Fatty acids composition has considerable effects on the diet and health relationship, since each fatty acid affects the plasmatic lipid differently (Jimenez-Colmenero et al., 2001). Table 4.3 shows the fatty acids composition, total lipid content and cholesterol content of C. porosus meat. In general, thigh meat contains the highest amount of fatty acids (1050.01 ± 636.40 mg/100g), followed by tail meat (827.57 ± 184.17 mg/100g) and back meat (700.02 ± 424.24 mg/100g). There are no significant differences between different parts, indicating that the fatty acids content is not affected by parts of meat in crocodile. The high content of fatty acids in thigh meat is due to the presence membranes present between the skin and muscle layer, causing a release of fat from membrane (Al-Najdawi and Abdullah, 2002). As compared to the total fatty acids content of pigs (2200 mg/100g), sheep (4900 mg/100g) and cattle (3800 mg/100g) (Wood et al., 2008; Enser et al., 1996), C. porosus meat is shown to have lowest fatty acids.
The percentage of saturated fatty acids (SFA) in back meat is the highest (53.22 ± 1.58%) as compared to thigh meat (51.31 ± 5.44%) and tail meat (50.59 ± 2.56%). The total unsaturated fatty acids (UFA) which includes monounsaturated fatty acids (MUFA) and polyunsaturated fatty acids (PUFA) show highest percentage in tail meat (49.41%), followed by thigh meat (48.7%) and back meat (46.79%). The ratio between PUFA and SFA has a range of 0.60 - 0.66, which is higher than that of beef muscles (0.11), lamb muscles (0.15) and pork muscles (0.58) as reported by Enser et al. (1996), indicating C. porosus meat as a better choice among commonly available meat source in terms of PUFA content. While comparing the ratio of PUFA and SFA with other exotic wild meats, C. porosus meat exhibits higher ratio value as compared to goat meat (0.32), while red deer meat shows almost the same ratio (0.63) (Mushi et al., 2010; Polak et al., 2008). Vincente-Neto et al. (2010) also showed that the ratio of PUFA and SFA in Caiman crocodilus yacare meat is 0.43, which is lower than that of C. porosus meat analyzed. The PUFA/SFA ratio of 0.4 or more is recommended as a balanced fatty acid intake for healthy diet, thus C. porosus meat is categorized as a healthy choice for daily diet (Caldironi and Manes, 2006).
High MUFA and PUFA percentages in meat indicated their suitability for healthier diets, as MUFA and PUFA rich diets increases the High Density Lipoprotein (HDL) concentration and decreases the Low Density Lipoprotein (LDL) concentration in blood (McGuire and Beerman, 2007; Vanschoonbeek et al., 2003). The uptake of the cholesterol-rich LDL is necessary for immune cells to synthesize important substances such as eicosaniods and immune factors, but excessive LDL can result in buildup of plaque in blood vessels and causing blockage (Lawrie and Ledward, 2006). Epidemiological studies suggested that high levels of LDL in blood are related to increased risk for cardiovascular diseases (Chilton, 2004). On the other hand, HDLs are well-established to be associated with lowering the risk of cardiovascular diseases by salvaging excess cholesterol from cells and transporting it back to the liver (Lewis and Rader, 2005). Studies showed that high values of PUFA/SFA ratio is related to a low incidence of cardiovascular diseases (Caldironi and Manes, 2006; Padre et al., 2006). Thus, it can be concluded that inclusion of C. porosus meat in daily diet is a healthier choice as compared to other meat sources.
Table 4.3: Fatty acid composition, total lipid content and cholesterol content
of Crocodylus porosus meat
Variables
Thigh Meat
Tail Meat
Back Meat
Fat Content (g/100g)
0.38a±0.11
0.36a±0.05
0.26b±0.05
Individual Fatty Acids (mg/100g)
Lauric Acid
C12:0
ND
10.58a±0.81
0.42a±0.59
Myristic Acid
C14:0
0.69a±0.98
0.83a±1.17
0.35a±0.49
Pentadecanoic Acid
C15:0
ND
ND
0.29±0.41
Palmitic Acid
C16:0
204.12a±12.23
189.20a±25.63
164.07a±96.68
Palmitoleic Acid
C16:1
15.66a±18.86
7.37a±6.75
6.95a±7.89
Margaric Acid
C17:0
1.12a±1.57
0.55a±0.78
2.08a±1.02
Stearic Acid
C18:0
172.31a±82.15
117.86a±27.89
104.82a±63.86
Oleic Acid
C18:1
181.95a±16.00
121.37a±6.68
90.35a±7.39
Linoleic Acid
C18:2
255.99a±14.19
218.73a±22.84
175.10a±98.11
Linolenic Acid
C18:3
3.24a±2.31
3.02a±0.49
1.62a±0.78
Eicosenoic Acid
C20:1
5.21a±2.86
3.05a±0.49
2.41a±0.19
Eicosadienoic Acid
C20:2
5.38a±3.05
3.54a±1.07
3.54a±1.03
Dihomoylinolenic Acid
C20:3
5.64a±5.29
5.46a±2.17
5.68a±4.07
Behenic Acid
C22:0
129.23a±59.09
97.96a±13.90
88.16a±5.00
Docosahexanoic Acid
C22:6
49.85a±3.11
45.52a±9.67
41.06a±2.35
Hexacosanoic Acid
C23:0
2.59a±3.65
1.69a±2.38
1.78a±2.52
Lignoceric Acid
C24:0
11.38a±4.85
7.67a±0.97
7.26a±2.04
Nervonic Acid
C24:1
5.67a±1.49
4.56a±0.49
4.10a±0.48
Total SFA (mg/100g)
521.43a±269.49
416.32a±71.97
369.21a±214.69
Total MUFA (mg/100g)
208.48a±183.23
136.34a±74.08
103.82a±82.05
Total PUFA (mg/100g)
320.10a±183.68
274.92a±38.12
226.99a±127.49
Total FA (mg/100g)
1050.01a±636.40
827.57a±184.17
700.02a±424.24
% of SFA
51.31a±5.44
50.59a±2.56
53.22a±1.58
% of MUFA
17.85a±6.64
15.87a±5.42
13.82a±3.34
% of PUFA
30.85a±1.20
33.54a±2.86
32.97a±1.76
Ratio of PUFA/SFA
0.6012
0.6630
0.6195
Cholesterol (mg/100g)
24.35a±8.98
22.05a±1.48
18.65a±12.66
SFA = Saturated Fatty Acids
MUFA = Monounsaturated Fatty Acids
PUFA = Polyunsaturated Fatty Acids
ND = Not Detected
1Means in the same row with different letters presented significant differences (p<0.05).
4.3.1 Saturated Fatty Acids in Crocodile Meat
The main SFAs available in C. porosus meat are palmitic acid (C16:0), stearic acid (C18:0) and behenic acid (C22:0). C. porosus thigh meat has highest value in all three SFAs, followed by tail meat and back meat. Valsta et al. (2004) stated that the palmitic acid content in various meat sources is usually around 30 - 40% of the total fatty acid, but the palmitic acid content showed in Table 4.3 is 19.44% for thigh meat, 22.86% for tail meat and 23.44% for back meat. Similar results were reported by Mitchell et al. (1995) on C. porosus and C. johnsoni meat, in which the palmitic acid content is as high as 22.5%. Osthoff et al. (2010) reported captive Nile crocodile (C. niloticus) contains 20.2% of palmitic acid, which is similar to results of C. porosus meat. The palmitic acid content of red deer meat (23.62%), goat meat (23.13%) and Caiman yacare meat (22.00%) also show similarities with C. porosus meat (Mushi et al., 2010; Vincente-Neto et al., 2010; Polak et al., 2008). Palmitic acid is one of the main fatty acids that increase the total cholesterol and LDL in blood with studies showing that LDL contents in blood was increased when SFAs of 12 - 16 carbon atoms are increased in daily diet (Jimenez-Colmenero et al., 2001; Chizzolini et al., 1998; Wiseman, 1997).
Being second most abundant SFA in C. porosus meat, stearic acid is highly available in thigh meat (172.31 ± 82.15 mg/100g) with 16.41% of total fatty acids, followed by tail meat (117.86 ± 27.89 mg/100g) with 14.24% and back meat (104.82 ± 63.86 mg/100g) with 14.97%. Stearic acid percentage in C. niloticus (7.9%), Caiman yacare (11.62%) and red deer (13.04%) are lower than that of C. porosus meat, whereas goat meat has much higher stearic acid content (27.0 %) (Mushi et al., 2010; Osthoff et al., 2010; Vincente-Neto et al., 2010; Polak et al., 2008). Although shown to be one of the highest concentration among SFA, stearic acid is less likely to be incorporated into cholesterol esters, thus poses less harm to health as compared to palmitic acid (Emken, 1994). Dietary stearic acid is oxidatively desaturated to oleic acid in vivo at a rate of 2.4 times higher than the desaturation of palmitic acid to palmitoleic acid and has not shown to elevate blood cholesterol in the human body (Valsta, 2004; Emken, 1994). In clinical studies, stearic acid was associated with lowered LDL cholesterol in comparison with other SFAs, indicating that stearic acid may be healthier than other SFAs (Hunter et al., 2010). Behenic acid is the third most abundant SFA in C. porosus meat, where back meat (12.59%) shows highest percentage of behenic acid from total fatty acids, followed by thigh meat (12.31%) and tail meat (11.84%). As a dietary fatty acid, behenic acid is poorly absorbed, but it is a cholesterol-raising SFA despite its low bioavailability as compared to oleic acid (Caterm and Margo, 2001).
4.3.2 Monounsaturated Fatty Acids in Crocodile Meat
In C. porosus meat, the percentage of total MUFA present is 17.85% of total fatty acids in thigh meat, 15.87% in tail meat and 13.82% in back meat. Oleic acid (C18:1) is highly abundant among other MUFA which include palmitoleic acid (C16:1), eicosenoic acid (C20:1) and nervonic acid (C24:1). The thigh meat of C. porosus contains highest amounts of oleic acid (181.95 ± 16.00 mg/100g), which is equivalent to 17.33% of total fatty acids. Tail meat has second highest amount of oleic acid among different parts of C. porosus meat (121.37 ± 6.68 mg/100g) with 14.67% total fatty acids, followed by back meat (90.35 ± 7.39 mg/100g) with 12.91% total fatty acids. The oleic acid content of goat meat (28.20%), C. niloticus (27.3%) and Caiman yacare (25.86%) are higher than that of C. porosus meat (Mushi et al., 2010; Osthoff et al., 2010; Vincente-Neto et al., 2010), and Mitchell et al. (1995) reported high oleic acid content (33.1%) in C. porosus and C. johnsoni meat in their study. Differences in the oleic acid content might be due to the freshness of meat, as the rate of desaturation of stearic acid to oleic acid has to be taken into consideration (Higgs, 2000).
MUFA content is an important part of total fatty acids, as it aids in the reduction of the level of plasma LDL cholesterol (Chilton, 2004). Oleic acid, which is a product from denaturation of stearic acid by the enzyme stearoyl Co-A denaturase, works in increasing the HDL-cholesterol concentration and decreases the LDL concentration (Wood et al., 2008; Katan et al., 1994). As only LDL is related to cardiovascular diseases, higher oleic acid concentration will have a positive effect on human health (Prado et al., 2003). Studies have shown that oleic acid that is very abundant in olive oil poses hypotensive effect that regulates membrane lipid structure and further reduces blood pressure in human (Teres et al., 2008). Despite its function in reducing blood pressure, previous studies has showed that oleic acids along with MUFA levels in the membranes of red blood cells are positively associated with the risk of breast cancer, while MUFA is also found to be predictors of postmenopausal breast cancer (Pala et al., 2001). This can be concluded that the consumption of C. porosus meat might be less effective in preventing cardiovascular diseases, but it has less effect on breast cancer as well.
4.3.3 Polyunsaturated Fatty Acids in Crocodile Meat
The percentage of PUFA in C. porosus meat is shown to be 33.54% in tail meat, 32.97% in back meat and 30.85% in thigh meat as shown in Table 4.3. The results are slightly lower than similar studies done on C. niloticus meat by Osthoff et al. (2010), which show 38.1% of total PUFA. Caiman yacare meat (27.33%) and red deer meat (25.87%) shows lower total PUFA value as compared to C. porosus meat, which means that crocodile meat is a good source of PUFA (Vincente-Neto et al., 2010; Polak et al., 2008). Major PUFAs in C. porosus meat include linoleic acid (C18:2) and docohexanoic acid (C22:6). Other PUFAs present in C. porosus meat are linolenic acid (C18:3), eicosadieonic acid (C20:2) and dihomoylinolenic acid (C20:3). Linoleic acid content is the highest among PUFAs, with 255.99 ± 14.19 mg/100g (24.38% of total fatty acids) in thigh meat, followed by tail meat (218.73 ± 22.84 mg/100g; 26.43%) and back meat (175.10 ± 98.11 mg/100g; 25.01%). Similar studies on linoleic acid content of C. porosus and C. johnsoni meat shows a percentage of 15.2% in the meat, which is lower than that of this study (Mitchell et al., 1995). Hoffman (2008) stated that differences in lipid composition should be attributed to species differences and variations in diet. Despite being an essential fatty acid along with linoleic acid, the linolenic acid content in C. porosus meat is low, which contributes 0.23 - 0.36% of the total fatty acids in C. porosus meat. Similar results have been reported for linolenic content in Caiman yacare meat (1.8%), C. niloticus meat (1.6%) and goat meat (0.64%).
Both SFA and MUFA can be synthesized by the human body; however linoleic acid and linolenic acid are essential fatty acids that must be obtained from a dietary source to avoid deficiency (Jones and Kobow, 1999). Linoleic acid and linolenic acid are needed to provide basic building blocks to make ω-3 and ω-6 fatty acids such as arachidonic acid and eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA) with the assistance of desaturases and elongase enzymes (Wood et al., 2008; McGuire and Beerman, 2007). Linolenic acid, a ω-3 fatty acid, has cardioprotective effects in the human body. Scheeder et al. (2001) reported that linolenic acid together with oleic acid and linoleic acid is considered as antiatherogenic factors, preventing substances and processes that cause artherosclerosis. The essential fatty acids can also be converted to other important compounds that are not fatty acids, such as eicosaniods, which is a group of compounds made of arachidonic acid and EPA (Calder, 2005). Eicosanoids have profound, hormone-like effects that assist and regulate the immune and cardiovascular systems, acting as chemical messengers that direct a variety of additional functions (Shahidi and Miraliakbari, 2005). As C. porosus meat is high in PUFA content, particularly linoleic content, the inclusion of C. porosus meat in the diet will can bring such benefits as mentioned.
4.3.4 Effects of Fatty Acids on the Physical Properties of Crocodile Meat
In terms of physical characteristics of C. porosus meat, high amounts of UFA give better structure (Lawrie and Ledward, 2006). The different parts of C. porosus meat have UFA content of 46.79 - 49.41%, which is considered average in meat (O'Sullivan and Kerry, 2009). UFAs have lower melting points that of SFAs, and fat tissue with high proportions of UFA will be less solid and more transluscent at a given temperature due to the high proportion of glycerides of SFAs that tends to be solids whilst those containing predominant UFA esters tend to be liquid (Mourot, 2009). However, higher UFA content increases the concentration of PUFA, causing the occurance of lipid oxidation within the meat, thus leading to meat rancidity, off-odours, flavor and colour changes as well as nutrient deterioration (Wood et al., 2008; Esteves and Cava, 2004).
Studies by Sheard et al. (2000) and Kouba et al. (2003) reported increased PUFA content in meat increases off-odours after seven days of retail display, and sensory evaluation on flavor liking of the meats was significantly reduced as compared from the results before display. Elmore et al. (2005) also showed that very high levels of lipid oxidation products have low levels of Vitamin E. It is observed that the rate of lipid oxidation can be controlled by the usage of Vitamin E (Kouba et al., 2003). A change in muscle colour seen during retail display in the study of Scollan et al. (2006b) suggested a link between lipid oxidation, vitamin E concentration and colour, where the intensity of the red colour declined gradually as the display period progressed. It can be concluded that C. porosus meat is prone to lipid oxidation due to high PUFA contents in meat.
4.3.5 Cholesterol Content in Crocodile Meat
The cholesterol content of C. porosus meat does not show significant differences (p>0.05) between different parts of meat. Thigh meat has the highest cholesterol content (24.35 ± 8.98 mg/100g), followed by tail meat (22.05 ± 1.48 mg/100g) and back meat (18.65 ± 12.66 mg/100g). Piironen et al. (2002) reported cholesterol values of chicken (56.2 mg/100g), beef (52 mg/100g) and pork (45 mg/100g) which are all higher than that of C. porosus meat. As compared to cholesterol values of wild meat, red deer meat provides cholesterol content of 73.45 mg/100g which is higher than C. porosus meat, while tegu lizards provide 18.2 mg/100g, which is lower than C. porosus meat (Polak et al., 2008; Caldironi and Manes, 2006). The magnitude of variation of the cholesterol contents is dependent of muscle types due to difference in fiber types, which explains the differences of cholesterol contents between different muscles of the same species as exhibited in C. porosus meat (Piironen et al., 2002; Chizzolini et al., 1999).
According to Valsta et al. (2005), the cholesterol content of meats varies between 30 and 120 mg/100g, and offals show even higher cholesterol content, however, the C. porosus meat showed cholesterol content of 18.65 - 24.35 mg/100g. From the comparison between different species of meat, it can be concluded that that the cholesterol content is directly proportional to fat content in meat (Caldironi and Manes, 2006). Past and present studies on the correlation of cholesterol levels and intake of food considered rich in cholesterol showed negative results, confirming that dietary cholesterol has only a minor effect on serum cholesterol levels (Chizzolini et al., 1999; Hu et al., 1997; Nelson et al., 1995). It is advisable that cholesterol intake should not exceed 300mg per day (Polak et al., 2008), thus making C. porosus meat a healthy choice of meat in terms of low cholesterol level.
Cholesterol is transported in the plasma by lipoproteins, which are Very Low Density Lipoproteins (VLDL), LDL and HDL (Lawrie and Ledward, 2006). High levels of HDL and low levels of LDL have been associated with low incidences of coronary diseases, thus related to low cholesterol levels. This is because high levels of serum cholesterol have been positively correlated with death from cardiovascular diseases in women and younger men (Buege et al., 1998). By consuming a diet with high levels of HDL and low levels of LDL, it is proven to significantly reduce the accumulation of blood cholesterol, as HDLs function to remove excess cholesterol from cells and transport them to the liver (Lewis and Rader, 2005). With PUFA/SFA ratio at 0.60 - 0.66 in C. porosus meat, it can be concluded that consuming C. porosus meat will help increase the HDL cholesterol levels in the body, reducing the risks of cardiovascular diseases. Moreover, as C. porosus meat is relatively low in cholesterol as compared to other meat sources, it is a healthier choice than other meat sources.
