320
Views
0
CrossRef citations to date
0
Altmetric
Articles

Romanowsky staining: history, recent advances and future prospects from a chemistry perspective

ORCID Icon, ORCID Icon & ORCID Icon

References

  • Abdullah O, Salh DM, Mohamad AH, Jamal GM, Ahmed HT, Mustafa BS, Suhail MH. 2022. Linear and nonlinear optical characterization of dye–polymer composite films based on methylcellulose incorporated with varying content of methylene blue. J Electron Mater. 51:675–683. doi: 10.1007/s11664-021-09322-8.
  • Adams CE, Awad GA, Rathbone J, Thornley B, Soares-Weiser K. 2014. Chlorpromazine versus placebo for schizophrenia. Cochrane Database Syst Rev. 1:CD000284. doi: 10.1002/14651858.cd000284.pub3.
  • Agarwal A, Sharma R, Gupta S, Finelli R, Parekh N, Panner Selvam MK, Henkel R, Durairajanayagam D, Pompeu C, Madani S, Belo A, Singh N, Covarrubias S, Darbandi S, Sadeghi R, Darbandi M, Vogiatzi P, Boitrelle F, Simopoulou M, Saleh R, Arafa M, Majzoub A, Kandil H, Zini A, Ko E, Alvarez JG, Martinez M, Ramsay J, Jindal S, Busetto GM, Sallam H, Maldonado I, Anagnostopoulou C, Alves MG, Sengupta P, Gilany K, Evenson DP, Lewis SEM, Gosalvez J, Ambar RF, Shah R. 2022. Sperm morphology assessment in the era of intracytoplasmic sperm injection: reliable results require focus on standardization, quality control, and training. World J Mens Health. 40:347–360. doi: 10.5534/wjmh.210054.
  • Allison RW, Velguth KE. 2010. Appearance of granulated cells in blood films stained by automated aqueous versus methanolic Romanowsky methods. Vet Clin Pathol. 39:99–104. doi: 10.1111/j.1939-165X.2009.00187.x.
  • Asadullin AR, Yuldashev VL, Asadullina GM, Akhmetova EA, Ishchenko KA. 2018. The safety and efficacy of alimemazine (teraligen) in relieving anxiety in patients with alcohol addiction. Z Nevrol Psikhiatr im SS Korsakova. 118:39–44. doi: 10.17116/jnevro20181181239-44.
  • Aydin E, Hallner A, Grauers Wiktorin H, Staffas A, Hellstrand K, Martner A. 2019. NOX2 inhibition reduces oxidative stress and prolongs survival in murine KRAS-induced myeloproliferative disease. Oncogene. 38:1534–1543. doi: 10.1038/s41388-018-0528-1.
  • Azoulay T, Slouzky I, Karmona M, Filatov M, Hayun M, Ofran Y, Sarig G, Ringelstein-Harlev S. 2023. Compromised activity of natural killer cells in diffuse large B-cell lymphoma is related to lymphoma-induced modification of their surface receptor expression. Cancer Immunol Immunother. 72:707–718. doi: 10.1007/s00262-022-03284-4.
  • Ban TA. 2007. Fifty years chlorpromazine: a historical perspective. Neuropsych Dis Treat. 3:495–500. doi: 10.2147/ndt.s12160195.
  • Barcia JJ. 2007. The Giemsa stain: its history and applications. Int J Surg Pathol. 15:292–296. doi: 10.1177/1066896907302239.
  • Barger AM. 2022. Erythrocyte morphology. In: Brooks M, Harr K, Seelig D, Wardrop K, Weiss J, Eds., Schalm’s veterinary hematology. 7th ed. Blackwell Publishing, Hoboken, NJ; p. 188–197. doi: 10.1002/9781119500537.ch24.
  • Belgaumi U, Shetty P. 2013. Leishman Giemsa cocktail as a new, potentially useful cytological technique comparable to Papanicolaou staining for oral cancer diagnosis. J Cytol. 30:18–22. doi: 10.4103/0970-9371.107507.
  • Bezrukov A. 2017. Romanowsky staining, the Romanowsky effect and thoughts on the question of scientific priority. Biotech Histochem. 92:29–35. doi: 10.1080/10520295.2016.1250285.
  • Bhattarai G, Lee JB, Kim M-H, Ham S, So H-S, Oh S, Sim H-J, Lee J-C, Song M, Kook S-H. 2019. Maternal exposure to fine particulate matter during pregnancy induces progressive senescence of hematopoietic stem cells under preferential impairment of the bone marrow microenvironment and aids development of myeloproliferative disease. Leukemia. 34:1481–1484. doi: 10.1038/s41375-019-0665-8.
  • Binder T, Diem H, Fuchs R, Gutensohn K, Nebe T. 2012. Pappenheim-Färbung: Beschreibung einer hämatologischen Standardfärbung–Geschichte, Chemie, Durchführung, Artefakte und Problemlösungen. J Lab Med. 36:293–309. doi: 10.1515/labmed-2012-0027.
  • Boguzaite R, Ratautaite V, Mikoliunaite L, Pudzaitis V, Ramanaviciene A, Ramanavicius A. 2021. Towards analytical application of electrochromic polypyrrole layers modified by phenothiazine derivatives. J Electroanal Chem. 886:115132. doi: 10.1016/j.jelechem.2021.115132.
  • Brar APS, Sood NK, Singla LD, Kaur P, Gupta K, Sandhu BS. 2017. Validation of Romanowsky staining as a novel screening test for the detection of faecal cryptosporidial oocysts. J Parasit Dis. 41:260–262. doi: 10.1007/s12639-016-0788-z.
  • Buck STG, Bettanin F, Orestes E, Homem-de-Mello P, Imasato H, Viana RB, Perussi JR, da Silva ABF. 2017. Photodynamic efficiency of xanthene dyes and their phototoxicity against a carcinoma cell line: a computational and experimental study. J Chem. 2017:1–9. doi: 10.1155/2017/7365263.
  • Cardiff RD, Miller CH, Munn RJ. 2014. Manual hematoxylin and eosin staining of mouse tissue sections. C S Harb Protoc. 2014:pdb.prot073411. doi: 10.1101/pdb.prot073411.
  • Chantziantoniou N, Donnelly AD, Mukherjee M, Boon ME, Austin RM. 2017. Inception and development of the Papanicolaou stain method. Acta Cytol. 61:266–280. doi: 10.1159/000457827.
  • Choi J-H, Chin LK, Woo BM, Song Y, Seol MJ, Hong Y, Liu A-Q, Jang S, Ploegh H, Im H, Lee D. 2021. Hydrogel-based stamping technology for solution-free blood cell staining. ACS Appl Mater Interfaces. 13:22124–22130. doi: 10.1021/acsami.0c22521.
  • Chuang S-T, Papp H, Kuczmog A, Eells R, Condor Capcha JM, Shehadeh LA, Jakab F, Buchwald P. 2022. Methylene blue is a nonspecific protein–protein interaction inhibitor with potential for repurposing as an antiviral for Covid-19. Pharmaceuticals. 15:621. doi: 10.3390/ph15050621.
  • Cooksey C. 2018. Quirks of dye nomenclature. 10. Eosin Y and its close relatives. Biotech Histochem. 93:211–219. doi: 10.1080/10520295.2017.1413207.
  • Cooksey C, Dronsfield A. 2015. Quirks of dye nomenclature. 4. Fuchsine: four shades of magenta. Biotech Histochem. 90:288–293. doi: 10.3109/10520295.2014.989543.
  • Cox L, Darvill E, Dorman S. 2015. Levomepromazine for nausea and vomiting in palliative care. Cochrane Database Syst Rev. 11:CD009420. doi: 10.1002/14651858.cd009420.pub3.
  • Dang N, Saraf V, Khanna A, Gupta D, Sheikh TH. 2020. Malaria detection on Giemsa-stained blood smears using deep learning and feature extraction. Adv Intel Sys Comput. 1:789–803. doi: 10.1007/978-981-15-1286-5_70.
  • Deepthi B, Prayaga A, Rukmangadha N. 2022. Comparison of modified ultrafast Giemsa stain with the standard May Grunwald Giemsa stain in FNAC of various organs. J Cytol. 39:174–179. doi: 10.4103/joc.joc_43_22.
  • DeGroote LW, Rodewald PG. 2010. Blood parasites in migrating wood-warblers (Parulidae): effects on refueling, energetic condition, and migration timing. J Avian Biol. 41:147–153. doi: 10.1111/j.1600-048x.2009.04782.x.
  • Demyanov IA, Boyko EO, Zaitceva OG, Pogodina MG. 2019. The efficacy of alimemazine (solution for intramuscular injection) in complex with antidepressants in the treatment of anxiety and depressive disorders. Z Nevrol Psikhiatr im SS Korsakova. 119:32–37. doi: 10.17116/jnevro201911908132.
  • Ehrlich P. 1879. Methodologische Beiträge zur Physiologie und Pathologie der verschiedenen Formen der Leukocyten. Z Klin Med. 1:553–560. doi: 10.1016/B978-0-08-009054-2.50013-4.
  • Ehrlich P. 1913. Erinnerungen aus der Zeit der ätiologischen Tuberkuloseforschung Robert Kochs. Dtsch Med Woch. 39:2444–2446. doi: 10.1055/s-0028-1128964.
  • Eltarahony M, El-Fakharany E, Abu-Serie M, ElKady M, Ibrahim A. 2021. Statistical modeling of methylene blue degradation by yeast-bacteria consortium; optimization via agro-industrial waste, immobilization and application in real effluents. Microb Cell Fact. 20:234. doi: 10.1186/s12934-021-01730-z.
  • Eslami H, Khavidak SS, Salehi F, Khosravi R, Ali Fallahzadeh R, Peirovi R, Shahram S. 2017. Biodegradation of methylene blue from aqueous solution by bacteria isolated from contaminated soil. J Adv Env Health Res. 5:10–15. doi: 10.22102/jaehr.2017.46690.
  • Fan BE, Lim KGE, Chong VCL, Chan SSW, Ong KH, Kuperan P. 2020. COVID‐19 and mycoplasma pneumoniae coinfection. Am J Hematol. 95:723–724. doi: 10.1002/ajh.25785.
  • Farley A, Lloyd S, Dayton M, Biben C, Stonehouse O, Taoudi S. 2021. Severe thrombocytopenia is sufficient for fetal and neonatal intracerebral hemorrhage to occur. Blood. 138:885–897. doi: 10.1182/blood.2020010111.
  • Fasakin KA, Okogun GRA, Omisakin CT, Adeyemi AA, Esan AJ. 2014. Modified Leishman stain: the mystery unfolds. Br J Med Res. 4:4591–4606. doi: 10.9734/BJMMR/2014/10855.
  • Ferreira-Leitão VS, da Silva JG, Bon EPS. 2003. Methylene blue and azure B oxidation by horseradish peroxidase: a comparative evaluation of class II and class III peroxidases. Appl Catal B. 42:213–221. doi: 10.1016/s0926-3373(02)00238-2.
  • Ferreira VS, Magalhães DB, Kling SH, Da Silva JG, Bon EPS. 2000. N-Demethylation of methylene blue by lignin peroxidase from Phanerochaete chrysosporium. Appl Biochem Biotechnol. 84–86:255–266. doi: 10.1385/abab:84-86:1-9:255.
  • Figueiredo-Godoi LMA, Garcia MT, Pinto JG, Ferreira-Strixino J, Faustino EG, Pedroso LLC, Junqueira JC. 2022. Antimicrobial photodynamic therapy mediated by fotenticine and methylene blue on planktonic growth, biofilms, and burn infections of Acinetobacter baumannii. Antibiotics. 11:619. doi: 10.3390/antibiotics11050619.
  • Foko LPK, Pande V, Singh V. 2021. Field performances of rapid diagnostic tests detecting human plasmodium species: a systematic review and meta-analysis in India, 1990–2020. Diagnostics. 11:590. doi: 10.3390/diagnostics11040590.
  • Friedrich K, Seiffert W, Zimmermann HW. 1990. Romanowsky dyes and Romanowsky-Giemsa effect 5. Structural investigations of the purple DNA-AB-EY dye complexes of Romanowsky-Giemsa staining. Histochemistry. 93:247–256. doi: 10.1007/bf00266385.
  • Garbyal RS, Agarwal N, Kumar P. 2006. Leishman-Giemsa cocktail. Acta Cytol. 50:403–406. doi: 10.1159/000325981.
  • Garcia GC, Alves‐Júnior JRF, Santana ÁE, Stas CMF, Silva CC, Kanayama CY, Bittar ER, Bittar JFF. 2021. Hematologic variables of the Arrau turtle (Podocnemis expansa) under the effects of different anticoagulants and cytologic stains. Vet Clin Pathol. 50:209–215. doi: 10.1111/vcp.12960.
  • Gendrot M, Andreani J, Duflot I, Boxberger M, Le Bideau M, Mosnier J, Jardot P, Fonta I, Rolland C, Bogreau H. 2020. Methylene blue inhibits replication of SARS–CoV–2 in vitro. Int J Antimicrob Agents. 56:106202. doi: 10.1016/j.ijantimicag.2020.106202.
  • Giemsa G. 1902. Färbemethoden für malariaparasiten. Zentralbl Bakteriol. 31:429–430. German.
  • Gonçalves JMLA, Monteiro CM, Machado GB, Pavani C. 2023. The combination of methylene blue and sodium dodecyl sulfate enhances the antimicrobial photodynamic therapy of Candida albicans at lower light parameters. Photodiagn Photodyn Ther. 42:103583. doi: 10.1016/j.pdpdt.2023.103583.
  • Gunawardena D, Priyankara I, Jayamanne H, Suresh S. 2022. Modified Giemsa stain: a solution to improve the quality of hypercellular bone marrow smears. Int J Lab Hematology. 44:504–509. doi: 10.1111/ijlh.13824.
  • Habibi A, Mehrabi Z. 2017. Aerobic degradation of methylene blue from colored effluents by Ralstonia eutropha. Pollution. 3:363–375. doi: 10.7508/pj.2017.03.002.
  • Higuchi K, Urano M, Akiba J, Nogami M, Hirata Y, Zukeran Y, Moriyoshi K, Tada Y, Fukushima M, Obayashi M, Sakamoto S, Kuraoka K, Kira K, Kawahara A, Kato T, Tanigawa M, Nakaguro M, Yamamoto H, Nagao T. 2021. A multi‐institutional study of salivary gland cytopathology: application of the Milan System for Reporting Salivary Gland Cytopathology in Japan. Cancer Cytopathol. 130:30–40. doi: 10.1002/cncy.22505.
  • Holmes WC, Snyder EF. 1929. The atmospheric oxidation, or dealkylation, of aqueous solutions of methylene blue. Stain Technol. 4:7–10. doi: 10.3109/10520292909115576.
  • Horobin R. 2011. How Romanowsky stains work and why they remain valuable—including a proposed universal Romanowsky staining mechanism and a rational troubleshooting scheme. Biotech Histochem. 86:36–51. doi: 10.3109/10520295.2010.515491.
  • Horobin RW, Boon ME. 1988. Understanding microwave-stimulated Romanowsky-Giemsa staining of plastic embedded bone marrow. Histochem J. 20–20:329–334. doi: 10.1007/bf01002725.
  • Horobin RW, Walter KJ. 1987. Understanding Romanowsky staining I. The Romanowsky-Giemsa effect in blood smears. Histochemistry. 8:331–336. doi: 10.1007/bf00490267.
  • Horobin RW, Curtis D, Pindar L. 1989. Understanding Romanowsky staining. 2. The staining mechanism of suspension-fixed cells, including influences of specimen morphology on the Romanowsky-Giemsa effect. Histochemistry. 91:77–80. doi: 10.1007/bf00501915.
  • Hough VA, Wycislo KL, Hofmeister EH, Piech TL, Maki LC, Shaver SL. 2023. Effect of Romanowsky-stained concentrated preparations versus direct smears on veterinary students’ ability to identify bacterial sepsis in fluid cytology samples from dogs, cats, and horses. J Vet Med Ed. 50:228–233. doi: 10.3138/jvme-2021-0138.
  • Howe B, Umrigar A, Tsien F. 2014. Chromosome preparation from cultured cells. J Vis Exp. 83:e50203. doi: 10.3791/50203.
  • Hye RA, Gisuthan B, Kariveettil I. 2021. A comparative study between conventional and modified Leishman stain. Int L Res Rev. 8:5–12. doi: 10.52403/ijrr.20210202.
  • ICHS. 1984. ICSH reference method for staining of blood and bone marrow films by azure B and eosin Y (Romanowsky stain). International committee for standardization in haematology. Br J Haematol. 57:707–710. doi: 10.1111/j.1365-2141.1984.tb02949.x.
  • Jackson DE, Selting KA, Spoor MS, Henry CJ, Wiedmeyer CE. 2012. Evaluation of fixation time using Diff-Quik for staining of canine mast cell tumor aspirates. Vet Clin Pathol. 42:99–102. doi: 10.1111/vcp.12012.
  • Jambrec D, Gebala M. 2022. DNA electrostatics: from theory to application. ChemElectrochem. 9:202101415. doi: 10.1002/celc.202101415.
  • Jayasinghe C, Imtiaj A, Lee G-W, Im K-H, Hur H, Lee M-W, Yang H-S, Lee T-S. 2008. Degradation of three aromatic dyes by white rot fungi and the production of ligninolytic enzymes. Mycobiology. 36:114–120. doi: 10.4489/MYCO.2008.36.2.114.
  • Jenner L. 1899. A new preparation for rapidly fixing and staining blood. Lancet. 153:370–371. doi: 10.1016/S0140-6736(01)63525-6.
  • Jörundsson E, Lumsden JH, Jacobs RM. 1999. Rapid staining techniques in cytopathology: a review and comparison of modified protocols for hematoxylin and eosin, Papanicolaou and Romanowsky stains. Vet Clin Pathol. 28:100–108. doi: 10.1111/j.1939-165x.1999.tb01057.x.
  • Kappo D, Shurpik D, Padnya P, Stoikov I, Rogov A, Evtugyn G. 2022. Electrochemical DNA sensor based on carbon black-poly(methylene blue)-poly(neutral red) composite. Biosensors. 12:329. doi: 10.3390/bios12050329.
  • Karaghool H. 2021. Biodecolorization of methylene blue using Aspergillus consortium. IOP Conf Ser. 779:012111. doi: 10.1088/1755-1315/779/1/012111.
  • Kehrmann F, Havas E, Grandmougin E. 1913. Zur Kenntnis der Farbsalze der Azin‐Farbstoffe II. Ber Dtsch Chem Ges. 46:2802–2808. doi: 10.1002/cber.19130460351.
  • Kellogg JA, Seiple JW, Klinedinst JL, 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. J Clin Microbiol. 34:2590–2592. doi: 10.1128/jcm.34.10.2590-2592.1996.
  • Khadieva A, Mostovaya O, Padnya P, Kalinin V, Grishaev D, Tumakov D, Stoikov I. 2021. Arylamine analogs of methylene blue: substituent effect on aggregation behavior and DNA binding. Int J Mol Sci. 22:5847. doi: 10.3390/ijms22115847.
  • Khadieva A, Rayanov M, Shibaeva K, Piskunov A, Padnya P, Stoikov I. 2022. Towards asymmetrical methylene blue analogues: synthesis and reactivity of 3-n′-arylaminophenothiazines. Molecules. 27:3024. doi: 10.3390/molecules27093024.
  • Khan H, Rauf F, Muhammad N, Javaid M, Alam S, Nasir S. 2022a. Comparison of special stains (Giemsa stain and modified toluidine blue stain) with immunohistochemistry as gold standard for the detection of H. pylori in gastric biopsies. Arab J Gastroenterol. 23:75–81. doi: 10.1016/j.ajg.2021.12.005.
  • Khan I, Saeed K, Zekker I, Zhang B, Hendi AH, Ahmad A, Ahmad S, Zada N, Ahmad H, Shah LA, Shah T, Khan I. 2022a. Review on methylene blue: its properties, uses, toxicity and photodegradation. Water (Switzerland). 14:242. doi: 10.3390/w14020242.
  • Kishor R, Saratale GD, Saratale RG, Romanholo Ferreira LF, Bilal M, Iqbal HMN, Bharagava RN. 2021. Efficient degradation and detoxification of methylene blue dye by a newly isolated ligninolytic enzyme producing bacterium Bacillus albus MW407057. Colloids Surf B. 206:111947. doi: 10.1016/j.colsurfb.2021.111947.
  • Kostjukova LO, Leontieva SV, Kostjukov VV. 2021a. TD‐DFT absorption spectrum of azure A in aqueous solution: vibronic transitions and electronic properties. Int J Quant Chem. 121:26662. doi: 10.1002/qua.26662.
  • Kostjukova LO, Leontieva SV, Kostjukov VV. 2021b. TD-DFT/DFT study of thionine in aqueous solution: vibronic absorption spectrum and electronic properties. Optik. 242:167156. doi: 10.1016/j.ijleo.2021.167156.
  • Kostjukova LO, Leontieva SV, Kostjukov VV. 2021c. The vibronic absorption spectrum and electronic properties of azure B in aqueous solution: TD-DFT/DFT study. J Mol Graph Mod. 107:107964. doi: 10.1016/j.jmgm.2021.107964.
  • Kostjukova LO, Leontieva SV, Kostjukov VV. 2021d. Vibronic absorption spectrum and electronic properties of azure C in aqueous solution: TD-DFT study. Theor Chem Acc. 140:114. doi: 10.1007/s00214-021-02808-y.
  • Kostjukova LO, Leontieva SV, Kostjukov VV. 2021e. Vibronic absorption spectrum and electronic properties of methylene blue in aqueous solution: TD-DFT study. J Mol Liq. 336:116369. doi: 10.1016/j.molliq.2021.116369.
  • Kotani E, Takeya T, Shimizu H, Egawa H, Yamamoto T, Tobinaga S. 1997. Iron(iii) picolinate-catalyzed oxidative demethylation of N,N-dimethylaniline with hydrogen peroxide in the presence of acetic anhydride. Chem Pharm Bull (Tokyo). 45:2089–2092. doi: 10.1248/cpb.45.2089.
  • Krafts K, Hempelmann E, Oleksyn B. 2011. The color purple: from royalty to laboratory, with apologies to Malachowski. Biotech Histochem. 86:7–35. doi: 10.3109/10520295.2010.515490.
  • Kulikova T, Shiabiev I, Padnya P, Rogov A, Evtugyn G, Stoikov I, Porfireva A. 2023. Impedimetric DNA sensor based on electropolymerized N-phenylaminophenothiazine and thiacalix[4]arene tetraacids for doxorubicin determination. Biosensors. 13:513. doi: 10.3390/bios13050513.
  • Kumar R, Mishra S, Gwal A, Shanmugam R. 2021. Evaluation of paper-based point of care screening test for sickle cell disease. Ind J Clin Biochem. 37:185–191. doi: 10.1007/s12291-021-00962-5.
  • Kutsaya BF, Dain BY. 1951. Vosstanovitel’noe fotovycvetanie metilenovogo golubogo i ego tormozhenie v rastvore. Ukrain Himicheskij Zhur. 17:820–826.
  • Kuzin YI, Khadieva AI, Padnya PL, Khannanov AA, Kutyreva MP, Stoikov II, Evtugyn GA. 2021. Electrochemistry of new derivatives of phenothiazine: electrode kinetics and electropolymerization conditions. Electrochim Acta. 375:137985. doi: 10.1016/j.electacta.2021.137985.
  • Kuzin YI, Padnya PL, Stoikov II, Gorbatchuk VV, Stoikov DI, Khadieva AI, Evtugyn GA. 2020. Electrochemical behavior of the monomeric and polymeric forms of N-phenyl-3-(phenylimino)-3H-phenothiazin-7-amine. Electrochim Acta. 345:136195. doi: 10.1016/j.electacta.2020.136195.
  • Ladu AI, Satumari NA, Abba AM, Abulfathi FA, Jeffery C, Adekile A, Bates I, Paul D. 2023. Evaluation of two red cell inclusion staining methods for assessing spleen function among sickle cell disease patients in North-East Nigeria. Paul D, Ed. PLOS Glob Public Health. 3:0001552. doi: 10.1371/journal.pgph.0001552.
  • Le Calvez B, Eveillard M. 2022. Strike while the iron is hot: diagnosis of pediatric idiopathic pulmonary hemosiderosis. Blood. 139:2411–2411. doi: 10.1182/blood.2021015109.
  • Leishman WB. 1901. Note on a simple and rapid method of producing Romanowsky staining in malarial and other blood films. Br Med J. 2125:757–758. doi: 10.1136/bmj.2.2125.757.
  • Leung HHL, Perdomo J, Ahmadi Z, Zheng SS, Rashid FN, Enjeti A, Ting SB, Chong JJH, Chong BH. 2022. Netosis and thrombosis in vaccine-induced immune thrombotic thrombocytopenia. Nat Commun. 13:5206. doi: 10.1038/s41467-022-32946-1.
  • Lillie RD. 1942. Studies on polychrome methylene blue. II. Acid oxidation methods of polychroming. Stain Technol. 17:97–110. doi: 10.3109/10520294209105768.
  • Lillie RD. 1943. A Giemsa stain of quite constant composition and performance, made in the laboratory from eosin and methylene blue. Publ Health Rep. 58:449–452. doi: 10.2307/4584400.
  • Lillie RD. 1978. Romanowsky-malachowski stains, the so-called Romanowsky stain: Malachowski’s 1891 use of alkali polychromed methylene blue for malaria plasmodia. Stain Technol. 53:23–28. doi: 10.3109/10520297809111439.
  • Lillie RD, Donaldson PT, Pizzolato P, Russo A, Schefstad F. 1978. Preparation of eosinates and Giemsa stains of low azure B content from hot acid dichromate oxidized commercial medicinal methylene blue. Stain Technol. 53:337–343. doi: 10.3109/10520297809111956.
  • Lindman B, Medronho B, Alves L, Norgren M, Nordenskiöld L. 2021. Hydrophobic interactions control the self-assembly of DNA and cellulose. Q Rev Biophys. 54:3. doi: 10.1017/s0033583521000019.
  • Liu C-Y, Chen C-C, Bychkov A, Agarwal S, Zhu Y, Hang J-F, Lai C-R, Na HY, Park SY, Li W, Liu Z, Jain D, Suzuki A, Hirokawa M, Chia N, Nga ME, Jitpasutham T, Keelawat S, Satoh S, Gunawardena D, Kumarasinghe P, Jung CK, Kakudo K. 2021. Constitutive cytomorphologic features of medullary thyroid carcinoma using different staining methods. Diagnostics. 11:1396. doi: 10.3390/diagnostics11081396.
  • MacNeal WJ. 1906. Methylene violet and methylene azure. J Infect Dis. 3:412–433. doi: 10.1093/infdis/3.3.412.
  • MacNeal WJ. 1925. Methylene violet and methylene azure A and B. J Infect Dis. 36:538–546. doi: 10.1093/infdis/36.6.538.
  • Malanina A, Kuzin Y, Khadieva A, Shibaeva K, Padnya P, Stoikov I, Evtugyn G. 2023. Voltammetric sensor for doxorubicin determination based on self-assembled DNA-polyphenothiazine composite. Nanomaterials. 13:2369. doi: 10.3390/nano13162369.
  • Ma H, Murray JB, Luo H, Cheng X, Chen Q, Song C, Duan C, Tan P, Zhang L, Liu J, Morgan BA, Li J, Wan J, Baker LM, Finnie W, Guetzoyan L, Harris R, Hendrickson N, Matassova N, Simmonite H, Smith J, Hubbard RE, Liu G. 2022. PAC-FragmentDEL–photoactivated covalent capture of DNA-encoded fragments for hit discovery. RSC Med Chem. 13:1341–1349. doi: 10.1039/d2md00197g.
  • Marshall PN. 1976. The composition of stains produced by the oxidation of methylene blue. Histochem J. 8:431–442. doi: 10.1007/bf01003831.
  • Marshall PN, Bentley SA, Lewis SM. 1975. An evaluation of some commercial Romanowsky stains. J Clin Pathol. 28:680–685. doi: 10.1136/jcp.28.8.680.
  • Mathi A, Renuka IV, Imandi S. 2022. Efficacy of modified Leishman stain in peripheral blood smears using a scoring system. J Cardiovasc Des Res. 13:3230–3235.
  • Laboratorytests. 2023. May Grunwald-Giemsa stain: principle, preparation and procedure [accessed 2023 Jul 16]. https://laboratorytests.org/may-grunwald-giemsa-stain-principle-preparation-and-procedure/.
  • Meinel C. 1992. August Wilhelm Hofmann – “Regierender Oberchemiker”. Angew Chem. 104:1293–1309.
  • Michelle, Siregar RAN, Sanjaya A, Lucy J, Pinontoan R. 2020. Methylene blue decolorizing bacteria isolated from water sewage in Yogyakarta, Indonesia. Biodiversitas. 21:1136–1141. doi: 10.13057/biodiv/d210338.
  • Mohammed MI, Yahia IS, Abd El-Mongy S. 2023. Simple fabrication of PVA/PEG blend doped with methyl blue dye with superior optical limiting performance: enhanced luminescence property, structural, and dielectric properties. Mater Sci Eng B. 291:116390. doi: 10.1016/j.mseb.2023.116390.
  • Moriconi C, Dzieciatkowska M, Roy M, D’Alessandro A, Roingeard P, Lee JY, Gibb DR, Tredicine M, McGill MA, Qiu A, La Carpia F, Francis RO, Hod EA, Thomas T, Picard M, Akpan IJ, Luckey CJ, Zimring JC, Spitalnik SL, Hudson KE. 2022. Retention of functional mitochondria in mature red blood cells from patients with sickle cell disease. Br J Haematol. 198:574–586. doi: 10.1111/bjh.18287.
  • Mughal FP, Bergmann AC, Huynh HUB, Jørgensen SH, Mansha I, Kesmez M, Schürch PM, Theocharides APA, Hansen PR, Friis T, Holmström MO, Ciplys E, Slibinskas R, Højrup P, Houen G, Trier NH. 2022. Production and characterization of peptide antibodies to the C-terminal of frameshifted calreticulin associated with myeloproliferative diseases. Int J Mol Sci. 23:6803. doi: 10.3390/ijms23126803.
  • Müller-Walz R, Zimmermann HW. 1987. Uber Romanowsky-Farbstoffe und den Romanowsky-Giemsa-Effekt 4. Mitteilung. 87:157–172. doi: 10.1007/bf00533401.
  • Nabilah B, Purnomo AS, Rizqi HD, Putro HS, Nawfa R. 2022. The effect of Ralstonia pickettii bacterium addition on methylene blue dye biodecolorization by brown-rot fungus. Daed Dickin Heliyon 8:08963. doi: 10.1016/j.heliyon.2022.e08963.
  • Noraini CHC, Morad N, Norli I, Teng TT, Ogugbue CJ. 2012. Methylene blue degradation by Sphingomonas paucimobilis under aerobic conditions. Water Air Soil Pollut. 223:5131–5142. doi: 10.1007/s11270-012-1264-8.
  • Obata H. 1961. Photoreduction of methylene blue by visible light in the aqueous solution containing certain kinds of inorganic salts. II. Photobleached product. Bull Chem Soc Jpn. 34:1057–1063. doi: 10.1246/bcsj.34.1057.
  • Obata H, Koizumi M. 1957a. Photochemical reactions between methylene blue and tri-, di- and monomethylamine. I. Bull Chem Soc Jpn. 30:136–141. doi: 10.1246/bcsj.30.136.
  • Obata H, Koizumi M. 1957b. Photochemical reactions between methylene blue and tri-, di- and monomethylamine. II. Bull Chem Soc Jpn. 30:142–147. doi: 10.1246/bcsj.30.142.
  • Okia CC, Aine B, Kiiza R, Omuba P, Wagubi R, Muwanguzi E, Apecu Onyuthi R, Okongo B, Oyet C. 2019. Prevalence, morphological classification, and factors associated with anemia among pregnant women accessing antenatal clinic at Itojo Hospital, South Western Uganda. J Blood Med. 10:351–357. doi: 10.2147/jbm.s216613.
  • Oktiyani N, Muhlisin A, Roebiakto E, Norsiah W, Mahpolah M. 2022. Utilization of alternative buffer solutions for staining thin blood smears by the Giemsa, Wright stain and Romanowsky method. Trop H Med Res. 5:34–45. doi: 10.35916/thmr.v4i1.76.
  • Ornstein RL, Rein R. 1979. Energetic and structural aspects of ethidium cation intercalation into DNA minihelices. Biopolymers. 18:2821–2847. doi: 10.1002/bip.1979.360181112.
  • Padnya PL, Khadieva AI, Stoikov II. 2023. Current achievements and perspectives in synthesis and applications of 3,7-disubstituted phenothiazines as methylene blue analogues. Dyes Pigm. 208:110806. doi: 10.1016/j.dyepig.2022.110806.
  • Pal A, Ambulkar P, Waghmare J, Wankhede V, Shende M, Tarnekar A. 2018. Chromosomal aberrations in couples with pregnancy loss: a retrospective study. J Hum Reprod Sci. 11:247–253. doi: 10.4103/jhrs.jhrs_124_17.
  • Patel A, Klubo-Gwiezdzinska J, Hoperia V, Larin A, Jensen K, Bauer A, Vasko V. 2011. BRAF V600E mutation analysis from May-Grünwald Giemsa-stained cytological samples as an adjunct in identification of high-risk papillary thyroid carcinoma. Endocr Pathol. 22:195–199. doi: 10.1007/s12022-011-9180-9.
  • Paul P, Kumar GS. 2013. Spectroscopic studies on the binding interaction of phenothiazinium dyes toluidine blue O, azure A and azure B to DNA. Spectrochim Acta Part A. 107:303–310. doi: 10.1016/j.saa.2013.01.063.
  • Paul P, Hossain M, Yadav RC, Kumar GS. 2010. Biophysical studies on the base specificity and energetics of the DNA interaction of photoactive dye thionine: spectroscopic and calorimetric approach. Biophys Chem. 148:93–103. doi: 10.1016/j.bpc.2010.02.015.
  • Piaton E, Fabre M, Goubin-Versini I, Bretz-Grenier M-F, Courtade-Saïdi M, Vincent S, Belleannée G, Thivolet F, Boutonnat J, Debaque H, Fleury-Feith J, Vielh P, Cochand-Priollet B, Egelé C, Bellocq JP, Michiels JF. 2015. Recommandations techniques et règles de bonne pratique pour la coloration de May-Grünwald-Giemsa : revue de la littérature et apport de l’assurance qualité. Ann Pathol. 35:294–305. doi: 10.1016/j.annpat.2015.05.019.
  • Piaton E, Fabre M, Goubin-Versini I, Bretz-Grenier M-F, Courtade-Saïdi M, Vincent S, Belleannée G, Thivolet F, Boutonnat J, Debaque H,Fleury–Feith J, Vielh P, Egelé C, Bellocq JP, Michiels JF, Cochand–Priollet B. 2016. Guidelines for May-Grunwald-Giemsa staining in haematology and non-gynaecological cytopathology: recommendations of the French Society of Clinical Cytology (SFCC) and of the French Association for Quality Assurance in Anatomic and Cytologic Pathology (AFAQAP). Cytopathol. 27:359–368. doi: 10.1111/cyt.12323.
  • Pittman ME, Khararjian A, Wood LD, Montgomery EA, Voltaggio L. 2016. Prospective identification of Helicobacter pylori in routine gastric biopsies without reflex ancillary stains is cost-efficient for our health care system. Hum Pathol. 58:90–96. doi: 10.1016/j.humpath.2016.07.031.
  • Purnomo AS, Asranudin A, Prasetyoko D, Azizah YDN. 2021. The biotransformation and biodecolorization of methylene blue by xenobiotic bacterium Ralstonia pickettii. Indones J Chem. 21:1418–1430. doi: 10.22146/ijc.65806.
  • Purnomo AS, Prameswari AS, Rizqi HD, Alkas TR, Ediati R, Kusumawati Y. 2022. Biotransformation of methylene blue by mixed fungal cultures of Gloeophyllum trabeum and Aspergillus oryzae. Int J Technol. 13:1768–1777. doi: 10.14716/ijtech.v13i8.6111.
  • Raskin RE, Vickers J, Ward JG, Toland A, Torrance AG. 2019. Optimized immunocytochemistry using leukocyte and tissue markers on Romanowsky‐stained slides from dogs and cats. Vet Clin Pathol. 48:88–97. doi: 10.1111/vcp.12759.
  • Ree IMC, Lopriore E. 2019. Updates in neonatal hematology. hematology/oncology clinics of North America. Hematol Oncol Clin North Am. 33:521–532. doi: 10.1016/j.hoc.2019.01.013.
  • Reinke S, Bröckelmann PJ, Iaccarino I, Garcia-Marquez M, Borchmann S, Jochims F, Kotrova M, Pal K, Brüggemann M, Hartmann E, Sasse S, Kobe C, Mathas S, Soekler M, Keller U, Bormann M, Zimmermann A, Richter J, Fuchs M, von Tresckow B, Borchmann P, Schlößer H, von Bergwelt-Baildon M, Rosenwald A, Engert A, Klapper W. 2020. Tumor and microenvironment response but no cytotoxic T-cell activation in classic Hodgkin lymphoma treated with anti-PD1. Blood. 136:2851–2863. doi: 10.1182/blood.2020008553.
  • Roe MA, Lillie RD, Wilcox A. 1940. American azures in the preparation of satisfactory Giemsa stains for malaria parasites. Public Health Rep. 55:1272–1278. doi: 10.2307/4583362.
  • Roe MA, Wilcox A, Lillie RD. 1941. Eosinates of the azures and methylene blue in preparation of a satisfactory Giemsa stain from dyes of American manufacture. Public Health Rep. 56:1906–1909. doi: 10.2307/4583874.
  • Romanowsky DL. 1890. K voprosu o stroenii chuzhejadnyh maljarii. Vrach. 52:1171–1173.
  • Romanowsky DL. 1891. K voprosu o parazitologii i terapii bolotnoj lihoradki. Dissertacija na stepen’ doktora mediciny.
  • Sánchez-Viesca F, Gómez R. 2021. On the mechanism of the Caro synthesis of methylene blue. Earthline J Chem Sci. 6:209–214. doi: 10.34198/ejcs.6221.209214.
  • Savelev DV, Reznik AM, Chernov AS, Andreyuk DS, Mudrak AV. 2020. Alimemazine in treatment of agitation in schizophrenia. Z Nev Psikhiatr SS Korsakova. 120:68–76. doi: 10.17116/jnevro202012006268.
  • Schaefer FC, Zimmermann WD. 1968. Self-oxidation of methylene blue. Nature. 220:66–67. doi: 10.1038/220066a0.
  • Schwartz D, Beaufrère H. 2022. Hematology of psittacines. In: Brooks M, Harr K, Seelig D, Wardrop K, Weiss J, editors. Schalm’s veterinary hematology. 7th ed. Blackwell Publishing, Hoboken, NJ; p. 1127–1139. doi: 10.1002/9781119500537.ch124.
  • Seo JY, Jeong JH, Kim KH, Ahn J-Y, Park P-W, Seo Y-H. 2017. Laboratory diagnosis of Clostridium difficile infection: comparison of Techlab C. Diff Quik chek complete, xpert C. difficile, and multistep algorithmic approach. J Clin Lab Anal. 31:e22135. doi: 10.1002/jcla.22135.
  • Seo S-H, Joe A, Han H-W, Manivasagan P, Jang E-S. 2022. Methylene blue-loaded mesoporous silica-coated gold nanorods on graphene oxide for synergistic photothermal and photodynamic therapy. Pharmaceutics. 14:2242. doi: 10.3390/pharmaceutics14102242.
  • Shao H, Calvo KR, Grönborg M, Tembhare PR, Kreitman RJ, Stetler-Stevenson M, Yuan CM. 2013. Distinguishing hairy cell leukemia variant from hairy cell leukemia: development and validation of diagnostic criteria. Leuk Res. 37:401–409. doi: 10.1016/j.leukres.2012.11.021.
  • Singh J, Bhattacharji LM. 1944. Rapid staining of malarial parasites by a water soluble stain. Ind Med Gaz. 79:102–104.
  • Smyth MJ, Kelly JM, Sutton VR, Davis JE, Browne KA, Sayers TJ, Trapani JA. 2001. Unlocking the secrets of cytotoxic granule proteins. J Leuk Biol. 70:18–29. doi: 10.1189/jlb.70.1.18.
  • Snoek A, James P, Arenas-López S, Durward A. 2015. Levomepromazine for difficult sedation in pediatric intensive care. J Pediatr Intens Care. 3:53–57. doi: 10.3233/pic-14089.
  • Spegarova JS, Lawless D, Mohamad SMB, Engelhardt KR, Doody G, Shrimpton J, Rensing-Ehl A, Ehl S, Rieux-Laucat F, Cargo C, Griffin H, Mikulasova A, Acres M, Morgan NV, Poulter JA, Sheridan EG, Chetcuti P, O’Riordan S, Anwar R, Carter CR, Przyborski S, Windebank K, Cant AJ, Lako M, Bacon CM, Savic S, Hambleton S. 2020. Germline TET2 loss of function causes childhood immunodeficiency and lymphoma. Blood. 136:1055–1066. doi: 10.1182/blood.2020005844.
  • Stefanović D, Stefanović M, Nikin Z. 2013. Romanowsky-Giemsa as a counterstain for immunohistochemistry: optimizing a traditional reagent. Biotech Histochem. 88:329–335. doi: 10.3109/10520295.2013.785595.
  • Stip E, Rizvi TA, Mustafa F, Javaid S, Aburuz S, Ahmed NN, Abdel Aziz K, Arnone D, Subbarayan A, Al Mugaddam F, Khan G 2020. The large action of chlorpromazine: translational and transdisciplinary considerations in the face of covid-19. Front Pharmacol. 11:577678. doi: 10.3389/fphar.2020.577678.
  • Subapriya S, Vairamuthu S, Pazhanivel N, George RS, Vijayarani K, Mohamed Ali MG. 2018. Histopathological and immunohistochemical diagnosis of canine haemangiopericytoma. Int J Curr Microbiol App Sci. 7:1344–1348. doi: 10.20546/ijcmas.2018.706.158.
  • Suzuki H, Gen K, Takahashi Y. 2014. A naturalistic comparison study of the efficacy and safety of intramuscular olanzapine, intramuscular haloperidol, and intramuscular levomepromazine in acute agitated patients with schizophrenia. Hum Psychopharmacol Clin Exp. 29:83–88. doi: 10.1002/hup.2376.
  • Swenson CL, Boisvert AM, Gibbons-Burgener SN, Kruger JM. 2011. Evaluation of modified Wright-staining of dried urinary sediment as a method for accurate detection of bacteriuria in cats. Vet Clin Pathol. 40:256–264. doi: 10.1111/j.1939-165x.2011.00314.x.
  • Takahashi T, Suzuki T, Hiroshige S, Nouno S, Matsumura T, Tominaga T, Yujiri T, Katano H, Sato Y, Hasegawa H. 2019. Transient appearance of plasmablasts in the peripheral blood of Japanese patients with severe fever with thrombocytopenia syndrome. J Infect Dis. 220:23–27. doi: 10.1093/infdis/jiz054.
  • Tvedten H. 2020. Routine stains and automated stainers. In: Sharkey L, Radin M, Seelig D, Eds., Veterinary cytology. Blackwell Publishing, Hoboken, NJ; p. 12–17. doi: 10.1002/9781119380559.ch2.
  • Upendar G, Dutta S, Bhattacharya P, Dutta A. 2017. Bioremediation of methylene blue dye using Bacillus subtilis MTCC 441. Water Sci Technol. 75:1572–1583. doi: 10.2166/wst.2017.031.
  • Usui Y, Obata H, Koizumi M. 1961. Photoreduction of methylene blue by visible light in the aqueous solution containing certain kinds of inorganic salts. I. General features of the reaction. Bull Chem Soc Jpn. 34:1049–1056. doi: 10.1246/bcsj.34.1049.
  • Wakely PE Jr. 2022. Giant cell tumor of soft tissue: FNA cytopathology of 4 cases, review of the literature, and comparison with giant cell tumor of bone. Cancer Cytopathol. 130:120–127. doi: 10.1002/cncy.22517.
  • Wakely PE Jr, Lott‐Limbach AA. 2021. Cytopathology of acinic cell carcinoma: a study of 50 cases, including 9 with high‐grade transformation. Cancer Cytopathol. 129:973–983. doi: 10.1002/cncy.22496.
  • Weil L. 1948. Photochemical oxidation of nicotine in the presence of methylene blue. Science. 107:426–427. doi: 10.1126/science.107.2782.426.
  • Wittekind DH, Gehring T. 1985. On the nature of Romanowsky-Giemsa staining and the Romanowsky-Giemsa effect. I. Model experiments on the specificity of azures B-eosin Y stain as compared with other thiazine dye-eosin Y combinations. Histochem J. 17:263–289. doi: 10.1007/bf01004591.
  • Wright JH. 1902. A rapid method for the differential staining of blood films and malarial parasites. J Med Res. 7:138–144.
  • Xue H, Thaivalappil A, Cao K. 2021. The potentials of methylene blue as an anti-aging drug. Cells. 10:3379. doi: 10.3390/cells10123379.
  • Yunis JJ, Sanchez O. 1973. G-banding and chromosome structure. Chromosoma. 44:15–23. doi: 10.1007/bf00372570.
  • Zaied M, Peulon S, Bellakhal N, Desmazières B, Chaussé A. 2011. Studies of N-demethylation oxidative and degradation of methylene blue by thin layers of birnessite electrodeposited onto SnO2. Appl Catal B. 101:441–450. doi: 10.1016/j.apcatb.2010.10.014.
  • Zeng G, Cheng M, Huang D, Lai C, Xu P, Wei Z, Li N, Zhang C, He X, He Y. 2015. Study of the degradation of methylene blue by semi-solid-state fermentation of agricultural residues with Phanerochaete chrysosporium and reutilization of fermented residues. Waste Manag. 38:424–430. doi: 10.1016/j.wasman.2015.01.012.
  • Zinin N. 1842. Beschreibung einiger neuer organischen Basen, dargestellt durch die Einwirkung des Schwefelwasserstoffes auf Verbindungen der Kohlenwasserstoffe mit Untersalpetersäure. J Prakt Chem. 27:140–153. doi: 10.1002/prac.18420270125.
  • Zipfel E, Grezes J-R, Naujok A, Seiffert W, Wittekind DH, Zimmermann HW. 1984. Uber Romanowsky-Farbstoffe und den Romanowsky-Giemsa-Effekt 3. Mitteilung: Mikrospektralphotometrische Untersuchung der Romanowsky-Giemsa-Fiirbung. Spektroskopischer Nachweis eines DNA-Azur B-Eosin Y-Komplexes, der den Romanowsky-Giemsa-Effekt verursacht. Histochemistry. 81:337–351. doi: 10.1007/BF00514328.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.