Katerina Rebok, Irena Tavčiovska-Vasileva, Maja Jordanova


In past decades macrophage aggregates (MACs) were being used in many monitoring studies as useful immu-nological biomarkers of environmental pollution and they are still encountered in the so-called “future biomarkers”, since quantitative studies in aquaculture and/or field of their normal fluctuations as a result of the influence of natural factors are extremely rare. Our investigation was designed to quantitatively evaluate the influence of the seasons on MAC's relative volume, number and diameter in the Ohrid trout (Salmo letnica Kar.) spleen. Data showed that all investigated parameters had significantly higher values in fish collected during spring and winter. Correlation anal-yses revealed that the increasing of the relative volume of MACs is a result of the increasing of the relative volume of melanin loaded MACs, as well as the increasing of their number and diameter. These results confirmed that the sea-son can affect MACs variations and should be taken into consideration, especially when spleen MACs are used as pollution biomarkers in monitoring studies.


spleen; macrophage aggregates; Ohrid trout; season

Full Text:



R. van der Oost, J. Beyer, N. P. E. Vermeulen, Fish bioaccumulation and biomarkers in environ-mental risk assessment: A review, Environ. Toxi-col. Pharmacol., 13:2 (2003), pp. 57–149.

R. E. Wolke, Piscine macrophage aggregates: A review, Annu. Rev. Fish Dis. (1992), pp. 91–108.

D. E. Facey, V. S. Blazer, M. M. Gasper, C. L. Turcotte, Using fish biomarkers to monitor im-provements in environmental quality, J. Aquat. Anim. Health., 17 (2005), pp. 263–266.

C. Agius, R. J. Roberts, Melano-macrophage centers and their role in fish pathology, J. Fish Dis., 26 (2003), pp. 499–509.

V. S. Blazer, R. E. Wolke, J. Brown, C. A. Powell, Piscine macrophage aggregate parameters as health monitors: effect of age, sex, relative weight, season and quality in largemouth bass (Micro-pterus salmoides), Aquat. Toxicol., 10 (1987), pp. 199–215.

F. A. Vigliano, R. Bermúdez, Ma. I. Quiroga, J. M. Nieto, Evidence for melano-macrophage cen-tres of teleost as evolutionary precursors of germi-nal centres of higher vertebrates: An immuno-histochemical study, Fish Shell. Immunol., 21 (2006), pp. 467–471.

R. E. Wolke, C. J. George, V. S. Blazer, Pigmented macrophage accumulations (MMC, PMB): Possible monitors of fish health, in: Parasitology and Pathology of Marine Organisms of the World Ocean, W. J. Hargis Jr. (Eds), NOAA Tech. Rep. NMFS 25, 1985, pp. 93–97.

V. S. Blazer, D. E. Facey, J. W. Fournie, L. A. Courtney, J. K. Summers, Macrophage aggregates as indicators of environmental stress, in: Modula-tors of Fish Immune Responses: Volume 1, Models for Environmental Toxicology, Biomarkers, Im-munostimulators, J. S. Stolen, T. C. Fletcher, D. P. Anderson, J. T. Zelikoff, L. E. Twerdok, S. L. Kaattari, C. C. Bayne (Eds), SOS Publications, Fair Haven, New Jersey, 1994, pp. 169–185.

T. Meinelt, R. Krüger, M. Pietrock, R. Osten, C. Steinberg, Mercury pollution and macrophage centres in pike (Esox lucius) Tissues, Environ. Sci. Pollut. Res., 4:1 (1997), pp. 32–36.

D. E. Facey, C. Leclerc, D. Dunbar, D. Arruda, V. S. Blazer, Physiological indicators of stress among fishes exposed to contaminated sediments from Lake Champlain, in: Stress in Fish, T. Barry, B. Barton, D. MacKinlay (Eds), International Congress on the Biology of Fish, Towson University, Baltimore, MD, 1998, pp. 83–88.

J. W. Fournie, J. K. Summers, L. A. Courtney, V. D. Engle, V. S. Blazer, Utility of splenic macrophage aggregates as an indicator of fish exposure to degraded environment, J. Aquat. Anim. Health., 13:2 (2001), pp. 105–116.

R. Roberts, Melanin-containing cells of teleost fish and their relation to disease, in: The Pathology of Fishes, E. Ribelin, G. Migaki (Eds), The University of Wisconsin Press, 1975, pp. 399–441.

C. Agius, The role of melano-macrophage centres in iron storage in normal and diseased fish, J. Fish Dis., 2 (1979), pp. 337–343.

C. Agius, The melano-macrophage centres of fish: A rewiew, in: Fish Immunology, M. J. Manning, M. F. Tatner (Eds), Academic Press, London, 1985, pp. 85–105.

N. K. El-Fiky, Effect of starvation on the melano-macrophage centres of carp, Cyprinus carpio, J. Egypt. Ger. Soc. Zool., 27:B (1998), pp. 35–44.

D. Montero, V. S. Blazer, J. Socorro, M. S. Izquierdo, L. Tort, Dietary and culture influences on macrophage aggregate parameters in gilthead seabream (Sparus aurata) juveniles, Aquaculture, 179 (1999), pp. 523–534.

M. Jordanova, N. Miteva, E. Rocha, A qualitative and quantitative study of the hepatic pigmented macrophage aggregates during the breeding cycle of Ohrid trout, Salmo letnica Kar. (Teloestei, Salmonidae), Microscopy Res. Tech., 830 (2008), pp. 822–830.

M. Jordanova, M. Rocha, K. Rebok, E. Rocha, Changes in the amount of kidney pigmented mac-rophage aggregates throughout the breeding cycle of female Ohrid trout, Salmo letnica Kar. (Tele-ostei, Salmonidae), Microsc. Res. Tech., 75:2 (2012), pp. 176–181.

A. R. Schwindt, N. Truelove, C. B. Schreck, J. W. Fournie, D. H. Landers, M. L. Kent, Quantitative evaluation of macrophage aggregates in brook trout Salvelinus fontinalis and rainbow trout On-corhynchus mykiss, Dis. Aquat. Org., 68 (2006), pp. 101–113.

H. Freere, E. R. Weibel, Stereologic techniques in microscopy, J. R. Microsc. Soc., 87 (1967), pp. 25–34.

B. K. Gupta, U. K. Sarkar, S. K. Bhardwaj, A. Pal, Condition factor, length–weight and length–length relationships of an endangered fish Ompok pabda(Hamilton 1822) (Siluriformes: Siluridae) from the River Gomti, a tributary of the River Ganga, India, J. Appl. Ichthyol., 27 (2011), pp. 962–964.

F. L. Mayer, D. J. Versteeg, M. J. McKee, L. C. Fol-mar, R. L. Graney, D. C. McCume, B. A. Rattner, Metabolic products as biomarkers, in: Biomarkers: Biochemical, Physiological and Histological Mark-ers of Anthropogenic Stress, R. J. Huggett, R. A. Ki-merly, P. M. Mehrle, H. L. Bergman (Eds), Lewis Publishers, Chelsea, MI, 1992, pp. 5–86.

D. Bernet, H. Segner, Effektstudie: Zusam-menstellung von Fischgesundheitsdaten in der Schweiz, in: Fischnetz-Publikation. Teilprojekt 01/19. Zentrum für Fisch- und Wildtiermedizin, Universität Bern und EAWAG, Bern / Dübendorf, (2004).

A. S. Holzer, O. Schachner, Myxosporidia and macrophage centers in chub (Leuciscus cephalus) – quantitative interactions focus on Myxobolus cyprini, Parasitology, 122 (2001), pp. 55–62.

R. Krüger, M. Pietrock, T. Meinelt, T. Yoshida, W. Steffens, Ch. Steinberg, Distribution of macrophage centres in bream (Abramis brama L.) liver from the Oder River (Germany/Poland) within the nature reserve “Unteres Odertal” near the town of Schwedt, Int. Revue ges. Hydrobiol., 81 (1996), pp. 635–644.

M. Manera, R. Serra, G. Isani, E. Carpené, Macro-phage aggregates in gilthead sea bream fed copper, iron and zinc enriched diets, J. Fish Biol., 57 (2000), pp. 457–465.

M. Sakthivel, B. Deivasigamani, S. Kumaran, S. Balamurugan, T. Rajasekar, Seasonal variation in immune organs and immune response of catfish Arius maculatus in Parangipettai coastal area, J. Chem. Pharm. Res., 4:7 (2012), pp. 3342–3348.

M. Watts, B. L. Munday, C. M. Burke, Immune responses of teleost fish, Aust. Vet. J., 79:8 (2001), pp. 570–574.

M. Tatner, Natural changes in the immune system of fish, in: The Fish Immune System: Organism, Pathogen and Environment, G. K. Iwama, T. Nakanishi (Eds), Academic Press, Inc., San Diego, California, USA, 1985, pp. 255–288.

M. E. Collazos, C. Barriga, E. Ortega, Seasonal variations in the immune system of the tench, Tin-ca tinca. Phagocytic function, Comp. Immunol. Microbiol. Infect. Dis., 18 (1995), pp. 105–113.

C. Agius, R. J. Roberts, Effects of starvation on the melano-macrophage centres of fish, J. Fish Bi-ol., 19 (1981), pp. 161–169.

S. Mizuno, N. Misaka, Y. Miyakoshi, K. Takeuchi, N. Kasahara, Effects of starvation on melano-macrophages in the kidney of masu salm-on (Oncorhynchus masou), Aquaculture, 209 (2002), pp. 247–255.

J. W. Hur, S. R. Woo, J. H. Jo, I. S. Park, Effects of starvation on kidney melano-macrophage centre in olive flounder, Paralichthys olivaceus (Tem-minck and Schlegel), Aquaculture Res., 37 (2006), pp. 821–825.

M. K. Tripathi, R. Singh, Seasonal variation and innate immune responses of spleen in fresh-water snake, Natrix piscator, J. Stress Physiol. Biochem., 10:1 (2014), pp. 292–300.



  • There are currently no refbacks.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.

Contact details

Bul. Krste Misirkov br.2
1000 Skopje, Republic of Macedonia
Tel. ++389 2 3235-400
cell:++389 71 385-106
About the journal

CSNMBS is a part of the MASA Contribution series. Published by the Section Natural, Mathematical and Biotechnical Sciences.
About this site

Maintained by the Researh center for Materials and Enviroment - MANU/MASA.
Site (including the theme) set, adapted by MASA - CSIT.