Unveiling the potential application of intraoperative brain smear for brain tumor diagnosis in low-middle-income countries: A comprehensive systematic review
- Department of Surgery, Section of Neurosurgery, Aga Khan University Hospital, Karachi, Pakistan
- Medical School, Aga Khan University Hospital, Karachi, Pakistan,
- Duke University School of Medicine, Durham, North Carolina, United States,
- Department of Pathology, Aga Khan University Hospital, Karachi, Pakistan.
S. Ather Enam, Department of Surgery, Section of Neurosurgery, Aga Khan University Hospital, Karachi, Pakistan.
DOI:10.25259/SNI_491_2023Copyright: © 2023 Surgical Neurology International This is an open-access article distributed under the terms of the Creative Commons Attribution-Non Commercial-Share Alike 4.0 License, which allows others to remix, transform, and build upon the work non-commercially, as long as the author is credited and the new creations are licensed under the identical terms.
How to cite this article: Muhammad Shakir1, Ahmed Altaf1, Hawra Hussain2, Syed Muhammad Aqeel Abidi2, Zoey Petitt3, Mahnoor Tariq1, Ahmed Gilani4, S. Ather Enam1. Unveiling the potential application of intraoperative brain smear for brain tumor diagnosis in low-middle-income countries: A comprehensive systematic review. 08-Sep-2023;14:325
How to cite this URL: Muhammad Shakir1, Ahmed Altaf1, Hawra Hussain2, Syed Muhammad Aqeel Abidi2, Zoey Petitt3, Mahnoor Tariq1, Ahmed Gilani4, S. Ather Enam1. Unveiling the potential application of intraoperative brain smear for brain tumor diagnosis in low-middle-income countries: A comprehensive systematic review. 08-Sep-2023;14:325. Available from: https://surgicalneurologyint.com/?post_type=surgicalint_articles&p=12530
Background: Immediate intraoperative histopathological examination of tumor tissue is indispensable for a neurosurgeon to track surgical resection. A brain smear is a simple, rapid, and cost-effective technique, particularly important in the diagnosis of brain tumors. The study aims to determine the effectiveness of intraoperative brain smear in the diagnosis of brain tumors in low- and middle-income countries (LMICs), while also evaluating its sensitivity, specificity, positive predictive value (PPV), negative predictive value (NPV), and overall accuracy.
Methods: A comprehensive search of the literature was conducted using PubMed, Scopus, and Google Scholar. The retrieved articles were independently screened by two reviewers. The data was extracted, processed, and organized using Microsoft Excel.
Results: A total of 59 out of 553 articles screened were included in the final analysis. The sensitivity and specificity of the intraoperative smear of brain tumors were found to be over 90% in most studies. The PPV was consistently above 90% in 11 studies, reaching 100% in one study and the NPV varied, ranging from 63% to 100%, and the accuracy was found to be >80% in most studies. One recurrent theme in the majority of the included studies was that an intraoperative brain smear is a cost-effective, quick, accessible, and accurate method of diagnosing brain tumors, requiring minimal training and infrastructure.
Conclusion: Intraoperative brain smear is a simple, rapid, cost-effective, and highly sensitive diagnostic modality for brain tumors. It can be a viable and accessible alternative to more traditional methods such as frozen sections and can be incorporated into neurosurgical practice in LMICs as a reliable and efficient diagnostic tool.
Keywords: Brain tumors, Intraoperative brain smear, Low- and middle-income countries
Brain tumors are a group of malignancies that can originate from cells within the brain (primary tumors) or from systemic tumors that have spread to the brain (secondary tumors).[
For a neurosurgeon, an instant intraoperative histopathological examination of tumor tissue is a critical tool to monitor surgical resection by differentiating normal brain histology from a tumor.[
The process of obtaining a frozen section, the gold standard for intraoperative histopathological examination, is time-consuming and can delay surgical treatment. It involves delivering tissue to a laboratory, processing the specimen, preparing slides by technicians, and interpreting the slides by a pathologist.[
Since 1930, when Eisenhardt and Cushing proposed the use of a touch imprint for rapid tumor identification, cytological methods have been utilized to diagnose brain tumors.[
The main goals of intraoperative neuropathologic consultation for neurosurgeons are to guarantee that the diagnostic specimen was collected with the least amount of trauma and to ensure an immediate and appropriate treatment.[
Brain smear techniques are relatively cheap compared to other modalities available and can be conducted within the operating room without any specialized equipment or specialized technicians being involved, which holds advantages for low- and middle-income countries (LMICs).[
The objective of this study is to determine the usefulness of intraoperative brain smears in the diagnosis of brain tumors in LMICs through a systematic review of the existing literature. The review aims to evaluate the sensitivity, specificity, positive predictive value (PPV), negative predictive value (NPV), and accuracy of intraoperative brain smears as a diagnostic tool in LMICs.
This systematic review was conducted following our research protocol, which was based on the research question using population, intervention, control, and outcome. The preferred reporting items for systematic reviews and meta-analyses reporting standards were followed.[
This review analyzes the use of intraoperative brain smears during surgical procedures of brain tumors, both primary and metastatic. Studies eligible for inclusion were observational studies, including cohort studies, and randomized and nonrandomized controlled trials. The literature searched included articles that presented epidemiological, clinical, and laboratory aspects of the use of brain smears during tumor procedures. All age groups were included in this review. Studies were excluded from the study: editorials, case reports, case series (n < 10), studies published as abstracts only, letters to the editor, book chapters, and theses, as well as articles on spine tumors or other brain pathologies.
Final histopathology served as the gold standard test for evaluating diagnostic accuracy. This provided a definitive diagnosis based on tissue examination and has been widely recognized for its reliability and validity. Only studies utilizing the final histopathology report as the reference standard were included in our analysis.
A comprehensive search was conducted across multiple electronic databases, including PubMed, Scopus, and Google Scholar, with no language restrictions. The search encompassed articles from inception to December 25, 2022, and all searches were performed on the same date. We searched for relevant phrases in the Medical Subject Headings database and selected the following free-text terms as keywords: “brain neoplasms” OR “brain tumor*” AND “brain smear” OR “intraoperative cytology” OR “intraoperative squash cytology” OR “imprint cytology” OR “touch cytology” to yield a comprehensive and inclusive dataset. The included studies were searched for forward citations to ensure that all the relevant literature are included in the study. The detailed search strategy for each database is available in the supplementary document.
All retrieved studies’ titles and abstracts were initially screened by two reviewers (SAA and HH) for duplication and relevancy according to our research question. The final study selection was made after an independent review by two reviewers (SAA and HH) of the full texts of all possibly pertinent studies. A consensus was reached by a third author (MS) to settle conflicts.
Study characteristics (study title, authors, date of publication, publication type, study location, and sample size), population characteristics, study objective, advantages of the mentioned brain smear techniques, test characteristics (accuracy, sensitivity, specificity, PPV, and NPV), and study outcomes were extracted from eligible articles. Two authors independently extracted the data (SAA, HH). A third author (MS) corrected errors in data extraction and double-checked the information collected. Two authors (SAA and AA) independently evaluated each study’s quality using the Newcastle–Ottawa scale quality assessment.[
The review underwent rigorous data validation, involving cross-referencing data from multiple sources, applying validation criteria, and resolving discrepancies through reviewer consensus. Data cleaning removed errors and inconsistencies while missing data were managed using the method of exclusion.
The data were processed and analyzed using Microsoft Excel. For ease of reporting and comprehension, the extracted data were cleaned and organized into tables.
Our initial search for relevant studies identified a total of 553 articles. After removing duplicates and reviewing the titles and abstracts, 88 studies were reviewed in full text. A total of 59 articles were included in the final analysis.[
The process of screening and selecting these studies, including the removal of duplicates and review of titles and abstracts, is shown in
The results of the analysis indicate that the sensitivity of intraoperative smear in detecting brain tumors was found to be more than 90% in the majority of cases (12 studies) and 100% in two studies. However, it should be noted that one study reported a sensitivity of 56%. In terms of specificity, the findings showed greater variability, with six studies reporting a specificity of >90%, while one study reported a specificity of 100%. The lowest reported specificity was observed in the range of 75–76%.
The PPV was reported above 90% in the majority of the studies (11 studies) and in one study, it was 100%. However, the lowest value reported was 75%. The NPV demonstrated a wide range, with the lowest value reported being 63% and the highest being 100%, as documented in three studies. However, the majority of studies (seven in total) that reported NPV fell within the range of 80–100%.
Overall, the accuracy of intraoperative smears for detecting brain tumors was reported >80% in the majority of studies (47 studies). It is important to note that the accuracy of any diagnostic test can be influenced by various factors, including the specific technique used and the characteristics of the population being tested. The detailed results of the studies on sensitivity, specificity, PPV, NPV, and accuracy are shown in
The Y-axis of the graph represents the frequency (%) of studies reporting the values of accuracy, sensitivity, and specificity of brain smear, while the X-axis represents the actual values of accuracy, sensitivity, and specificity. The values on the X-axis are categorized as ≥ 90, 90–80, and ≥ 50, which correspond to different levels of sensitivity, specificity, and accuracy.
Articles in this review also discussed numerous advantages of intraoperative smear including cost-effectiveness, minimal infrastructure requirements, rapid (10–15 min), accessibility, and accuracy in diagnosis. Intraoperative smear was reported to be relatively inexpensive compared to more complex tests, and it can be performed using basic equipment and facilities.
This is the first comprehensive review that evaluates the sensitivity, specificity, positive and NPVs, and accuracy of an intraoperative brain smear. It also highlights its advantages for resource-limited settings where there is a shortage of trained histopathologists and histopathology facilities.
This review reported the diagnostic accuracy of the intraoperative brain smear as >80%, as reported in the majority of studies. Sensitivity and specificity values were similarly high, with more than 90% reported in most studies. In addition, most studies reported positive and NPVs >90%. The main advantages reported include it being a rapid, simple, reliable, and cost-effective tool for diagnosis. Other advantages include high accuracy,[
A frequently cited benefit of intraoperative brain smears, as noted in many of the studies, is the considerably shorter time required for diagnosis compared to conventional techniques. As per the study by Jaiswal et al.,[
False positives and false negatives were reported in a few of the studies, as a small minority of the total sample size. One reason for this misdiagnosis through a squash smear was due to specific tumors such as ependymomas and meningiomas not being able to smear due to their firm nature.[
Intraoperative brain smears are highly accurate (95.3%) and reliable as a primary diagnostic tool for planning treatment.[
This review highlighted some of the limitations of squash smears in the diagnosis of certain brain tumors. One is the misrepresentation of tumor tissue due to absent histological artifacts, which leads to inaccurate diagnoses being made.[
This study is the first systematic review, to the best of our knowledge, conducted on the utility of intraoperative brain smears in brain tumor diagnosis. Overall, the results show that intraoperative brain smear is a rapid, simple, safe, cost-effective, and fairly accurate method of diagnosis of brain tumors which can improve service delivery efficiency and reduce the burden on healthcare systems in LMICs. This method could be especially beneficial in resource-limited settings, where the equipment for frozen sections is not often available and histopathological diagnosis also faces obstacles. There is a lack of trained histopathologists, limited availability of laboratory infrastructure, and limited advanced equipment to support the high demand for histopathological diagnosis. Our study reports the advantages of brain smear specifically for resource-limited settings, where other modalities of diagnosis are often not available.
This systematic review has some limitations, which should be taken into consideration when interpreting the findings. The majority of the articles taken into consideration were observational studies and may not provide strong evidence for the diagnostic accuracy of brain smears. Most of the studies reviews were also conducted in LMICs, namely, India, so the results may not be applicable to other parts of the world.
Further research is necessary to fully explore and understand the feasibility and implementation of intraoperative brain smears as a diagnostic modality for brain tumors in LMICs. Conducting further controlled studies, especially those that gather data from a larger range of countries, will provide better insight into the utility of the brain smear. Further, a comparison of the brain smear technique with other diagnostic modalities available will also provide valuable insight. Finally, guideline development regarding the use of brain smears in brain tumor diagnosis will be necessary for regulating the approach and improving the quality of care given worldwide.
Our systematic review revealed that intraoperative brain smear is a simple, rapid, cost-effective, and highly sensitive diagnostic modality for brain tumors in LMICs. It appears from the included literature that brain smears in settings with limited resources can be a viable and accessible alternative to more traditional methods such as frozen sections. Furthermore, the results of the studies reviewed suggest that brain smears could be incorporated into neurosurgical practice in LMICs as a reliable and efficient diagnostic tool.
Patients’ consent not required as patients’ identities were not disclosed or compromised.
There are no conflicts of interest.
The author(s) confirms that there was no use of Artificial Intelligence (AI)-Assisted Technology for assisting in the writing or editing of the manuscript and no images were manipulated using AI.
The views and opinions expressed in this article are those of the authors and do not necessarily reflect the official policy or position of the Journal or its management. The information contained in this article should not be considered to be medical advice; patients should consult their own physicians for advice as to their specific medical needs.
“Intraoperative Period”[Mesh] OR “Intraoperative Care”[Mesh]
Concept#2: (Brain Smear)
(“Brain Smear” OR “Intraoperative cytology” OR “Intraoperative squash cytology” OR “Intraoperative squash smear” OR “Squash Smear” OR “Imprint cytology” OR “touch cytology”)
Concept#3 (Brain Tumor)
“Brain Neoplasms”[Mesh] OR “Central Nervous System Neoplasms”[Mesh] OR “Brain tumor*” OR “brain cancer*” OR “CNS tumor*” OR “Nervous system tumor*” OR “NeuroOncology” OR “Intracranial neoplasm*” OR “Primary brain tumor*”
((“Brain Neoplasms”[Mesh] OR “Central Nervous System Neoplasms”[Mesh] OR “Brain tumor*” OR “brain cancer*” OR “CNS tumor*” OR “Nervous system tumor*” OR “NeuroOncology” OR “Intracranial neoplasm*” OR “Primary brain tumor*”) AND (“Brain Smear” OR “Intraoperative cytology” OR “Intraoperative squash cytology” OR “Intraoperative squash smear” OR “Squash Smear” OR “Imprint cytology” OR “touch cytology”))
((“Brain Neoplasms” OR “Central Nervous System Neoplasms” OR “Brain tumor*” OR “brain cancer*” OR “CNS tumor*” OR “Nervous system tumor*” OR “NeuroOncology” OR “Intracranial neoplasm*” OR “Primary brain tumor*”) AND (“Brain Smear” OR “Intraoperative cytology” OR “Intraoperative squash cytology” OR “Intraoperative squash smear” OR “Squash Smear” OR “Imprint cytology” OR “touch cytology”))
Google Scholar: (Using Publish or Perish)
“Brain Neoplasms” | “Central Nervous System Neoplasms” | “Brain tumor” | “Primary brain tumor” “Brain Smear” | “Intraoperative cytology” | “Intraoperative squash cytology” | “Intraoperative squash smear” | “Squash Smear” | “Imprint cytology” | “touch cytology”
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