Cytological analysis of sputum specimens obtained from COVID-19 patients, Khartoum State-Sudan
Keywords:
cytology, diff-quick’s stain, SARS-COV-2, Sudan, sputum, Papanicolaou’s stainAbstract
Background: Severe acute respiratory syndrome (SARS) is a recently described form of atypical pneumonia linked to a novel Coronavirus (SARS-CoV-2). Sputum cytology can help to differentiate SARS-CoV-2 infection from other opportunistic infections.
Methods. Sputum samples were collected from 100 patients previously diagnosed with COVID-19. Sputum was stained with Papanicolaou’s and Diff-Quick’s stains for cytomorphological changes. Data were analyzed using the SPSS program.
Results. Among 100 patients, 74 (74%) were male, and 26 (26%) were female. The age group between 25-56 years was 76 (76%), while the age group between 57 and older was 24 (24%). The background of smears represents different components with strong evidence of PMNs, mucus spiral and less evidence of RBCs and epithelial cells displayed the cellular changes due to SARS-COV-2 virus in squamous and columnar cells. Nuclear enlargement and perinuclear halo were detected in squamous cells whereas columnar cells showed cytolysis and rounding. There was a significant association between staining quality and stain types whereas there was no significant association between cellular changes and age.
Conclusion. This study concluded that sputum smears were adequate for the detection of cytopathic effects of SARS-COV-2 infections. Diff-quick’s stain showed better quality than Papanicolaou’s stain.
References
Ball, M., Hossain, M. y Padalia, D. (2023). Anatomy, Airway. En StatPearls [internet]. StatPearls Publishing.
Bradley, B. T., Maioli, H., Johnston, R., Chaudhry, I., Fink, S. L., Xu, H., Najafian, B., Deutsch, G., Lacy, J. M., Williams, T., Yarid, N. y Marshall, D. A. (2020). Histopathology and ultrastructural findings of fatal COVID-19 infections in Washington State: A case series. Lancet (London, England), 396(10247), 320–332. https://doi.org/10.1016/S0140-6736(20)31305-2
Bui, M. T., Nguyen Le, C. A., Duong, K. L., Hoang, V. T. y Nguyen, T. K. (2024). Transplacental Transmission of SARS-CoV-2: A Narrative Review. Medicina (Kaunas, Lithuania), 60(9), 1517. https://doi.org/10.3390/medicina60091517
Bwire G. M. (2020). Coronavirus: Why Men are More Vulnerable to Covid-19 Than Women?. SN Comprehensive Clinical Medicine, 2(7), 874–876. https://doi.org/10.1007/s42399-020-00341-w
Cibas, E. S. y Ducatman, B. S. (2014). Cytology: Diagnostic principles and clinical correlates. (4ª ed.). Elsevier/Saunders.
Faez Habib, M., Alameer M. Zeen, A., Hussain, S. M., Almajed ALtaher, T. A., Mahjaf, G. M. y Hamad, M. N. M. (2023). Cytological Changes in Sputum Sample among Sudanese COVID-19 Patient among Different Town in Sudan 2021. SAR J Pathol Microbiol, 4(1), 1-6. https://doi.org/10.36346/sarjpm.2023.v04i01.001
Fujimoto, D., Fukuya, M., Terao, S., Irei, I., Akiyama, T., Watanabe, A., Yasuda, Y., Yoshioka, D., Takada, K., Hayakawa, S. y Moriya, T. (2022). Sputum characteristics of patients with severe COVID-19: report of two cases with immunocytochemical detection of SARS-CoV-2 spike protein. Medical Molecular Morphology, 55(4), 316–322. https://doi.org/10.1007/s00795-022-00326-9
Gelardi, M. y Ciprandi, G. (2019). Ciliocytophthoria of nasal epithelial cells after viral infection: A sign of suffering cell. Acta bio-medica: Atenei Parmensis, 90(2-S), 7–9. https://doi.org/10.23750/abm.v90i2-S.8103
Giani, M., Seminati, D., Lucchini, A., Foti, G. y Pagni, F. (2020). Exuberant Plasmocytosis in Bronchoalveolar Lavage Specimen of the First Patient Requiring Extracorporeal Membrane Oxygenation for SARS-CoV-2 in Europe. Journal of thoracic oncology: Official publication of the International Association for the Study of Lung Cancer, 15(5), e65–e66. https://doi.org/10.1016/j.jtho.2020.03.008
González-García, P., Fiorillo Moreno, O., Zarate Peñata, E., Calderón-Villalba, A., Pacheco Lugo, L., Acosta Hoyos, A., Villarreal Camacho, J. L., Navarro Quiroz, R., Pacheco Londoño, L., Aroca Martínez, G., Moares, N., Gabucio, A., Fernández-Ponce, C., García-Cozar, F. y Navarro Quiroz, E. (2023). From Cell to Symptoms: The Role of SARS-CoV-2 Cytopathic Effects in the Pathogenesis of COVID-19 and Long COVID. International Journal of Molecular Sciences, 24(9), 8290. https://doi.org/10.3390/ijms24098290
Guan, W. J., Ni, Z. Y., Hu, Y., Liang, W. H., Ou, C. Q., He, J. X., Liu, L., Shan, H., Lei, C. L., Hui, D. S. C., Du, B., Li, L. J., Zeng, G., Yuen, K. Y., Chen, R. C., Tang, C. L., Wang, T., Chen, P. Y., Xiang, J., Li, S. Y., … China Medical Treatment Expert Group for Covid-19. (2020). Clinical Characteristics of Coronavirus Disease 2019 in China. The New England Journal of Medicine, 382(18), 1708–1720. https://doi.org/10.1056/NEJMoa2002032
Harrison, A. G., Lin, T. y Wang, P. (2020). Mechanisms of SARS-CoV-2 Transmission and Pathogenesis. Trends in Immunology, 41(12), 1100–1115. https://doi.org/10.1016/j.it.2020.10.004
Inde, Z., Croker, B. A., Yapp, C., Joshi, G. N., Spetz, J., Fraser, C., Qin, X., Xu, L., Deskin, B., Ghelfi, E., Webb, G., Carlin, A. F., Zhu, Y. P., Leibel, S. L., Garretson, A. F., Clark, A. E., Duran, J. M., Pretorius, V., Crotty-Alexander, L. E., Li, C., … Sarosiek, K. A. (2021). Age-dependent regulation of SARS-CoV-2 cell entry genes and cell death programs correlates with COVID-19 severity. Science aAdvances, 7(34), eabf8609. https://doi.org/10.1126/sciadv.abf8609
Kellogg, J. A., Seiple, J. W., Klinedinst, J. L. y Stroll, E. (1996). Diff-Quik stain as a simplified alternative to Papanicolaou stain for determination of quality of endocervical specimens submitted for PCR detection of Chlamydia trachomatis. Journal of Clinical Microbiology, 34(10), 2590–2592. https://doi.org/10.1128/jcm.34.10.2590-2592.1996
Kumar, S. S., Binu, A., Devan, A. R. y Nath, L. R. (2021). Mucus targeting as a plausible approach to improve lung function in COVID-19 patients. Medical Hypotheses, 156, 110680. https://doi.org/10.1016/j.mehy.2021.110680
Liu, Y., Lv, J., Liu, J., Li, M., Xie, J., Lv, Q., Deng, W., Zhou, N., Zhou, Y., Song, J., Wang, P., Qin, C., Tong, W. M. y Huang, B. (2020). Mucus production stimulated by IFN-AhR signaling triggers hypoxia of COVID-19. Cell Research, 30(12), 1078–1087. https://doi.org/10.1038/s41422-020-00435-z
Onder, G., Rezza, G. y Brusaferro, S. (2020). Case-Fatality Rate and Characteristics of Patients Dying in Relation to COVID-19 in Italy. JAMA, 323(18), 1775–1776. https://doi.org/10.1001/jama.2020.4683
Pambuccian, S. E. (2020). The COVID-19 pandemic: implications for the cytology laboratory. Journal of the American Society of Cytopathology, 9(3), 202–211. https://doi.org/10.1016/j.jasc.2020.03.001
Ren, S. Y., Wang, W. B., Hao, Y. G., Zhang, H. R., Wang, Z. C., Chen, Y. L. y Gao, R. D. (2020). Stability and infectivity of coronaviruses in inanimate environments. World Journal of Clinical Cases, 8(8), 1391–1399. https://doi.org/10.12998/wjcc.v8.i8.1391
Scientific Brief. (9 de julio de 2020). Transmission of SARS-CoV-2: Implications for Infection Prevention Precautions. World Health Organization. https://www.who.int/news-room/commentaries/detail/transmission-of-sars-cov-2-implications-for-infection-prevention-precautions
Shim, E., Tariq, A., Choi, W., Lee, Y. y Chowell, G. (2020). Transmission potential and severity of COVID-19 in South Korea. International journal of infectious diseases : IJID : official publication of the International Society for Infectious Diseases, 93, 339–344. https://doi.org/10.1016/j.ijid.2020.03.031
Shiratori, Y., Ikeya, T. y Nakamura, K. (2020). Comparison of Papanicolaou and Diff-Quick staining in pancreatic endoscopic ultrasound-fine needle aspiration biopsy with rapid on-site cytologic evaluation. Digestive endoscopy: Official journal of the Japan Gastroenterological Endoscopy Society, 32(3), 434. https://doi.org/10.1111/den.13604
Singhal, T. (2020). A Review of Coronavirus Disease-2019 (COVID-19). Indian Journal of Pediatrics, 87(4), 281–286. https://doi.org/10.1007/s12098-020-03263-6
Yang, M. S., Oh, B. K., Yang, D., Oh, E. Y., Kim, Y., Kang, K. W., Lim, C. W., Koh, G. Y., Lee, S. M. y Kim, B. (2021). Ultra- and micro-structural changes of respiratory tracts in SARS-CoV-2 infected Syrian hamsters. Veterinary Research, 52(1), 121. https://doi.org/10.1186/s13567-021-00988-w
Youning, L. y Military Medical Expert Group on the Front-line. (2020). Diagnosis and Treatment Protocol for COVID-19 from Military Medical Team Supporting Wuhan (Trial Version 2). journals of Chinese Medical Association, 43(5), 414–420. https://doi.org/10.3760/cma.j.cn112147-20200315-00338
Zhu, N., Zhang, D., Wang, W., Li, X., Yang, B., Song, J., Zhao, X., Huang, B., Shi, W., Lu, R., Niu, P., Zhan, F., Ma, X., Wang, D., Xu, W., Wu, G., Gao, G. F., Tan, W. y China Novel Coronavirus Investigating and Research Team. (2020). A Novel Coronavirus from Patients with Pneumonia in China, 2019. The New England Journal of Medicine, 382(8), 727–733. https://doi.org/10.1056/NEJMoa2001017
Zubieta-Calleja, G. R., Zubieta-DeUrioste, N., de Jesús Montelongo, F., Sánchez, M. G. R., Campoverdi, A. F., Rocco, P. R. M., Battaglini, D., Ball, L. y Pelosi, P. (2023). Morphological and functional findings in COVID-19 lung disease as compared to Pneumonia, ARDS, and High-Altitude Pulmonary Edema. Respiratory Physiology & Neurobiology, 309, 104000. https://doi.org/10.1016/j.resp.2022.104000
Zupin, L., Fontana, F., Gratton, R., Milani, M., Clemente, L., Pascolo, L., Ruscio, M. y Crovella, S. (2021). SARS-CoV-2 Short-Time Infection Produces Relevant Cytopathic Effects in Vero E6 Cell Line. International Journal of Environmental Research and Public Health, 18(17), 9020. https://doi.org/10.3390/ijerph18179020
Downloads
Published
Issue
Section
License
Copyright (c) 2026 Alaa Yousef Yaggop, Alshima Nasraldain Babeker, Barah Moustafa Mohammed, Gaidaa Mohammed Bushra, Israa Hashim Khalid, Fadol Nasraldain Fadol, Mugtaba Ahmed Abdelrazig, Hind Haidar Ahmed, May Mohammed Ali, Samar M. Saeed, Mohamed Siddig Abd Elaziz, Tagwa Salah Ahmed (Autor/a)
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
License CC Attribution-NonCommercial 4.0 (CC BY-NC 4.0). This Creative Commons license that allows others to copy, distribute, remix, and build upon a work for non-commercial purposes, provided they credit the original creator.
