Original Report

Diagnostic Performance of a Sonographic Volume and Solid

Vascular Tissue Score (VSVTS) for Preoperative Risk Assessment
of Pediatric and Adolescent Adnexal Masses
s Roca MD 1,2, Ebtehaj D. Alshehri MD 1,2, Hanna R. Goldberg MD, MS 3,
Lara Farra
Afsaneh Amirabadi PhD 1, Sari Kives MD 4,5, Lisa Allen MD 4,5, Oscar M. Navarro MD 1,2,
Christopher Z. Lam MD 1,2,*
1
Department of Diagnostic Imaging, The Hospital for Sick Children, Toronto, Ontario, Canada
2
Department of Medical Imaging, University of Toronto, Toronto, Ontario, Canada
3
Faculty of Medicine, University of Toronto, Toronto, Ontario, Canada
4
Section of Gynecology, The Hospital for Sick Children, Toronto, Ontario, Canada
5
Department of Obstetrics and Gynecology, University of Toronto, Ontario, Canada

a b s t r a c t
Study Objective: To evaluate the diagnostic performance of a Volume and Solid Vascular Tissue Score (VSVTS) for preoperative risk
assessment of pediatric and adolescent adnexal masses.
Design: A retrospective cohort study comprised of all female individuals who presented with an adnexal mass that was managed surgically
between April 2011 and March 2016.
Setting: The Hospital for Sick Children (Toronto, Ontario, Canada).
Participants: Female individuals 1e18 years of age who presented to a large tertiary pediatric hospital with an adnexal mass that was
managed surgically.
Main Outcome Measures: Main outcome measures included diagnostic performance of the VSVTS for malignancy via sensitivity, specificity,
positive predictive value (PPV), negative predictive value (NPV), positive likelihood ratio (LRþ), negative likelihood ratio (LR), and
receiver operating characteristic area-under-the-curve (AUC) analysis.
Results: A total of 179 masses in 169 subjects were included. The malignancy rate was 10.6%. The AUC for the VSTVS was 0.919. A VSTVS cut-
off value of 4 achieved a sensitivity of 79% (95% CI 0.54-0.93), specificity of 88% (95% CI 0.82-0.93), PPV of 0.44 (95% CI 0.33-0.56), NPV of
0.97 (95% CI 0.94-0.99), LRþ of 6.77 (95% CI 4.18-10.97), and LR of 0.24 (95% CI 0.10-0.57).
Conclusions: A sonographic scoring system based on the volume and presence of solid vascular tissue improves PPV for preoperative risk
stratification of adnexal masses in the pediatric and adolescent population compared to existing ultrasound-only approaches. Further
prospective research is needed to determine how best to incorporate components of such scoring systems into clinical management
algorithms.
Key Words: Adnexal mass, Benign, Malignancy, Oophorectomy, Ovarian cystectomy, Preoperative procedure, Risk stratification,
Sonography

Introduction A previous retrospective study conducted at our insti-

The incidence of adnexal masses in girls and adolescents is
approximately 2.6/100,000 girls per year.1 Up to 10-20% of
surgically managed masses are malignant.2 Accurate preop-
erative risk assessment is critical, as it affects the surgical
approach.3 For presumed benign masses that require inter-
vention, a conservative approach with laparoscopic cys-
tectomy is preferred. Malignancies, on the other hand,
usually require an open laparotomy with oophorectomy,
which has a consequent impact on patient fertility.2,3 None-
theless, the optimal method for preoperative risk assessment
in the pediatric and adolescent population remains elusive.
None of the authors have any conflicts of interest or financial ties to disclose.
The authors report no funding for this work.
* Address correspondence to: Christopher Z. Lam, MD, Department of Diagnostic
Imaging, The Hospital for Sick Children, 555 University Avenue, Toronto, Ontario
M5G 1X8, Canada; Phone: (416) 823-2887; fax: (416) 813-8389
E-mail address: Christopher.lam@sickkids.ca (C.Z. Lam).
1083-3188/$ - see front matter Ó 2020 North American Society for Pediatric and Adolescent Gynecology. Published by Elsevier Inc.
https://doi.org/10.1016/j.jpag.2020.11.017
tution showed that malignant masses can be preoperatively
identified using a threshold of greater than 8 cm in size and
presence of “complex” features by ultrasound. These criteria
yielded a negative predictive value (NPV) of 100% but a
positive predictive value (PPV) of only 37.1%.3 Therefore,
relying on such criteria alone would lead to a high propor-
tion of undesirable oophorectomies for benign lesions.
Multiple more-complicated risk assessment algorithms
have been studied in attempts to improve the preoperative
PPV.2e10 Most recently, we attempted replication of the
Decision Tree System (DTS) proposed by Stankovic et al,4
which in their study demonstrated a preoperative NPV of
99% and PPV of 86%. The results of our replication attempt
were less encouraging, as we achieved an NPV of 98% but a
PPV of only 30% in our population.4
Concurrently, we hypothesized that a scoring system
accounting for the vascularity of adnexal masses as has
been introduced in adult algorithms, such as in the IOTA

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378
L. Farra
rules and O-RADS,11,12 might improve the PPV. These algo-
rithms incorporate a subjective degree of vascularity in risk
assessment, whereas in our experience any solid vascular
tissue alone increases malignancy risk. The purpose of this
study was therefore to evaluate the diagnostic performance
of a preoperative sonographic adnexal mass scoring system
based on mass volume and amount of solid vascular tissue
in the pediatric and adolescent population.
Materials and Methods
Patient Population
This is a retrospective study of all female individuals 1-
18 years of age presenting with an adnexal mass to The
Hospital for Sick Children (Toronto, Ontario, Canada) be-
tween April 2011 and March 2016 and was conducted with
approval of our institutional Research Ethics Board. Patients
who did not receive surgical management or preoperative
ultrasound that included spectral Doppler were excluded.
The inclusion dates mirror a similar cohort used in previous
risk stratification studies from our institution,4 which al-
lows for direct comparisons of diagnostic performance. A
separate representative training cohort was derived from
ultrasound examinations of surgically managed adnexal
masses in patients presenting between March 2016 and
March 2019.
Ultrasound Technique
All ultrasound studies were performed by dedicated pe-
diatric sonographers with a transabdominal approach. All
examinations included gray scale, color Doppler, and spectral
Doppler performed on Samsung RS80 A (Samsung Medison
Corp., Korea), Philips iU22 (Philips Ultrasound, USA), Toshiba
Aplio 500, or Toshiba Aplio XG (Toshiba Medical Systems
Corp., Japan) ultrasound machines using a low-frequency
convex-array transducer (1-7 MHz Samsung CA1-7A, 2-
5 MHz Philips C5-2, 2-6 MHz Toshiba PVT-375BT) and in
some cases a high-frequency linear-array transducer (3-
12 MHz Samsung L3-12A, 3-12 MHz Philips L12-3, 7-14 MHz
Toshiba PLT-1005BT). All ultrasound machines were repre-
sented in both the test and training cohorts.
Scoring System: Volume and Solid Vascular Tissue Score
All adnexal masses were assigned a sonographic volume
score (0-3) and solid vascular score (0-3) (Table 1). Thick-
ness of at least 3 mm with confirmation of flow via spectral
Doppler was required to qualify as solid vascular tissue (Fig
1). Therefore, thin septations with flow did not qualify. The
volume and solid vascular scores were summed for each
case to create a combined Volume and Solid Vascular Tissue
Score (VSVTS) ranging from 0 to 6. All other ultrasound
features were not considered in this study.
Ultrasound Analysis
Two in-training pediatric radiology fellows (LFR and EA)
who were blinded to pathologic results independently
analyzed a training cohort of 21 representative cases that
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s Roca et al. / J Pediatr Adolesc Gynecol 34 (2021) 377e382
Table 1
Volume and Solid Vascular Tissue Score (VSVTS)
Solid vascular tissue score*
1. No solid vascular tissue
2. Solid vascular tissue !25% of lesiony
3. Solid vascular tissue 25-50% of lesion
4. Solid vascular tissue O50% of lesion
Volume Scorez
1. !100 mL
2. 100-250 mL
3. 250-500 mL
4. O500 mL
* Requirement: presence of spectral Doppler flow.
y
Minimum size of O3 mm with confirmation of flow with spectral Doppler to
qualify.
z
Volume 5 length  height  width  0.523.
included a variety of adnexal mass sizes and pathologies,
which were separate from the study cohort. Subsequently,
the same 2 in-training pediatric radiology fellows sepa-
rately analyzed all presenting ultrasounds in the study
cohort, again blinded to the pathologic results. All cases in
the training cohort and discrepancies in the study cohort
were reviewed with 2 staff pediatric radiologists (CZL and
OMN) to achieve group consensus agreement, for training
purposes and for final consensus interpretation,
respectively.
Statistical Analysis
All analyses were carried out with SAS University Edition
(Base SAS, SAS Institute Inc, Cary, NC). Diagnostic perfor-
mance was assessed using sensitivity, specificity, PPV, NPV,
positive likelihood ratio (LRþ), and negative likelihood ratio
(LR), considering P ! .05 (2-tailed) as statistically signif-
icant. Receiver operating characteristic (ROC) curves and
area-under-the-curve (AUC) values were also obtained,
with optimum cut-off values determined by the Youden
index. Final pathologic diagnosis was used as the reference
standard. Interobserver variability was assessed using k
statistics with quadratic weighting. The k value was inter-
preted according to Landis and Koch13 with 0.0-0.20 rep-
resenting slight agreement, 0.21-0.40 fair agreement, 0.41-
0.6 moderate agreement, 0.61-0.80 good agreement, and
0.81-1.00 very good agreement.
Results
In total, 169 patients with 179 masses with surgical
management of adnexal masses were identified, with 10.6%
of the lesions being malignant. The mean age of the study
population was 13.0  3.4 years. 73.7% of the study popu-
lation was postmenarchal. All pathologic diagnoses are lis-
ted in Table 2.
The distribution of pathologic entities per VSVTS is
depicted in Table 3. The distribution of pathologic entities
per volume score and solid vascular tissue score is available
in Supplemental Table 1.
The sensitivity, specificity, PPV, NPV, LRþ, and LR for
malignancy for each component of the scoring system is
shown in Table 4. A volume score of $2 showed a PPV of
 s Roca et al. / J Pediatr Adolesc Gynecol 34 (2021) 377e382
L. Farra 379
web 4C=FPO

Fig. 1. Solid vascular tissue score examples on color Doppler (left) and corresponding spectral Doppler images (right). (A) Score of 0 for a cystic lesion with no internal flow. Note
that some flow is seen in the adjacent normal ovarian tissue (arrow). This was a mature teratoma. (B) Score of 1 for a cystic lesion with a hyperechoic papillary projection comprising
!25% of the lesion size and with some internal flow. This was a mature teratoma. (C) Score of 2 for a cystic lesion with a central solid component comprising 25-50% of the lesion
size and with internal flow. This was an immature teratoma. (D) Score of 3 for a mixed solid-cystic lesion with solid component comprising O50% of the lesion and with internal
flow. This was a juvenile granulosa cell tumor.

0.19 (95% CI 0.15-0.22), NPV of 0.98 (95% CI 0.92-0.99), LRþ
of 2.00 (95% CI 1.59-2.51), and LR of 0.19 (95% CI 0.05-
0.71). The presence of any solid vascular tissue defined by
scores 1, 2, or 3 showed a PPV of 0.35 (95% CI 0.28-0.44),
0.52 (95% CI 0.36-0.68), and 0.67 (95% CI 0.43-0.84), NPV of
0.98 (95% CI 0.94-0.99), 0.96 (95% CI 0.92-0.97), and 0.95
(95% CI 0.91-0.96), LRþ of 4.65 (95% CI 3.27-6.61), 9.24 (95%
CI 4.75-17.99), and 16.95 (95% CI 6.47-44.37), and LReof 0.13
(95% CI 0.04 -0.48), 0.40 (95% CI 0.22-0.71), and 0.49 (95% CI
0.30-0.79), respectively. A VSVTS of $4 showed a PPV of
0.44 (95% CI 0.33-0.56), NPV of 0.97 (95% CI 0.94-0.99), LRþ
of 6.77 (95% CI 4.18-10.97), and LReof 0.24 (95% CI 0.10-
0.57). The ROC AUCs for the volume score, solid vascular
tissue score, and VSVTS were 0.734, 0.890, and 0.919
respectively (Fig. 2).
Table 2
Pathology of Adnexal Masses (n 5 179)
Interrater reliability via weighted k-statistics showed
very good agreement for the volume score, solid vascular
tissue score, and VSVTS with k values of 0.998 (95% CI
0.995-1.002), 0.894 (95% CI 0.829-0.959), and 0.969 (95% CI
0.950-0.988), respectively.
Targeted review of the 4 cases misclassified as benign
using a VSVTS of 4 revealed 2 mixed germ cell tumors, 1
borderline tumor, and 1 juvenile granulosa cell tumor. The 2
mixed germ cell tumors had a volume score of 3 and solid
vascular tissue score of 0, showing apparent avascular
heterogeneous solid tissue occupying up to 50% of the
lesion. The borderline tumor similarly had a volume score of
3 and solid vascular tissue score of 0. It was a O20-cm
multicystic lesion with apparent avascular papillary pro-
jections. The juvenile granulosa cell tumor was a predom-
inantly solid vascular mass with volume of 95.3 mL, which
classified as a volume score of 0 and solid vascular score
of 3.

Benign 160 (89.4%) Discussion

Mature teratoma 72 (40.2%)
Cystadenoma 50 (28.0%)
Paratubal cyst 20 (11.2%) In this study, we evaluate the diagnostic performance of
Hemorrhagic cyst 8 (4.4%) a sonographic volume and solid vascular tissue score for
Simple/follicular cyst 4 (2.2%)
preoperative risk stratification of adnexal masses in the
Benign sex cord stromal tumor 3 (1.7%)
Corpus luteum 2 (1.1%) pediatric and adolescent population. The major finding of
Ovarian edema 1 (0.5%) our study is that the addition of a solid vascular tissue score
Malignant 19 (10.6%)
to preoperative assessment shows incremental benefit to
Borderline tumor 4 (2.2%)
Immature teratoma 3 (1.7%) PPV and LR þ while maintaining reasonable NPV and
Mixed germ cell tumor 3 (1.7%) LRefor prediction of malignancy in pediatric and adolescent
Juvenile granulosa cell tumor 2 (1.1%)
adnexal masses.
Dysgerminoma 2 (1.1%)
Sertoli-Leydig tumor 2 (1.1%) Multiple ultrasound-based scoring systems for preoper-
Mucinous carcinoma 1 (0.5%) ative risk assessment of adnexal masses in the pediatric
Neuroendocrine tumor 1 (0.5%)
population have been proposed.2e5,7,9 Although they all
Yolk sac tumor 1 (0.5%)
achieve acceptable NPV, the PPV has been difficult to

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L. Farra

Table 3 optimize, ranging from 13.0% to 37.1%. So far, only by

Distribution of Tumor Histology by VSVTS
VSVTS Benign
score
0 n 5 49
Mature teratoma 5 19
Cystadenoma 5 13
Paratubal cyst 5 10
Hemorrhagic cyst 5 4
Simple/follicular cyst 5 2
Corpus luteum 5 1
1 n 5 32
Mature teratoma 5 16
Cystadenoma 5 11
Hemorrhagic cyst 5 2
Paratubal cyst 5 2
Simple/follicular cyst 5 1
2 n 5 16
Mature teratoma 5 6
Cystadenoma 5 6
Paratubal cyst 5 2
Corpus luteum 5 1
Hemorrhagic cyst 5 1
3 n 5 44
Mature teratoma 5 19
Cystadenoma 5 15
Paratubal cyst 5 6
Simple/follicular cyst 5 1
Hemorrhagic cyst 5 1
Ovarian edema 5 1
Benign sex cord stromal
tumor 5 1
4 n 5 14
Mature teratoma 5 10
Cystadenoma 5 4
5 n52
Mature teratoma 5 1
Benign sex cord stromal
tumor 5 1
6 n53
Mature teratoma 5 1
Cystadenoma 5 1
Benign sex cord stromal
tumor 5 1
VSVTS, Volume and Solid Vascular Tissue Score.
including additional clinical information has PPV been able
Malignant to be improved. A scoring system by Loh et al7 combining
the presence of sex hormoneerelated symptoms with ul-
n50
trasound features similar to those in our study (size of solid
component and presence of vascular flow) was able to
achieve an NPV of 98.5% and a PPV of 90.9%. An algorithm
developed by Stankovic et al5 that involved segregation of
patients by presenting symptoms combined with morpho-
n50 logic ultrasound features achieved a NPV of 99% and PPV of
86%. However, we were not able to replicate this latter study
retrospectively in our own population.4 Nonetheless, the
literature to date seems to imply that preoperative risk
stratification based on ultrasound features alone has a
n50
limitation in specificity for malignancy, which could lead to
excessive oophorectomies for benign tumors.
Part of the challenge in the pediatric and adolescent
population in this regard is the high proportion of germ
n54 cell tumors in premenarchal girls, the majority of which
Mixed germ cell tumor 5 2
are benign.14,15 Large benign mature cystic teratomas have
Borderline tumor 5 1
Juvenile granulosa cell overlapping imaging appearances with malignant germ
tumor 5 1 cell tumors, and can lead to suboptimal specificity and
PPV, particularly when attempting to apply algorithms
developed in adult populations to children. In our expe-
rience, these large teratomas have little to no detectable
n55
Borderline tumor 5 3
spectral Doppler flow within solid-appearing components
Immature teratoma 5 1 despite their large size and complexity. While studied in
Mixed germ cell tumor 5 1 adults, few data are available regarding the utility of
n55
Dysgerminoma 5 1
assessing vascularity of adnexal masses in the pediatric
Juvenile granulosa cell population. Depoers et al2 recently applied the Interna-
tumor 5 1 tional Ovarian Tumor Analysis (IOTA) rules that included
Sertoli-Leydig tumor 5 1
Mucinous carcinoma 5 1
subjective assessments of color Doppler signal strength
Neuroendocrine tumor 5 1 into an algorithm, which apparently did not contribute to
n55 risk analysis. Our sense, however, was that rather than the
Immature teratoma 5 2
Dysgerminoma 5 1
strength of color Doppler signal as validated in adults,
Yolk sac tumor 5 1 even small amounts of tissue with flow could portend
Sertoli-Leydig tumor 5 1 malignancy or higher-grade, given our unique population.
This is supported by the work by Loh et al,7 in which a
binary discriminator of presence of absence of vascular

Table 4
Statistical Analysis for Volume, Solid Vascular Tissue, and Total Score

Score Sensitivity [95% CI] Specificity [95% CI] PPV [95% CI] NPV [95% CI] LRþ [95% C] LRe [95% CI]

Volume score $0 1.00 [0.82-1.00] 0.00 [0.00-0.22] 0.10 [1.00-1.00] e [e] 1.00 [0.10-0.10] e [e]
$1 0.95 [0.74-1.00] 0.34 [0.26-0.41] 0.14 [0.12-0.16] 0.98 [0.89-0.99] 1.43 [1.23-1.67] 0.16 [0.02-1.06]
$2 0.89 [0.67-0.99] 0.55 [0.47-0.63] 0.19 [0.15-0.22] 0.98 [0.92-0.99] 2.00 [1.59-2.51] 0.19 [0.05-0.71]
3 0.68 [0.43-0.87] 0.67 [0.59-0.74] 0.20 [0.14-0.26] 0.95 [0.90-0.97] 2.10 [1.44-3.07] 0.47 [0.24-0.91]
Solid vascular tissue score $0 1.00 [0.82-1.00] 0.00 [0.00-0.23] 0.11 [0.10-0.10] e [e] 1.00 [1.00-1.00] e [e]
$1 0.89 [0.67-1.00] 0.81 [0.74-0.86] 0.35 [0.28-0.44] 0.98 [0.94-0.99] 4.65 [3.27-6.61] 0.13 [0.04-0.48]
$2 0.63 [0.38-0.84] 0.93 [0.88-0.96] 0.52 [0.36-0.68] 0.96 [0.92-0.97] 9.24 [4.75-17.99] 0.40 [0.22-0.71]
3 0.53 [0.29-0.75] 0.97 [0.93-0.99] 0.67 [0.43-0.84] 0.95 [0.91-0.96] 16.95 [6.47-44.37] 0.49 [0.30-0.79]
VSVTS $0 1.00 [0.82-1.00] 0.00 [0.00-0.22] 0.10 [0.10-0.10] e [e] 1.00 [1.00-1.00] e [e]
$1 1.00 [0.82-1.00] 0.31 [0.24-0.39] 0.15 [0.13-0.16] 1.00 [e] 1.46 [1.31-1.61] 0.00 [e]
$2 1.00 [0.82-1.00] 0.52 [0.43-0.59] 0.19 [0.17-0.22] 1.00 [e] 2.06 [1.76-2.42] 0.00 [e]
$3 1.00 [0.82-1.00] 0.61 [0.53-0.69] 0.23 [0.19-0.27] 1.00 [e] 2.59 [2.13-3.14] 0.00 [e]
$4 0.79 [0.54-0.93] 0.88 [0.82-0.93] 0.44 [0.33-0.56] 0.97 [0.94-0.99] 6.77 [4.18-10.97] 0.24 [0.10-0.57]
$5 0.53 [0.29-0.75] 0.97 [0.93-0.99] 0.67 [0.43-0.84] 0.95 [0.92-0.96] 17.16 [6.55-44.93] 0.49 [0.30-0.79]
6 0.26 [0.09-0.51] 0.98 [0.95-0.99] 0.63 [0.30-0.86] 0.92 [0.89-0.93] 14.30 [3.71-55.1] 0.75 [0.57-0.98]

CI, confidence interval; LRþ, positive likelihood ratio; LR, negative likelihood ratio; NPV, negative predictive value; PPV, positive predictive value; VSVTS, Volume and Solid
Vascular Tissue Score.

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 s Roca et al. / J Pediatr Adolesc Gynecol 34 (2021) 377e382
L. Farra 381
web 4C=FPO

Fig. 2. Receiver operating characteristic curves for the volume score (A), solid vascular tissue score (B), and total Volume and Solid Vascular Tissue Score (VSVTS) (C) with area under
the curve (AUC) provided. Cut-off value based on the Youden index (red “ 5 ” sign) for the volume score (A) is 2 (sensitivity 89%, specificity 55%), for the solid vascular tissue score
(B) is 1 (sensitivity 89%, specificity 81%), and for the total VSTVS (C) is 4 (sensitivity 79%, specificity 88%).

flow contributed to assessment. Therefore, we hypothe-
sized that the degree of solid vascular tissue rather than
the morphology itself or subjective strength of vascularity
could help with PPV and LRþ.
The simplified sonographic scoring system tested in this
work using only size and presence of solid vascular tissue
criteria demonstrates slightly higher PPV of 0.44 and
reasonable NPV of 0.97 as compared to that of other
ultrasound-only scoring systems, including comparison
with more complicated algorithms.2e4,9 This further sup-
ports the utility of incorporating vascularity into the eval-
uation of adnexal masses.
Although we achieved our goal of improving PPV, it
was also important for us to look more closely at the 4
cases misclassified as benign when using a VSVTS of $4
as the sole criterion, as diagnostic tests are always a
balance between sensitivity and specificity. These 4 cases
all had other features that made them suspicious for
malignancy, whether it was the 2 mixed germ cell tumors
and 1 borderline tumor that each contained a significant
proportion of heterogenous solid tissue despite apparent
avascularity, or the juvenile granulosa cell tumor that
contained clearly vascular neoplastic tissue but measured
just 5 mL beneath the cut-off to be classified as malig-
nant. Therefore, human judgment still seems to be
important.
Ultimately, our work supports future prospective work
incorporating presence and percentage of solid vascular
tissue into more sophisticated algorithms, which may
further improve preoperative risk stratification, particularly
with inclusion of non-imaging clinical parameters. None-
theless, although the use of structured preoperative algo-
rithms has potential for establishing standardized starting
points, for now a multidisciplinary discussion on a case-by-
case basis with expert consensus likely will continue to be
required.3,13,16
The strength of our study is the sizeable group of surgi-
cally managed patients using a similar cohort as previous
works from our institution, allowing for direct comparison
with other approaches. Limitations relate to the retrospec-
tive review of ultrasound examinations, in which diagnostic
performance can be operator dependent, and the demon-
stration of solid vascularized tissue by spectral Doppler may
have been variable.
Conclusion
A sonographic scoring system based on the volume and
presence of solid vascular tissue improved PPV for preop-
erative risk stratification of adnexal masses in the pediatric
and adolescent population compared to existing
ultrasound-only approaches. Further prospective research
is needed to determine how best to incorporate compo-
nents of such scoring systems into clinical management
algorithms.
Acknowledgments
The authors would like to acknowledge the support from
the Ontasian Imaging Lab (OIL).
Supplementary Data
Supplementary data related to this article can be found at
https://doi.org/10.1016/j.jpag.2020.11.017.
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