394
ISSN 1990-7931, Russian Journal of Physical Chemistry B, 2019, Vol. 13, No. 3, pp. 394–400. © Pleiades Publishing, Ltd., 2019.
Russian Text © The Author(s), 2019, published in Khimicheskaya Fizika, 2019, Vol. 38, No. 6, pp. 8–14.
Morphological Changes in Malignant Tumor Cells at Photodynamic
Treatment Assessed by Digital Holographic Microscopy
A. A. Zhikhoreva
a
, A. V. Belashov
a,
*, D. A. Gorbenko
a
, N. A. Avdonkina
b
, I. A. Baldueva
b
,
A. B. Danilova
b
, M. L. Gelfond
b
, T. L. Nekhaeva
b
, I. V. Semenova
a
, and O. S. Vasyutinskii
a
a
Ioffe Institute, Russian Academy of Sciences, St. Petersburg, Russia
b
N.N. Petrov National Medical Research Center, Ministry of Health of Russia, St. Petersburg, Russia
*e-mail: belashov.andrey.93@gmail.com
Received November 19, 2018; revised December 6, 2018; accepted January 21, 2019
Abstract—The paper presents an investigation of cell death dynamics and changes of cellular morphology
induced by the intracellular generation of singlet oxygen as a result of photodynamic treatment. The response
of kidney carcinoma, osteosarcoma, and skin melanoma cells to photodynamic treatment was analyzed
through the changes in their thickness, average phase shift, and refractive index distribution. It was demon-
strated that an irradiation dose of 42 J results in the necrosis of sarcoma and kidney carcinoma cells, although
melanoma cells show no statistically significant changes in optical or morphological parameters.
Keywords: digital holographic microscopy, singlet oxygen, morphology of living cells, necrosis, photody-
namic treatment
DOI: 10.1134/S1990793119030242
INTRODUCTION
The increasing incidence rate of malignant diseases
and the high frequency of recurrencies are the most
important problems in modern oncology, requiring
improvements of methods aimed at treatment of
patients with this pathology. Photodynamic therapy
(PDT) is one of the promising tools being used world-
wide for treatment of various cancers. It uses the phys-
icochemical properties of photosensitizers (PSs),
which selectively accumulate in pathological tissues
with increased metabolism [1] and can be activated by
local irradiation with light of a wavelength corre-
sponding to the absorption band of PS molecules.
This activation causes generation of singlet oxygen
(the first excited state a
1
Δ
g
of the O
2
molecule) and
other reactive oxygen species that are detrimental to
the tumor cells and cause tumor resorption and ablas-
tics in the tumor bed [2, 3]. At present, PDT is being
actively implemented in clinical practice, both as a
main method and in combination with other methods
for treatment of malignant neoplasms of various local-
izations. In particular, it has been shown in a number
of works [4–6] that this approach provides efficient
treatment of cervical, esophageal, tracheal, and other
cancers.
A large number of photosensitizers have been
developed by now [7–10], and detailed studies of their
physical and chemical properties have been carried
out, the most important of which are the quantum
yield of reactive oxygen species, absorption spectrum,
stability under irradiation, dark phototoxicity, rate of
elimination from the body, and intracellular localiza-
tion [11–13]. An analysis of the PS efficiency for PDT
usually includes four stages: (1) investigation of photo-
physical properties of the PS in solutions; (2) study of
the response of malignant cells to photodynamic treat-
ment with this PS in vitro and (3) in vivo; and (4) clinical
study of its effectiveness in PDT.
The modern approach to studies of cellular
response to photodynamic treatment suggests that it is
important not only to determine treatment doses and
irradiation modes at which cell death occurs but also
to reliably identify cell death mechanisms. Necrosis is
characterized by the destruction of organelles and
plasma membrane, which leads to the release of intra-
cellular contents into the extracellular space and the
development of inflammatory processes. Apoptosis is
characterized by cell rounding, tighter packaging of
the cytoplasm and organelles, followed by the intense
formation of small bubbles on the plasma membrane
(blebbing) and creation of individual apoptotic bodies,
which are phagocytosed in vivo by macrophages or
neighboring normal cells [14, 15].
The distinguishing between cell apoptosis and
necrosis is usually conducted by evaluating the integ-
rity of the cell membrane using standard fluorescent
dyes and by analysis in a confocal fluorescent micro-
scope. Other approaches have been developed, based