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Diagnosis of solitary pulmonary nodules: An updated review

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Small lung nodule is a common problem in pulmonary practice. The definition of a classical solitary pulmonary nodule is a single, spherical, well-circumscribed, radiographic opacity less than or equal to 30 mm in diameter that is completely surrounded by aerated lung and is not associated with atelectasis, hilar enlargement, or pleural effusion. Ideally, the goal of diagnosis and management is to promptly bring to surgery all patients with operable malignant nodules while avoiding unnecessary thoracotomy in patients with benign disease. In fact, causes of solitary pulmonary nodules can be benign or malignant. In order to diagnose causes of solitary pulmonary nodules, we can use many different methods, including clinical symptoms, radiographic features, liquid biopsy, bronchoscopy, CT-guided fine-needle aspiration biopsy and surgery. Each method has its own value. It is very meaningful if we can diagnose these causes early. Based on these results, doctors can determine the strategy to manage disease.

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DIAGNOSIS OF SOLITARY PULMONARY NODULES:

AN UPDATED REVIEW

Dao Ngoc Bang 1 ; Ta Ba Thang 1 ; Do Quyet 2

SUMMARY

Small lung nodule is a common problem in pulmonary practice The definition of a classical solitary pulmonary nodule is a single, spherical, well-circumscribed, radiographic opacity less than or equal to 30 mm in diameter that is completely surrounded by aerated lung and is not associated with atelectasis, hilar enlargement, or pleural effusion Ideally, the goal of diagnosis and management is to promptly bring to surgery all patients with operable malignant nodules while avoiding unnecessary thoracotomy in patients with benign disease In fact, causes of solitary pulmonary nodules can be benign or malignant In order to diagnose causes of solitary pulmonary nodules, we can use many different methods, including clinical symptoms, radiographic features, liquid biopsy, bronchoscopy, CT-guided fine-needle aspiration biopsy and surgery Each method has its own value It is very meaningful if we can diagnose these causes early Based on these results, doctors can determine the strategy to manage disease

* Keywords: Solitary pulmonary nodule; Diagnosis

1 Causes and proportion of solitary

pulmonary nodules

The definition of a classical solitary

pulmonary nodule (SPNs) is a

single, spherical, well-circumscribed,

radiographic opacity less than or equal to

30 mm in diameter that is completely

surrounded by aerated lung and is

not associated with atelectasis, hilar

enlargement, or pleural effusion [1]

Causes of SPNs are very variety, with 2 main groups: benign or malignant

ones ( table 1) The estimated prevalence

of each etiology varies among different populations Even among screening studies of smokers who are at increased risk of malignancy, the number of malignant nodules is small Among 12,029 nodules found in a large Canadian study, only 144 (1%) were malignant [2]

1 103 Military Hospital

2 Vietnam Military Medical University

Corresponding author: Dao Ngoc Bang (bsdaongocbang@yahoo.com.vn)

Date received: 24/07/2019

Date accepted: 23/08/2019

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Table 1: Differential diagnosis of SPNs [2]

Infectious granuloma (atypical mycobacteria, coccidioidomycosis,

histoplasmosis, tuberculosis)

80%

Benign Arteriovenous malformation; intrapulmonary lymph node; sarcoidosis Rare

Malignant

Characteristics of each cause are

extremely different, including clinical

symptoms and paraclinical changes

Depending on the characteristics of SPNs,

doctors should apply some suitable

methods in diagnosis and management

2 Diagnosis of SPNs

* Characteristics of risk factors:

The probability of malignancy can be

assessed clinically or by quantitative

predictive models as falling into 1 of 3 risk

categories: very low probability (less than 5%), low/moderate probability (5% to 65%),

or high probability (greater than 65%) The most commonly used model estimates the probability of malignancy using six independent predictors: smoking history, older age, history of extrathoracic cancer more than five years before nodule detection, nodule diameter, spiculation presence, and upper lobe location

An online calculator is available at http://reference.medscape.com/calculator/ solitary-pulmonary-nodule-risk [3]

Table 2: Calculating the malignancy probability of a pulmonary nodule [3]

Cancer history 1: if patient has a history of extrathoracic cancer diagnosed more than five

years before nodule detection (otherwise = 0) Diameter Diameter of the solitary pulmonary nodule in mm

Location 1: if nodule is located in the upper lobe (otherwise = 0)

Smoking history 1: if patient is a current or former smoker (otherwise = 0)

Spiculation 1: if spiculation is present (otherwise = 0)

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* Radiographic features and PET/CT:

Incidentally found SPNs are most

commonly discovered on CT (computed

tomography) scans Although some may

be seen on chest radiographs, a CT-scan

affords superior detail for evaluating

specific characteristics of the nodule Of

particular importance is a thorough review

of all previous imaging to assess both

changes in size and the rate of

change over time Numerous studies had

demonstrated that increasing nodule size

corresponding with increasing risk of

malignance: a nodule smaller than 5 mm,

less than 1% malignancy risk; a nodule

of 5 - 9 mm, 2 - 6% malignancy risk;

a nodule of 10 - 20 mm, 18% malignancy

risk; a nodule 20 mm or larger, more than 50% malignancy risk Signs of growth on serial imaging are highly suggestive of malignancy The growth rate of an SPN

is also used to evaluate the potential for malignancy, with most malignancies doubling in volume between 20 and 400 days A solid SPN that has been stable for more than 2 years is likely to be benign,

as is a subsolid nodule that has been stable for more than 3 years Attenuation

of the nodule on CT imaging may be characterized as solid or subsolid, with subsolid lesions further divided as pure subsolid and part solid Although solid lesions are more common, subsolid lesions are more likely to be malignant [4, 6]

Table 3: Radiologic features suggested benign or malignant SPNs [4]

Calcification Concentric, central,

or popcorn pattern

Typically noncalcified or eccentric calcification

Doubling time Less than one month or

CT examinations of the thorax performed to follow lung nodules should use a low-radiation technique Techniques to reduce low-radiation dose are important, given the frequency with which follow-up CT examinations are performed

Table 4: Summary of management pathway for SPNs by ACCP guideline [6]

Size

(5 - 65%)

High (> 65%)

surveillance*

PET/CT and optional biopsy/resection

Staging for treatment

(*: Timing and term of CT surveillance depend on nodule size and appearance; ACCP: American College of Clinical Pharmacy)

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Table 5: Summary of management pathway for single SPNs by Fleischner Society

guideline 2017 [5]

Risk for lung cancer Size (volume)

6 - 8 mm (100 - 250 mm3) CT surveillance*

> 8 mm (> 250 mm3) CT surveillance* with optional PET/CT, biopsy and/or resection

(*: Timing and term of CT surveillance depend on nodule size and appearance)

National Comprehensive Cancer Network

(NCCN) guideline proposes different cut-off

for size, follow-up interval and surveillance

term depending on the appearance of the

nodule, e.g., solid, part-solid, or non-solid

Follow-up methods proposed by the

Fleischner Society (2017) vary depending

on whether the nodule is solid or sub-solid

American College of Clinical Pharmacy

(ACCP) guidelines outline similar

methodology; follow-up methods mainly

depend on nodule appearance, nodule

size, and risk or probability of malignancy

[3] If the nodule appears highly suspicious

for malignancy, non-surgical biopsy or

surgical resection should be carried out

Most guidelines recommend non-surgical

biopsy or surgical resection when the

nodule develops a solid component The

BTS suggests resection in cases where

the nodule grows more than 2 mm in

maximum diameter even if the nodule

retains a pure ground glass appearance

PET/CT: Studies have shown that the

sensitivity and specificity of PET for the

diagnosis of malignant lesions can reach

87% and 83%, respectively However,

PET also has its shortcomings Firstly,

PET is not sensitive for nodules smaller

than 8 - 10 mm in diameter For patients

with in situ adenocarcinoma, carcinoids and mucinous adenocarcinoma, PET may provide a false negative result, and false positive findings may occur in patients

(sarcoidosis or rheumatoid nodules) or in

a status of infection (fungal or mycobacterial infections) [5, 6]

* Liquid biopsy:

Liquid biopsy, which analyzes biological fluids especially blood specimen to detect and quantify circulating cancer biomarkers, have been rapidly introduced and represents

a promising potency in clinical practice of lung cancer diagnosis and prognosis Unlike conventional tissue biopsy, liquid biopsy is non-invasive, safe, simple in procedure, and is not influenced by manipulators’ skills Notably, some circulating cancer biomarkers are already detectable in disease with low-burden, making liquid biopsy feasible in detecting early stage lung cancer [7, 8] Currently, varieties of circulating cancer biomarkers are available for liquid biopsy including tumor-associated antigens (TAAs), tumor-associated autoantibodies (TAAbs), circulating tumor cells (CTCs), circulating tumor DNA (ctDNA), microRNA (miRNA),

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exosomes and so on TAA markers

detectable in serum like carcinoembryonic

antigen (CEA), carbohydrate antigen (CA)

125, CA199, neuron specific enolase

(NSE), cytokeratin 19 fragment 21-1

(Cyfra 21-1) and squamous cell carcinoma

(SCC) are hard to be used in detection

of early lung cancer with poor sensitivity

and specificity However, serum TAAbs,

autoantibodies against overexpressed,

mutated, misfolded, or aberrant autologous

cellular antigens, may be associated with

unique advantages in identifying individuals

with early lung cancer That has been

theoretically supported for reasons, which

include: immuno-surveillance occurs in

the early phase of cancer immuno-editing

process and autoantibodies may be

detectable in early stage of lung cancer;

TAAbs can be present at high titers even

tumor mass is low and are stable in blood

CTCs are cancer cells directly shed off

from primary tumor sites or metastatic

sites and float in the circulation, which can

be isolated as either single cells or

clusters Ct-DNA is cell-free fragments of

DNA shed into the bloodstream by tumor

cells undergoing necrosis, apoptotic or

active secretion events It is tumor specific

and provides molecular clues about

fragmented DNAs of tumor cells and

their specific mutations Quantitative and

qualitative analysis respectively on the

amount and biological characteristics of

ct-DNA provide real-time evaluations for

diagnostic and prognostic assessments

There is some other source of liquid

considered for early detection of lung

cancer likes exosomes, MiRNAs and so

on [7]

* Bronchoscopy:

Development of technologies like virtual bronchoscopy (VB), electromagnetic navigation bronchoscopy (ENB), ultra-miniature (UM) radial probe EBUS (RP-EBUS) and ultrathin bronchoscopes has been a boon for bronchoscopists [9]

- Traditional flexible bronchoscopy: Many

studies have proved that this method has

a low sensitivity of the lesion with the size less than 2 cm, especially when the lesion

is peripheral [9]

- Virtual bronchoscopy and virtual

bronchoscopy navigation: VB utilizes

non-contrast CT of the chest to generate three-dimensional virtual image of the airways, which closely mimics the actual airways As selection of endobronchial pathway to the lesion can be a potential major source of error in reaching a peripheral lesion VB guidance can be very useful in selecting the appropriate airway Virtual bronchoscopic navigation (VBN) involves navigation to the peripheral lesion-using pathway based on airways leading to lesion planned using VB and simultaneous aligning and superimposition

of virtual views on the actual bronchoscopic views [9]

- Ultrathin bronchoscopy: Small

bronchoscopes with an outer diameter of 2.8 - 3.5 mm are considered ultrathin although a formal definition doesn’t exist The small size of ultrathin bronchoscopes allows better maneuverability and they can visualize deeper into the tracheobronchial tree and can reach up to the 6 - 8 generation bronchi The ultrathin bronchoscopes are usually used with image guidance technology

to reach close to the peripheral lesions [9]

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- Radial probe EBUS: The UM

RP-EBUS has a 20 MHz transducer at the tip

which rotates 360° perpendicular to the

direction of insertion and obtains real-time

high-resolution images of the structures

surrounding the airways The RP-EBUS

can be inserted directly through the

working channel of bronchoscopes or can

be used with a guide system or through

extended working channel (EWC) of

electromagnetic navigation systems into

the target bronchus to confirm appropriate

localization of the area of interest Once

the lesion is confirmed, the guide system

is fixed in place and RP-EBUS is removed

and various sampling instruments can be

advanced through the guide system to

sample the lesion Based on systemic

reviews and meta-analysis, the overall

sensitivity of RP-EBUS for diagnosis of

peripheral lesions is around 70% although

there is considerable heterogeneity in

nodule characteristics and variable use of

additional image guiding technology in

included studies Major limitation of the

technique is operator dependence [9]

bronchoscopy: The ENB system works

similar to the global positioning system

(GPS) of the vehicles Like VB, the ENB

technology requires thin-section CT to

create a virtual bronchial tree This CT is

performed prior to the procedure The

lesion is reviewed in the axial, sagittal,

and coronal planes and marked as the

target Endobronchial pathways to the

lesion are planned and marked using the

virtual airways Many of the studies of

ENB are small non-randomized single

center studies with yield diagnostic yields

ranging from 63% to 85% Significant

factors associated with higher sensitivity were larger nodule size, presence of bronchus sign, nodule visualization with RP-EBUS and so on [9]

* CT-guided fine-needle aspiration biopsy (FNAB):

FNAB is a common method for lung tissue biopsies in clinical settings, particularly for SPNs located close to the chest wall The diagnostic accuracy mainly depends

on an operator’s positioning and puncturing skills, in addition to the pathology technical level that may have a certain impact on the results With the established role of

CT screening for lung cancer, and the broad application of high-resolution CT, the SPN are increasingly detected In recent years, an important type of pulmonary nodules has gradually increased, namely the subcentimeter nodules, which refer to those with a diameter < 8 mm Although most SPN is benign, the pathology of the nodule is crucial to a patient with a history

of cancer even if the SPN is small and peripheral FNAB is a minimally invasive diagnostic method, with a high positive diagnostic rate, less injury and low cost;

so, it has been widely used in the routine diagnosis of SPN Diagnosis by FNAB on small nodules has the following features:

- Wide adaptation range: Except for central type lesions, the diagnostic rate of bronchoscopy on the peripheral type and diffuse lesions is little while FNAB can be applied both in central type lesions or peripheral type and diffuse lesions, as long as there is no apparent adhesion in blood vessels

- FNAB has a high accuracy: For lesions about 0.5 - 1 cm, it can also successfully conduct biopsy under CT guidance

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- High diagnostic accuracy: FNAB is

a well-established, useful procedure

However, the diagnostic accuracy of

FNAB depends on the size and location

of the lesion, as well as the guidance

technique, and decreases from over 90%

to 25% when the malignant nodule is

small (< 1 cm), and to 70% when the

lesion is benign

- High safety: Although FNAB is a safe

and reliable examination method, it is still

a traumatic investigation, so there are still

some complications The main complications

of FNAB mainly include pneumothorax

and haemorrhage According to literature

reports, the incidence of pneumothorax is

about 10 - 40% while the incidence of

pulmonary injury is about 26 - 33% [10]

* Surgery:

In the case of a high probability of

malignant pulmonary nodules (> 60 - 70%),

video-assisted thoracoscopic surgery

(VATS) is the recommended strategy, for

it satisfies the needs of both diagnosis

and further treatment With a benign result

from intraoperative frozen pathology,

only wedge resection will be needed

For malignant pathological findings,

surgical resection should be selected in

combination with systematic lymph node

dissection [10]

CONCLUSSIONS

The management of SPNs involves

both clinical and paraclinical assessment

including risk assessment, morphology

and histopathology of the nodule To

assess each characteristic, doctors should

apply different methods, with their own

advantages and disadvantages Full use

of newer techniques should play an important role in diagnosis and management

of SPNs

REFERENCES

1 Zhou Z, Zhan P, Jin J et al The imaging

of small pulmonary nodules Translational

Lung Cancer Research 2017, 6 (1), pp.62-67

2 Kikano G.E, Fabien A, Schilz R Evaluation

of the solitary pulmonary nodule American Family Physician 2015, 92 (12), pp.1084-1092

3 NCCN Lung Cancer Screening Panel Members Lung cancer screening, Version

3.2018 Journal of the National Comprehensive Cancer Network 2018, 16 (4), pp.412-441

4 Gould M.K, Donigton J, Lynch W.R et al

Evaluation of individuals with pulmonary nodules: When is it lung cancer? Chest

2013, 143 (5), pp.93-120

5 MacMahon H, Naidich D.P, Goo J.M et

al Guidelines for management of incidental

pulmonary nodules detected on CT images: From the Fleischner Society Radiology 2017,

284 (1)

6 Ito M, Myiata Y, Okada M Management

pathways for solitary pulmonary nodules Journal of Thoracic Disease 2018, 10 (7), pp.860-866

7 Liang W, Zhao Y, Hoang W Liquid

biopsy for early stage lung cancer Journal of Thoracic Disease 2018, 10 (7), pp.876-881

8 Castro-Giner F, Gkoutela S, Donato C et

al Cancer diagnosis using a liquid biopsy:

Challenges and expections Diagnostics (Basel) 2018, 8 (2), p.31

9 Dhillon S.S and Harris K Bronchoscopy

for the diagnosis of peripheral lung lesions Journal of Thoracic Disease 2017, 9 (10), pp.1047-1058

10 Xu C, Hao K, Song Y et al Early

diagnosis of solitary pulmonary nodules Journal

of Thoracic Disease 2013, 5 (6), pp.830-840.

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