A Propolis Extract and the Labeling of Blood Constituents with Technetium-99m

Abstract

Since ancient times propolis has been employed for many human purposes because to their favourable properties. Blood constituents labeled with technetium-99m (99mTc) have been used in nuclear medicine procedures. Some authors have reported that synthetic or natural drugs can interfere with the labeling of blood constituents with 99mTc. The aim of this work was to evaluate the action of a propolis extract on the labeling of blood elements with 99mTc. Samples of whole blood of male Wistar rats were incubated in sequence with an aqueous propolis extract at different concentrations, stannous chloride and 99mTc, as sodium pertechnetate. Blood samples were centrifuged to separate plasma and blood cells, soluble and insoluble fractions of plasma and blood cells were also separated after precipitation in trichloroacetic acid solution and centrifugation. The radioactivity was counted and the percentage of incorporated radioactivity (%ATI) for each fraction was calculated. The data obtained showed that the aqueous propolis extract used decreased significantly the %ATI in plasma proteins at higher concentration studied. Results suggest that at high concentration the constituents of this extract could alter the labeling of plasma proteins competing with same binding sites of the 99mTc on the plasma proteins or acting as antioxi-dant compounds.

References

  1. 1.

    Ahn, M. R., Kumazawa, S., Hamasaka, T., Bang, K. S., Nakayama, T. (2004) Antioxidant activity and constituents of propolis collected in various areas of Korea. J. Agric. Food Chem. 52, 7286–7292.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. 2.

    Aliyazicioglu, Y., Deger, O., Ovali, E., Barlak, Y., Hosver, I., Tekelioglu, Y., Karahan, S. C. (2005) Effects of Turkish pollen and propolis extracts on respiratory burst for K-562 cell lines. Int. Immunopharmacol. 5, 1652–1657.

    Article  CAS  Google Scholar 

  3. 3.

    Artiko, V., Obradovic V., Petrovic, M., Perisic-Savic, M., Suvajdzic, N. (2004) Hemangioma of the spleen confirmed by blood pool scintigraphy. Clin. Nucl. Med. 29, 670–671.

    Article  PubMed  PubMed Central  Google Scholar 

  4. 4.

    Bankova, V., Christov, R., Kujumgiev, A., Marcucci, M. C., Popov, S. (1995) Chemical composition and antibacterial activity of Brazilian propolis. Z. Naturforsch Section C. Bioscience 50, 167–172.

    Article  CAS  Google Scholar 

  5. 5.

    Bankova, V. S., De Castro, S. L., Marcucci, M. C. (2000) Propolis: recent advances in chemistry and plant origin. Apidologie 31, 3–15.

    Article  CAS  Google Scholar 

  6. 6.

    Banskota, A. H., Tezuka, Y., Adnyana, I. K., Ishii, E., Midorikawa, K., Matsushige, K., Kadota, S. (2001) Hepatoprotective and anti-Helicobacter pylori activities of constituents from Brazilian propolis. Phytomed. 8, 16–23.

    Article  CAS  Google Scholar 

  7. 7.

    Banskota, A. H., Tezuka, Y., Adnyana, I. K., Midorikawa, K., Matsushige, K., Message, D., Huertas, A. A., Kadota, S. (2000) Cytotoxic, hepatoprotective and free radical scavenging effects of propolis from Brazil, Peru, the Netherlands and China. J. Ethnopharmacol. 72, 239–246.

    Article  CAS  Google Scholar 

  8. 8.

    Bernardo-Filho, M., Caniné, M. S., Lopes, R. L. F., Boasquevisque, E. M. (1986) Effect of temperature on the “in vitro“ labeling of red blood cells with technetium-99m. Arq. Biol. Technol. 29, 407–412.

    CAS  Google Scholar 

  9. 9.

    Bernardo-Filho, M., Gutfilen, B., Maciel, O. S. (1994) Effect of different anticoagulants on the labeling of red blood cells and plasma proteins with Tc-99m. Nucl. Med. Commun. 15, 730–734.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. 10.

    Bernardo-Filho, M., Moura, I. N. S., Boasquevisque, E.M. (1983) 99m-technetium-labeled red blood cells “in vitro”. Arq. Biol. Tecnol. 26, 455–461.

    CAS  Google Scholar 

  11. 11.

    Bernardo-Filho, M., Pires, E. T., Boasquevisque, E. M., Hassón-Voloch, A. (1993) Studies on the incorporation of 99mtechnetium to the platyhelmint Dugesia tigrina. Rev. Parasitol. 44, 7–11.

    Google Scholar 

  12. 12.

    Bernardo-Filho, M., Silva, J. R. M., Reis, R. J. N., Boasquevisque, E. M., Hassón-Voloch, A. (1992) Conditions for labeling of Schistosoma mansoni cercaria with technetium-99m. J. Nucl. Biol. Med. 36, 56–59.

    CAS  PubMed  Google Scholar 

  13. 13.

    Botushanov P. I., Grigorov, G. I., Aleksandrov, G. A. (2001) A clinical study of a silicate toothpaste with extract from propolis. Folia Med (Plovdiv). 43, 28–30.

    CAS  Google Scholar 

  14. 14.

    Burdock, G. A. (1998) Review of the biological properties and toxicity of bee propolis (propolis). Food Chem. Toxicol. 36, 347–363.

    Article  CAS  Google Scholar 

  15. 15.

    Callahan, R. J., Rabito, C. A. (1990) Radiolabeling of erythrocytes with technetium-99m: role of band-3 protein in the transport of pertechnetate across the cell membrane. J. Nucl. Med. 31, 2004–2008.

    CAS  PubMed  Google Scholar 

  16. 16.

    Castaldo, S., Capasso, F. (2002) Propolis, an old remedy used in modern medicine. Fitoterapia 73 Suppl. 1, S1–S6

    Article  CAS  Google Scholar 

  17. 17.

    Chen, C. N., Wu, C. L., Shy, H. S., Lin, J. K. (2003) Cytotoxic prenylflavanones from Taiwanese propolis. J. Nat. Prod. 66, 503–506.

    Article  CAS  Google Scholar 

  18. 18.

    Cirasino, L., Pisati, A., Fasani, F. (1987) Contact dermatitis from propolis. Contact Dermatitis 16, 110–111.

    Article  CAS  Google Scholar 

  19. 19.

    Coprean, D., Rusu, M., Giurgea, R., Popescu, H., Polinicencu, C. (1986) Effect of standardized propolis extract in the experimentally intoxicated liver of rats. Clujul Med. 59, 333–337. (in Rumanian)

    CAS  Google Scholar 

  20. 20.

    Cortes, J., Alonso, J. I., Ruiz-Oliva, F., Alvarez, S., Ormijana, J. S., Caton, B., Alcorta, P. (2003) Renal cell carcinoma detected on Tc-99m-labeled red blood cell imaging. Clin. Nucl. Med. 28, 920–922.

    Article  PubMed  Google Scholar 

  21. 21.

    Cushnie, T. P., Lamb, A. J. (2005) Detection of galangin-induced cytoplasmic membrane damage in Staphylococcus aureus by measuring potassium loss. J. Ethnopharmacol. 101, 243–248.

    Article  CAS  Google Scholar 

  22. 22.

    D’Auria, F. D., Tecca, M., Scazzocchio, F., Renzini, V., Strippoli, V. (2003) Effect of propolis on virulence factors of Candida albicans. J. Chemother. 15, 454–460.

    Article  Google Scholar 

  23. 23.

    de Castro, S. L., Higashi, K. O. (1995) Effect of different formulations of propolis on mice infected with Trypanosoma cruzi. J. Ethnopharmacol. 46, 55–58.

    Article  Google Scholar 

  24. 24.

    Dewanjee, M. K. (1974) Binding of 99mTc ion to hemoglobin. J. Nucl. Med. 15, 703–706.

    CAS  PubMed  Google Scholar 

  25. 25.

    Diré, G., Lima, E. A. C., Gomes, M. L., Moreno, S., Marques, M. T. Q., Jales, R. L., Caldeira-De-Araújo, A., Bernardo-Filho, M. (2004) An in vitro study of a natural product (chayote): an analysis on the labeling of blood components with technetium-99m an on the morphology of DNA. J. Food Technol. 2, 71–75.

    Google Scholar 

  26. 26.

    Early, P. J., Sodee, D. B. (1995) Principles and Practice of Nuclear Medicine. Mosby, Toronto.

    Google Scholar 

  27. 27.

    Feres, M., Figueiredo, L. C., Barreto, I. M., Coelho, M. H., Araujo, M. W., Cortelli, S. C. (2005) In vitro antimicrobial activity of plant extracts and propolis in saliva samples of healthy and periodon-tally-involved subjects. J. Int. Acad. Periodontol. 7, 90–96.

    PubMed  Google Scholar 

  28. 28.

    Fonseca, A. S., Frydman, J. N. G., Santos, R., Bernardo-Filho, M. (2005) Influence of antipyretic drugs on the labeling of blood elements with technetium-99m. Acta Biol. Hung. 56, 275–282.

    Article  CAS  Google Scholar 

  29. 29.

    Frenkel, K., Wei, H., Bhimani, R., Ye, J., Zadunaisky, J. A., Huang, M. T., Ferraro, T., Conney, A. H., Grunberger, D. (1993) Inhibition of tumor promoter-mediated processes in mouse skin and bovine lens by caffeic acid phenethyl ester. Cancer Res. 53, 1255–1261.

    CAS  PubMed  Google Scholar 

  30. 30.

    Frydman, J. N. G., Oliveira, M. B. N., Santos, A. E. O., Fonseca, A. S., Santos, R., Bernardo-Filho, M. (2004) Influence of methylxanthines on the labeling of blood elements with 99mTechnetium. Pak. J. Biol. Sci. 4, 521–524.

    Article  Google Scholar 

  31. 31.

    Gonzalez, R., Corcho, I., Remirez, D., Rodriguez, S., Ancheta, O., Merino, N., Gonzalez, A., Pascual, C. (1995) Hepatoprotective effects of propolis extract on carbon tetrachloride-induced liver injury in rats. Phytother. Res. 9, 114–117.

    Article  Google Scholar 

  32. 32.

    Greenaway, W., May, J., Scaysbrook, T., Whatley, F. R. (1991) Identification by gas chromatogra-phymass spectrometry of 150 compounds in propolis. Z. Naturforschung 46c, 111–121.

    Article  Google Scholar 

  33. 33.

    Greenaway, W., Scaysbrook, T., Whatley, F. R. (1987) The analysis of bud exudate of Poppulus × euramericana, and of propolis, by gas chromatography-mass spectrometry. Proc. Royal Soc. London B, 232, 249–272.

    Article  CAS  Google Scholar 

  34. 34.

    Greenaway, W., Scaysbrook, T., Whatley, F. R. (1990) The composition and plant origins of propolis: a report of work at Oxford. Bee World 71, 107–118.

    Article  Google Scholar 

  35. 35.

    Gutfilen, B., Boasquevisque, E. M., Bernardo-Filho, M. (1992) Calcium channel blockers: interference on red blood cells and plasma proteins labeling with 99mTc. Ver. Espanola Med. Nucl. 11, 195–199.

    Google Scholar 

  36. 36.

    Harel, F., Dupuis, J., Benelfassi, A., Ruel, N., Gregoire, J. (2005) Radionuclide plethysmography for non-invasive evaluation of peripheral arterial blood flow. Am. J. Physiol. Heart Circ. Physiol. (in press).

    Google Scholar 

  37. 37.

    Havsteen, B. H. (2002) The biochemistry and medical significance of the flavonoids. Pharmacol. Ther. 96, 67–202.

    Article  CAS  Google Scholar 

  38. 38.

    Hladik III, W. B., Saha, G. B., Study, K. T. (1987) Essentials of Nuclear Medicine Sciences. Williams and Wilkins, Sydney.

    Google Scholar 

  39. 39.

    Hu, F., Hepburn, H. R., Li, Y., Chen, M., Radloff, S. E., Daya, S. (2005) Effects of ethanol and water extracts of propolis (bee glue) on acute inflammatory animal models. J. Ethnopharmacol. 14 (in press).

  40. 40.

    Ikeno, K., Ikeno, T., Miyazawa, C. (1991) Effects of propolis on dental caries in rats. Caries Res. 25, 347–351.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. 41.

    Jin, R. B., Ma, X. L., Wen, J. L., Tang, W. J. (2004) Application of radionuclide imaging to hepatic impact injury in rabbits. Chin. J. Traumatol. 7, 45–48.

    PubMed  PubMed Central  Google Scholar 

  42. 42.

    Johnson, K. S., Eischen, F. A., Giannasi, D. E. (1994) Chemical composition of North American bee propolis and biological activity towards larvae of greater wax moth (Lepidoptera: Pyralidae). J. Chem. Ecol. 20, 1783–1792.

    Article  CAS  Google Scholar 

  43. 43.

    Koo, H., Cury, J. A., Rosalen, P. L., Ambrosano, G. M., Ikegaki, M., Park, Y. K. (2002) Effect of a mouthrinse containing selected propolis on 3-day dental plaque accumulation and polysaccharide formation. Caries Res. 36, 445–448.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. 44.

    Liu, C. F., Lin, C. C., Lin, M. H., Lin, Y. S., Lin, S. C. (2002) Cytoprotection by propolis ethanol extract of acute absolute ethanol-induced gastric mucosal lesions. Am. J. Chin. Med. 30, 245–254.

    Article  Google Scholar 

  45. 45.

    Manach, C., Morand, C., Crespy, V., Demigne, C., Texier, O., Regerat, F., Remesy, C. (1998) Quercetin is recovered in human plasma as conjugated derivatives which retain antioxidant properties. FEBS Lett. 426, 331–336.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. 46.

    Marcucci, M. C. (1995) Propolis: Chemical composition, biological properties and therapeutic activity. Apidologie 26, 8399.

    Article  Google Scholar 

  47. 47.

    Marquele, F. D., Di Mambro, V. M., Georgetti, S. R., Casagrande, R., Valim, Y. M., Fonseca, M. J. (2005) Assessment of the antioxidant activities of Brazilian extracts of propolis alone and in topical pharmaceutical formulations. J. Pharm. Biomed. Anal. (in press).

    Google Scholar 

  48. 48.

    Marques, R. G., Petroianu, A., de Oliveira, M. B., Bernardo-Filho, M., Portela, M. C. (2004) Evaluation of possible failure of the mononuclear phagocyte after total splenectomy in rats. Braz. Arch. Biol. Technol. 47, 199–204.

    Article  Google Scholar 

  49. 49.

    Mirzoeva, O. K., Grishanin, R. N., Calder, P. C. (1997) Antimicrobial action of propolis and some of its components: the effects on growth, membrane potential and motility of bacteria. Microbiol. Res. 152, 239–246.

    Article  CAS  Google Scholar 

  50. 50.

    Protection of plasmid DNA by a Ginkgo biloba extract from the effects of stannous chloride and the action on the labeling of blood elements with technetium-99m. Braz. J. Med. Biol. Res. 37, 267–271.

  51. 51.

    Na, H. K., Wilson, M. R., Kang, K. S., Chang, C. C., Grunberger, D., Trosko, J. E. (2000) Restoration of gap junctional intercellular communication by caffeic acid phenethyl ester (CAPE) in a ras-trans-formed rat liver epithelial cell line. Cancer Lett. 157, 31–38.

    Article  CAS  Google Scholar 

  52. 52.

    Niemeyer, M. G., van der Wall, E. E., Kuijper, A. F., Cleophas, A. T., Pauwels, E. K. (1995) Nuclear cardiology, current applications in clinical practice. Angiology 46, 591–602.

    Article  CAS  Google Scholar 

  53. 53.

    Olds, G. D., Cooper, G. S., Chak, A., Sivak, M. V. Jr., Chitale, A. A., Wong, R. C. (2005) The yield of bleeding scans in acute lower gastrointestinal hemorrhage. J. Clin. Gastroenterol. 39, 273–277.

    Article  PubMed  PubMed Central  Google Scholar 

  54. 54.

    Okutan, H., Ozcelik, N., Yilmax, H. R., Uz, E. (2005) Effects of caffeic acid phenethyl ester on lipid peroxidation and antioxidant enzymes in diabetic rat heart. Clin. Biochem. 38, 191–196.

    Article  CAS  Google Scholar 

  55. 55.

    Oliveira, J. F., Oliveira, M. B. N., Avila, A. S., Braga, A. C. S., Catanho, M. T. J., Jales, R. L., Cardoso, V. N., Bernardo-Filho, M. (2003a) Assessment of the effect of Fucus vesiculosus extract on the labeling of blood constituents with technetium-99m and the histological modifications on the shape of the red blood cells. Food Chem. Toxicol. 41, 15–20.

    Article  Google Scholar 

  56. 56.

    Oliveira, J. F., Santos-Filho, S. D., Catanho, M. T. J., Srivastava, S. C., Lima-Filho, G., Bernardo-Filho, M. (2003b) Effect of extract of medicinal plant on the labeling of blood elements with tech-netium-99m and on the morphology of red blood cells (RBC): toxicological action of roast coffee beans (Coffea arabica). Ind. J. Nucl. Med. 18, 52–56.

    Google Scholar 

  57. 57.

    Oliveira, M. B., Fonseca, A. S., Bernardo-Filho, M., Santos, R. (2002) Study of the biodistribution of the amantadine labelled with technetium-99m in Wistar female rats. Cell Mol. Biol. (Noisy-legrand) 48, 767–769.

    CAS  Google Scholar 

  58. 58.

    Plotkowski, M. C., Bernardo-Filho, M., Meirelles, M. N., Tournier, J. M., Puchelle, E. (1993) Pseudomonas aeruginosa binds to soluble cellular fibronectin. Current Microbiol. 26, 91–95.

    Article  CAS  Google Scholar 

  59. 59.

    Podhajcer, O. L., Friedlander, M., Graziani, Y. (1980) Effect of liposome-encapsulated quercetin on DNA synthesis, lactate production, and cyclic adenosine 3′:5′-monophosphate level in Ehrlich ascites tumor cells. Cancer Res. 40, 1344–1350.

    CAS  PubMed  Google Scholar 

  60. 60.

    Rao, C. V., Desai, D., Simi, B., Kulkarni, N., Amin, S., Reddy, B. S. (1993) Inhibitory effect of caf-feic acid esters on azoxymethane-induced biochemical changes and aberrant crypt foci formation in rat colon. Cancer Res. 53, 4182–4188.

    CAS  PubMed  Google Scholar 

  61. 61.

    Rodriguez, S., Ancheta, O., Ramos, M. E., Remirez, D., Rojas, E., Gonzalez, R. (1997) Effects of Cuban red propolis on galactosamine-induced hepatitis in rats. Pharmacol. Res. 35, 1–4.

    Article  CAS  PubMed  Google Scholar 

  62. 62.

    Russo, A., Cardile, V., Sanchez, F., Troncoso, N., Vanella, A., Garbarino, J. A. (2004) Chilean propolis: antioxidant activity and antiproliferative action in human tumor cell lines. Life Sci. 76, 545–558.

    Article  CAS  PubMed  Google Scholar 

  63. 63.

    Saha, G. B. (2003) Fundamentals of Nuclear Pharmacy. Springer-Verlag, New York.

    Google Scholar 

  64. 64.

    Sahinler, N., Kaftanoglu, O. (2005) Natural product propolis: chemical composition. Nat. Prod. Res. 19, 183–188.

    Article  CAS  PubMed  Google Scholar 

  65. 65.

    Sampson, C. B. (1996) Complications and difficulties in radiolabelling blood cells: a review. Nucl. Med. Commun. 17, 648–658.

    Article  CAS  PubMed  Google Scholar 

  66. 66.

    Scheller, S., Krol, W., Swiacik, J., Owczarek, S., Gabrys, J., Shani, J. (1987) Antitumoral property of ethanolic extract of propolis in mice-bearing Ehrlich carcinoma, as compared to bleomycin. Z. Naturforsch. [C] 44, 1063–1065.

    Article  Google Scholar 

  67. 67.

    Slart, R. H., Phan, T. T., Talsma, M. D., Jager, P. L. (2004) Different splenic uptake of Tc-99m sulfur colloid and Tc-99m heat-denatured red blood cells in an infant with complete situs inversus. Clin. Nucl. Med. 29, 590–591.

    Article  Google Scholar 

  68. 68.

    Song, Y. S., Park, E. H., Hur, G. M., Ryu, Y. S., Lee, Y. S., Lee, J. Y., Kim, Y. M., Jin, C. (2002) Caffeic acid phenethyl ester inhibits nitric oxide synthase gene expression and enzyme activity. Cancer Lett. 175, 53–61.

    Article  CAS  Google Scholar 

  69. 69.

    Verdu, J., Martinez, A., Anton, M. A., Munoz, J. M., Riera, M., Jover, R., Caballero, O. (2005) Increased thallium-201 uptake and Tc-99m red blood cell accumulation in hemangioma. Clin. Nucl. Med. 30, 25–26.

    Article  Google Scholar 

  70. 70.

    Volpert, R., Elstner, E. F. (1996) Interactions of different extracts of propolis with leukocytes and leukocytic enzymes. Arzneimittelforschung 46, 47–51.

    CAS  PubMed  PubMed Central  Google Scholar 

  71. 71.

    Wong, K. T., Beauvais, M. M., Melchior, W. R., Snyder, S. P. (2004) Enhanced liver uptake of Tc-99m-labeled RBCs during gastrointestinal bleed scintigraphy using transfused RBCs compared with autologous RBCs. Clin. Nucl. Med. 29, 522–523.

    Article  Google Scholar 

  72. 72.

    Zaman, M. U., Hussain, R., Sajjad, Z., Ahmad, M. N. (2004) Localization of upper GI bleed on delayed imaging with 99mTc tagged RBC angiogram. J. Pak. Med. Assoc. 54, 490–491.

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to A. S. Fonseca.

Rights and permissions

This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Reprints and Permissions

About this article

Cite this article

Jesus, L.M., Abreu, P.R.C., Almeida, M.C. et al. A Propolis Extract and the Labeling of Blood Constituents with Technetium-99m. BIOLOGIA FUTURA 57, 191–200 (2006). https://doi.org/10.1556/ABiol.57.2006.2.6

Download citation

Keywords

  • Propolis
  • blood constituents
  • plasma proteins
  • technetium-99m