This study analyzed histopathological features of 94 early lung adenocarcinoma samples using image analysis. Samples were classified as adenocarcinoma in situ, microinvasive adenocarcinoma, or lepidic predominant adenocarcinoma. Several parameters were measured from images of gland structures and nuclei, including generalized line reference number density of cancer cells, adhesion rate of nuclei, nucleolus occurrence rate, maximum distance between glands, and nuclear morphology parameters. Statistical analysis found several parameters had significant differences among the three pathological types, while others did not. These parameters may help with quantitative analysis and differential diagnosis of early lung adenocarcinoma types.

1. 112
Analytical and Quantitative Cytopathology and Histopathology®
0884-6812/20/4204-0112/$18.00/0 © Science Printers and Publishers, Inc.
Analytical and Quantitative Cytopathology and Histopathology®
OBJECTIVE: To quantitatively analyze the histopatho­
logical features and explore the application value of im­
age analysis parameters in different pathological types
of early lung adenocarcinoma.
STUDY DESIGN: A total of 94 surgical specimens of
early lung adenocarcinoma were collected and classified
into adenocarcinoma in situ (AIS), microinvasive ade­
nocarcinoma (MIA), and lepidic predominant adenocar­
cinoma (LPA). In each case, 10 relatively intact glands
were photographed under 20-fold objective lens, and
100–150 cells in the corresponding gland cavity were
photographed under 40-fold objective lens. The relation­
ship between AIS, MIA, LPA, and related parameters
were statistically analyzed.
RESULTS: There were significant differences in gener­
alized line reference number density of cancer cells in
glands, the adhesion rate of nucleus in glands and the
nucleolus occurrence rate in glands, the maximum dis­
tance between glands, nuclear area, long axis, short
axis, and nuclear perimeter in the AIS, MIA, and LPA
(p<0.05). However, nuclear roundness, nuclear regu­
latory shape factor, and the minimum distance between
glands were not significantly different among AIS, MIA,
and LPA (p>0.05).
CONCLUSION: The generalized line reference num­
ber density of cancer cells in glands, the adhesion rate of
nucleus in glands, the nucleolus occurrence rate in
glands, the maximum distance between glands, and nu­
cleus morphometric parameters have important appli-
cation value in the quantitative analysis of early lung
adenocarcinoma and can be used as quantitative param­
eters for the differential diagnosis of AIS, MIA, and LPA.
(Anal Quant Cytopathol Histpathol 2020;42:112–
118)
Keywords: early lung adenocarcinoma; image
analysis; image processing, computer-assisted; lung
cancer quantitative study; pathological typing.
In the quantitative study of lung cancer, scholars
have explored the significance of many parameters
in normal lung tissue and lung cancer tissue. For
example, nucleus morphological parameters (area,
long axis, short axis, perimeter, roundness, and
Image Analysis of Early Lung Adenocarcinoma
and Its Significance in Pathological Typing
Jiao Luo, M.D., Rong Duan, M.D., Hui Li, M.D., and Hong Shen, Ph.D.
From the Department of Pathology, Nanfang Hospital, Southern Medical University, Guangzhou, and the Department of Pathology,
School of Basic Medical Sciences, Southern Medical University, Guangzhou, People’s Republic of China.
Jiao Luo is Resident Physician, Department of Pathology, Nanfang Hospital, Southern Medical University.
Rong Duan is Resident Physician, Department of Pathology, Nanfang Hospital, Southern Medical University.
Hui Li is Resident Physician, Department of Pathology, Nanfang Hospital, Southern Medical University.
Hong Shen is Professor, Department of Pathology, Nanfang Hospital, Southern Medical University, and Department of Pathology,
School of Basic Medical Sciences, Southern Medical University.
Jiao Luo and Rong Duan contributed equally.
Address correspondence to: Hong Shen, Ph.D., Department of Pathology, Nanfang Hospital, Southern Medical University, Guangzhou
510515, People’s Republic of China, or Department of Pathology, School of Basic Medical Sciences, Southern Medical University 1023,
Sha-Tai South Road, Baiyun District, Guangzhou 510515, People’s Republic of China (shenhong2010168@163.com).
Financial Disclosure: The authors have no connection to any companies or products mentioned in this article.

2. Volume 42, Number 4/August 2020 113
Image Analysis of Early Lung Adenocarcinoma
regulatory shape factor) of lung adenocarcinoma,
squamous cell carcinoma, small cell carcinoma,
and large cell carcinoma have been tested and
applied to establish diagnostic and discrimina-
tive functions,1-3 which have an important role for
quantitative pathological studies of lung cancer.
What are the implications of these parameters
in adenocarcinoma in situ (AIS), microinvasive
adenocarcinoma (MIA), and lepidic predominant
adenocarcinoma (LPA) as defined by the 2015
WHO lung adenocarcinoma classification? In the
image analysis of early lung adenocarcinoma, we
proposed some new research parameters: the gen-
eralized line reference number density of cancer
cells in glands, the adhesion rate of nucleolus in
glands, the nucleolus occurrence rate in glands,
and the maximum and the minimum distance be-
tween glands. Are these new structural parameters
different in these 3 types of early lung adenocar-
cinomas? Is there pathological significance? Are
these nucleus morphological parameters previous-
ly used in lung cancer research differential signif-
icance in the early lung adenocarcinoma defined
by the 2015 WHO lung adenocarcinoma classifica-
tion? The current research is not yet able to an-
swer these questions, for which we had explored
these issues in our study.
Materials and Methods
Case Material
Surgical specimens of 94 early lung adenocarci-
noma patients with a diameter ≤3 cm were di-
agnosed from January 2014 to December 2017 in
Nanfang Hospital of Southern Medical Universi-
ty, including 31 males and 63 females with an age
range of 30–84 years, mean age 58±10.7, and 66
patients with right lung disease and 28 patients
with left lung disease. The inclusion criteria were
as follows: all cases were surgically resected and
histologically diagnosed as early lung adenocarci-
noma with a diameter ≤3 cm, the pulmonary nod-
ules of all patients were solitary, and no history of
systemic radiotherapy and chemotherapy. All pa-
tients had complete pathological diagnosis data,
imaging data, and general data, and the pathologi-
cal diagnosis was interpreted by 2 pathologists.
Main Instruments and Software
The main instruments and software used in this
study were as follows: light microscope column
(Olympus; FRAME_MANUAL; Japan), objective
lens (Olympus; model no. UPlanFLN; 20×, NA:
0.50; 40×, NA: 0.75), microscopic camera (Olym-
pus; model no. DP21; 20×, 219.54 nm/pixel; 40×,
109.33 nm/pixel), and image analysis software
(Image-Pro Plus 6.0).
Experimental Methods
Ninety-four patients with early lung adenocarci-
noma were included according to the inclusion
criteria. Patients were divided into 3 types refer-
ring to the new classification criteria for WHO lung
adenocarcinoma published in 20154: adenocarcino-
ma in situ (AIS), microinvasive adenocarcinoma
(MIA), and lepidic predominant adenocarcinoma
(LPA) (Figure 1). AIS is a localized small (≤3 cm)
adenocarcinoma with growth restricted to neo­
plastic cells along preexisting alveolar structures
(lepidic growth), lacking stromal, vascular, or pleu-
ral invasion. Acinar, papillary, solid, or micropap-
illary patterns and intraalveolar tumor cells are
absent. MIA is a small (≤3 cm), solitary adenocar-
cinoma with a predominantly lepidic pattern and
≤5 mm invasion in greatest dimension in any one
focus. Multiple infiltrates are based on the largest
diameter, rather than adding multiple infiltrates.
Figure 1 Pathological classification of early lung adenocarcinoma. (A) Adenocarcinoma in situ, 4×10 times). (B) Microinvasive
adenocarcinoma (4×10 times). (C) Lepidic predominant adenocarcinoma (4×10 times).

3. 114 Analytical and Quantitative Cytopathology and Histopathology®
Luo et al
LPA typically consists of lepidic neoplastic cells
growing along the surface of alveolar walls sim-
ilar to the morphology defined in the above sec-
tion on AIS and MIA. Invasive adenocarcinoma is
present in at least 1 focus measuring >5 mm in
greatest dimension. Invasion is defined as (1) his-
tological subtypes other than a lepidic pattern
(acinar, papillary, micropapillary, and/or solid),
(2) myofibroblastic stroma associated with inva-
sive tumor cells, (3) invades lymphatics, blood ves-
sels, or pleura, and (4) airway dissemination and
tumor necrosis. Next, the test software was cali-
brated using the objective micrometer,5 and then
10 relatively intact glands were photographed in
20× objective lens, and 100–150 cells in the corre-
sponding gland cavity were photographed under
40× objective lens. The images were saved in TIF
format and analyzed by Image-Pro Plus 6.0 image
analysis software (Figure 2). The tested parameters
included the circumference of the gland (the linear
length of the outer edge of the gland), the number
of tumor nuclei in the gland (the total number of
nuclei in the gland), the number of nucleoli in the
gland (the number of nucleoli in the nucleus of the
gland), the number of adhesion nuclei in the gland
(the number of adjacent nucleus in the gland that
are close together or overlap), the maximum dis-
tance between glands (the maximum linear dis-
tance between the outer edge of the gland and the
peripheral gland of the adjacent gland), the min-
imum distance between glands (the minimum lin-
ear distance between the outer edge of the gland
and the peripheral gland of the adjacent gland),
nuclear long axis, nuclear short axis, nuclear pe-
rimeter, and nuclear area. Calculation of the gener-
alized line reference number density of the cancer
cells in glands (Formula 1), the nucleolus occur-
rence rate in glands (Formula 2), the adhesion rate
of nucleus in glands (Formula 3), the roundness
of the nucleus (Formula 4), and the nuclear regu­
Figure 2 (A) Measurement of the circumference of the gland (the linear length of the outer edge of the gland) and counting of nucleus in
glands (200 times high magnification view of the picture). (B) Counting of nucleolus and adhered nucleus in glands (400 times high
magnification view of the picture; counting by Image-Pro Plus 6.0 software; red arrow shows adhered nucleus and black arrow shows
nucleolus). (C) Measurement of nucleus long axis, short axis, perimeter, area, and roundness (400 times high magnification view of the
picture, taking clear and complete nucleus for measurement by Image-Pro Plus 6.0 software). (D) The maximum distance between glands
and the minimum distance between glands (the maximum distance between glands in this example is 59.35 µm, and the minimum
distance between glands in this example is 19.47 µm).

4. Volume 42, Number 4/August 2020 115
Image Analysis of Early Lung Adenocarcinoma
lation Shape factor (Formula 5) were carried out.
The formulas are as follows:
The generalized line reference number density of cancer cells in
glands (Number/unit length) =
Number of tumor nuclei in the gland
__________________________________ (1)
Outer edge length of gland
The nucleolus occurrence rate in glands (%) =
Number of nucleoli in the gland
_________________________________ ×100 (2)
Number of tumor nuclei in the gland
The adhesion rate of nucleus in glands (%) =
Number of overlapped nuclei in the gland
______________________________________ ×100 (3)
Number of tumor nuclei in the gland
Nuclear perimeter2
The roundness of the nucleus = __________________ (4)
4×π×Nuclear area
The nuclear regulation Shape factor =
Nuclear area×[3×(Nuclear long axis+Nuclear short
axis)−2×√Nuclear long axis×Nuclear short axis
___________________________________________________ (5)
Nuclear long axis×Nuclear short axis×Nuclear perimeter
Statistical Analysis
All data of image analysis parameters of differ­
ent pathological types were analyzed by SPSS 25.0
software statistical package for one-way analysis
of variance and comparison between groups. The
significance criterion of the test was p<0.05, the dif-
ference was significant, p<0.01, and the difference
was highly significant.
Results
The Test Results of the Generalized Line Reference
Number Density of Adenocarcinoma Cells in Glands
and the Adhesion Rate of Nucleus in Glands Among
AIS, MIA, and LPA
In our research we obtained the minimum, maxi-
mum, mean, and standard deviation of the gener-
alized line reference number density of the cancer
cells in glands and the adhesion rate of nucleus
in glands by using software SPSS 25.0 analysis of
variance to analyze 94 patients with early lung
adenocarcinoma with different pathological types
(Table I). Simultaneously, there were significant
differences in the generalized line reference num-
ber density of the cancer cells in glands and the
adhesion rate of nucleus in glands between AIS
and MIA, MIA and LPA, and AIS and LPA (p<
0.005) (Table I). It indicated that the generalized
line reference number density of adenocarcinoma
cells in glands and the adhesion rate of nucleus
in glands were with a continuous increasing trend
in AIS, MIA, and LPA (Chart 1).
The Test Results of the Nucleolus Occurrence Rate
in Glands, the Maximum and Minimum Distance
Between Glands, and Nucleus Morphological
Parameters (Nuclear Long Axis, Short Axis, Area,
Perimeter, Roundness, and Regulatory Shape Factor)
Among AIS, MIA, and LPA
We obtained the minimum, maximum, mean, and
standard deviation of the nucleolus occurrence
rate in glands, the maximum and minimum dis-
tance between glands, and nucleus morphologi-
cal parameters (nuclear long axis, short axis, area,
perimeter, roundness, and regulatory shape factor)
of the 3 different types of early lung adenocarci-
noma through software analysis, and different im-
age analysis parameters were compared between
groups. Our results showed that the minimum
distance between glands, nuclear roundness, and
nuclear regulatory shape factor were not signifi­
cantly different in AIS, MIA, and LPA (p>0.05).
The nucleolus occurrence rate in glands and the
maximum distance between glands were signifi-
cantly different between AIS and LPA and between
MIA and LPA (p<0.05), but there was no signi-
ficant difference between AIS and MIA (p>0.05),
indicating that the nucleolus occurrence rate in
glands of LPA was the highest, and the maxi-
mum distance between glands was the smallest.
The long axis, short axis, perimeter, and area of
the nucleus were significantly different between
AIS and MIA and between AIS and LPA (p<0.05).
There was no significant difference in MIA and
LPA (p>0.05). It indicated that the nuclear long
axis, short axis, perimeter, and area of the AIS
were the smallest in these 3 different types of early
lung adenocarcinoma (Table II).
Discussion
Image analysis technology has been applied to the
quantitative study of some tumors. At present,
scholars have quantitatively tested the morpho-
logical structure of partial tumor cells. It is noted
that the quantitative parameters of tumor cell nu-
clei have important value in pathological diagnosis
and classification.6-9 In our study the generalized
line reference number density of cancer cells in
glands, the adhesion rate of nucleus in glands, the
nucleolus occurrence rate in glands, the maximum

5. 116 Analytical and Quantitative Cytopathology and Histopathology®
Luo et al
distance between glands, and the area, perimeter,
long axis, and short axis of the nucleus were sig­
nificantly different and had a certain application
value in the quantitative analysis of pathological
types of early lung adenocarcinoma.
In the image analysis of early lung adenocarci-
noma, the density of the cancer cells in the gland
of AIS, MIA, and LPA can be quantitatively de-
scribed by the generalized line reference number
density of cancer cells in glands and the adhesion
rate of nucleus in glands; these parameters pre­
sented an increasing trend. The density of the can-
cer cells in the gland of AIS was the sparsest and
had the lowest adhesion rate of nucleolus in the
glands. Conversely, the generalized line reference
number density of cancer cells in glands of LPA
was the largest and the adhesion rate of nucle-
us in the glands was the highest. Therefore, when
the generalized line reference number density of
cancer cells in glands is increased or the adhesion
rate of nucleus in glands is high, it should be con-
sidered first that these glands are likely to have
invasive characteristics, which will help us to iden-
tify some different types of early lung adenocarci-
noma that are difficult to diagnose.
The nucleolus is a site for the synthesis of ribo-
Table I Results of Measuring Generalized Line Reference Number Density of Cancer Cells in Glands, the Adhesion Rate of Nucleus in
Glands of Various Pathological Subtypes, and the Results of Multiple Comparison
Mean±
Adeno- Minimum Maximum standard
Parameter carcinoma Cases value value deviation p Value
Generalized line reference AIS (a) 26 48 137 88±19.21b3,c3
number density of cancer MIA (b) 38 72 167 120±19.35a3,c3 0.000
cells in glands (no./mm) LPA (c) 30 93 208 142±31.23a3,b3
Adhesion rate of nucleus in AIS (a) 26 0.00 0.15 0.08±0.04b3,c3
glands (%) MIA (b) 38 0.08 0.30 0.16±0.06a3,c3 0.000
LPA (c) 30 0.04 0.47 0.25±0.11a3,b3
Superscript letters indicate comparison with this group; 1 indicates p<0.05, 2 indicates p<0.01, and 3 indicates p<0.001.
Chart 1 Mean contrast bar chart of (A) generalized line reference number density of cancer cells in glands (number/mm) and (B) the
adhesion rate of nucleus in glands (%) of AIS, MIA, and LPA.

6. Volume 42, Number 4/August 2020 117
Image Analysis of Early Lung Adenocarcinoma
somal RNA (rRNA), which is closely related to
protein synthesis. The number of nucleoli reflects
the physiological state of the cell. In cells with ac-
tive protein synthesis, the nucleolus is developed,
large and obvious, or with multiple nucleoli, while
in cells with inactive protein synthesis the nucleo-
lus is small or nonexistent.10,11 In the image anal-
ysis of early lung adenocarcinoma, we quantita­
tively analyzed the nucleolus occurrence rate in
glands, and the results showed that LPA had the
highest nucleolus occurrence rate, indicating that
the intracellular protein synthesis was the most
active. There was no significant difference in the
nucleolus occurrence rate in glands of the AIS and
MIA, which indicated that the level of cellular pro-
tein synthesis in the gland was comparable.
Two new parameters, the maximum and mini­
mum distance between glands in early lung ade-
nocarcinoma, can quantitatively describe the inter­
stitial width between the glands. The maximum
distance between glands is the quantitative anal-
ysis of the maximum width of the interstitial be-
tween the glands. The maximum interstitial width
refers to the degree of interstitial fibrosis and the
degree of density of the glands. The more serious
the degree of interstitial fibrosis is, the larger the
measurement parameter of maximum distance be-
tween glands we measured. The minimum distance
between glands is the quantitative analysis of the
minimum width of the interstitial fibrosis between
the glands. The smaller the minimum distance be-
tween glands, the closer the glands are. The min-
imum interstitial distance of the gland can reflect
the degree of density between the glands. When
Table II Results of Measuring Nucleolus Occurrence Rate in Glands, the Maximum and Minimum Distance Between Glands, and Nucleus
Morphological Parameters of Various Pathological Subtypes and the Results of Multiple Comparisons
Mean±
Adeno- Minimum Maximum standard
Parameter carcinoma Cases value value deviation p Value
Nucleolus occurrence rate AIS (a) 26 0.00 0.52 0.12±0.11c1
in glands (%) MIA (b) 38 0.02 0.46 0.14±0.11c1 0.030
LPA (c) 30 0.04 0.42 0.20±0.12a1,b1
Minimum distance between AIS (a) 26 6.98 24.79 13.94±4.68
glands (µm) MIA (b) 38 7.63 19.45 13.10±2.49 0.132
LPA (c) 30 7.13 23.58 12.07±3.28
Maximum distance between AIS (a) 26 21.03 52.29 35.61±7.76c3
glands (µm) MIA (b) 38 21.86 46.70 32.58±6.15c1 0.002
LPA (c) 30 20.72 39.73 29.60±4.13a3,b1
Nuclear long axis (µm) AIS (a) 26 5.95 8.71 7.09±0.72b3,c3
MIA (b) 38 6.50 10.00 8.14±0.98a3 0.000
LPA (c) 30 5.81 9.85 8.18±0.87a3
Nuclear short axis (µm) AIS (a) 26 4.38 6.38 5.11±0.47b3,c3
MIA (b) 38 4.63 6.77 5.75±0.65a3 0.000
LPA (c) 30 4.88 7.12 5.73±0.64a3
Nuclear perimeter (µm) AIS (a) 26 16.50 23.98 19.33±1.89b3,c3
MIA (b) 38 17.68 26.66 22.06±2.59a3 0.000
LPA (c) 30 17.84 26.61 22.16±2.24a3
Nuclear area (µm2) AIS (a) 26 20.32 42.54 27.86±5.50b3,c3
MIA (b) 38 23.17 68.51 36.70±9.66a3 0.000
LPA (c) 30 24.01 51.96 36.24±7.47a3
Nuclear roundness AIS (a) 26 1.05 1.14 1.10±0.02
MIA (b) 38 1.07 1.18 1.11±0.02 0.214
LPA (c) 30 1.07 2.61 1.17±0.27
Nuclear regulatory shape AIS (a) 26 0.94 1.00 0.96±0.01
factor MIA (b) 38 0.95 0.99 0.96±0.01 0.506
LPA (c) 30 0.95 0.96 0.96±0.01
Superscript letters indicate comparison with this group; 1 indicates p<0.05, 2 indicates p<0.01, and 3 indicates p<0.001.

7. 118 Analytical and Quantitative Cytopathology and Histopathology®
Luo et al
the gland interstitial distance is 0, the glands are
merged with each other and there is a back-to-
back phenomenon, which is considered to be one
of the growth characteristics of the cancerous
glands. Our results showed that the maximum dis-
tance between glands is significantly different in
different pathological types of early lung adeno-
carcinoma, while the difference in the minimum
distance between glands is not significant. The
maximum distance between glands of LPA was
the smallest, the interstitial width was the small-
est, and the gland was relatively dense. There was
no significant difference in the maximum distance
between AIS and MIA, indicating that the glandu-
lar interstitial width was not significantly differ-
ent, and the gland interstitial structure was simi-
lar. Therefore, in early lung adenocarcinoma the
glands of AIS and MIA are relatively sparse and
the interstitial fibrosis is more obvious.
The morphological parameters of the nucleus
(long axis, short axis, perimeter, and area of the
nucleus) were significantly different in different
pathological types of early lung adenocarcinoma.
The long axis, short axis, perimeter, and area of
the AIS cells were the smallest. There was no sig­
nificant difference in the long axis, short axis, pe-
rimeter, and area of MIS and LPA cells, indicating
that the size of the nucleus was equivalent. The
nuclear roundness and nuclear regulatory shape
factor were not significantly different in AIS, MIA,
and LPA. The nuclear regulatory shape factor of
cancer cells was 0.96, and the nuclear roundness
ranged from 1.10–1.17, which was close to 1. There-
fore, it is considered that the long axis, short axis,
perimeter, and area of the nucleus have applica-
tion value in the quantitative analysis of early lung
adenocarcinoma, which can be used as a quantita-
tive parameter for differential diagnosis between
AIS and MIA. In different pathological types of
early lung adenocarcinoma, the nucleus of cancer
cells in the gland is relatively regular and relatively
close to ellipse or circle, and the degree of variation
between nuclei is not large.
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