Collagen can be visualized using a number of meth
ods. Routine techniques such as histology (hematoxylin
eosin staining), histochemistry (van Gieson staining,
picrosirius red, etc.), immunohistochemistry, and elec
tron microscopy are the most accessible and can be per
formed in virtually any biological laboratory. On the other
hand, they require multistep treatment of tissue samples
and can cause undesirable morphological changes in the
extracellular matrix, of which collagen is a predominant
component. However, the most essential limitation of
these techniques is that they are performed ex vivo. Some
techniques, e.g., smallangle Xray scattering [1, 2] and
magnetic resonance imaging (MRI) [3, 4], allow collagen
visualization in real time without tissue pretreatment and
can be potentially used for in vivo monitoring, although
they require expensive and technically sophisticated
equipment. Another method that has recently attracted a
considerable interest of researchers is nonlinear
microscopy based on the second harmonic generation
(SHG) phenomenon. SHG microscopy is a highly specif
ic optical method of direct visualization of extracellular
fibrillar collagen that can be carried out using most two
photon fluorescence microscopes [5, 6]. SHG
microscopy is a noninvasive technique (i.e., does not
involve phototoxicity and photobleaching); it does not
require additional contrasting agents for collagen moni
toring, and, hence, can be readily used as an auxiliary
technique in in vivo studies or as an alternative to the tra
ditional methods mentioned above. Despite the fact that
most SHG microscopy studies of collagen have been con
ducted ex vivo so far, this method offers tremendous
potential for in vivo examination, including in clinical
practice [79].
Examination of connective tissue based on the SHG
images requires quantitative processing in order to mini
mize interpretation errors and ensure unbiased compari
ISSN 00062979, Biochemistry (Moscow), 2019, Vol. 84, Suppl. 1, pp. S89S107. © Pleiades Publishing, Ltd., 2019.
Russian Text © V. V. Dudenkova, M. V. Shirmanova, M. M. Lukina, F. I. Feldshtein, A. Virkin, E. V. Zagainova, 2019, published in Uspekhi Biologicheskoi Khimii, 2019,
Vol. 59, pp. 181218.
REVIEW
S89
Abbreviations: FFT, fast Fourier transform; FOS, firstorder
statistics; GLCM, gray level cooccurrence matrix; ROI, region
of interest; SHG, second harmonic generation; SOS, second
order statistics.
* To whom correspondence should be addressed.
Examination of Collagen Structure and State
by the Second Harmonic Generation Microscopy
V. V. Dudenkova
1
, M. V. Shirmanova
1
, M. M. Lukina
1
,
F. I. Feldshtein
1
, A. Virkin
2
, and E. V. Zagainova
1,a
*
1
Scientific Research Institute of Biomedical Technologies, Privolzhsky Research Medical University,
603104 Nizhny Novgorod, Russia
2
Ontario Cancer Institute, University Health Network, Toronto, Canada
a
email: orannge@mail.ru
Received August 8, 2018
Revised September 13, 2018
Accepted September 13, 2018
Abstract—Collagen is the major component of the extracellular matrix in mammals and its characteristics provide impor
tant information about the state of connective tissue. There are only few methods of labelfree visualization of collagen
fibers; the most frequently used is the second harmonic generation (SHG) microscopy. SHG microscopy is a noninvasive
technique for the assessment of the abundance and structure of fibrillar collagen with a high resolution and specificity. At
constant measurement parameters (magnification, excitation power, resolution, digital gain of registration matrix), quanti
tative analysis of SHG images provides a reliable characterization of collagen state. Current approaches to the SHG signal
quantification are numerous and typically should be adapted to a specific task. In this review, we systematize the variety of
these approaches and present the examples of biomedical application of the SHG signal quantitative analysis, as well of
combined application of SHG and autofluorescence imaging.
DOI: 10.1134/S0006297919140062
Keywords: second harmonic generation, collagen, quantitative analysis, first order statistics, gray level cooccurrence
matrix, fast Fourier transform