Nutritional Evaluation of Seasonal Changes in Muscle Fatty Acid Composition of Common Carp (Cyprinus carpio) in Karamik Lake, Turkey

Abstract

The present study aims to determine seasonal changes of nutritional value of common carp in Karamık Lake by determining the fatty acid composition. The levels of saturated, monounsaturated, and polyunsaturated fatty acids in 100 g total fatty acid were found to be 28.73, 25.31, and 38.19 g in winter; 29.39, 24.06, and 35.75 g in spring; 31.05, 35.02, and 24.86 g in summer; 29.85, 32.39, and 30.92 g in autumn, respectively. Total ω3 and ω6 polyunsaturated fatty acid levels in 100 g fatty acid in muscle of the common carp ranged from 12.90 g to 25.97 g and from 10.73 g to 14.59 g, respectively. The ratio of total ω3 polyunsaturated fatty acids was higher than that of total ω6 polyunsaturated fatty acids in all seasons. The ratios of ω6/ω3 polyunsaturated fatty acids and arachidonic/eicosapentaenoic acids were the lowest in winter (0.41, 0.64) and highest (0.98, 2.72) in autumn. The amount of eicosapentaenoic + docosahexaenoic acids was also highest in winter and was composed of 22.50 g of 100 g total fatty acid in muscle of pike.

Keywords:

• Fatty acids
• Common carp
• Seasonal change
• Nutritional value
• Karamık Lake

INTRODUCTION

Fish is an excellent choice of food for human nutrition. This especially arises from long chain ω3 polyunsaturated fatty acid (ω3 PUFAs). ω3 PUFAs in fish oil have extremely beneficial and therapeutic properties for the prevention of coronary artery disease,[1–3] sudden cardiac death,[4] rheumatoid arthritis,[5] breast and colon cancer,[6,7] inflammatory disease and diabetes,[8–10 cognitive decline and dementia,[11] Alzheimer disease,[12] depression,[13] asthma, and disorders of the immune system.[14,15] All of these diseases can be prevented or at least reduced by increased consumption of fish. However, the fatty acid composition of fish species varies with season,[16,17] geographical location of the catch,[18–21] diet and feeding,[22] size,[23] and sex and the state of their reproductive cycle.[24] Therefore, nutritional value of fish varies based on the factors aforementioned. For instance, fish must adapt the biophysical properties of their cell membranes to fluctuating environmental temperatures. Fatty acid composition of membrane lipids plays a major role as regulators of membrane fluidity while fish adapt themselves to low temperature specific habitat conditions.[25] Therefore, fish in a cold region or season have higher amounts of PUFAs because of PUFAs low melting points.[26] Because of higher amounts of PUFAs, fish in cold conditions have more beneficial effect on human health than those in temperate conditions.[18]

The common carp (Cyprinus carpio) was successfully spread throughout Asia and Europe, and was domesticated as an ornamental and aquaculture species.[27] In Turkey, common carp is stocked into natural waters, reservoirs, and temporarily inundated areas in order to utilize the natural food production of these waters for enhanced capture fisheries. Common carp production in Turkey was nearly 38% of the total freshwater capture production in 2004.[28] Therefore, common carp is the most commercially important freshwater fish in many freshwater reservoirs of Turkey as well as in Karamık Lake, and common carp is largely consumed in Turkey. There have been no studies encountered on fatty acid composition of common carp in Karamık Lake. Thus, the aim of the present study is to determine seasonal variations in nutritional values with respect to the proportions of ω3 PUFAs of common carp in the Lake of Karamık.

MATERIALS AND METHODS

Study Area and Fish Samples

Lake Karamık is situated in the district of the Middle Anatolia of Turkey with an altitude of 1067 m above sea level. The surface may be partly covered with ice in some winters and the water temperature may also reach up to 25–30°C in summer and autumn. Common carp (Cyprinus carpio) and pike (Esox lucius) were the dominant economic fish species in Karamık Lake. Common carp were caught with the trammel net in every season. The carp used in the experiment were fit to human consumption and older than 5 years (Table 1). The fish were first wrapped into polyethylene plastic, put into an isolated container, and brought to the Biology Laboratory of Afyon Kocatepe University. After biometric measurements, the fish were immediately frozen and stored at –25°C until used for analysis.

Table 1 Lengths, weights, and condition factors of investigated specimens

				Fork length	Condition
Seasons	n	Age	Weight (g)	(cm)	factor
Winter	8	5.10 ± 0.70	916.67 ± 57.92	37.02 ± 1.68	1.80
Spring	8	5.05 ± 0.79	937.47 ± 77.38	38.15 ± 1.53	1.68
Summer	7	5.30 ± 0.64	984.10 ± 65.10	36.27 ± 1.95	2.06
Autumn	9	5.60 ± 0.92	995.17 ± 40.08	36.57 ± 2.26	2.03

Determination of Fatty Acids

The AOAC Official Method was carried out to obtain total lipid and fatty acid methyl esters.[29] A 10-g muscle tissue taken from the dorsal muscle along the lateral line of each fish was homogenized and lipid was extracted with 100 ml of chloroform/methanol (2:1) mixture. The solvent was removed by evaporation under vacuum. The residual chloroform was then removed by nitrogen. The fatty acids in the total lipid were esterified into methyl esters by saponification with 0.5 N methanolic NaOH and transesterified with 14% BF3 (w/v) in methanol. Routine analysis of fatty acid methyl esters samples were carried out with HP Agilent 7890A (Agilent Technologies Inc., Palo Alto, CA, USA) model gas chromatography equipped with flame ionization detector (FID) using a capillary column (100-m length and 0.25-mm internal diameter and 0.20-μm film thickness; HP 88 [Agilent Technologies, Inc.]). The oven temperature was programmed to the initial temperature of 170°C, was increased at a rate of 1°C per min to 208°C, was further increased at a rate of 2°C per min to 240°C and then held at that temperature for 5 min. The injector and flame ionization detector were set at 250°C. Nitrogen was used as a carrier gas. The injection volume was 1 μl with a split ratio of 1:50. Fatty acid peaks were identified by comparison of their retention times with appropriate fatty acid methyl ester standards. Individual fatty acid concentrations were expressed as percentages of the total content.

Statistical Analyses

The results are presented as means ± SD (standard deviation). The statistical differences of major fatty acids (palmitic, palmitoleic, stearic, oleic, arachidonic, eicosapentaenoic, and docosahexaenoic acids) and main fatty acid groups (total saturated fatty acids, total monounsaturated fatty acids, total polyunsaturated fatty acids, total ω3 polyunsaturated fatty acids, and total ω6 polyunsaturated fatty acids) among the season were analyzed using multiple comparison tests (SPSS package program, version 16.0, SPSS Inc., USA). One-way ANOVA was utilized to compare the data by season. Results were considered significant at p < 0.05.

RESULTS AND DISCUSSION

The common carp (Cyprinus carpio) investigated in the present study were older than 5 years, showed sexual maturation, and were favorable sizes for human consumption (Table 1). Condition factors of the specimens were the lowest in spring (1.68) and highest in summer (2.06). Spring is the reproductive period and emptied the ovariums, which are approximately composed of 1/4 or 5 of total weight of fish. Summer and autumn after the reproductive period are also a dense feeding period for common carp.[27]

Seasonal changes in muscle fatty acid compositions of the common carp in Karamık Lake are given in Table 2. The levels of saturated fatty acids (SFAs), monounsaturated fatty acids (MUFAs), and polyunsaturated fatty acids (PUFAs) are illustrated in Fig. 1. The ω3 polyunsaturated fatty acids (ω3 PUFAs), ω6 polyunsaturated fatty acids (ω6 PUFAs), and ω9 monounsaturated fatty acids (ω9 MUFAs) are also illustrated in Fig. 2. In this study, palmitic and stearic acids were dominant SFAs and their levels did not change significantly among the seasons (p > 0.05). The amounts of palmitic and stearic acids in 100 g total fatty acids varied from 14.87 g (spring) to 16.79 g (summer), and from 5.11 g (summer) to 6.03 g (winter), respectively. Palmitic acid is a key metabolite in fish and its level is not remarkably influenced by diet.[30] The level of SFAs in 100 g total fatty acid ranged from 28.73 g to 31.05 g during the season (Fig. 1). Although there was no statistical significance, the SFA amounts in muscle of the common carp were the highest in summer and lowest in winter.

Table 2 The amounts (g/100 g fatty acids) of fatty acids in muscle of the common carp

Fatty acids	Winter n = 8	Spring n = 8	Summer n = 7	Autumn n = 9
C12:0	0.07 ± 0.02	0.06 ± 0.01	0.07 ± 0.01	0.06 ± 0.01
C13:0	0.13 ± 0.03	0.01 ± 0.00	0.03 ± 0.01	0.03 ± 0.00
C14:0	1.49 ± 0.22	0.67 ± 0.18	1.00 ± 0.11	1.08 ± 0.22
C14:1	0.44 ± 0.03	0.47 ± 0.08	0.42 ± 0.04	0.62 ± 0.13
C15:0	1.26 ± 0.24	2.34 ± 0.51	2.72 ± 0.41	1.47 ± 0.19
C15:1	0.49 ± 0.06	0.79 ± 0.06	0.72 ± 0.10	0.49 ± 0.05
C16:0	16.56 ± 0.91	14.87 ± 0.75	16.79 ± 0.89	16.19 ± 0.63
C16:1	6.78 ± 0.88	7.08 ± 0.66	10.78 ± 0.75	10.49 ± 0.63
C17:0	0.88 ± 0.11	0.76 ± 0.09	0.66 ± 0.09	0.90 ± 0.09
C17:1	0.99 ± 0.32	0.97 ± 0.22	1.06 ± 0.28	1.22 ± 0.13
C18:0	6.03 ± 0.64	5.30 ± 0.50	5.11 ± 0.35	5.21 ± 0.37
C18:1 ω9	12.23 ± 0.88	9.49 ± 0.91	17.93 ± 0.90	15.30 ± 0.93
C18:1 ω9	0.20 ± 0.05	0.31 ± 0.02	0.28 ± 0.05	0.37 ± 0.07
C18:2 ω6	4.87 ± 0.78	3.38 ± 0.79	2.85 ± 0.46	3.28 ± 0.37
C20:0	0.17 ± 0.05	0.15 ± 0.01	0.17 ± 0.02	0.15 ± 0.02
C18:3 ω6	0.25 ± 0.05	0.08 ± 0.02	0.10 ± 0.06	0.08 ± 0.04
C18:3 ω3	2.69 ± 0.39	1.27 ± 0.18	1.67 ± 0.53	1.27 ± 0.19
C20:1 ω9	0.72 ± 0.07	0.83 ± 0.18	1.19 ± 0.18	1.23 ± 0.32
C21:0	0.48 ± 0.12	0.17 ± 0.03	0.26 ± 0.03	0.29 ± 0.10
C20:2	0.88 ± 0.17	0.69 ± 0.15	0.64 ± 0.16	1.14 ± 0.22
C20:3 ω3	0.76 ± 0.09	0.82 ± 0.11	0.72 ± 0.03	0.79 ± 0.06
C22:0	0.13 ± 0.02	0.62 ± 0.39	1.41 ± 0.42	0.12 ± 0.03
C20:4 ω6	5.59 ± 035	10.71 ± 0.80	7.87 ± 0.62	11.22 ± 0.87
C22:2	0.60 ± 0.13	0.51 ± 0.02	0.48 ± 0.04	0.38 ± 0.08
C20:5 ω3	8.64 ± 0.87	7.19 ± 0.55	5.08 ± 0.76	4.11 ± 0.64
C23:0	0.74 ± 0.14	2.33 ± 0.35	1.31 ± 0.23	1.99 ± 0.32
C24:0	0.74 ± 0.09	2.05 ± 0.31	1.48 ± 0.36	2.33 ± 0.32
C24:1 ω9	3.44 ± 0.23	4.09 ± 0.35	2.62 ± 0.61	2.64 ± 0.29
C22:6 ω3	13.86 ± 0.66	11.07 ± 0.74	5.42 ± 0.92	8.61 ± 0.95
Total	92.24	89.20	90.94	93.17
Unknown	7.76	10. 80	9.06	6.83
ω6 PUFAs/ω3 PUFAs	0.41	0.69	0.83	0.98
AA/EPA	0.64	1.48	1.54	2.72
EPA + DHA	22.50	18.26	10.50	12.72

Figure 1 The ratios of fatty acid groups in muscle of the common carp.

Figure 2 The ratios of ω3 PUFAs, ω6 PUFAs, and ω9 MUFAs in muscle of the common carp.

Oleic and palmitoleic acids were the main MUFAs and their levels in 100 g total fatty acids varied from 9.49 g (spring) to 17.93 g (summer) for oleic acid and from 6.78 g (winter) to 10.78 g (summer) for palmitoleic acid. Similar levels for the these fatty acids in the muscle of common carp and various freshwater fish have also been reported.[18,31–34] Oleic and palmitoleic acids are two specific fatty acids for freshwater fish and their amount in freshwater fish is higher than that in sea fish. As seen in Table 2 and Figs. 1 and 2, the ratios of oleic acid, palmitoleic acid, total MUFAs, and ω9 MUFAs of the common carp were the highest in summer, a dense feeding period. Relating to this result, it may be said that the seasonal variation patterns of MUFAs are similar to SFAs rather than PUFAs.

The levels of PUFAs in 100 g total fatty acid were found in the range of 24.85 g (summer) to 38.10 g (winter) during the season in the present study (Fig. 1). Eicosapentaenoic (EPA) and docosahexaenoic (DHA) acids were dominant polyunsaturated fatty acids. High levels of PUFAs in cell membranes of fish were characteristic of adaptation of fish to aquatic habitats.[35,36] The muscle levels of these fish-specific fatty acids varied from 4.11 g (autumn) to 8.64 g (winter) for EPA, and from 5.42 g (summer) to 13.86 g (winter) for DHA. PUFAs were also the most flactuated fatty acids among the seasons. Although arachidonic acid (AA) was the third most abundant PUFAs in muscle of the common carp, the variations of AA and EPA during the seasons was contrary to each other. While the level of AA was the lowest in winter, the level of EPA was the highest. Melting temperatures of EPA are lower than those of AA. Therefore, EPA contents of fish in cold regions are higher than those of fish in warm regions.[18] This charasteristic of fish oil in cold regions made fish a healthy choice for human nutrition. That is, AA and EPA possess a vital function as the main precursor of a wide variety of biologically active compounds known as the eicosanoids. The eicosanoids are involved in a great variety of physiological functions like cardiovascular, neural, and reproductive functions. However, eicosanoids formed from EPA are biologically less active than those formed from AA. Moreover, EPA competitively inhibits the formation of eicosanoids from AA. Therefore, eicosanoid actions in the body are determined inter alia by the ratio of AA/EPA.[37] In this study, the proportion of AA to EPA was also significantly lower in winter (0.64) than in spring (1.48), summer (1.54), and autumn (2.72)

As seen in Table 2, the ratio of EPA + DHA contributed to approximately 10–20 g of the 100 g total fatty acids content in the muscle of common carp. The ratio of EPA + DHA was also significantly increased in winter (p < 0.05). This ratio is also accepted as an important health criterion for humans. The risk of sudden cardiac death is reported to be associated with an ω3 index. This index is measured in red blood cells, and is expressed as a percentage of EPA + DHA of total fatty acids. An ω3 index of >8% is associated with 90% less risk for sudden cardiac death, as compared to an ω3 index of <4%.[3] The ratio of EPA + DHA in muscle of the common carp was composed of 22.50 g of 100 g total fatty acid in winter. Thus, common carp consumed in winter will increase the ω3 index of red blood cells of humans and will be more beneficial.

In this study, the amounts of ω3 PUFAs and ω6 PUFAs in 100 g total fatty acid were found to be 25.97 g and 10.73 g in winter, 20.37 g and 14.17 g in spring, 12.90 g and 10.82 g in summer, and 14.80 g and 14.59 g in autumn, respectively (Fig. 2). The ω3 and ω6 PUFAs are two biochemical families within the PUFAs, and they also have different biological effects. A very high ω6/ω3 ratio promotes the pathogenesis of many diseases like cardiovascular, cancer, inflammatory, and autoimmune diseases, whereas a low ω6/ω3 PUFAs ratio exerts suppressive effects. For instance, in the secondary prevention of cardiovascular disease, an ω6/ω3 ratio of 4/1 was associated with a 70% decrease in total mortality. Therefore, a lower ratio of ω6/ω3 fatty acids is more desirable in reducing the risk of many of the chronic diseases of high prevalence in Western societies, as well as in developing countries. It has been suggested that an increase in fish intake is one of the contributing factors to a decreased ratio of ω6 to ω3 PUFAs in the diet.[14, 15, 38] In this study, the ratio of ω6 PUFAs to ω3 PUFAs in the muscle total fatty acid of common carp was found to be lower than 1 in all seasons. As seen in Table 2, the ratio of ω6 PUFAs to ω3 PUFAs in the muscle of common carp in Karamık Lake was also remarkably lower in winter than that of the other seasons (p < 0.05). We may suggest that the common carp captured in winter from Karamık Lake is an excellent food and more beneficial for human health than those captured in other seasons due to the ratio of lower ω6/ω3 PUFAs, AA/EPA, and the ratio of higher EPA + DHA.