen, Cai Yuan, Rui Li, Ke Zheng, Xiaolei Zhou,
Jincan Chen, Ping Hu, and Mingdong Huang

Part 5 SMALL ANIMAL IMAGING 275

14 Vascular imaging in photodynamic therapy 277

Bin Chen
15 Photosensitizer activity imaging on the microscopic scale 293
Steffen Hackbarth
16 Bioluminescence imaging for monitoring the effectiveness of photodynamic therapy
for infections in animal models 313
Pawel Mroz and Michael R. Hamblin

Part 6 CLINICAL IMAGING 323

17 Imaging of photosensitizers in skin 325

Marica B. Ericson, Danni Wang, Despoina Kantere, John Paoli, and Ann-Marie Wennberg
18 Brain tumor imaging with ALA 347
Herbert Stepp and Oliver Schnell
19 PDT of non-muscle-invasive bladder cancer with Hexylester Aminolevulinate:
Optimization of the illumination wavelengths by fluorescence spectroscopy and imaging 385
Matthieu Zellweger, Claude-André Porret, Norbert Lange, Patrice Jichlinski,
Hubert van den Bergh, and Georges Wagnières
20 Endoscopic imaging and photodynamic therapy 395
Harubumi Kato, Kinya Furukawa, Yasufumi Kato, Jitsuo Usuda, Kuniharu Miyajima,
and Keishi Ohtani
21 Spectroscopic imaging in prostate PDT 419
Rozhin Penjweini, Brian C. Wilson, and Timothy C. Zhu
22 Fluorescent-guided resection in clinical oncology 455
Ron R. Allison

Index 469
Series preface

A picture is worth a thousand words.

This proverb says everything. Imaging began in 1021 with use of a pinhole lens in a camera in Iraq; later in
1550, the pinhole was replaced by a biconvex lens developed in Italy. This mechanical imaging technology
migrated to chemical-based photography in 1826 with the first successful sunlight picture made in France.
Today, digital technology counts the number of light photons falling directly on a chip to produce an image
at the focal plane; this image may then be manipulated in countless ways using additional algorithms and
software. The process of taking pictures (“imaging”) now includes a multitude of options—it may be either
invasive or noninvasive, and the target and details may include monitoring signals in two, three, or four
dimensions.
Microscopes are an essential tool in imaging used to observe and describe protozoa, bacteria, spermato-
zoa, and any kind of cell, tissue, or whole organism. Pioneered by Antonie van Leeuwenhoek in the 1670s and
later commercialized by Carl Zeiss in 1846 in Jena, Germany, microscopes have enabled scientists to better
grasp the often misunderstood relationship between microscopic and macroscopic behavior, by allowing for
the study of the development, organization, and function of unicellular and higher organisms, as well as
structures and mechanisms at the microscopic level. Further more, the imaging function preserves tempo-
ral and spatial relationships that are frequently lost in traditional biochemical techniques and gives two- or
three-dimensional resolution that other laboratory methods cannot. For example, the inherent specificity
and sensitivity of fluorescence and the high-temporal, spatial, and three-dimensional resolution that is pos-
sible and the enhancement of contrast resulting from detection of an absolute rather than relative signal (i.e.,
unlabeled features do not emit) are the advantages of fluorescence techniques. Additionally, the plethora of
well-described spectroscopic techniques providing different types of information and the commercial avail-
ability of fluorescent probes such as visible fluorescent proteins (many of which exhibit an environment- or
analytic-sensitive response) increase the range of possible applications, such as the development of biosensors
for basic and clinical research. Recent advancements in optics, light sources, digital imaging systems, data
acquisition methods, and image enhancement, analysis, and display methods have further broadened the
applications in which fluorescence microscopy can be applied successfully.
Another development has been the establishment of multiphoton microscopy as a three-dimensional imag-
ing method of choice for studying biomedical specimens from single cells to whole animals with submicron
resolution. Multiphoton microscopy methods utilize naturally available endogenous fluorophores—including
NADH, TRP, and FAD—whose autofluorescent properties provide a label-free approach. Researchers may
then image various functions and organelles at molecular levels using two-photon and fluorescence life-
time imaging microscopy to distinguish normal from cancerous conditions. Other widely used nonlabeled
imaging methods are coherent anti-Stokes Raman scattering spectroscopy and stimulated Raman scattering
microscopy, which allow imaging of molecular function using the molecular vibrations in cells, tissues, and
whole organisms. These techniques have been widely used in gene therapy, single-molecule imaging, tissue
engineering, and stem cell research. Another nonlabeled method is harmonic generation (SHG and THG),
which is also widely used in clinical imaging, tissue engineering, and stem cell research. There are many
more advanced technologies developed for cellular and clinical imaging including multiphoton tomography,
thermal imaging in animals, and ion imaging (calcium, pH) in cells.
The goal of this series is to highlight these seminal advances and the wide range of approaches currently
used in cellular and clinical imaging. Its purpose is to promote education and new research across a broad
spectrum of disciplines. The series emphasizes practical aspects, with each volume focusing on a particular

ix
x Series preface

theme that may cross various imaging modalities. Each title covers basic to advanced imaging methods, as
well as detailed discussions dealing with interpretations of these studies. The series also provides cohesive,
complete state-of-the-art, cross-modality overviews of the most important and timely areas within cellular
and clinical imaging.
Since my graduate student days, I have been involved and interested in multimodal imaging techniques
applied to cellular and clinical imaging. I have pioneered and developed many imaging modalities through-
out my research career. The series manager, Luna Han, recognized my genuine enthusiasm and interest to
develop a new book series on cellular and clinical imaging. This project would not have been possible without
the support of Luna. I am sure that all the volume editors, chapter authors, and myself have benefited greatly
from her continuous input and guidance to make this series a success.
Equally important, I personally thank the volume editors and the chapter authors. It has been an incred-
ible experience working with colleagues who demonstrate such a high level of interest in educational proj-
ects, even though they are all fully occupied with their own academic activities. Their work and intellectual
contributions based on their deep knowledge of the subject matter will be appreciated by everyone who reads
this book series.

Ammasi Periasamy, PhD

Series Editor
Professor and Center Director
W.M. Keck Center for Cellular Imaging
University of Virginia
Charlottesville, Virginia
Preface

In this book, we have aimed to cover the broad field of cellular, molecular, preclinical, and clinical imaging
associated or combined with photodynamic therapy (PDT). PDT uses a nontoxic photosensitizer, which is
a colored dye, together with harmless visible light of the correct wavelength to be absorbed by the dye. The
excited state dye can then undergo different chemical reactions with ambient oxygen-producing reactive
oxygen species that damage biomolecules, kill targeted cells, and destroy unwanted tissues. Clinically, PDT
is used for cancer, infections, and diseases such as atherosclerosis or blindness characterized by unwanted
tissues. Because photosensitizers are also fluorescent, various imaging systems such as confocal microscopy
and small animal imaging systems have been widely used to follow and optimize treatment and to answer
important mechanistic questions. In several cases (skin, bladder, and brain) imaging has made an important
contribution to clinical outcomes. PDT has made an important contribution to the development of theranos-
tics (agents that can both detect and treat diseases).
Many of the advances in imaging and PDT have been technology driven. Highly sophisticated confocal
microscopes have become readily available in most departments. In vivo small animal imaging systems again
have made large strides and now will often cover several modalities that can be chosen from fluorescence, bio-
luminescence, and photoacoustic imaging, CT, PET, high-resolution ultrasound, etc. Because of the expan-
sion in available technologies, many investigators have been able to take advantage of the new capabilities to
answer questions that have until now remained elusive. Moreover, the advent of the field of “seek and destroy”
theranostics has also increased the demand for research studies that are combinations of imaging and ther-
apeutics. Photosensitizers can act as fluorescent reporters for imaging of tissue localization, can mediate
photogeneration of reactive oxygen species, and can even monitor effectiveness of treatment due to photo-
bleaching. They can also be incorporated into an array of nanoparticles and nanocarriers to take advantage of
the nanotechnology revolution. As PDT becomes more often used clinically and as the awareness of imaging
grows, more and more clinical studies are including an imaging element to optimize the treatment. This book
is designed to reflect these advances and to provide a resource for physicians and research scientists in the
fields of cell biology, microscopy, PDT, cell signaling, nanotechnology, and drug discovery. It is also aimed at
scientists in optics, molecular imaging, lasers, cancer diagnostics and treatment, and pharmaceuticals.

xi
Acknowledgment

The editors acknowledge the valuable assistance of Xiaoshen Zhang from Tongji University, School of
Medicine, Shanghai, China.

xiii
Editors

Michael R. Hamblin, PhD, is a principal investigator at the Wellman Center for Photomedicine at
Massachusetts General Hospital, an associate professor of dermatology at Harvard Medical School, and a
member of the affiliated faculty of the Harvard-MIT Division of Health Science and Technology. His research
interests lie in the areas of photodynamic therapy (PDT) for infections, cancer, and stimulation of the immune
system and in low-level light therapy or photobiomodulation for wound healing, traumatic brain injuries,
neurodegenerative diseases, and psychiatric disorders. He directs a laboratory of around a dozen postdoctoral
fellows, visiting scientists, and graduate students. His research program is supported by the NIH, CDMRP,
USAFOSR, and CIMIT, among other funding agencies. He has published more than 340 peer-reviewed a­rticles
and more than 150 conference proceedings, book chapters, and international abstracts and holds 8 patents.
He is an associate editor and editorial board member on numerous journals and serves on NIH study s­ections.
For the past several years, Dr. Hamblin has chaired the annual conference at SPIE Photonics West titled
“Mechanisms for low level light therapy” and has edited proceedings, volumes, and major textbooks on PDT
and photomedicine. In 2011 Dr. Hamblin was honored by election as a fellow of SPIE.

Ying-Ying Huang, MD, is a scientist in Dr. Michael Hamblin’s lab at the Wellman Center for Photomedicine
at Massachusetts General Hospital and an instructor of dermatology at Harvard Medical School. She was
trained as a dermatologist in China. Her research interests lie in the areas of photodynamic therapy for
infections and cancer and in the mechanism of low-level light therapy for traumatic brain injuries. She has
published almost 50 peer-reviewed articles and numerous conference proceedings and book chapters. She is
the coeditor of the recent publication Handbook of Photomedicine.

xv
Contributors

Heidi Abrahamse Bin Chen

Faculty of Health Sciences Department of Pharmaceutical Sciences
Laser Research Centre University of the Sciences
Laser Applications in Health Philadelphia, Pennsylvania
University of Johannesburg Jincan Chen
Doornfontein, South Africa State Key Laboratory of Structural Chemistry
Vefa Ahsen and
Department of Chemistry Danish-Chinese Centre for Proteases and
Gebze Technical University Cancer
Gebze-Kocaeli, Turkey Fujian Institute of Research on the Structure
of Matter
Ron R. Allison
Chinese Academy of Sciences
Department of Radiation Oncology
Fuzhou, Fujian, People’s Republic of China
Brody School of Medicine
East Carolina University Zhuo Chen
Greenville, North Carolina State Key Laboratory of Structural Chemistry
and
Devrim Atilla
Danish-Chinese Centre for Proteases and Cancer
Department of Chemistry
Fujian Institute of Research on the Structure
Gebze Technical University
of Matter
Gebze-Kocaeli, Turkey
Chinese Academy of Sciences
Isabel O.L. Bacellar Fuzhou, Fujian, People’s Republic of China
Institute of Chemistry
Anthony Davies
University of São Paulo
Institute of Health and Biomedical Innovation
São Paulo, Brazil
Queensland University of Technology
Maurício S. Baptista Woolloongabba, Brisbane, Australia
Institute of Chemistry Marica B. Ericson
University of São Paulo Department of Chemistry and Molecular
São Paulo, Brazil Biology
Hubert van den Bergh University of Gothenburg
Laboratory of Organometallic and Medicinal Gothenburg, Sweden
Chemistry Kinya Furukawa
Swiss Federal Institute of Technology Department of Thoracic Surgery
in Lausanne Tokyo Medical University Ibaraki Medical Center
Lausanne, Switzerland Ibaraki, Japan
Jonathan P. Celli Ayşe Gül Gürek
Department of Physics Department of Chemistry
University of Massachusetts Gebze Technical University
Boston, Massachusetts Gebze-Kocaeli, Turkey

xvii
xviii Contributors

Steffen Hackbarth Patrice Jichlinski

Department of Physics Department of Urology
Humboldt-Universität zu Berlin CHUV Hospital
Berlin, Germany Lausanne, Switzerland
Despoina Kantere
Michael R. Hamblin
Department of Dermatology and Venereology
Department of Dermatology
University of Gothenburg
Harvard Medical School
Gothenburg, Sweden
and
Wellman Center for Photomedicine Harubumi Kato
Massachusetts General Hospital Department of Thoracic Surgery
Boston, Massachusetts Niizashiki Central General Hospital
Saitama, Japan
Ping Hu
and
State Key Laboratory of Structural Chemistry
and Department of Surgery
Danish-Chinese Centre for Proteases and Cancer Tokyo Medical University
Fujian Institute of Research on the Structure International University of Health and Welfare
of Matter Tokyo, Japan
Chinese Academy of Sciences Yasufumi Kato
Fuzhou, Fujian, People’s Republic of China Department of Thoracic Surgery
Tokyo Medical University Ibaraki Medical Center
Mingdong Huang Ibaraki, Japan
College of Chemistry
Fuzhou University Anil Kishen
Fuzhou, People's Republic of China Faculty of Dentistry
University of Toronto
Hsin-I Hung Toronto, Ontario, Canada
Department of Drug Discovery and
Norbert Lange
Biomedical Sciences
School of Pharmaceutical Sciences
Medical University of South Carolina
University of Geneva
Charleston, South Carolina
University of Lausanne
Geneva, Switzerland
Zafar Iqbal
Department of Chemistry John J. Lemasters
COMSATS Institute of Information Department of Drug Discovery and
Technology Biomedical Sciences
Abbottabad, Khyber Pakhtunkhwa, Pakistan Medical University of South Carolina
Charleston, South Carolina
and
and
State Key Laboratory of Structural Chemistry
Institute of Theoretical and Experimental
and
Biophysics
Danish-Chinese Centre for Proteases and Cancer
Russian Academy of Science
Fujian Institute of Research on the Structure
Pushchino, Russia
of Matter
Chinese Academy of Sciences Buhong Li
Fuzhou, Fujian, People’s Republic of China MOE Key Laboratory of OptoElectronic
Science and Technology for Medicine
Longguang Jiang Fujian Provincial Key Laboratory for Photonics
College of Chemistry Technology
Fuzhou University Fujian Normal University
Fuzhou, People’s Republic of China Fuzhou, People’s Republic of China
 Contributors xix

Rui Li John Paoli

State Key Laboratory of Structural Chemistry Department of Dermatology and Venereology
and University of Gothenburg
Danish-Chinese Centre for Proteases Gothenburg, Sweden
and Cancer Leonardo Barcelos de Paula
Fujian Institute of Research on the Structure Department of Chemistry
of Matter Center of Nanotechnology and Tissue
Chinese Academy of Sciences Engineering
Fuzhou, Fujian, People’s Republic of China Photobiology and Photomedicine Research
Group
Lisheng Lin Faculty of Philosophy, Sciences and Letters of
MOE Key Laboratory of OptoElectronic Ribeirão Preto
Science and Technology for Medicine University of São Paulo
Fujian Provincial Key Laboratory for Photonics São Paulo, Brazil
Technology
Fujian Normal University Christiane Pavani
Fuzhou, Fujian, People's Republic of China Postgraduate Program in Applied Biophotonics
in Science and Health
Hui Liu July Ninth University
Department of Physics São Paulo, Brazil
University of Massachusetts Rozhin Penjweini
Boston, Massachusetts Department of Radiation Oncology
University of Pennsylvania
Jonathan F. Lovell Philadelphia, Pennsylvania
Department of Biomedical Engineering
University at Buffalo Michael Pfitzner
State University of New York Department of Physics
Buffalo, New York Humboldt-Universität zu Berlin
Berlin, Germany
Kuniharu Miyajima
Claude-André Porret
Department of Thoracic Surgery
Laboratory of Organometallic and Medicinal
Niizashiki Central General Hospital
Chemistry
Saitama, Japan
Swiss Federal Institute of Technology
in Lausanne
Pawel Mroz Lausanne, Switzerland
Department of Pathology
University of Michigan Medical School Fernando Lucas Primo
University of Michigan Health System Department of Bioprocess and
Ann Arbor, Michigan Biotechnology
São Paulo State University
Anna-Liisa Nieminen Araraquara, Brazil
Department of Drug Discovery and
Marcin Ptaszek
Biomedical Sciences
Department of Chemistry and Biochemistry
Medical University of South Carolina
University of Maryland
Charleston, South Carolina
Baltimore, Maryland

Keishi Ohtani Beate Röder

Department of Surgery Department of Physics
Tokyo Medical University Humboldt-Universität zu Berlin
Tokyo, Japan Berlin, Germany
xx Contributors

Ričardas Rotomskis Antonio Claudio Tedesco

Biomedical Physics Laboratory Department of Chemistry
National Cancer Institute Center of Nanotechnology and Tissue
and Engineering
Biophotonics Laboratory Photobiology and Photomedicine Research
Vilnius University Group
Vilnius, Lithuania Faculty of Philosophy, Sciences and Letters of
Ribeirão Preto
Sarah-Louise Ryan
University of São Paulo
Institute of Health and Biomedical Innovation
São Paulo, Brazil
Queensland University of Technology
Woolloongabba, Brisbane, Australia Duygu Aydın Tekdaş
Department of Chemistry
Jan C. Schlothauer
Gebze Technical University
Department of Physics
Gebze-Kocaeli, Turkey
Humboldt-Universität zu Berlin
Berlin, Germany Tayana M. Tsubone
Institute of Chemistry
Oliver Schnell
University of São Paulo
Deparment of Neurosurgery
São Paulo, Brazil
Klinikum der Universität München
München, Germany Jitsuo Usuda
and Department of Thoracic Surgery
Nippon Medical School
Medical Center
Tokyo, Japan
University of Freiburg
Freiburg, Germany Gisela M.F. Vaz
Institute of Molecular Medicine
Mathias O. Senge
Trinity College Dublin
School of Chemistry
St. James’s Hospital
Trinity College Dublin
Dublin, Ireland
University of Dublin
Dublin, Ireland Georges Wagnières
Wentao Song Laboratory of Organometallic and Medicinal
Department of Biomedical Engineering Chemistry
University at Buffalo Swiss Federal Institute of Technology
State University of New York in Lausanne
Buffalo, New York Lausanne, Switzerland

Herbert Stepp Danni Wang

LIFE Center Department of Chemistry and Molecular
Laser-Forschungslabor Biology
Klinikum der Universität München University of Gothenburg
München, Germany Gothenburg, Sweden

Giedre Streckyte Ann-Marie Wennberg

Biophotonics Laboratory Department of Dermatology and Venereology
Vilnius University University of Gothenburg
Vilnius, Lithuania Gothenburg, Sweden
 Contributors xxi

Brian C. Wilson Xiaolei Zhou

Department of Medical Biophysics State Key Laboratory of Structural Chemistry
University Health Network and
and Danish-Chinese Centre for Proteases
University of Toronto and Cancer
Toronto, Ontario, Canada Fujian Institute of Research on the Structure
of Matter
Cai Yuan
Chinese Academy of Sciences
College of Bioscience and Biotechnology
Fuzhou, Fujian, People’s Republic of China
Fuzhou University
Fuzhou, People's Republic of China Yang Zhou
Matthieu Zellweger College of Chemistry
Laboratory of Organometallic and Medicinal Shandong Normal University
Chemistry Jinan, Shandong, People’s Republic of China
Swiss Federal Institute of Technology
in Lausanne Timothy C. Zhu
Lausanne, Switzerland Department of Radiation Oncology
University of Pennsylvania
Ke Zheng
Philadelphia, Pennsylvania
State Key Laboratory of Structural Chemistry
and
Danish-Chinese Centre for Proteases
and Cancer
Fujian Institute of Research on the Structure
of Matter
Chinese Academy of Sciences
Fuzhou, Fujian, People’s Republic of China
 PART
1
INTRODUCTION

1 Looking out the optical window: Physical principles and instrumentation of imaging
in photodynamic therapy 3
Hui Liu and Jonathan P. Celli
2 Photochemistry and photophysics of PDT and photosensitizers 29
Marcin Ptaszek
 1
Looking out the optical window
Physical principles and instrumentation
of imaging in photodynamic therapy
HUI LIU AND JONATHAN P. CELLI

1.1 Introduction 4
1.2 Physical principles: Light propagation and interactions with matter 4
1.2.1 Light as wave and particle 4
1.2.2 Phase and coherence 6
1.2.3 Light propagation 6
1.2.3.1 Reflection 7
1.2.3.2 Refraction 8
1.2.3.3 Diffraction 9
1.2.4 Light–matter interactions and the optical window 10
1.2.4.1 Scattering 10
1.2.4.2 Absorption 10
1.2.4.3 Attenuation models and tissue optics 12
1.3 Physical processes following light absorption: Imaging and therapeutic applications 13
1.3.1 Radiationless dissipation ➔ Heat 14
1.3.2 Fluorescence 14
1.3.3 Intersystem crossing ➔ Photodynamic therapy 16
1.3.4 Nonlinear optical processes 16
1.4 Instrumentation and technologies for imaging and PDT 17
1.4.1 Light sources 17
1.4.1.1 Lasers 17
1.4.1.2 Light-emitting diodes 19
1.4.1.3 Lamps 19
1.4.2 Endoscopes 20
1.4.3 Photodetectors and cameras 20
1.4.3.1 Cameras 21
1.4.4 Image processing 21
1.5 Conclusion, perspectives, and emerging directions 22
References 23

3
4 Looking out the optical window

1.1 INTRODUCTION

As a light-based treatment modality, photodynamic therapy (PDT) is inherently conducive to integration

with optical imaging. The central principle of PDT is to leverage photochemistry that occurs following activa-
tion of a photosensitizing chemical [photosensitizer (PS)] using a light source of the appropriate wavelength
and mode of delivery to achieve destruction of target tissues (Dougherty et al. 1998). Importantly, some
degree of specificity is achieved as PSs have been almost universally observed to exhibit quasi-selective accu-
mulation in neoplastic tissues, going back to the early observations of Policard, who studied accumulation of
hematoporphyrin in rat sarcomas (Policard 1924). Since clinical PS should have little or no dark toxicity, an
additional degree of selectivity is afforded by restriction of light to the target tissue. This basic photodynamic
process, the fundamentals of which are discussed more extensively throughout this volume, has been devel-
oped and adapted for treatment of numerous cancer and noncancer pathologies at diverse anatomical sites
using appropriate chemical modifications of the PS and innovative light delivery strategies. Importantly, the
same photosensitizing agents employed in PDT for targeted tissue destruction also have a finite probability
to undergo a radiative transition back to the ground state following light absorption. In other words, PS can
act as both therapeutic agents and diagnostic fluorophores. Therefore, upon illumination, longer wavelength
fluorescence emission is generated from the malignant tissues in which the PS accumulates, thus marking
the tumor location and margins otherwise difficult to visualize. This process has been extensively leveraged
to confirm PS uptake and localization and to guide surgical resection as discussed at length in the literature
and reviewed elsewhere (Celli et al. 2010).
In this chapter, we review the basic physical principles underlying PDT-related optical imaging and
underscore points where these basic principles have particularly important implications for PDT and imag-
ing and/or its key enabling technologies. This discussion will include a brief review of the fundamental nature
of light itself, how it interacts with matter as both a particle and a wave, and how these interactions manifest
in the propagation of light through tissue to allow therapy and imaging. Also of central importance to PDT
and its associated imaging applications is the probabilistic nature of quantum mechanics and the allowability
of transitions between quantum states, which ultimately determine excited state lifetimes. Finally, techno-
logical developments in light sources and light detectors will be briefly discussed in the context of their role
in enabling PDT and associated optical imaging applications.

1.2 PHYSICAL PRINCIPLES: LIGHT PROPAGATION

AND INTERACTIONS WITH MATTER

1.2.1 Light as wave and particle

When we talk about light in this chapter, we are referring to the narrow slice of the spectrum of electro-
magnetic (EM) radiation that is visible to the human eye (Figure 1.1a). EM radiation, which includes radio
waves, microwaves, infrared, visible light, ultraviolet, and x-ray and gamma radiation, is produced when
charged particles accelerate, generating electric (E) and magnetic fields (B) propagating through space in a
manner that satisfies the set of equations set down by James Clerk Maxwell (1865). For this to be true, the
electric and magnetic fields are necessarily sinusoidal in space and time, and mutually perpendicular to
the direction of propagation (Figure 1.1b). The descriptive categories of EM waves stated earlier are defined
purely on the basis of their frequency, ν, or wavelength, λ, where λν = c. The frequency of a wave is its oscil-
lation rate, typically reported in the SI units of Hertz (Hz), oscillations per second. The wavelength of an
EM wave is its propagation distance in a vacuum during a full oscillation cycle (between two adjacent crests
or troughs). In a vacuum, all EM radiation propagates at the speed of light, c, approximately 3.00 × 108 m/s,
though its speed is different in other media (such as biological tissue). However, although the propaga-
tion speed of EM radiation is medium dependent, it maintains the same frequency or wavelength. For the
 1.2 Physical principles 5

Wavelength, 104 103 102 101 100 10–1 10–2 10–3 10–4 10–5 10–6 10–7 10–8 10–9 10–10 10–11 10–12
λ (m)
105 106 107 108 109 1010 1011 1012 1013 1014 1015 1016 1017 1018 1019 1020
Frequency,
ν (Hz) Radio waves Microwaves Infrared Ultraviolet x-rays Gamma rays

Visible
light

Shortest visible blue/violet Longest visible red

10 nge
90 ow
40 en
60 e
nm

nm

nm
nm
~4 Blu
~400 nm ~750 nm

~5 re

~5 Yell

~6 ra
G

O
(a)

x
E field

y
z
B field

(b)

Figure 1.1 Electromagnetic radiation and visible light. (a) The spectrum of electromagnetic (EM) radiation.
(b) The electrical field (red) and magnetic field (blue) are mutually perpendicular to the direction of propagation.

example of an EM wave propagating in the z-direction through a vacuum (empty space), this description
can be written more succinctly as

æ 2p ö
E ( z ,t ) = E 0 cos ç ( z - ct ) ÷ xˆ
è l ø

E0 æ 2p ö
B ( z ,t ) = cos ç ( z - ct ) ÷ yˆ
c è l ø

where x̂ and ŷ are the unit vectors in the x- and y-directions, respectively. The energy carried by EM radia-
tion is reported by the Poynting vector, the vector cross-product of its electric and magnetic fields, with
SI units of Watts per meter squared (W/m 2). Notwithstanding this universality, however, the physical pro-
cesses that are relevant to the interaction of EM radiation with matter are indeed highly dependent on
wavelength. Hence, our review of the light–matter interaction in the following section will be limited to
the discussion of processes that are energetically allowed and relevant for light of visible and near-infrared
wavelengths used in PDT and optical imaging, approximately 400–750 nm (Figure 1.1a). For example, this
chapter does not deal with effects such as Compton scattering or other important processes more relevant to
the interaction of ionizing EM radiation with matter. For a more complete discussion of the basic principles
of electrodynamics, the curious reader is referred to any number of texts on this subject, such as the classic
by J.D. Jackson (1999).
Yet simultaneously, light can be described as photons, particles that carry discrete packets of energy,
E = hν, where h = 6.626 × 10−34 J ⋅ s, is Planck’s constant (Einstein 1905). Photons are massless particles and
have no electronic charge, but do carry momentum, p = h /l, such that interactions with other particles are
governed by the conservation of momentum. This well-known duality, in which light can be described as
6 Looking out the optical window

both a particle and as a wave, is left over from historic debates on the quantum nature of light and matter in
the early twentieth century. Although the wave description is used to describe certain phenomena (coher-
ence, interference, diffraction, etc.) and the particle description is needed for other processes (quantized
transitions, photoelectric effect, etc.), both descriptions must always coexist. Indeed, even a single photon can
be modeled by wave propagation and, conversely, massive particles such as electrons can also be described as
waves, having a de Broglie wavelength, λ = h/p. Here too, in this chapter, we will go back and forth between
both descriptions as we discuss the physics of PDT and optical imaging.

1.2.2 Phase and coherence

Phase, φ, is a parameter in any periodical sinusoidal function that specifies where in its oscillation cycle it
is at t = 0:

y (t ) = sin ( wt + j )

In general, EM waves are out of phase, with a difference in φ from 0 to 2p radians (0°–360°). Only
when Δφ = 0 or 2p are the waves in phase. This becomes important when calculating the power ( P ) or
­intensity ( I ) , which are proportional to the square of the amplitude of electric field: P µ E 2 and I µ E 2 .
Since EM waves are typically not in phase, the resultant amplitude is typically not just the direct addition
of each amplitude. Hence, the power at a given point in space where two sources of EM radiation combine
cannot in general be thought of as a direct addition. A mathematical illustration of this important point is
provided next and also illustrates the phenomenon of interference:

E1 (t ) = E 0 sin ( wt ) , E 2 (t ) = E 0 sin ( wt + 2p ) , E 3 (t ) = E 0 sin ( wt + p ) ,

E12 (t ) = E1 + E 2 = 2E 0 sin ( wt ) , I 12 µ 4E 02

E13 (t ) = E1 + E 3 = 0, I 13 = 0

Interference is critical for all aspects of image formation in optical systems and can also be exploited in
various innovative ways. For example, the interference patterns formed from rays of a monochromatic and
coherent (Figure 1.2) light source that are back reflected from different depths in tissue can be used to obtain
depth-resolved specimen structure. This principle is at the heart of optical coherence tomography, a powerful
3D imaging approach that may be implemented in conjunction with PDT (Korde et al. 2007, Jung et al. 2012,
Themstrup et al. 2014).
When two EM waves have a constant phase difference and have the same frequency, they are called per-
fectly coherent. Common light sources, such as sunlight and lamps, do not produce coherent waves. In fact,
there is no truly perfectly coherent source since there is no absolute single-frequency source that is infinitely
small. That being said, lasers are very nearly perfectly coherent light sources, a powerful property that has
enabled myriad different technologies and even new industries, since the invention of lasers. The different
light sources, along with their properties, are discussed in Section 1.3. The characteristics of different light
sources with relevance to their applications in PDT and optical imaging are further developed later in this
chapter.

1.2.3 Light propagation
When light traveling through any given medium encounters a change in medium, the direction and speed of
propagation will generally change. Depending on the details of the media involved, this interaction may give
rise to reflection, refraction, scattering, and absorption processes (Figure 1.3; Jackson 1999).
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