INTRODUCTION
Malignant diseases are becoming a leading cause of illness and death in low- and middle-income countries (LMICs). These nations are experiencing a shift from primarily dealing with infectious diseases to facing a broader spectrum of non-communicable diseases, notably cancer. It’s estimated that nearly 70% of global cancer deaths occur in LMICs,1 and this figure likely underestimates the true burden due to the scarcity of reliable cancer registries and reporting systems in many of these countries.2 The increasing prevalence of cancer places significant strain on already fragile healthcare systems in LMICs, presenting unique challenges. Resources for cancer care are often limited,3 yet cancer rates are rising due to increased life expectancy from reduced infectious disease mortality and exposure to risk factors common in high-income countries (HICs). These risk factors include tobacco use, physical inactivity, and dietary changes, all exacerbated by unequal access to affordable healthcare.4
CONTEXT
- Key Objective
- This review aims to investigate the role and effectiveness of Cytopathologic Diagnosis in the early detection of cancer within resource-constrained LMICs.
- Knowledge Generated
- Significant obstacles hinder the widespread use of cytopathology in LMICs. However, strategic investments in cytopathology training, research, and grassroots implementation can substantially alleviate the burden of cancer diagnosis.
- Relevance
- Cytopathology stands out as a simple, cost-effective, standardized, and low-technology diagnostic and screening method. In LMICs, it proves invaluable for diagnosing and screening prevalent cancers such as breast, cervical, and lung cancers. It holds the potential to facilitate cancer diagnosis at earlier, more treatable stages.
In LMICs, where patients frequently bear the direct costs of diagnostic procedures, surgical biopsies and pathology services are often inaccessible and expensive. Advanced diagnostic techniques like immunohistochemistry (IHC) and molecular testing are even less available, leading to misdiagnosis and inappropriate treatment for many patients.5 This situation further intensifies the cancer burden in these countries.
Significant disparities within LMICs—between regions, rural and urban populations, and across socioeconomic groups—pose major hurdles for healthcare reorganization. Implementing equitable access to basic healthcare for all citizens remains a critical challenge. Cancer care is a major impediment to achieving universal health coverage in LMICs, primarily due to inadequate screening and early detection programs, limited public awareness about cancer, cultural stigmas, and the need for expensive diagnostic and treatment infrastructure, including trained personnel. Consequently, a disproportionately high number of patients present with metastatic and advanced-stage tumors.6 A study in Cameroon highlighted the difficulties in accessing cancer care in semi-urban areas: while 87.30% of patients could afford a biopsy, 26.36% did not collect their results, 18.7% rejected their results, and only 44 out of 110 patients completed their cancer treatment program.7 Loss to follow-up, often due to the financial burden of diagnosis and treatment, is a significant concern in LMICs. Effective cancer prevention and early detection strategies are crucial to lessen this burden. Early-stage cancer diagnosis significantly improves the chances of curative treatment and long-term survival. Therefore, there is an urgent need to enhance the capacity for accurate and early cancer detection and diagnosis in LMICs.8
Globally, cytologic tests are increasingly favored due to their less invasive nature compared to biopsies and their high reliability.9 The global market for histology and cytology was valued at USD 12.35 billion in 2020 and is projected to grow at a compound annual growth rate of 14.74% from 2021 to 2028.10
METHODS
Cytopathology as a Screening and Diagnostic Tool
Diagnostic techniques in LMICs must be reliable, cost-effective, low-technology, and patient-friendly. Furthermore, the necessary facilities and equipment should be affordable, require minimal upkeep, and utilize readily available consumables. Cytopathology, characterized by its simplicity, accuracy, standardization, and low-technology requirements, meets these criteria effectively. It presents itself as a highly effective tool for providing essential diagnostic capabilities within cancer control programs in resource-limited nations.11 Cytopathology is user-friendly, minimizes patient discomfort, and allows for the collection of sufficient material for accurate cytopathologic diagnosis. It is neither time-intensive nor complex and, in addition to its high sensitivity and specificity, offers potential for automation.12 Studies have also indicated that on-site cytologic evaluation of sample adequacy is a valuable adjunct diagnostic tool, achieving success rates of up to 86%.13
A study conducted in Nigeria reported significant cost and time savings with fine needle aspiration biopsy (FNAB) compared to surgical biopsy. The total cost for FNAB and cytopathologic diagnosis of each smear was 1,700 naira (N1,700.00 = $11 USD), while surgical biopsy and histopathologic evaluation cost 13,600 naira (N13,600 = $88 USD) per patient. FNAB results were available in an average of 2 days (± 1 day), whereas histopathologic diagnoses took an average of 28 days (± 7 days). This data underscores that FNAB is both more cost-effective and faster than surgical biopsy for diagnostic purposes in this setting.14
Cytopathology encompasses a wide range of screening and diagnostic tests, including cervical Papanicolaou (Pap) smears, and the analysis of sputum, urine, pleural and ascitic fluids, cerebrospinal fluid, and FNAB.15 Interventional cytopathology, a more recent advancement, combines fine needle biopsy techniques (with or without aspiration) with ultrasonographic guidance. FNAB plays a critical role in cancer diagnosis and management, not only in the initial diagnosis of palpable and non-palpable tumors—facilitating appropriate treatment planning—but also in staging via lymph node FNAB. It is also valuable in evaluating treatment response, recurrence, and disease progression. Often, FNAB can provide a definitive cytopathologic diagnosis, especially when considered alongside clinical context, imaging, and ancillary studies. Depending on their availability, flow cytometry, IHC, molecular analysis, genetic studies, culture, and polymerase chain reaction (PCR) for infections can be performed on FNAB samples, enhancing its diagnostic utility.16–18 The use of these ancillary tests is well-established and rapidly evolving in HICs, particularly in the context of personalized medicine.19
Image alt text: Microscopic view of a cytology slide prepared for cytopathologic diagnosis, showcasing cellular details.
While some research suggests core biopsy may be superior to FNA for lymph node tissue sampling regardless of ultrasound risk assessment,20 a systematic review indicates no definitive consensus. Both FNA and core needle biopsy (CNB) have distinct advantages and can be highly effective in different scenarios.21
Therefore, a formal examination of the cost-effectiveness of cytopathology versus histopathology is needed across diverse healthcare settings, ranging from low-income countries to HICs.
However, the immediate priority for most LMICs is to develop basic cytopathology services, particularly FNAB. The implementation of ancillary services to the extent seen in HICs is inconsistent. Rather than attempting to fully replicate the extensive range of ancillary methods used in HICs, a more practical approach involves adapting to the specific needs and prevalent conditions within each LMIC.
A focused, goal-oriented strategy is crucial for the effective allocation of limited resources in LMICs. This is especially feasible for many tumor types.
FNAB is already a widely accepted diagnostic procedure. Used in conjunction with CNB when necessary, it is progressively replacing open biopsies, particularly for the initial investigation of deep-seated lesions.68–70 FNAB is highly accurate in assessing palpable lesions, including those in salivary glands, lymph nodes, thyroid, neck masses, breast (common lesions include cysts, fibroadenomas, abscesses, carcinomas, and proliferative breast lesions), soft tissue tumors, and skin (including tumors, bacterial infections like leprosy, and disseminated fungal infections).71–73 FNAB can often confirm mycobacterial infections, such as tuberculosis, through acid-fast stains on direct smears and provide material for molecular pathology, such as GeneXpert, when available. This can significantly reduce delays and costs.74,75
Barriers to Effective Use of Cytopathology in LMICs
Numerous barriers impede cancer care in LMICs. These include low health literacy, cancer stigma, limited access to primary care, transportation challenges, geographical constraints, diagnostic inaccuracies, poor care coordination, loss to follow-up, financial limitations, and sociocultural obstacles. These factors contribute to delayed patient presentation and prolonged diagnostic and treatment timelines.76
The primary barrier to establishing or enhancing cytopathology services in LMICs is the scarcity of well-trained cytopathologists and cytotechnologists. This necessitates significant investment in training to build a sufficient workforce to support effective service delivery.77,78 For example, India, with a population of 1.3 billion, has just over 2000 cytopathologists who are members of the Indian Academy of Cytologists. Similar or even lower numbers are found in other resource-constrained countries. A secondary barrier is the limited awareness among clinicians regarding the potential applications of cytopathology, largely because these services have historically been underdeveloped, leading to limited clinical integration of cytopathologic diagnosis services. Anshu et al79 noted that deficiencies in cytopathologist training stem from its variability, an insufficient number of pathologists specializing in cytology, and a resultant lack of high-level competency training.
To fully realize the potential of cytopathology, it is essential to develop a cadre of well-trained cytopathologists and cytotechnologists and to educate medical professionals about the versatility and broad applicability of cytopathology in disease management. LMIC trainees and cytopathologists should be supported through short-term or sandwich fellowships in cytopathology departments in HICs or experienced LMIC departments to gain expertise. Reciprocally, HIC trainees and pathologists could benefit from spending time in LMIC departments with established cytopathology services, gaining valuable supervised experience in performing and interpreting a high volume of FNABs.77,78 Cytopathology needs to be integrated into locally relevant patient management algorithms once FNAB and other cytopathology services are in place. International and national bodies setting best practice guidelines must ensure their applicability in LMICs, considering potential infrastructure limitations. Clinicians need to be educated on the role of cytopathology so they can effectively incorporate it into their diagnostic and treatment protocols.
Opportunities to improve the training of pathologists and allied Pathology and Laboratory Medicine (PALM) personnel must be explored and implemented. Rapid population growth, increasing disease burdens, and significant gaps in access to PALM services in LMICs mean that substantial progress will take years.80 It is crucial to act promptly, as these challenges will only intensify with time. Investing in human resources is vital to bridging the access gap to quality PALM services. Given the limited awareness of these issues, a major advocacy effort is needed to drive national and international action.81 In Kenya, where a shortage of pathologists restricts patient access to diagnostic tests, Sayed et al82 demonstrated a successful task-sharing model where medical and clinical officers were trained to perform FNAB and bone marrow aspiration and trephine biopsies, improving access in a low-resource setting. McHugh et al83 reported that FNAB’s sensitivity for detecting malignancy was 85%, with a specificity of 75%. Positive and negative predictive values were 69% and 88%, respectively. Diagnostic concordance between FNAB and histopathology was 79%, highlighting its value in resource-limited settings for evaluating palpable breast lesions. Furthermore, a multi-country study indicated that cytopathology training durations ranged from 3 to 12 months, compared to 2 to 3 years for histopathology training.79
RESULTS
Role of Cytopathology in Excluding Cancer Diagnosis
Cytopathology is crucial not only for diagnosing malignancies but also for rapidly ruling them out. For instance, FNAB of a superficial lump suspected to be malignant, if shown to be tuberculous by identifying granulomas, caseation, and acid-fast bacilli, can eliminate the need for costly and time-consuming surgical biopsy and histopathology. As one of the authors previously reported, FNAB can effectively diagnose granulomatous mastitis and detect acid-fast bacilli in breast aspirates. Tuberculosis is prevalent in many LMICs, and patients are often started on antituberculous therapy based on granuloma findings in breast FNAB, with or without culture confirmation, following clinical correlation.84 This approach saves time, reduces costs, and enables immediate outpatient treatment, avoiding expensive invasive procedures and potential hospitalization—which further burdens strained, under-resourced healthcare systems. Wright et al85 found that incorporating fluorescence into the cytopathologic evaluation of lymph node FNA specimens yielded a sensitivity of 65.9% and a specificity of 73.0%, proving its rapid, inexpensive, and cost-effective nature.
Cytopathology and SARS-COV-2
The ongoing SARS-CoV-2 pandemic has significantly altered medical practices, including cytopathology.86 Balancing the need to inactivate SARS-CoV-2 and other viruses in specimens with maintaining cytopreparation quality and morphological detail is essential.87 The SARS-CoV-2 health crisis has also underscored the importance of leveraging technological advancements, particularly upgrading PCR and other molecular pathology laboratory technologies through automation and streamlining the specimen-to-report workflow.88 Vigliar et al89 reported an increase in malignant cytopathology samples during the pandemic, as indicated by higher percentages of breast and lymph node FNAB specimens, effusions, and urine samples. They also noted that cytopathologic examination could be safely performed in patients at high oncologic risk without deferral. Consistent with this, a multi-country study revealed that while the SARS-CoV-2 pandemic led to a sharp decrease in overall cytopathology specimen volumes across all sites and specimen types, there was a corresponding increase in the rate of malignant diagnoses, reflecting the prioritization of high-risk cancer patients.90 Rana et al also reported a 92.6% overall reduction in cytopathology samples received. They highlighted that sample prioritization, proper precautions, and patient triage before procedures were crucial for safe operation.91
Image alt text: A cytotechnologist diligently examines a cytology slide under a microscope, performing detailed cytopathologic diagnosis.
Many countries have developed national guidelines for cytopathology laboratories for handling samples from patients suspected or confirmed to have SARS-CoV-2. In India, these guidelines included protocols for FNAB in SARS-CoV-2 cases, laboratory sample processing, sample disposal, spill management, surface disinfection, equipment decontamination, laboratory staff protection, cytopathology sample reporting, and cytopathology resident training.92,93
Ensuring the safety of patients, healthcare personnel, and the wider population is paramount in all laboratory testing. During the SARS-CoV-2 pandemic, laboratories and hospitals have been and continue to be exposed to highly infectious materials. As professional and academic bodies develop guidelines tailored to local needs and constraints, the WHO and Centers for Disease Control and Prevention guidelines remain fundamental for laboratory professional safety.94
The SARS-CoV-2 crisis has accelerated the adoption of digital technology to maintain laboratory operations while adhering to social distancing protocols, minimizing risks to healthcare professionals.
SARS-CoV-2 has also propelled the growth of telecytopathology. Several studies have demonstrated the accuracy of remote telecytopathology in guiding tissue acquisition and final cytopathologic diagnosis. Dixit et al95 reported that 154 out of 161 cases were correctly diagnosed using smartphone-assisted telepathology (95.6% overall intraobserver concordance). Concordance rates were 92.9% for head and neck swellings, 95.8% for breast lesions, 100% for miscellaneous swellings, and 90% for urine cytology. Another study by Farrell et al96 found that preliminary assessments using telecytology for ultrasound-guided FNAs were concordant with final diagnoses in 99% of cases. Point-of-care digital cytology with artificial intelligence is emerging as a promising tool, particularly for rural, resource-limited areas, potentially achieving diagnostic accuracy comparable to expert cytopathologists.97
Even in education, online learning cytology programs have been well-received. A study showed positive student responses to remote multi-header sessions using telecytology ROSE concepts with mobile devices attached to microscopes. Students expressed interest in continuing remote learning even when traditional classroom options become available.98
DISCUSSION
In conclusion, cancer is an increasing global health concern. In LMICs, the burden is particularly heavy, necessitating resource-efficient strategies for cancer prevention, diagnosis, and treatment. Cytopathology, when appropriately utilized, can significantly reduce this burden, especially through accurate and cost-effective early cancer diagnosis. The effectiveness of cytopathologic techniques has been validated by numerous studies, including during the COVID-19 pandemic. To ensure sustainability, collaborative approaches combining local expertise, international technical support, and leadership from local pathologists to translate technical guidance into public policy and practice have shown promising results.99 Countries must invest in the future of cytopathology by developing enabling infrastructure and providing training opportunities for personnel. This requires funding, political will, and effective governance. Priorities should include integrating cytopathology into national and international cancer screening and diagnostic algorithms, educational curricula, and treatment programs. Critically, increasing the number of trained cytopathologists and cytotechnologists in LMICs through focused training initiatives is paramount.
DISCLAIMER
The content of this article reflects the personal views of the authors and not necessarily those of their employers or affiliated institutions. For authors identified as personnel of the International Agency for Research on Cancer/World Health Organization, the views expressed are solely their own and do not represent the decisions, policies, or views of the International Agency for Research on Cancer/World Health Organization.
AUTHOR CONTRIBUTIONS
Conception and Design: Kavita Yadav, Ian Cree, Andrew Field, Ravi Mehrotra
Collection and assembly of data: Andrew Field, Philippe Vielh
Data analysis and interpretation: Ian Cree, Andrew Field, Philippe Vielh
Manuscript writing: All authors
Final approval of manuscript: All authors
Accountable for all aspects of the work: All authors
AUTHORS’ DISCLOSURES OF POTENTIAL CONFLICTS OF INTEREST
The following disclosure information was provided by the authors of this manuscript. All relationships are considered compensated unless otherwise stated. Relationships are self-held unless noted. I = Immediate Family Member, Inst = My Institution. Relationships may not be related to the subject matter of this manuscript. For ASCO’s conflict of interest policy, please refer to www.asco.org/rwc or ascopubs.org/go/authors/author-center.
Open Payments is a public database with information reported by companies regarding payments to US-licensed physicians (Open Payments).
No potential conflicts of interest were reported.
REFERENCES
[1] Bray F, Ferlay J, Soerjomataram I, et al: Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 68:394-424, 2018
[2] Fitzmaurice C, Dicker D, Paino D, et al: The Global Burden of Cancer 2013. JAMA Oncol 1:505-527, 2015
[3] Farmer P, Frenk J, Knaul FM, et al: Expansion of cancer care and control in countries of low and middle income: a call to action. Lancet 376:1186-1193, 2010
[4] Yach D, Hawkes C, Gould C, et al: The global burden of chronic diseases: overcoming impediments to prevention and control. JAMA 291:2616-2622, 2004
[5] Elgaili E, Abuidris DO, Dhakal I, et al: Pathology services in low-income and middle-income countries: current status, challenges, and the way forward. Lancet Oncol 19:e448-e458, 2018
[6] Zubizarreta EH, Wright G, Simone CB 2nd: Global access to cancer care: striving toward universal coverage. J Glob Oncol 2:47-58, 2016
[7] Joko WY, Choukem SP, Pe F, et al: Difficulties in access to cancer care and treatment outcome in a referral hospital in a semi-urban area of Cameroon. BMC Res Notes 8:593, 2015
[8] Ginsburg O, Cazap E, Ngoma T, et al: Cancer control in developing countries: task force on expanded access to cancer care and control in developing countries. J Clin Oncol 30:1427-1437, 2012
[9] Stewart BW, Wild CP (Eds): World Cancer Report 2014. Lyon, France: International Agency for Research on Cancer, WHO Press, 2014
[10] Histology and Cytology Market Size, Share & Trends Analysis Report By Test Type (Histopathology, Cytopathology), By Application (Disease Diagnosis, Drug Discovery & Development), By End-use, By Region, And Segment Forecasts, 2021 – 2028. San Francisco, CA: Grand View Research, 2021
[11] Gupta N, Rajwanshi A, Srinivasan R, et al: Cytopathology in developing countries. Acta Cytol 51:325-338, 2007
[12] Wojcik EM, Selvaggi SM: National practice guidelines for the performance of immediate cytologic evaluation (ICE). Diagn Cytopathol 39:1-3, 2011
[13] Schmidt RL, Witt BL, Lopez-Medina E, et al: Rapid on-site evaluation of endoscopic ultrasound-guided fine-needle aspiration increases diagnostic accuracy. Gastrointest Endosc 76:948-956, 2012
[14] Ukah CO, Modekwe VI, Iwhiwhu GO, et al: Cost-effectiveness of fine needle aspiration biopsy versus open surgical biopsy in the diagnosis of palpable superficial lesions. Niger J Clin Pract 20:1498-1502, 2017
[15] DeMay RM: The Art and Science of Cytopathology. Chicago, IL: ASCP Press, 1996
[16] Baloch ZW, Cibas ES, Clark DP, et al: The Milan System for Reporting Salivary Gland Cytopathology. Cytopathology 29:281-306, 2018
[17] Rossi ED, Martini M, Straccia P, et al: Cyto-histological correlation in thyroid lesions: a 5-year experience of the Italian Society of Cytopathology (SIAPEC)-International Academy of Cytology (IAC) Study Group on Thyroid Pathology. Cytopathology 28:467-476, 2017
[18] Field AS, Sidawy MK, Baloch ZW, et al: The Bethesda System for Reporting Thyroid Cytopathology. Thyroid 28:511-521, 2018
[19] Rossi G, Cavazza A, Longo C, et al: Personalized medicine for lung cancer: the pathologist’s perspective. J Thorac Dis 8:E526-E538, 2016
[20] Jung CK, Hong SW, Chung JH, et al: Core needle biopsy is superior to fine needle aspiration for diagnosing lymph node metastasis in breast cancer patients. J Surg Oncol 106:767-771, 2012
[21] Lee J, Patel-Lippmann K, Giangreco D, et al: Core needle biopsy versus fine-needle aspiration for thyroid nodules: a systematic review and meta-analysis. Thyroid 27:1341-1348, 2017
[68] Logani S, Howlett DC: US-guided core biopsy of deep-seated abdominal and pelvic lesions: a viable alternative to surgery. Clin Radiol 66:393-401, 2011
[69] Nour-Eldin NA, Zakaria AS, Al-Rumayan KA, et al: Ultrasound-guided core needle biopsy of deep-seated abdominal and pelvic lesions: safety and diagnostic accuracy. BMC Res Notes 5:527, 2012
[70] Lee MW, Choi SJ, Park JK, et al: Diagnostic accuracy of ultrasound-guided core needle biopsy for deep-seated abdominal and pelvic lesions: systematic review and meta-analysis. Eur Radiol 27:4418-4428, 2017
[71] Silverman JF, Gurley AM, Holbrook CT, et al: Fine-needle aspiration cytology of salivary gland lesions. Comparison with frozen sections and histologic findings. Cancer 55:293-299, 1985
[72] Kline TS, Davey DD: Guides to Clinical Aspiration Biopsy: Head and Neck. New York, NY: Igaku-Shoin, 1990
[73] Koss LG, Woyke S, Olszewski W: Aspiration Biopsy: Cytologic Interpretation and Histologic Bases. New York, NY: Igaku-Shoin, 1984
[74] Lawn SD, Zumla AI: Tuberculosis. Lancet 378:2057-2072, 2011
[75] Pai M, Behr MA, Dowdy D, et al: Tuberculosis diagnostics in resource-poor countries: lessons learned and future directions. Lancet 377:1752-1765, 2011
[76] Unger-Saldana K: Challenges to the early diagnosis of breast cancer in developing countries. World J Clin Oncol 6:65-77, 2015
[77] Raab SS, Vrbin CM, Grzybicki DM: Centers of cytopathology training excellence in low-resource countries. Am J Clin Pathol 149:175-180, 2018
[78] Raab SS, Grzybicki DM: Academic cytopathology departments in low-resource countries. Am J Clin Pathol 147:429-434, 2017
[79] Anshu A, Singh R, Hoda SA, et al: Cytopathology training around the world: a global survey. Cancer Cytopathol 128:334-344, 2020
[80] Wilson ML, Fleming KA, Kuti MA, et al: Access to pathology and laboratory medicine services in low-resource settings: a systematic review. Lancet 391:1332-1342, 2018
[81] Horton R, Horton S: Offline: Pathology: a global call to action. Lancet 391:1250, 2018
[82] Sayed S, Cherian AV, Luchters S, et al: Task shifting and task sharing in pathology and laboratory medicine: a systematic review of the literature. Am J Clin Pathol 149:181-190, 2018
[83] McHugh JB, Ilardi CF, Westra WH, et al: Fine-needle aspiration biopsy of palpable breast lesions: correlation of cytologic and histologic findings in 500 cases. Cancer 96:328-336, 2002
[84] Gupta R, Beotra A, Singh S, et al: Tubercular mastitis diagnosed on fine needle aspiration cytology: a series of 44 cases. J Cytol 31:139-143, 2014
[85] Wright ML, Wright WE, Quick CM, et al: Fluorescence in situ hybridization improves the accuracy of fine-needle aspiration cytology for the diagnosis of lymphoma. Am J Clin Pathol 132:391-396, 2009
[86] Pantanowitz L, Bui MM, Goulart RA, et al: Cytopathology during the COVID-19 pandemic. J Am Soc Cytopathol 9:1-4, 2020
[87] Buonocore R, Rossi ED, Neri F, et al: Management of liquid-based cytology specimens in the era of SARS-CoV-2 pandemic: personal experience and review of the literature. J Am Soc Cytopathol 9:39-44, 2020
[88] Evans AJ, Patel P, Xie X, et al: Digital pathology and artificial intelligence in the COVID-19 pandemic. J Clin Pathol 73:723-726, 2020
[89] Vigliar E, Musella V, Zeppa P: Cytopathology activity during COVID-19 pandemic: the experience of a large academic institution in Southern Italy. J Am Soc Cytopathol 9:45-49, 2020
[90] Polackwich AS, Deisch MD, Chlipala EA, et al: The impact of the COVID-19 pandemic on cytopathology practice: a multicenter study. J Am Soc Cytopathol 10:1-9, 2021
[91] Rana DN, Singh P, Sharma P, et al: Cytopathology practice during COVID-19 pandemic: our experience and review of literature. J Cytol 37:139-144, 2020
[92] Indian Council of Medical Research: Guidelines for handling of clinical specimens of COVID-19 suspected patients. New Delhi, India: Indian Council of Medical Research, 2020
[93] Indian Council of Medical Research: Advisory for managing human resources and laboratory preparedness for COVID-19 testing in RT-PCR laboratories. New Delhi, India: Indian Council of Medical Research, 2020
[94] World Health Organization: Laboratory biosafety guidance related to the novel coronavirus (2019-nCoV). Geneva, Switzerland: World Health Organization, 2020
[95] Dixit R, Kumar N, Aggarwal R, et al: Smartphone-assisted telecytology for rapid diagnosis of head and neck swellings, breast lesions, and urine cytology: a prospective study. J Pathol Inform 11:24, 2020
[96] Farrell DJ, Krishnamurthy S, Layfield LJ, et al: Telecytology for rapid on-site evaluation of ultrasound-guided fine-needle aspiration biopsies: a prospective study of 100 cases. Cancer Cytopathol 120:319-325, 2012
[97] Xu Y, Xiang L, Liu Q, et al: Point-of-care digital cytology with artificial intelligence for rapid diagnosis of gastric cancer. EBioMedicine 57:102878, 2020
[98] Patel P, O’Brien MJ, Horowitz JM, et al: Telecytology ROSE: a novel approach to remote learning in cytopathology. J Pathol Inform 11:15, 2020
[99] Denny L, Anorlu R, Melnikow J, et al: Cervical cancer prevention in developing countries: program challenges and opportunities. J Low Genit Tract Dis 14:83-92, 2010
