Citation: Szadkowska, P.; Roura,
A.-J.; Wojtas, B.; Wojnicki, K.;
Licholai, S.; Waller, T.; Gubala, T.;
Zukowski, K.; Karpeta, M.; Wilkus,
K.; et al. Improvements in Quality
Control and Library Preparation for
Targeted Sequencing Allowed
Detection of Potentially Pathogenic
Alterations in Circulating Cell-Free
DNA Derived from Plasma of Brain
Tumor Patients. Cancers 2022, 14,
3902. https://doi.org/10.3390/
cancers14163902
Academic Editor: Evi S. Lianidou
Received: 4 July 2022
Accepted: 9 August 2022
Published: 12 August 2022
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cancers
Article
Improvements in Quality Control and Library Preparation for
Targeted Sequencing Allowed Detection of Potentially
Pathogenic Alterations in Circulating Cell-Free DNA Derived
from Plasma of Brain Tumor Patients
Paulina Szadkowska
1,2
, Adria-Jaume Roura
1
, Bartosz Wojtas
1
, Kamil Wojnicki
1
, Sabina Licholai
3
,
Tomasz Waller
3
, Tomasz Gubala
3,4
, Kacper Zukowski
3
, Michal Karpeta
5
, Kinga Wilkus
2,5
,
Wojciech Kaspera
6
, Sergiusz Nawrocki
7
and Bozena Kaminska
1,
*
1
Nencki Institute of Experimental Biology, 02-093 Warsaw, Poland
2
Postgraduate School of Molecular Medicine, Medical University of Warsaw, 02-007 Warsaw, Poland
3
Academic Computer Centre CYFRONET AGH, 30-950 Krakow, Poland
4
Sano Centre for Computational Medicine, 30-054 Krakow, Poland
5
Regional Science and Technology Centre, 26-060 Podzamcze, Poland
6
Department of Neurosurgery, Medical University of Silesia, Regional Hospital, 41-200 Sosnowiec, Poland
7
Department of Oncology, University of Warmia and Mazury in Olsztyn, 10-228 Olsztyn, Poland
* Correspondence: b.kaminska@nencki.edu.pl
Simple Summary: Malignant brain tumors present an enormous challenge due to their genetic
heterogeneity, and the difficulties in accessing them impede a precise diagnosis. Numerous genetic
alterations have been described, and some of them can assist in personalized therapy for glioma
patients. Brain biopsy is an invasive procedure with potentially deleterious complications. Liquid
biopsy from a patient’s plasma may provide a less invasive method for diagnosis and personalized
therapy selection. We performed targeted next-generation sequencing of tumors and circulating
cell-free DNA (ccfDNA) from 84 brain tumor patients. We detected tumor-specific genetic alterations
in ccfDNA in 5 out of 80 glioma patients and potentially pathogenic alterations in ccfDNA from
the plasma of 29 out of 80 glioma patients. Despite a low efficacy, with further improvements, the
detection of genetic alterations in ccfDNA holds promise for noninvasive diagnosis, which may
revolutionize personalized therapy for these deadly tumors.
Abstract: Malignant gliomas are the most frequent primary brain tumors in adults. They are geneti-
cally heterogenous and invariably recur due to incomplete surgery and therapy resistance. Circulating
tumor DNA (ctDNA) is a component of circulating cell-free DNA (ccfDNA) and represents genetic
material that originates from the primary tumor or metastasis. Brain tumors are frequently located in
the eloquent brain regions, which makes biopsy difficult or impossible due to severe postoperative
complications. The analysis of ccfDNA from a patient’s blood presents a plausible and noninvasive
alternative. In this study, freshly frozen tumors and corresponding blood samples were collected
from 84 brain tumor patients and analyzed by targeted next-generation sequencing (NGS). The cohort
included 80 glioma patients, 2 metastatic cancer patients, and 2 primary CNS lymphoma (PCNSL)
patients. We compared the pattern of genetic alterations in the tumor DNA (tDNA) with that of
ccfDNA. The implemented technical improvements in quality control and library preparation allowed
for the detection of ctDNA in 8 out of 84 patients, including 5 out of 80 glioma patients. In 32 out of
84 patients, we found potentially pathogenic genetic alterations in ccfDNA that were not detectable
in tDNA. While sequencing ccfDNA from plasma has a low efficacy as a diagnostic tool for glioma
patients, we concluded that further improvements in sample processing and library preparation can
make liquid biopsy a valuable diagnostic tool for glioma patients.
Keywords: liquid biopsy; glioma; circulating tumor DNA; ccfDNA; targeted NGS
Cancers 2022, 14, 3902. https://doi.org/10.3390/cancers14163902 https://www.mdpi.com/journal/cancers