Original Article

Real-time and accuracy of rapid on-site cytological evaluation of

lung cancer
Zhongqin Huang1#, Dongchun Zhuang2#, Airan Feng2, Ling Ye2, Lingling Hong2
1
Department of Nursing, The Fifth Hospital of Xiamen, Xiamen, Fujian, China; 2Department of Respiration, The Fifth Hospital of Xiamen,
Xiamen, Fujian, China
Contributions: (I) Conception and design: L Hong; (II) Administrative support: L Hong; (III) Provision of study materials or patients: Department
of Respiration, The Fifth Hospital of Xiamen; (IV) Collection and assembly of data: Z Huang; (V) Data analysis and interpretation: Z Huang; (VI)
Manuscript writing: All authors; (VII) Final approval of manuscript: All authors.
#
These authors contributed equally to this work.
Correspondence to: Lingling Hong. Department of Respiration, The Fifth Hospital of Xiamen, 101 Minan Road, Xiamen, Fujian 361101, China.
Email: dazzle-posh@126.com.

Background: Although using pathological diagnosis is the gold standard for lung cancer diagnosis,
pathological reports take a long time. Rapid on-site assessment (ROSE) is a method to determine whether
the quality of the specimens is sufficient for cytopathological diagnosis, which issues a preliminary report
during the operation and takes shorter time. The aim of this study is to explore the clinical significance of
rapid on-site evaluation (ROSE) in the diagnosis of lung cancer in terms of real-time and accuracy.
Methods: A total of 38 suspected lung cancer cases were enrolled from August 2019 to July 2020. Patients
received ROSE and pathological examinations at the same time. The coincidence rate of the two diagnostic
approaches was calculated, and statistical analysis was carried out to evaluate whether the time difference
between the ROSE report and the pathological report reached statistical significance.
Results: A total of 38 suspected lung cancer cases were enrolled from August 2019 to July 2020. Patients
received ROSE and pathological examinations at the same time. The coincidence rate of the two diagnostic
approaches was calculated, and statistical analysis was carried out to evaluate whether the time difference
between the ROSE report and the pathological report reached statistical significance..
Conclusions: ROSE has the advantage of rapid and accurate diagnosis for lung cancer, and has great
clinical significance.

Keywords: Rapid on-site evaluation (ROSE); biopsy; pathology; lung cancer

Submitted Oct 19, 2020. Accepted for publication Jan 15, 2021.
doi: 10.21037/tcr-20-3294
View this article at: http://dx.doi.org/10.21037/tcr-20-3294

Introduction resulting in poor prognosis, and the average survival time of

patients with metastatic lung cancer is only 3–6 months (4).
Lung cancer is the most common cancer in China, followed
Pathological diagnosis through various techniques is the
by gastric cancer. According to an analysis of the prevalence gold standard, and includes cytological examination, pleural
of malignancies in 2015, 787,000 people were diagnosed biopsy, computed tomography (CT), or percutaneous lung
with lung cancer in China (1). Lung cancer has the highest biopsy, which provide evidence for diagnosis for lung cancer
mortality for both women and men, with a 5-year survival patients (5,6). Treatment against lung cancer depends on
rate of only 19.7% (2). In Europe, lung cancer is one the pathological type, so a clear pathological classification
of the 3 most common tumor diseases with the highest is the prerequisite for treatment. However, it usually takes
mortality rate (3). Lung cancer is susceptible to metastasis, 2–5 days for traditional approaches in most domestic

© Translational Cancer Research. All rights reserved. Transl Cancer Res 2021;10(1):479-486 | http://dx.doi.org/10.21037/tcr-20-3294
480 Huang et al. Rapid on-site cytological evaluation of lung cancer

A B C

Figure 1 Computed tomography of a 65-year-old male showing atelectasis caused by bronchial occlusion in the middle and lower lobes of
the right lung, and a soft tissue shadow in the right hilum.

hospitals to produce histological results, which not only had single or multiple nodules and pleural effusions in
prolongs the length of hospital stay but also increases the lungs as demonstrated by preoperative enhanced
financial burden. The frozen section allows rapid diagnosis chest CT scan, were immune to the regular anti-infective
during surgery, but this technology requires a large amount treatment; (II) patients suspected of lung cancer based on
of specimens. ROSE technology only needs a small comprehensive analysis of the patient’s medical history
amount of specimens for rapid diagnosis, avoiding the and auxiliary examination results; (III) patients have
risk of bleeding due to excessive clamping of specimens. completed general preoperative examination to exclude
In addition, preparation process of frozen section is contraindications related to lung biopsy; (IV) patients and
complicated, and such kind of report must be issued by a family members were told the risk of operation and have
specialist pathologist. However, pathologists are scarce and signed informed consent before surgery. Exclusion criteria
the patients have to bear huge economic burden, hardly were (I) contraindications to surgery such as coagulation
meeting their demands. Rapid on-site evaluation (ROSE) dysfunction, severe heart and lung failure; (II) without
technology provides an adequate evaluation and preliminary complete clinical data. Thirty-eight patients with suspected
diagnosis in a short time after a partial section is obtained lung cancer, who had pulmonary space-occupying lesions,
from the target site, printed on glass side, stained, and were enrolled at the Fifth Hospital of Xiamen from August
observed under a microscope (7,8). ROSE is divided into 2019 to July 2020 (28 males and 10 females, 43–89 years of
cytological ROSE (C-ROSE) and microbiological ROSE. age, average age: 67.32 years).Of these, 24 were examined by
In the present study, we discuss the clinical significance bronchoscopy, 10 by CT-guided percutaneous lung puncture
of C-ROSE for lung cancer. C-ROSE-guided biopsy has examination, and 4 by pleural biopsy and thoracic closed
been found to increase the positive rate of lung biopsy and drainage. When the pathological specimens were sent to the
can quickly clarify the type of pathology (9). C-ROSE is pathology department for routine examination, patients were
increasingly applied to clinical practice at home and abroad. subjected to ROSE. The results of 2 examinations and the
However, few studies have compared this technology time required for the report were recorded.
with traditional pathological report in terms of real-time
capability and accuracy. Therefore, the aim of the present
Sample collection and detection
study was to discuss the difference between ROSE report
and C-ROSE for diagnosing lung cancer. We present the Lesions involving the airway or that are close to the airway
following article in accordance with the MDAR checklist were detected by bronchoscopy (Figures 1 and 2). Chest
(available at http://dx.doi.org/10.21037/tcr-20-3294). CT and bronchoscope indicated the location of the lesion,
followed by bronchoscopic mucosal biopsy and lung biopsy.
A disposable 5-mL sterile syringe needle was used to obtain
Methods
tissue from the biopsy specimens. The tissue was then
Inclusion criteria include the following: (I) patients who placed on a slide and smeared to a 1-cm circle tissue block

© Translational Cancer Research. All rights reserved. Transl Cancer Res 2021;10(1):479-486 | http://dx.doi.org/10.21037/tcr-20-3294
Translational Cancer Research, Vol 10, No 1 January 2021 481

A B C

D E F

Figure 2 Sixty-five-year-old male patient. (A) Carina, (B) left main bronchus opening, (C) narrow right main bronchus opening, (D) biopsy
of right main bronchus mucosa, (E) post-biopsy of right main bronchus mucosa, (F) argon knife for right main bronchus mucosa.

print for ROSE (10,11); the remaining specimens were fixed drying with absorbent paper. The entire staining process
in 10% formaldehyde solution and sent to the pathology could complete within 1–2 min. The sections were then
department for examination. For peripheral lung lesions or viewed under a microscope for comprehensive analysis.
lesions that were not easily reached by bronchoscopy, CT- A study published in Chest in 2018 has showed that after
guided percutaneous lung biopsy was performed (Figure 3). 3 months of training in cytopathology knowledge, respiratory
The puncture needle was inserted into the puncture point physicians also can complete ROSE interpretation, and
indicated by CT to prepare tissue print, and the remaining the accuracy gets close to that of cytopathologists without
tissue block was sent to the pathology department. Pleural statistical difference (12). The ROSE report was issued by a
biopsy and closed pleural drainage were performed for respiratory specialist who has been trained in cytopathology
patients with moderate and large pleural effusions (Figure 4). If cells presented with tumor cell characteristics in the
The pleural tissue obtained by the pleural biopsy needle ROSE roll, they were considered to be a positive specimen.
and the drainage pleural effusion were centrifuged to make The results guided the subsequent treatment direction.
a ROSE tissue print. The remaining specimens were sent to
the pathology department for routine examination.
Pathological techniques

The tissues were fixed, dehydrated, cleared, and embedded

ROSE technology
into paraffin. The paraffin was cut into slides and then
The ROSE technology consists of preparation of section, stained. The slides were then observed by pathologists, and
dyeing, and observation (10,11). After preparing the if necessary, immunohistochemistry was conducted.
sections, the sections were immediately subjected to
modified Diff-Quick stain (Biotech Development Co., Ltd.,
Ethical statement
Zhuhai, China), immersed in solution A and solution B,
and washed with phosphate buffered solution, followed by The study was conducted in accordance with the

© Translational Cancer Research. All rights reserved. Transl Cancer Res 2021;10(1):479-486 | http://dx.doi.org/10.21037/tcr-20-3294
482 Huang et al. Rapid on-site cytological evaluation of lung cancer

A B C D

Figure 3 Computed tomography of a 61-year-old female showing soft tissue with a diameter of 0.79 cm next to the aortic arch of the left
upper lobe, followed by percutaneous lung biopsy. Red arrows indicate soft tissue.

A B C

Figure 4 Computed tomography of 44-year-old female showing pleural effusion on the left, followed by pleural biopsy and closed pleural
drainage to obtain specimens for examination.

Declaration of Helsinki (as revised in 2013). The study was only 1 ROSE report was negative, and the remaining
approved by ethics board of the Fifth Hospital of Xiamen ROSE diagnoses were malignant with complete tumor cell
(NO.:2020-XMSDWYY-002) and informed consent was characteristics. Of the 38 patients, 25 were diagnosed by
taken from all individual participants. electronic bronchoscopy, 9 by CT-guided lung biopsy, and
4 by pleural biopsy combined with closed thoracic drainage.
The diagnosis coincidence of the ROSE technique and
Statistical analysis pathology was 95.45% (Table 1).
SPSS version 22.0 (IBM, Armonk, NY, USA) was used for
the statistical analysis, and t-test was used to compare the Comparison of the time between ROSE diagnosis and
count data. P<0.05 was considered statistically significant. pathological diagnosis

After collecting the specimen, we calculated the time of the

Results ROSE report and pathological report. The timing of report
Results of diagnosis was calculated from the first specimen to the production
of final report. The ROSE report took 4–52 min to obtain
The final pathological diagnosis in the 38 patients the result, with an average time of 13.84 min, while the
was lung cancer for all patients, including 21 cases of pathological report time took 2,832–15,885 min, with an
adenocarcinoma, 11 cases of squamous cell carcinoma, average time of 6,222.05 min (103.70 h, 4.3 days) (Table 2).
and 6 cases of small cell lung cancer. In the ROSE report, The difference between the 2 reports was significant (P<0.05).

© Translational Cancer Research. All rights reserved. Transl Cancer Res 2021;10(1):479-486 | http://dx.doi.org/10.21037/tcr-20-3294
Translational Cancer Research, Vol 10, No 1 January 2021 483

Table 1 ROSE and pathological diagnosis result

Detection Positive Negative Positive ratio (%) Coincidence (%)

ROSE 37 1 97.37 97.37

Pathology detection 38 0 100

ROSE, rapid on-site evaluation.

Table 2 Comparison between ROSE time and pathological report time

Time x±s (min) t value P value

ROSE time 13.84±9.3 –17.79 <0.05

Pathological report time 6,222.05±2,151.02

ROSE, rapid on-site evaluation.

Characteristics of lung adenocarcinoma cells under ROSE cytoplasms or naked nuclei without plasma. Nucleoli were
microscope blurred or missing. Nuclear chromatin was granular and
unevenly distributed like “ghost faces”. Cancer cells were
After the tissue specimen print was processed, lung
arranged in rows or mosaics, often densely packed; and
adenocarcinoma cell characteristics were observed under
(II) necrosis and nuclear filaments (Figure 5E). The final
ROSE microscope as follows: (I) large and round cells
diagnosis was small cell lung cancer, as shown in Figure 5F.
distributed in piles and clusters; (II) large nucleus, abundant
cytoplasm with vacuoles; (III) acinus-, papillary-, and
mulberry-like cells; (IV) round nucleus with a cytoplasm; Discussion
(V) coarse and granular chromatin; and (VI) large and clear Diagnostic interventional techniques have good sensitivity
nucleolus (Figure 5A). The pathological diagnosis of the same and specificity, but there is a risk of trauma in the process
patient was lung adenocarcinoma, as shown in Figure 5B. of repeated sampling, so the times and scope of punctures
should be reduced to ensure sufficient specimens. ROSE
Characteristics of lung squamous cell carcinoma under technology is widely used in the clinical setting (9,13,14).
ROSE microscope When combined with biopsy technology, it not only
reduces the number of punctures (15,16), but also increases
Lung squamous cell carcinoma cells were observed under the positive rate of diagnosis, avoid traumas, and reduces
ROSE microscope with the following manifestations: (I) risk of complications. After obtaining the sample and after
irregular cell shape, not round, polygonal, and spindle- smearing, ROSE is immediately carried out to determine
shaped. Obvious deformity and clear edges; (II) keratinized whether the amount of specimens is sufficient and qualified,
and uniform plaster-like cytoplasm mainly in red. Some cells and a primary diagnosis can be obtained immediately (7).
with few cytoplasms and even a bare nucleus; (III) nuclear Once a sufficient amount of qualified specimens is obtained,
chromatin was densely stained, and the size of the nucleus the operation can be terminated immediately, saving time
was irregular and angled with obvious deformities; and and reducing patient trauma. However, if a sufficient
(IV) a “positive background” was obvious (Figure 5C). The amount of qualified specimens is not obtained, the location
histopathology of the same patient was finally diagnosed as and method of sampling can be adjusted to obtain an ideal
lung squamous cell carcinoma, as shown in Figure 5D. specimen. Through ROSE test takes longer to obtain
samples, it is worthwhile for patients since the eligibility
of the puncture specimen by ROSE test can increase the
Characteristics of small cell lung cancer under ROSE
positive rate of pathological results, thereby reducing the
microscope
risk of secondary puncture. In the present study, the samples
ROSE microscope indicated the following characteristics of 24 patients were obtained through bronchoscopy. After
of small cell lung cancer cells: (I) small cancer cells with less sampling, the ROSE interpreter immediately prepared,

© Translational Cancer Research. All rights reserved. Transl Cancer Res 2021;10(1):479-486 | http://dx.doi.org/10.21037/tcr-20-3294
484 Huang et al. Rapid on-site cytological evaluation of lung cancer

A B

C D

E F

Figure 5 Comparison between rapid on-site evaluation (ROSE) diagnosis and pathological diagnosis. (A) Adenocarcinoma cells of a 61-year-
old female patient seen under ROSE microscope (×200). Clumped distribution with a large nucleus. Vacuoles are seen in the abundant
cytoplasm. (B) Representative pathological images of specimens from a 61-year-old female patient [hematoxylin-eosin staining (HE) ×400].
Hyperplastic adenocarcinoma cells are seen under high power lens. (C) Representative ROSE images of lung squamous cell carcinoma under
a microscope for a 65-year-old male patient (×200). Irregular cancer cells are seen. (D) Representative pathological images of specimens
from a 65-year-old male patient (HE staining ×400). Keratinized squamous cancer cells are seen. (E) Representative ROSE images of small
cell lung cancer under a microscope (×200), with few cytoplasm, no nucleolus, necrosis, and nuclear filaments for a 44-year-old female
patient. (F) Immunohistochemical synaptophysin (+), CD56 (+), and Ki-67 (80%) for a 44-year-old female patient. Small cell lung cancer is
indicated pathologically (HE staining ×400).

stained, and observed the sections under a microscope. pleural effusion underwent pleural biopsy and closed pleural
When malignant cells were seen under the microscope and drainage. Of these patients, malignancies were detected in
the sample was sufficient, the operation was stopped. While the pleural tissue print of 3 patients, and 1 patient tested
obtaining specimens, we reduced the times of punctures negative .We can increase the number of smears on the same
as much as possible. Ten patients underwent CT-guided specimen, and secondly improve the technical capabilities
lung biopsy, as ROSE was performed during the puncture of respiratory specialists on-site ROSE, including smearing,
process to increase the positive rate of specimens (17-21). staining, and interpretation through specialist training,
The operation was stopped after the detection of malignant exchange for further education and learning to further
cells. All postoperative pathology results were positive, and increase the positive rate and coincidence rate of ROSE.
the ROSE diagnosis coincided with the pathology report Further experiments are required to verify the role of
(97.37%). The other 4 patients with a large amount of ROSE in pleural tissue.

© Translational Cancer Research. All rights reserved. Transl Cancer Res 2021;10(1):479-486 | http://dx.doi.org/10.21037/tcr-20-3294
Translational Cancer Research, Vol 10, No 1 January 2021 485

While obtaining biopsy tissue, ROSE is often performed reporting checklist. Available at http://dx.doi.org/10.21037/
routinely to quickly obtain a preliminary diagnosis. tcr-20-3294
Compared with histopathological examination, ROSE is
faster and more convenient. ROSE is important for the Data Sharing Statement: Available at http://dx.doi.
diagnosis of primary bronchial lung cancer, and some org/10.21037/tcr-20-3294
cases can be clearly classified by ROSE technology.
In addition, it has been reported that the molecular Conflicts of Interest: All authors have completed the
biologic and genetic technology of cells can be obtained ICMJE uniform disclosure form (available at http://dx.doi.
through detecting the ROSE print, such as polymerase org/10.21037/tcr-20-3294). The authors have no conflicts of
chain reaction, fluorescence in situ hybridization (FISH), interest to declare.
immunocytochemistry, and second-generation gene
sequencing (22,23). Lung cancer has a high incidence and Ethical Statement: The authors are accountable for all
high mortality in China, and most cases are already at aspects of the work in ensuring that questions related
advanced stage when diagnosed (24). The main treatment to the accuracy or integrity of any part of the work are
opinions for lung cancer include surgery, chemotherapy, appropriately investigated and resolved. The study was
targeted therapy, and immunotherapy. Treatment conducted in accordance with the Declaration of Helsinki (as
methods are mainly based on pathological diagnosis and revised in 2013). The study was approved by ethics board of
genetic test results. The demand for targeted therapy and the Fifth Hospital of Xiamen (NO.:2020-XMSDWYY-002)
immunotherapy is increasing, but these therapies depend on and informed consent was taken from all individual
genetic testing, and there must be an accurate diagnosis to participants.
receive specific therapies. In the early stage of the disease,
when the lesion is small, tumor cells can be reflected in Open Access Statement: This is an Open Access article
ROSE report, and when the pathological specimen report distributed in accordance with the Creative Commons
is negative, the ROSE print can be used for staining to Attribution-NonCommercial-NoDerivs 4.0 International
confirm the diagnosis and to guide treatment (25,26). In the License (CC BY-NC-ND 4.0), which permits the non-
present study, the average ROSE time was about 13.84 min, commercial replication and distribution of the article with
and the average pathology report time was 6,222.05 min the strict proviso that no changes or edits are made and the
(about 4.3 days), which significantly longer than the ROSE original work is properly cited (including links to both the
time. In the absence of ROSE, the possibility of negative formal publication through the relevant DOI and the license).
results and repeated examinations increases, further See: https://creativecommons.org/licenses/by-nc-nd/4.0/.
extending the diagnosis time, increasing hospitalization
costs, and causing extra trauma for the patient.
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© Translational Cancer Research. All rights reserved. Transl Cancer Res 2021;10(1):479-486 | http://dx.doi.org/10.21037/tcr-20-3294