Table of Contents Author Guidelines Submit a Manuscript
Anemia
Volume 2016, Article ID 9310905, 8 pages
http://dx.doi.org/10.1155/2016/9310905
Review Article

Erythropoiesis in Malaria Infections and Factors Modifying the Erythropoietic Response

1Department of Haematogenetics, National Institute of Immunohaematology (ICMR), KEM Hospital, Parel, Mumbai 400012, India
2Surat Raktadan Kendra & Research Centre, Udhna Khatodara Urban Health Centre, Udhna Magdalla Road, Surat, Gujrat 395002, India

Received 19 October 2015; Accepted 2 February 2016

Academic Editor: Maria Stella Figueiredo

Copyright © 2016 Vrushali A. Pathak and Kanjaksha Ghosh. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. B. M. Greenwood, “The epidemiology of malaria,” Annals of Tropical Medicine and Parasitology, vol. 91, no. 7, pp. 763–769, 1997. View at Publisher · View at Google Scholar · View at Scopus
  2. K. Ghosh and K. Ghosh, “Pathogenesis of anemia in malaria: a concise review,” Parasitology Research, vol. 101, no. 6, pp. 1463–1469, 2007. View at Publisher · View at Google Scholar · View at Scopus
  3. WHO, Haemoglobin Concentrations for the Diagnosis of Anaemia and Assessment of Severity, Vitamin and Mineral Nutrition Information System, World Health Organization, Geneva, Switzerland, 2011.
  4. R. E. Phillips and G. Pasvol, “Anaemia of Plasmodium falciparum malaria,” Baillière's Clinical Haematology, vol. 5, no. 2, pp. 315–330, 1992. View at Publisher · View at Google Scholar · View at Scopus
  5. T. Panichakul, W. Payuhakrit, P. Panburana, C. Wongborisuth, S. Hongeng, and R. Udomsangpetch, “Suppression of erythroid development in vitro by Plasmodium vivax,” Malaria Journal, vol. 11, article 173, 2012. View at Publisher · View at Google Scholar · View at Scopus
  6. N. Thawani, M. Tam, M.-J. Bellemare et al., “Plasmodium products contribute to severe malarial anemia by inhibiting erythropoietin-induced proliferation of erythroid precursors,” Journal of Infectious Diseases, vol. 209, no. 1, pp. 140–149, 2014. View at Publisher · View at Google Scholar · View at Scopus
  7. S. Abdalla, D. J. Weatherall, S. N. Wickramasinghe, and M. Hughes, “The anaemia of P. falciparum malaria,” British Journal of Haematology, vol. 46, no. 2, pp. 171–183, 1980. View at Publisher · View at Google Scholar · View at Scopus
  8. S. N. Wickramasinghe, S. Looareesuwan, B. Nagachinta, and N. J. White, “Dyserythropoiesis and ineffective erythropoiesis in Plasmodium vivax malaria,” British Journal of Haematology, vol. 72, no. 1, pp. 91–99, 1989. View at Publisher · View at Google Scholar · View at Scopus
  9. S. N. Wickramasinghe and S. H. Abdalla, “Blood and bone marrow changes in malaria,” Bailliere's Best Practice and Research in Clinical Haematology, vol. 13, no. 2, pp. 277–299, 2000. View at Publisher · View at Google Scholar · View at Scopus
  10. G. Vryonis, “Observations in the parasitisation of erythrocytes by Plasmodium vivax, with special reference to reticulocytes,” American Journal of Hygiene, vol. 30, article 41, 1939. View at Google Scholar
  11. T. Srichaikul, M. Wasanasomsithi, V. Poshyachinda, N. Panikbutr, and T. Rabieb, “Ferrokinetic studies and erythropoiesis in malaria,” Archives of Internal Medicine, vol. 124, no. 5, pp. 623–628, 1969. View at Publisher · View at Google Scholar · View at Scopus
  12. J. A. L. Kurtzhals, O. Rodrigues, M. Addae, J. O. O. Commey, F. K. Nkrumah, and L. Hviid, “Reversible suppression of bone marrow response to erythropoietin in Plasmodium falciparum malaria,” British Journal of Haematology, vol. 97, no. 1, pp. 169–174, 1997. View at Publisher · View at Google Scholar · View at Scopus
  13. G. R. Lee, Anemia: General Aspects, Lippincott Williams & Wilkins, Baltimore, Md, USA, 10th edition, 1999.
  14. T. Were, J. B. Hittner, C. Ouma et al., “Suppression of RANTES in children with Plasmodium falciparum malaria,” Haematologica, vol. 91, no. 10, pp. 1396–1399, 2006. View at Google Scholar
  15. T. Srichaikul, T. Siriasawakul, and M. Poshyachinda, “Ferrokinetics in patients with malaria: haemoglobin synthesis and normoblasts in vitro,” Transactions of the Royal Society of Tropical Medicine and Hygiene, vol. 70, no. 3, pp. 244–246, 1976. View at Publisher · View at Google Scholar · View at Scopus
  16. P. Dormer, M. Dietrich, P. Kern, and R. D. Horstmann, “Ineffective erythropoiesis in acute human P. falciparum malaria,” Blut, vol. 46, no. 5, pp. 279–288, 1983. View at Publisher · View at Google Scholar · View at Scopus
  17. S. H. Abdalla and S. N. Wickramasinghe, “A study of erythroid progenitor cells in the bone marrow of Gambian children with falciparum malaria,” Clinical and Laboratory Haematology, vol. 10, no. 1, pp. 33–40, 1988. View at Publisher · View at Google Scholar · View at Scopus
  18. S. H. Abdalla, “Hematopoiesis in human malaria,” Blood Cells, vol. 16, no. 2-3, pp. 401–419, 1990. View at Google Scholar
  19. H. Verhoef, C. E. West, R. Kraaijenhagen et al., “Malarial anemia leads to adequately increased erythropoiesis in asymptomatic Kenyan children,” Blood, vol. 100, no. 10, pp. 3489–3494, 2002. View at Publisher · View at Google Scholar · View at Scopus
  20. R. Carter and D. Walliker, “New observations on the malaria parasites of rodents of the Central African republic: Plamodium vinkei petteri subsp. Nov and Plasmodium chabaudi Landau, 1965,” Annals of Tropical Medicine and Parasitology, vol. 69, no. 2, pp. 187–196, 1975. View at Google Scholar
  21. K. Chotivanich, R. Udomsangpetch, J. A. Simpson et al., “Parasite multiplication potential and the severity of Falciparum malaria,” Journal of Infectious Diseases, vol. 181, no. 3, pp. 1206–1209, 2000. View at Publisher · View at Google Scholar · View at Scopus
  22. P. C. C. Garnham, R. G. Bird, J. R. Baker, S. S. Desser, and H. M. S. El-Nahal, “Electron microscope studies on motile stages of malaria parasites VI. The oöknete of Plasmodium berghei yoelii and its transformation into the early oocyst,” Transactions of the Royal Society of Tropical Medicine and Hygiene, vol. 63, no. 2, pp. 187–194, 1969. View at Publisher · View at Google Scholar · View at Scopus
  23. L. Maggio-Price, D. Brookhoff, and L. Weiss, “Changes in hematopoietic stem cells in bone marrow of mice with Plasmodium berghei malaria,” Blood, vol. 66, no. 5, pp. 1080–1085, 1985. View at Google Scholar · View at Scopus
  24. L. Weiss, J. Johnson, and W. Weidanz, “Mechanisms of splenic control of murine malaria: tissue culture studies of the erythropoietic interplay of spleen, bone marrow, and blood in lethal (strain 17XL) Plasmodium yoelii malaria in BALB/c mice,” The American Journal of Tropical Medicine and Hygiene, vol. 41, no. 2, pp. 135–143, 1989. View at Google Scholar · View at Scopus
  25. G. S. Yap and M. M. Stevenson, “Plasmodium chabaudi AS: erythropoietic responses during infection in resistant and susceptible mice,” Experimental Parasitology, vol. 75, no. 3, pp. 340–352, 1992. View at Publisher · View at Google Scholar · View at Scopus
  26. K.-H. Chang and M. M. Stevenson, “Malarial anaemia: mechanisms and implications of insufficient erythropoiesis during blood-stage malaria,” International Journal for Parasitology, vol. 34, no. 13-14, pp. 1501–1516, 2004. View at Publisher · View at Google Scholar · View at Scopus
  27. T. Panichakul, J. Sattabongkot, K. Chotivanich, J. Sirichaisinthop, L. Cui, and R. Udomsangpetch, “Production of erythropoietic cells in vitro for continuous culture of Plasmodium vivax,” International Journal for Parasitology, vol. 37, no. 14, pp. 1551–1557, 2007. View at Publisher · View at Google Scholar · View at Scopus
  28. P. Ponka and C. N. Lok, “The transferrin receptor: role in health and disease,” International Journal of Biochemistry and Cell Biology, vol. 31, no. 10, pp. 1111–1137, 1999. View at Publisher · View at Google Scholar · View at Scopus
  29. A. C. Sexton, R. T. Good, D. S. Hansen et al., “Transcriptional profiling reveals suppressed erythropoiesis, up-regulated glycolysis, and interferon-associated responses in murine malaria,” Journal of Infectious Diseases, vol. 189, no. 7, pp. 1245–1256, 2004. View at Publisher · View at Google Scholar · View at Scopus
  30. P. A. Tamez, H. Liu, A. Wickrema, and K. Haldar, “P. falciparum modulates erythroblast cell gene expression in signaling and erythrocyte production pathways,” PLoS ONE, vol. 6, no. 5, Article ID e19307, 2011. View at Publisher · View at Google Scholar · View at Scopus
  31. G. Pasvol, “The interaction between sickle haemoglobin and the malarial parasite Plasmodium falciparum,” Transactions of the Royal Society of Tropical Medicine and Hygiene, vol. 74, no. 6, pp. 701–705, 1980. View at Publisher · View at Google Scholar · View at Scopus
  32. C. R. Brockelman, B. Wongsattayanont, P. Tan-Ariya, and S. Fucharoen, “Thalassemic erythrocytes inhibit in vitro growth of Plasmodium falciparum,” Journal of Clinical Microbiology, vol. 25, no. 1, pp. 56–60, 1987. View at Google Scholar · View at Scopus
  33. R. F. Rieder and G. W. James III, “Imbalance in α and β globin synthesis associated with a hemoglobinopathy,” The Journal of Clinical Investigation, vol. 54, no. 4, pp. 948–956, 1974. View at Publisher · View at Google Scholar · View at Scopus
  34. J.-Y. Han, R.-P. Zeng, G. Cheng, B. Hu, H. Li, and Y.-R. Lai, “Quantitative analysis of human globin gene expression in beta-thalassemia using real-time RT-PCR,” Yi Chuan, vol. 27, no. 1, pp. 57–64, 2005. View at Google Scholar · View at Scopus
  35. C. Chaisue, S. Kitcharoen, P. Wilairat, A. Jetsrisuparb, G. Fucharoen, and S. Fucharoen, “α/β-Globin mRNA ratio determination by multiplex quantitative real-time reverse transcription-polymerase chain reaction as an indicator of globin gene function,” Clinical Biochemistry, vol. 40, no. 18, pp. 1373–1377, 2007. View at Publisher · View at Google Scholar · View at Scopus
  36. F. Maryami, R. Mahdian, S. Jamali et al., “Comparisons between RT-PCR, real-time PCR, and in vitro globin chain synthesis by α/β ratio calculation for diagnosis of α- from β-thalassemia carriers,” Archives of Iranian Medicine, vol. 16, no. 4, pp. 217–220, 2013. View at Google Scholar · View at Scopus
  37. S. H. Orkin, D. Swan, and P. Leder, “Differential expression of α and β globin genes during differentiation of cultured erythroleukemic cells,” The Journal of Biological Chemistry, vol. 250, no. 22, pp. 8753–8760, 1975. View at Google Scholar · View at Scopus
  38. P. Arese and E. Schwarzer, “Malarial pigment (haemozoin): a very active ‘inert’ substance,” Annals of Tropical Medicine and Parasitology, vol. 91, no. 5, pp. 501–516, 1997. View at Publisher · View at Google Scholar · View at Scopus
  39. F. Martinon, A. Mayor, and J. Tschopp, “The inflammasomes: guardians of the body,” Annual Review of Immunology, vol. 27, pp. 229–265, 2009. View at Publisher · View at Google Scholar · View at Scopus
  40. D. J. Perkins, T. Were, G. C. Davenport, P. Kempaiah, J. B. Hittner, and J. M. Ong'echa, “Severe malarial anemia: innate immunity and pathogenesis,” International Journal of Biological Sciences, vol. 7, no. 9, pp. 1427–1442, 2011. View at Publisher · View at Google Scholar · View at Scopus
  41. C. C. Keller, J. B. Hittner, B. K. Nti, J. B. Weinberg, P. G. Kremsner, and D. J. Perkins, “Reduced peripheral PGE2 biosynthesis in Plasmodium falciparum malaria occurs through hemozoin-induced suppression of blood mononuclear cell cyclooxygenase-2 gene expression via an interleukin-10-independent mechanism,” Molecular Medicine, vol. 10, no. 1–6, pp. 45–54, 2004. View at Google Scholar · View at Scopus
  42. C. C. Keller, P. G. Kremsner, J. B. Hittner, M. A. Misukonis, J. B. Weinberg, and D. J. Perkins, “Elevated nitric oxide production in children with malarial anemia: hemozoin-induced nitric oxide synthase type 2 transcripts and nitric oxide in blood mononuclear cells,” Infection and Immunity, vol. 72, no. 8, pp. 4868–4873, 2004. View at Publisher · View at Google Scholar · View at Scopus
  43. M. Jaramillo, I. Plante, N. Ouellet, K. Vandal, P. A. Tessier, and M. Olivier, “Hemozoin-inducible proinflammatory events in vivo: potential role in malaria infection,” The Journal of Immunology, vol. 172, no. 5, pp. 3101–3110, 2004. View at Publisher · View at Google Scholar · View at Scopus
  44. D. O. Ochiel, G. A. Awandare, C. C. Keller et al., “Differential regulation of β-chemokines in children with Plasmodium falciparum malaria,” Infection and Immunity, vol. 73, no. 7, pp. 4190–4197, 2005. View at Publisher · View at Google Scholar · View at Scopus
  45. A. A. Lamikanra, M. Theron, T. W. A. Kooij, and D. J. Roberts, “Hemozoin (malarial pigment) directly promotes apoptosis of erythroid precursors,” PLoS ONE, vol. 4, no. 12, Article ID e8446, 2009. View at Google Scholar · View at Scopus
  46. C. Casals-Pascual, O. Kai, J. O. P. Cheung et al., “Suppression of erythropoiesis in malarial anemia is associated with hemozoin in vitro and in vivo,” Blood, vol. 108, no. 8, pp. 2569–2577, 2006. View at Publisher · View at Google Scholar · View at Scopus
  47. G. Giribaldi, D. Ulliers, E. Schwarzer, I. Roberts, W. Piacibello, and P. Arese, “Hemozoin- and 4-hydroxynonenal-mediated inhibition of erythropoiesis. Possible role in malarial dyserythropoiesis and anemia,” Haematologica, vol. 89, no. 4, pp. 492–493, 2004. View at Google Scholar · View at Scopus
  48. O. A. Skorokhod, L. Caione, T. Marrocco et al., “Inhibition of erythropoiesis in malaria anemia: role of hemozoin and hemozoin-generated 4-hydroxynonenal,” Blood, vol. 116, no. 20, pp. 4328–4337, 2010. View at Publisher · View at Google Scholar · View at Scopus
  49. C. Coban, M. Yagi, K. Ohata et al., “The malarial metabolite hemozoin and its potential use as a vaccine adjuvant,” Allergology International, vol. 59, no. 2, pp. 115–124, 2010. View at Publisher · View at Google Scholar · View at Scopus
  50. S. C. Chaiyaroj, A. S. M. Rutta, K. Muenthaisong, P. Watkins, M. Na Ubol, and S. Looareesuwan, “Reduced levels of transforming growth factor-β1, interleukin-12 and increased migration inhibitory factor are associated with severe malaria,” Acta Tropica, vol. 89, no. 3, pp. 319–327, 2004. View at Publisher · View at Google Scholar · View at Scopus
  51. D. Dodoo, F. M. Omer, J. Todd, B. D. Akanmori, K. A. Koram, and E. M. Riley, “Absolute levels and ratios of proinflammatory and anti-inflammatory cytokine production in vitro predict clinical immunity to Plasmodium falciparum malaria,” Journal of Infectious Diseases, vol. 185, no. 7, pp. 971–979, 2002. View at Publisher · View at Google Scholar · View at Scopus
  52. C. Othoro, A. A. Lal, B. Nahlen, D. Koech, A. S. S. Orago, and V. Udhayakumar, “A low interleukin-10 tumor necrosis factor-α ratio is associated with malaria anemia in children residing in a holoendemic malaria region in western Kenya,” Journal of Infectious Diseases, vol. 179, no. 1, pp. 279–282, 1999. View at Publisher · View at Google Scholar · View at Scopus
  53. D. J. Perkins, J. B. Weinberg, and P. G. Kremsner, “Reduced interleukin-12 and transforming growth factor-β1 in severe childhood malaria: relationship of cytokine balance with disease severity,” Journal of Infectious Diseases, vol. 182, no. 3, pp. 988–992, 2000. View at Publisher · View at Google Scholar · View at Scopus
  54. D. Torre, F. Speranza, M. Giola, A. Matteelli, R. Tambini, and G. Biondi, “Role of Th1 and Th2 cytokines in immune response to uncomplicated Plasmodium falciparum malaria,” Clinical and Diagnostic Laboratory Immunology, vol. 9, no. 2, pp. 348–351, 2002. View at Publisher · View at Google Scholar · View at Scopus
  55. L. Malaguarnera, R. M. Imbesi, S. Pignatelli, J. Simporè, M. Malaguarnera, and S. Musumeci, “Increased levels of interleukin-12 in Plasmodium falciparum malaria: correlation with the severity of disease,” Parasite Immunology, vol. 24, no. 7, pp. 387–389, 2002. View at Publisher · View at Google Scholar · View at Scopus
  56. M. Musumeci, L. Malaguarnera, J. Simporè, A. Messina, and S. Musumeci, “Modulation of immune response in Plasmodium falciparum malaria: role of IL-12, IL-18 and TGF-β,” Cytokine, vol. 21, no. 4, pp. 172–178, 2003. View at Publisher · View at Google Scholar · View at Scopus
  57. S. Winkler, M. Willheim, K. Baier et al., “Reciprocal regulation of Th1- and Th2-cytokine-producing T cells during clearance of parasitemia in Plasmodium falciparum malaria,” Infection and Immunity, vol. 66, no. 12, pp. 6040–6044, 1998. View at Google Scholar
  58. K. L. Miller, J. C. Schooley, K. L. Smith, B. Kullgren, L. J. Mahlmann, and P. H. Silverman, “Inhibition of erythropoiesis by a soluble factor in murine malaria,” Experimental Hematology, vol. 17, no. 4, pp. 379–385, 1989. View at Google Scholar · View at Scopus
  59. D. Kwiatkowski, A. V. S. Hill, I. Sambou et al., “TNF concentration in fatal cerebral, non-fatal cerebral, and uncomplicated Plasmodium falciparum malaria,” The Lancet, vol. 336, no. 8725, pp. 1201–1204, 1990. View at Publisher · View at Google Scholar · View at Scopus
  60. C. Dufour, A. Corcione, J. Svahn et al., “TNF-α and IFN-γ are overexpressed in the bone marrow of Fanconi anemia patients and TNF-α suppresses erythropoiesis in vitro,” Blood, vol. 102, no. 6, pp. 2053–2059, 2003. View at Publisher · View at Google Scholar · View at Scopus
  61. I. A. Clark and G. Chaudhri, “Tumour necrosis factor may contribute to the anaemia of malaria by causing dyserythropoiesis and erythrophagocytosis,” British Journal of Haematology, vol. 70, no. 1, pp. 99–103, 1988. View at Publisher · View at Google Scholar · View at Scopus
  62. J. A. L. Kurtzhals, V. Adabayeri, B. Q. Goka et al., “Low plasma concentrations of interleukin 10 in severe malarial anaemia compared with cerebral and uncomplicated malaria,” The Lancet, vol. 351, no. 9118, pp. 1768–1772, 1998. View at Publisher · View at Google Scholar
  63. K. Mohan and M. M. Stevenson, “Dyserythropoiesis and severe anaemia associated with malaria correlate with deficient interleukin-12 production,” British Journal of Haematology, vol. 103, no. 4, pp. 942–949, 1998. View at Publisher · View at Google Scholar
  64. K. Mohan and M. M. Stevenson, “Interleukin-12 corrects severe anemia during blood-stage Plasmodium chabaudi AS in susceptible A/J mice,” Experimental Hematology, vol. 26, no. 1, pp. 45–52, 1998. View at Google Scholar · View at Scopus
  65. G. A. Awandare, P. Kempaiah, D. O. Ochiel, P. Piazza, C. C. Keller, and D. J. Perkins, “Mechanisms of erythropoiesis inhibition by malarial pigment and malaria-induced proinflammatory mediators in an in vitro model,” American Journal of Hematology, vol. 86, no. 2, pp. 155–162, 2011. View at Publisher · View at Google Scholar · View at Scopus
  66. H. E. Broxmeyer, “Regulation of hematopoiesis by chemokine family members,” International Journal of Hematology, vol. 74, no. 1, pp. 9–17, 2001. View at Publisher · View at Google Scholar · View at Scopus
  67. J. W. Lillard Jr., U. P. Singh, P. N. Boyaka, S. Singh, D. D. Taub, and J. R. McGhee, “MIP-1α and MIP-1β differentially mediate mucosal and systemic adaptive immunity,” Blood, vol. 101, no. 3, pp. 807–814, 2003. View at Publisher · View at Google Scholar · View at Scopus
  68. K. Bacon, M. Baggiolini, H. Broxmeyer et al., “Chemokine/chemokine receptor nomenclature,” Journal of Interferon and Cytokine Research, vol. 22, no. 10, pp. 1067–1068, 2002. View at Publisher · View at Google Scholar · View at Scopus
  69. A. D. Luster, “The role of chemokines in linking innate and adaptive immunity,” Current Opinion in Immunology, vol. 14, no. 1, pp. 129–135, 2002. View at Publisher · View at Google Scholar · View at Scopus
  70. D. E. Wright, E. P. Bowman, A. J. Wagers, E. C. Butcher, and I. L. Weissman, “Hematopoietic stem cells are uniquely selective in their migratory response to chemokines,” Journal of Experimental Medicine, vol. 195, no. 9, pp. 1145–1154, 2002. View at Publisher · View at Google Scholar · View at Scopus
  71. M. Majka, A. Janowska-Wieczorek, J. Ratajczak et al., “Numerous growth factors, cytokines, and chemokines are secreted by human CD34+ cells, myeloblasts, erythroblasts, and megakaryoblasts and regulate normal hematopoiesis in an autocrine/paracrine manner,” Blood, vol. 97, no. 10, pp. 3075–3085, 2001. View at Publisher · View at Google Scholar · View at Scopus
  72. M. A. McDevitt, J. Xie, G. Shanmugasundaram et al., “A critical role for the host mediator macrophage migration inhibitory factor in the pathogenesis of malarial anemia,” The Journal of Experimental Medicine, vol. 203, no. 5, pp. 1185–1196, 2006. View at Publisher · View at Google Scholar · View at Scopus
  73. J. A. Martiney, B. Sherry, C. N. Metz et al., “Macrophage migration inhibitory factor release by macrophages after ingestion of Plasmodium chabaudi-infected erythrocytes: possible role in the pathogenesis of malarial anemia,” Infection and Immunity, vol. 68, no. 4, pp. 2259–2267, 2000. View at Publisher · View at Google Scholar · View at Scopus
  74. G. A. Awandare, Y. Ouma, C. Ouma et al., “Role of monocyte-acquired hemozoin in suppression of macrophage migration inhibitory factor in children with severe malarial anemia,” Infection and Immunity, vol. 75, no. 1, pp. 201–210, 2007. View at Publisher · View at Google Scholar · View at Scopus
  75. G. S. Yap and M. M. Stevenson, “Inhibition of in vitro erythropoiesis by soluble mediators in Plasmodium chabaudi AS malaria: lack of a major role for interleukin 1, tumor necrosis factor alpha, and gamma interferon,” Infection and Immunity, vol. 62, no. 2, pp. 357–362, 1994. View at Google Scholar · View at Scopus
  76. K. L. Miller, P. H. Silverman, B. Kullgren, and L. J. Mahlmann, “Tumor necrosis factor alpha and the anemia associated with murine malaria,” Infection and Immunity, vol. 57, no. 5, pp. 1542–1546, 1989. View at Google Scholar · View at Scopus