Journal of Food Composition and Analysis 23 (2010) 1–8

Original Article

The nutritional value of lipids in various tropical aquatic animals from rice–fishfarming systems in northeast Thailand

Ioannis T. Karapanagiotidis a,*, Amararatne Yakupitiyage b, David C. Little c, Michael V. Bell c, Eleni Mente a

a School of Agricultural Sciences, Department of Ichthyology and Aquatic Environment, University of Thessaly, Fytoko Street, GR-38446 Nea Ionia Magnisia’s, Greeceb School of Environment, Resources and Development, Asian Institute of Technology, Pathumthani 12120, Thailandc Institute of Aquaculture, University of Stirling, Stirling FK9 4LA, Scotland, United Kingdom

A R T I C L E I N F O

Article history:

Received 1 March 2008

Received in revised form 21 July 2009

Accepted 5 August 2009

Keywords:

Lipids

Fatty acids

Fish nutrition

Freshwater fish

Aquaculture

Rice culture

Fisheries

Tropics

Food Security

Sustainable agriculture practice

Food analysis

Food composition

A B S T R A C T

Knowledge on the lipid compositions of tropical freshwater aquatic animals is limited despite their

importance in the human diet and the health-related benefits of fish lipids. This study examines the lipid

content and fatty acid composition from the edible muscle tissue of some common freshwater aquatic

animals that inhabit rice fields in Thailand, namely snakehead (Channa striatus), Gunther’s walking

catfish (Clarias macrocephalus), climbing perch (Anabas testudineus), blackline rasbora (Rasbora

borapetensis), swamp barb (Puntius brevis), and freshwater prawn (Macrobrachium nipponense). All

specimens were low in muscle fat (�1.1% of wet weight). There was considerable variation in the fatty

acid composition between species. All species were good sources of the essential fatty acids, and

particularly of C22:6n-3 (5.2–13.3% total FA) and C20:4n-6 (7.2–14.6% total FA), signifying their high

nutritional quality for human nutrition. The findings indicate that strategies for rural development, food

security, and alleviation of poverty in rural areas need to pay special attention to the management of

aquatic resources to ensure the health and well-being of rural people.

� 2009 Elsevier Inc. All rights reserved.

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1. Introduction

Aquatic animals play an important role in rural livelihoodsthroughout the rice-farming regions of Asia and are particularlycritical for the poor (Guttman, 1999). Rice fields and the associatedtrap ponds, which are either rain-fed or irrigated, are essentiallyfarmer-managed aquatic systems and provide habitats to a rangeof indigenous or introduced fish species, molluscs, crustaceans andamphibians, which can be harvested regularly and without regularstocking (Amilhat and Lorenzen, 2005; Nguyen Khoa et al., 2005).Such animals have been termed ‘‘self-recruiting species’’ (SRS) inaquaculture to differentiate them from species harvested fromunmanaged fisheries (Little, 2002). The catch from these rice–fishfarming systems is used mainly for consumption within thehousehold and often accounts for a large part of the animal proteinintake (Little, 2002). SRS can also be important as by-catch ofintensively managed fish ponds and can be sold for low prices,contributing to the nutrition of poor non-fish farmers in urban

* Corresponding author. Tel.: +30 24210 93069; fax: +30 24210 93068.

E-mail address: ikarapan@uth.gr (I.T. Karapanagiotidis).

0889-1575/$ – see front matter � 2009 Elsevier Inc. All rights reserved.

doi:10.1016/j.jfca.2009.08.001

areas (Little et al., 2004). An assessment in rural communities ofthree countries in SE Asia (Cambodia, Thailand and Viet Nam)identified snakehead, climbing perch, swamp catfish and smallprawns to be the most widely distributed and consumed types ofSRS (Morales et al., 2003).

Despite their diversity and importance as food for the localhuman populations, very little is known about the fatty acidcomposition of the freshwater aquatic animals in the tropicsconsidering the health-related benefits of fish lipids. In reviews offish lipids, references to freshwater tropical species usually aregreatly outnumbered by those dealing with cool-temperate marinespecies and commercially important freshwater species. Fish andseafood are the richest source of the n-3 polyunsaturated fatty acids(PUFA) in nature, and consumption of fish containing high levels oflong chain n-3 PUFA improves human health and nutrition (Ruxtonet al., 2007). The beneficial effects of n-3 fatty acids on health aregenerally accredited to oils from marine species, but the lipids fromfreshwater species can serve also as a valuable source of essentialfatty acids as they contain substantial concentrations of C20:5n-3and C22:6n-3 (Steffens, 1997). The aim of this study was to assess fatquality, especially the content in n-3 PUFA, of the most-consumedaquatic animal species from rice–fish farming systems.

I.T. Karapanagiotidis et al. / Journal of Food Composition and Analysis 23 (2010) 1–82

2. Materials and methods

2.1. Chemicals

Chloroform, methanol, isohexane and diethyl ether were HPLCgrade from Fisher (Loughborough, Leicestershire, UK). Concen-trated sulphuric acid (Aristar grade) and Merck silica gel 60 thinlayer chromatography (TLC) plates (no. 5721) and high perfor-mance TLC (HPTLC) plates (no. 5633) were obtained from VWR(Lutterworth, Leicestershire, UK). All other chemicals were fromSigma (Poole, Dorset, UK).

2.2. Study site and fish sampling

Fish sampling was conducted during the wet season from anumber of rain-fed rice fields in different localities in SisaketProvince, Thailand (Table 1). Sisaket Province is considered to beone of the least developed regions in Thailand according to the percapita GDP. Farming is the major occupation of 80% of thepopulation, while the region supplies 36% of the country’s rice.There is only one rice crop each year. The area is largely flat withconsiderable seasonal wetland areas, an extreme dry season and aninfertile soil. The fishing gear used in the rice fields was gillnets andfishing rods using small green frogs and worms as baits. A totalnumber of 15 climbing perch (Anabas testudineus), 15 walkingcatfish (Clarias macrocephalus), 15 snakehead (Channa striatus), 10blackline rasbora (Rasbora borapetensis), 5 swamp barb (Puntius

brevis) and 5 freshwater prawns (Macrobrachium nipponense) werecollected. Each specimen was placed in an air-tight polyethylenebag and immersed in plenty of crushed ice until being transportedto the laboratory. A portion of muscle was removed from eachspecimen, devoid of skin and bone, placed in an air-tightpolyethylene bag and stored at �20 8C. Samples were transportedto UK in dry ice for lipid analysis.

2.3. Lipid extraction and fatty acid analysis

The total lipid from wet muscle tissue was extracted andmeasured gravimetrically according to the method of Folch et al.(1957). Wet muscle samples were homogenised in chloroform/methanol (C:M 2:1, v/v) using an Ultra-Turrax tissue disrupter(Fisher Scientific, Loughborough, UK). The homogenates werefiltered and a Folch extract prepared. Samples were kept on iceunder nitrogen between procedures and lipid extracts stored inC:M (2:1, v/v) at a final concentration of 10 mg lipid/mL at �20 8C

Table 1The origin, number of specimens and muscle total lipid content of the aquatic animal

Aquatic animal species Location of the rice fi

Snakehead (Channa striatus) Pho, Mueang Sisaket

Nong Waeng, Kantha

Phon Kha, Mueang S

Catfish (Clarias macrocephalus) Pho, Mueang Sisaket

Phon Kha, Mueang S

Lom Sak, Khukhan d

Climbing perch (Anabas testudineus) Pho, Mueang Sisaket

Nong Waeng, Kantha

Lom Sak, Khukhan d

Blackline rasbora (Rasbora borapetensis) Nong Waeng, Kantha

Khup, Nam Kliang di

Swamp barb (Puntius brevis) Nong Waeng, Kantha

Freshwater prawn (Macrobrachium nipponense) Nong Waeng, Kantha

Note: Values for TL represent means� s.d. of 15samples for C. striatus, C. macrocephalus

nipponense.

under nitrogen. Solvents contained 0.05% (w/v) butylatedhydroxy-toluene (BHT) as an antioxidant. Fatty acid methyl esters(FAME) were prepared by acid-catalysed transesterification of1 mg total lipid with 0.1 mg heptadecanoic acid (Sigma ChemicalCompany, St. Louis, USA) as internal standard using 2 mL of 1% (v/v) sulphuric acid in methanol and 1 mL of toluene under nitrogenat 50 8C for 16 h. Crude FAME were purified by TLC in isohexane:diethyl ether: acetic acid (90:10:1, v/v) and visualised by sprayinglightly the edge of the plate with 1% (w/v) iodine in CHCl3. FAMEwere scraped from the plate and eluted with isohexane: diethylether (1:1, v/v). Purified FAME were re-dissolved in isohexanecontaining 0.05% BHT and stored under nitrogen at �20 8C prior togas–liquid chromatography.

Fatty acid methyl esters were separated and quantified by gas–liquid chromatography (Fisons 8000 series, Thermo-Finnegan,Hemel Hempstead, UK) using a CP Wax 52CB fused silica capillarycolumn (30 m � 0.32 mm i.d., 0.25 mm film thickness) (Chrompak,London, UK). Hydrogen was used as carrier gas at a flow rate of2.5 mL/min and temperature programming was from 50 8C to150 8C at 40 8C/min and from 150 8C to 225 8C at a rate of 2 8C/minand the final temperature of 225 8C was maintained for 5 min.Individual methyl esters were identified by comparison to knownstandards (marine fish oil). Peak areas of fatty acids werequantified with reference to the peak area of 17:0 internalstandards and computed automatically by a computing integrator(Chromcard for Windows, ThermoQuest, Milan, Italy).

2.4. Statistical analysis

Data from individual fish were treated as independent samples.Muscle total lipid and fatty acid composition were subjected toone-way analysis of variance (ANOVA) and differences wereconsidered significant at an alpha value of 0.01. Analyses wereperformed using SPSS statistical package (version 13.0, SPSS Inc.,Chicago, USA). Data that were identified as non-homogeneous(using Levene’s test of homogeneity) were subjected to either logor power transformation before analysis. Differences betweenmeans were determined by Tukey’s test.

3. Results and discussion

3.1. Total lipid (TL)

All aquatic animal species that were sampled in this studycontained low levels of mean TL, varying from 0.86% of wet weight

species collected.

eld No. of specimens TL (% of w.w.)

district 5 0.99�0.13

rarom district 5

isaket district 5

district 5 1.03�0.12

isaket district 5

istrict 5

district 5 0.99�0.15

rarom district 5

istrict 5

rarom district 5 0.86�0.19

strict 5

rarom district 5 0.90�0.17

rarom district 5 1.13�0.21

and A. testudineus, 10 samples for R. borapetensis and 5 samples for P. brevis and M.

I.T. Karapanagiotidis et al. / Journal of Food Composition and Analysis 23 (2010) 1–8 3

muscle tissue in R. borapetensis to 1.13% of w.w. in M. nipponense

with no significant differences in the muscle TL content among thesix species (Table 1). Within the same species, no significantdifferences were found for the TL content of fish from the differentlocalities. There is some information published on the total lipidcontent of C. macrocephalus, C. striatus and A. testudineus but nonefor the fat content of R. borapetensis, P. brevis, and M. nipponense. Itshould be noted here that the higher values for the TL of thesespecies in the literature are usually coming from studies in whichthe fish were obtained from cultured conditions, where feed inputsare higher, or from fish markets where again fish may had beenpreviously farmed. In the present study, the muscle TL content of C.

macrocephalus was 1.03% of w.w., which is lower than thatreported for the same species under cultivation (2.5% w.w., Shiraiet al., 2002; 3.25% of w.w., Rahman et al., 1995) but similar to themuscle TL (0.86% w.w.) of other wild catfish species (Hetero-pneustes fossilis, Nair and Gopakumar, 1978).

The muscle TL of C. striatus was 0.99% of w.w. (Table 1) which issimilar compared to that reported for the same species from thewild (1.2% w.w., Henderson and Tocher, 1987); and to other wildChanna sp., e.g. Channa argus, 0.9% w.w. (Henderson and Tocher,1987); Channa marulius, 0.8% w.w. (Henderson and Tocher, 1987)and Channa punctata, 0.8% w.w. (Henderson and Tocher, 1987). Onthe other hand, Rahman et al. (1995) reported much higher muscleTL for farm raised C. striatus 3.25% w.w. (Rahman et al., 1995). A.

testudineus contained similar levels of TL in their muscle tissues toC. striatus (Table 1). However, A. testudineus has been reported tobe a more fatty fish compared to several species of snakehead,including C. striatus (Wimalasena and Jayasuriya, 1996).

P. brevis sampled from the rice fields of Kanthararom district(Sisaket province, Thailand), was found to contain 0.90% w.w. of TL.Puntius species is known to be a lean to moderate-fat fish. Nair andGopakumar (1978) found that the Egyptian filamented barb (P.

filamentous) contained 1.14% w.w. of TL in their muscle tissues(Henderson and Tocher, 1987), while the muscle fat of P.

gonionotus ranges from 4 to 5% w.w. (Rahman et al., 1995;Mohanta et al., 2007). The muscle of R. borapetensis showed thelowest values for TL (0.86% w.w.) and M. nipponense the highestvalues (1.13% w.w.) compared to the other aquatic animal speciesin the present study (Table 1).

C. macrocephalus, C. striatus, A. testudineus, R. borapetensis, P.

brevis, and M. nipponense collected from their wild habitats aretherefore classified as lean fish on the basis of their muscle fatcontent according to Henderson and Tocher (1987). It is wellknown that wild fish tend to be leaner compared to their culturedcounterparts (Karapanagiotidis et al., 2006). In rice–fish farmingsystems the feed inputs are limited and the aquatic animals arefeeding opportunistically on the wild flora and fauna that inhabitthese environments. Therefore, it is not surprising that this studyfound the fat content of these aquatic animal species to be amongthe lowest reported.

The lipid content in the muscle tissues of the fish and prawnscollected from various rice fields in this study was relativelyconstant, both within and between the species. The fat content infish and shellfish, however, can vary according to numerousfactors, both endogenous (genetically controlled and associatedwith species-specific life cycle) and exogenous (environmental anddietary) that operate simultaneously (Shearer, 1994). Thus, the fatcontent is species-specific and could be affected by season,geographical variation, reproductive maturation, growth, watertemperature and dietary energy intake. Shirai et al. (2002) showedthat there was seasonal variation of the total lipid from edibleportion of Japanese (Silurus asotus) and Thai catfish (C. macro-

cephalus). Mohanty and Samantaray (1996) also showed theseasonal change of the lipid content of snakehead (C. striatus)which was correlated to the water temperature and the

reproductive cycle. During the summer period, in which theaquatic animal species were captured in the present study, fish andshellfish become reproductively more active causing highermetabolic rates and increased requirements for energy that arefulfilled by the lipid reserves. In winter, during the non-breedingphase, fish are less metabolically active and deposition of lipidreserves in the body usually occurs (Tiwary et al., 1989).

3.2. Fatty acid composition

A total number of 33 fatty acids of various chain lengths andsaturation levels were identified by gas–liquid chromatography(Table 2). Of the saturated fatty acids (SFA) palmitic acid (C16:0)and stearic acid (C18:0) were found to be the dominant ones in allspecies sampled. These fatty acids occur naturally in fish andshellfish lipids, as in all animal fats, and are the major products ofthe fatty acid synthetase system (Sargent et al., 2002). C16:0 andC18:0, as well as C18:1n-9, are also the major sources of metabolicenergy in fish for growth (Sargent et al., 2002). All other SFA wereminor components though C14:0 and C15:0 comprised 1.3–2.2% inR. borapetensis, P. brevis and M. nipponense (Table 2). R. borapetensis

had significantly higher SFA than all the other species. The higherSFA levels in R. borapetensis were attributed mainly to the higherlevels of C16:0 but also of C14:0 and C15:0 in these fish (Table 2). Ithas been suggested that levels of SFA are regulated within a narrowphysiological range as these are preferentially oxidized by fish togenerate energy for growth (Bell et al., 2002).

Oleic acid (C18:1n-9) was the major monounsaturated fattyacids (MUFA) in all samples (Table 2), with C18:1n-7 comprising2.6–5.5% and C16:1n-7 1.1–3.8% total FA. Many fish and shellfishspecies are well supplied with these fatty acids in their naturaldiets but they can also synthesise them de novo (Sargent et al.,2002). Fish and shellfish, in common with all animal organisms, arecapable of desaturating C16:0 and C18:0 by a microsomal D9 fattyacid desaturase to yield, respectively, C16:1n-7 and C18:1n-9. TheD9 desaturation system has been particularly well characterized infish, but less well studied is the extent to which C16:1n-7 andC18:1n-9 are chain elongated to higher homologues, includingC18:1n-7, C20:1n-9, C22:1n-9 and C24:1n-9, which were found inthe muscle lipids of all the collected species (Table 2). Vaccenicacid (18:1n-7) and nervonic acid (C24:1n-9) are commonly foundin small amounts in all fish oils. The tropical freshwater fish andshellfish analysed in the present study contained low amounts ofgadoleic acid (C20:1n-9) and cetoleic acid (C22:1n-11) (Table 2),which are found in higher quantities in fish from northern/temperate hemisphere and high latitude waters.

As far as the comparative MUFA levels among the six species areconcerned, there were marked differences, specifically in C16:1n-7and C18:1n-9. C. striatus contained the lowest levels of MUFA andthe P. brevis the highest (Table 3). There was also variation in theMUFA levels of A. testudineus coming from different localities(Table 2). The fact that MUFA comprised the lowest category of FAin all species is not surprising as in general wild fish are known tocontain low levels of MUFA, which is related to the limited energyintake (Shirai et al., 2002). In wild fish, it seems that MUFA ratherthan SFA are the preferred metabolisable substrate for energyneeds (Karapanagiotidis et al., 2006).

The muscle lipids of the fish and shellfish were characterized byhigher proportions of total polyunsaturated fatty acids (PUFA, 36.7–47.8% of total FA) compared to SFA (32.1–38.1%) and MUFA (14.6–25.2%) (Table 3). An exception to this was the muscle TL of R.

borapetensis where the PUFA fraction was similar to SFA but bothwere much higher than the MUFA fraction. The levels of PUFA werevariable among species (Table 2) with C. striatus containing thehighest and R. borapetensis the lowest level of PUFA and (Table 2).Docosahexaenoic acid (C22:6n-3) and arachidonic acid (C20:4n-6)

Table 2The fatty acid compositions (% of total FA) of the edible muscle tissue of the selected aquatic animal species.

Fatty acid C. macrocephalus A. testudineus

Pho Phon Kha Lom Sak Pho Nong Waeng Lom Sak

C14:0 0.95� 0.22 0.79� 0.20 1.10� 0.40 0.38�0.06 0.63� 0.17 0.61� 0.14

C15:0 1.09� 0.14 0.76� 0.12 1.18�0.31 0.53�0.06 0.85� 0.34 0.36� 0.07

C16:0 20.64�3.17 17.47� 0.70 21.32�2.73 19.38�0.82a 21.69�1.53ab 23.92�1.40b

C18:0 10.02�1.16 10.41� 0.42 9.84�0.79 12.03�0.48 10.90�1.04 10.61� 0.17

C20:0 0.37� 0.01 0.23� 0.05 0.36� 0.05 0.21�0.06 0.22� 0.04 0.34� 0.13

C22:0 0.77� 0.41a 0.26� 0.03b 0.39� 0.07ab 0.29�0.09 0.25� 0.08 0.34� 0.20

Total SFA 33.85�2.80 29.92� 0.52 34.19�2.66 32.82�0.55a 34.54�1.83ab 36.18�1.39b

C16:1n-9 0.41� 0.08a 0.31� 0.08a 0.76� 0.12b 0.12�0.08 0.21� 0.12 0.55� 0.18

C16:1n-7 2.77�0.51 2.41� 0.40 3.10�1.35 1.92�0.31 2.30� 0.78 2.72� 0.79

C18:1n-9 10.14�2.81 8.16� 0.78 13.34�3.89 8.74�0.45a 12.31�0.92b 26.19�8.55c

C18:1n-7 4.74�0.45 5.47� 0.67 5.35�0.63 4.06�0.42a 2.85� 0.26b 2.58� 0.36b

C20:1n-9 0.87� 0.33 1.01�0.39 0.71� 0.33 0.30� 0.12 0.47� 0.17 0.50�0.08

C20:1n-7 0.44� 0.11 0.46� 0.12 0.31� 0.21 n.d. 0.40�0.10 n.d.

C22:1 0.51� 0.34 0.34� 0.05 n.d. 0.13�0.12 0.28� 0.17 0.10�0.07

C24:1n-9 0.19� 0.06 0.17� 0.04 0.11� 0.06 0.24�0.02 0.16� 0.06 0.24� 0.05

Total MUFA 20.07�2.22 18.31�1.51 23.76�4.62 15.58�0.73a 18.98�1.18b 32.93�9.12c

C18:2n-6 7.10�1.51 5.81� 0.93 7.28�1.49 5.08�0.85 5.78�1.02 5.16�1.19

C18:3n-6 0.32� 0.11 0.26� 0.08 0.23� 0.07 0.23�0.06 0.42� 0.14 0.33� 0.07

C20:2n-6 1.08� 0.32 1.53� 0.48 1.20� 0.14 0.46�0.11 0.89� 0.27 0.61� 0.16

C20:3n-6 2.43�0.57 2.29� 0.31 1.57�0.34 0.86�0.12 1.33� 0.16 1.43� 0.40

C20:4n-6 12.29�1.79 15.79�1.78 11.35�3.80 15.42�1.08a 12.59�1.57ab 8.40�4.49b

C22:4n-6 1.65�0.44ab 2.80�0.46a 1.43�0.33b 2.14�0.35 2.28� 0.46 1.44� 0.60

C22:5n-6 1.51�0.75 1.71� 0.27 1.64�0.50 2.78�0.61 3.32�1.06 2.24� 0.89

Total n-6 26.39�2.25 30.20�2.30 24.70�3.15 26.97�1.20 26.62�2.19 19.61�6.81

C18:3n-3 3.42�0.89 2.47� 0.79 2.57�0.79 1.04�0.27a 2.03� 0.33b 0.76� 0.33a

C18:4n-3 0.49� 0.26 0.52� 0.20 0.38� 0.13 0.14�0.02 0.29� 0.10 0.16� 0.05

C20:3n-3 0.39� 0.10 0.54� 0.22 0.28� 0.05 0.40� 0.04 0.49� 0.07 n.d.

C20:4n-3 0.50� 0.06 0.45� 0.09 0.31� 0.07 0.16�0.03 0.20�0.02 n.d.

C20:5n-3 3.13�0.02 3.73� 0.61 2.62�0.88 1.52�0.44a 1.11� 0.35ab 0.54� 0.18b

C22:4n-3 n.d. 0.15� 0.14 n.d. n.d. n.d. n.d.

C22:5n-3 2.60� 0.69 3.00�0.38 2.23�0.65 3.82�0.44a 2.71� 0.28b 1.34� 0.44c

C22:6n-3 5.95�2.54 7.06�1.42 6.56�2.83 12.36�0.97a 9.41� 0.72a 5.04�2.04b

Total n-3 16.47�2.13 17.93�2.11 14.95�3.52 19.46�0.91a 16.26�0.62b 7.91�2.49c

Total PUFA 42.86�4.39 48.13�1.61 39.64�6.60 46.44�1.06a 42.88�2.27a 27.52�9.23b

(n-3)/(n-6) 0.62� 0.03 0.60�0.10 0.60� 0.07 0.72�0.06a 0.61� 0.05a 0.41� 0.05b

Total DMA 3.22�0.64 3.64� 0.40 2.41�0.66 5.16�0.53 3.61� 0.36 3.37�1.39

Total FA 100 100 100 100 100 100

Fatty acid C. striatus R. borapetensis P. brevis M. nipponense

Pho Nong Waeng Phon Kha Nong Waeng Khup Nong Waeng Nong Waeng

C14:0 0.46�0.04a 0.33�0.02b 0.38�0.05b 1.89� 0.74 2.24� 0.73 1.77�0.24 1.44�0.24

C15:0 0.55�0.06a 0.68�0.11b 0.60� 0.09ab 1.33� 0.49 1.55� 0.55 2.00�0.35 1.74�0.48

C16:0 20.58�0.54 17.34�1.15 18.48�1.10 22.75�1.14 23.13� 0.71 20.49�1.01 18.46�1.65

C18:0 14.33� 0.59 13.83�0.44 14.20�0.65 11.48�1.24 10.78�1.07 9.56�0.15 10.45�1.37

C20:0 0.30�0.03 0.30�0.02 0.28�0.02 0.33�0.05 0.33�0.05 0.56�0.07 0.48�0.11

C22:0 0.36�0.16 0.32�0.05 0.31�0.05 0.31�0.04 0.29�0.04 0.52�0.07 0.50� 0.12

Total SFA 36.58� 0.74a 32.79�1.40b 34.25�1.32ab 38.08�1.22 38.32� 0.96 34.90�0.45 33.06�1.98

C16:1n-9 0.30�0.08 0.26�0.05 0.30� 0.06 0.76�0.10 0.80�0.05 0.40�0.06 0.12�0.00

C16:1n-7 1.20�0.31 1.23�0.10 1.11�0.12 2.86� 0.52 3.07�0.39 3.05�0.65 3.82�0.83

C18:1n-9 8.98�1.39 7.18�0.74 8.32�0.93 14.29�1.13 14.31� 0.83 14.74�2.69 12.00�1.52

C18:1n-7 4.06�0.18 4.10�0.55 4.05�0.43 3.89� 0.81 4.07�1.01 4.45�0.23 4.30�0.69

C20:1n-9 0.31�0.10 0.33�0.15 0.30� 0.06 0.29�0.08 0.26�0.03 1.17�0.02 0.52�0.19

C20:1n-7 0.27�0.18 0.33�0.03 0.29�0.07 0.32�0.05 0.33�0.06 0.71�0.06 0.42�0.10

C22:1 0.32�0.26 0.16�0.06 0.19�0.02 0.16�0.06 0.17�0.08 0.35�0.14 0.13�0.12

C24:1n-9 0.33�0.01 0.31�0.04 0.33�0.02 0.23�0.10 0.18�0.10 0.35�0.18 0.18�0.07

Total MUFA 15.58�1.24 13.91�0.78 14.92�1.02 22.81�1.86 23.20� 0.27 25.21�2.48 21.49�1.91

C18:2n-6 4.76�0.59 4.26�0.95 4.39�0.65 5.90�0.44 5.88� 0.31 11.36�2.62 8.69�2.18

C18:3n-6 0.23�0.04 0.24�0.07 0.24�0.02 0.49�0.12 0.53�0.15 0.71�0.02 0.53�0.10

C20:2n-6 0.77�0.05 0.94�0.23 0.81�0.10 0.37�0.05 0.35�0.04 0.81�0.07 0.63�0.14

C20:3n-6 1.25�0.23 1.43�0.38 1.29�0.23 0.82�0.18 0.76�0.15 0.88�0.05 0.60� 0.26

C20:4n-6 13.95� 0.87 15.19�1.30 15.03�0.97 7.57�1.76 6.71�1.39 7.25�0.99 11.05�1.45

C22:4n-6 3.23�0.25 3.11�0.39 3.27�0.36 0.59�0.19 0.53�0.15 0.70�0.13 0.52�0.21

C22:5n-6 3.47�0.51 3.93�0.68 3.85�0.41 1.83� 0.34 1.65� 0.16 1.54�0.46 1.31�0.63

Total n-6 27.67�1.38 29.09�2.57 28.88�1.54 17.57�2.09 16.40�1.42 23.25�2.00 23.34�1.62

C18:3n-3 1.13�0.20 1.35�0.46 1.22�0.18 4.32�1.92 5.21�1.88 5.49�0.56 3.73�1.02

C18:4n-3 n.d. 0.12�0.02 0.10� 0.02 0.81�0.71 1.12� 0.80 0.63�0.07 0.31�0.06

C20:3n-3 0.56�0.09 0.57�0.13 0.59�0.09 0.41�0.27 0.47�0.35 0.39�0.03 0.25�0.02

C20:4n-3 0.17�0.02 0.22�0.06 0.20� 0.03 0.48�0.14 0.55�0.13 0.37�0.03 0.21�0.06

C20:5n-3 0.61�0.06 0.80�0.29 0.75�0.10 2.24� 0.13 2.32� 0.08 2.26�0.28 6.64�2.67

I.T. Karapanagiotidis et al. / Journal of Food Composition and Analysis 23 (2010) 1–84

Table 2 (Continued )

Fatty acid C. striatus R. borapetensis P. brevis M. nipponense

Pho Nong Waeng Phon Kha Nong Waeng Khup Nong Waeng Nong Waeng

C22:4n-3 n.d. 0.13� 0.01 n.d. n.d. n.d. 0.14� 0.04 n.d.

C22:5n-3 2.92�0.28 3.33� 0.50 3.24� 0.29 1.26�0.26 1.26�0.27 1.04� 0.14 0.71� 0.44

C22:6n-3 13.07� 0.34 13.55�1.84 13.59�1.22 10.05�2.44 9.38�1.42 5.17�1.57 5.38�4.81

Total n-3 18.49�0.74 20.07�1.33 19.77�1.10 19.55�1.81 20.31�0.64 15.47�1.80 17.23�2.12

Total PUFA 46.16�1.42 49.16�1.61 48.66�1.42 37.12�2.46 36.71�0.84 38.72�2.66 40.57�1.57

(n-3)/(n-6) 0.67� 0.05 0.70� 0.10 0.68� 0.09 1.13�0.19 1.25�0.14 0.67� 0.10 0.74� 0.14

Total DMA 1.69�2.07 4.14� 0.13 2.18� 0.55 1.99�0.61 1.77�0.48 1.16� 0.25 4.89�1.28

Total FA 100 100 100 100 100 100 100

Note: n.d., not detected (values <0.10); values represent means� s.d. (n = 5). For each species, values in the same row sharing the same superscript letters are significantly

different at a = 0.01. For R. borapetensis, the means of the two groups of fish that were collected from different locality were compared using the Student’s t-test. SFA, saturated fatty

acids; MUFA, monounsaturated fatty acids; PUFA, polyunsaturated fatty acids; DMA, dimethylacetal.

I.T. Karapanagiotidis et al. / Journal of Food Composition and Analysis 23 (2010) 1–8 5

were the most abundant PUFA in the muscle lipids of all species(Table 3), followed by linoleic acid (C18:2n-6), linolenic acid(C18:3n-3) and eicosapentaenoic acid (C20:5n-3). There was aconsiderable variation in the levels of the above fatty acids among thespecies (Table 2) but not within the species (Table 3). However, A.

testudineus, showed considerable variation in the levels of severalPUFA between fish coming from the three localities. A. tesudineusfrom Lom Sak had lower n-3/n-6 polyunsaturated fatty acid (PUFA)ratios compared to fish coming from rice fields in Pho and NongWaeng subdistricts (Table 2). A similar trend, although notsignificant, was also observed for C. macrocephalus sampled fromLom Sak and Pho subdistricts, which probably reflects the fatty acidcomposition of the natural food in these sites.

Furthermore, there was considerable variation in the levels ofPUFA between the six species (Table 3). C. striatus contained thehighest levels of C22:6n-3 (13.34% of total FA, Table 3) in musclelipids while M. nipponense, P. brevis and C. macrocephalus hadsignificantly lower levels. C. striatus also contained the highestlevels of C20:4n-6 (14.6% of total FA), which were significantlyhigher than those found in R. borapetensis and P. brevis. C. striatus

and A. testudineus had much lower levels of C18:3n-3 and ofC20:5n-3 compared to the other species. P. brevis had comparablelevels of C18:3n-3 and C22:6n-3 in their lipids, while the prawn M.

nipponense contained the highest levels of C20:5n-3 and was theonly species with more C20:5n-3 than C22:6n-3 (Tables 2 and 3).R. borapetensis contained the lowest levels of total n-6 PUFA andcomparably high levels of total n-3 fatty acids compared to the restof the species and consequently these fish contained significantlyhigher n-3/n-6 PUFA ratios in their tissues (Table 3).

Table 3The contents of the most important fatty acids (% of total FA) in the muscle tissue of t

Fatty acid R. borapetensis M. nipponense C. striatus

C16:0 22.89� 0.26a 18.46�1.67b 18.78�1.

C18:0 11.21�1.16b 10.45�1.35ab 14.06�0.

Total SFA 38.17�1.06a 33.06�1.98b 34.47�2.

C16:1n-7 2.94� 0.46bc 3.82� 0.83c 1.36�0.

C18:1n-9 14.30� 0.97b 12.00�1.52ab 7.98�1.

Total MUFA 22.95�1.43ab 21.49�1.91ab 14.65�1.

C18:2n-6 5.89� 0.37a 8.69�2.18b 4.48�0.

C20:4n-6 7.25�1.59a 11.05�1.45ab 14.64�1.

Total n-6PUFA 16.99� 0.83a 23.34�1.62ab 28.46�2.

C18:3n-3 4.65�1.82bc 3.73�1.06bc 1.25�0.

C20:5n-3 2.27� 0.12b 6.64�2.67c 0.71�0.

C22:6n-3 9.80�2.02ab 5.38�4.81a 13.34�1.

Total n-3PUFA 19.84�1.46a 17.23�2.12ab 19.37�1.

Total PUFA 36.97�1.92b 40.57�1.57ab 47.83�2.

(n-3)/(n-6) 1.17� 0.18a 0.74� 0.14b 0.68�0.

Note: Values for C. striatus, C. macrocephalus and A. testudineus represent means� SD (n =

nipponense represent means� SD (n = 5). Values in the same row, which do not share the sa

MUFA, monounsaturated fatty acid; PUFA, polyunsaturated fatty acid.

Comparative studies with species of the same order have shownthat these tropical freshwater species contain highly variablelevels of n-3 and n-6 PUFA in their muscle tissues. However, it isimportant to distinguish between wild and farmed fish since thelatter tend to be fed diets which as well as containing higher lipidlevels than found in natural food also have a high n-6 FA contentderived from plant seed oils and meals. The predominance ofC16:0, C18:1n-9, C18:2n-6, C20:4n-6, C22:6n-3 in the musclelipids of Thai catfish (C. macrocephalus) was also shown in a studyby Shirai et al. (2002). However, in contrast to our findings, thesecultured fish contained poor levels (<1% of total FA) of C22:6n-3,C20:5n-3 and C20:4n-6. In the same study, wild Japanese catfish (S.

asotus) contained moderate levels of the above fatty acids.Idoniboye-Obu et al. (1993) found small quantities of C22:6n-3and C20:4n-6 in three species of cultured clariid fish. In agreement,Rahman et al. (1995) analysing the FA composition of severalfreshwater fish including species of snakehead, catfish and carps,found very low contents of C20:4n-6, C20:5n-3 and C22:6n-3 inthe majority of them. Dutta et al. (1985) showed that there was aseasonal influence on the levels of C20:5n-3 and C22:6n-3 inIndian snakehead (C. punctatus), which were higher in the colderperiod. Very high levels of C20:4n-6 have also been found invarious snakehead species: C. argus (Choi et al., 1985), C. striatus

and C. melanosoma (Jais et al., 1995), C. gachua, C. punctatus and C.marulius (Sen et al., 1976). However, the levels of C20:5n-3 andC22:6n-3 in these species were very low (Choi et al., 1985; Jais etal., 1995).

The FA composition in fish is known to vary considerably, bothwithin and between species (Ackman, 1989; Henderson and

he aquatic animal species.

P. brevis C. macrocephalus A. testudineus

92b 20.49�1.01ab 19.45�2.66b 21.50�2.22ab

54c 9.56�0.15a 10.13�0.68ab 11.22� 0.90b

27b 34.90�0.45b 32.19�2.78b 34.39�1.87b

25a 3.05�0.65bc 3.14�0.98bc 2.56� 0.79b

38a 14.74�2.69b 10.40�3.40ab 15.00�8.58ab

28a 25.21�2.48b 20.61�3.80ab 21.75�8.71ab

81c 11.36�2.62d 6.58�1.34ab 5.35� 0.99a

25b 7.25�0.99a 13.54�3.27b 12.40�3.77ab

14b 23.25�2.00ab 27.51�3.56b 24.74�4.90b

37a 5.49�0.56c 2.68�0.81ab 1.31� 0.63a

23a 2.26�0.28b 3.22�0.81b 1.09� 0.52a

34b 5.17�1.57a 6.68�2.01a 9.21�3.26ab

33a 15.35�1.80b 16.58�2.81ab 15.02�5.05b

14a 38.72�2.66b 44.09�5.69ab 39.76�9.41b

08b 0.67�0.10b 0.60�0.07b 0.60� 0.14b

15), values for R. borapetensis represent means� SD (n = 10), values for P. brevis and M.

me superscript letters are significantly different at a = 0.01. SFA, saturated fatty acid;

Table 4Typical levels of n-3and n-6PUFA of selected fish oils and other food groups (values are expressed as g fatty acid/100 g total fatty acids).

Fatty acid C18:2n-6 C18:3n-3 C20:4n-6 C20:5n-3 C22:6n-3 n-3/n-6 Source

Warmwater-freshwater fish

Aquatic animals from rice fields 5.3–11.3 1.2–5.5 7.2–14.6 0.7–6.6 5.3–13.3 0.6–1.1 1

Wild Japanese catfish (Silorus asotus) 5.2 2.5 2.2 2.3 4.9 1.4 2

Farmed silver carp (Hypophthalmichthy molitrix) 4.3 7.0 3.3 6.6 2.0 2.0 3

Farmed snakehead (Channa striatus) 8.2 0.5 2.2 0.3 1.5 0.7 4

Farmed common carp (Cyprinus carpio) 7.9 2.9 8.6 8.8 6.5 1.1 3

Farmed nile tilapia (Oreochromis niloticus) 9.0 0.8 1.5 0.8 9.0 0.8 5

Coldwater-freshwater fish

rainbow trout (Oncorhynchus mykiss) 4.6 5.2 2.2 5.0 19.0 4.2 3

Perch (Perca fluviatilis) 1.5 0.5 9.1 8.8 26.5 2.7 6

Roach (Rutilus rutilus) 4.5 2.8 5.5 10.7 14.9 2.8 6

Marine fish

Atlantic herring (Clupea herengus) 0.7 0.3 0.4 7.4 3.9 7.7 3

Cod liver oil 1.8 0.7 1.7 8.9 9.3 7.4 7

Thai sardine (Sardinella gibbosa) 1.2 0.5 2.7 6.1 19.7 5.8 8

Wild Atlantic salmon (Salmo salar) 2.7 4.6 4.2 5.1 17.6 4.0 9

Farmed Atlantic salmon (Salmo salar) 5.4 0.9 10.6 5.7 11.9 1.2 9

Other foods

Human milk 8.9–17.6 0.4–1.5 C20 + C22PUFA<2.0 10

Lard 10.0 1.4 0.1 7

Chicken fat 18.9 1.3 <0.1 11

beef tallow 1.7 0.6 0.4 0.3 11

Pork fat 23.1 0.0 12

Duck fat (domesticeted, raw meat) 11.3 1.3 0.1 9

Water buffalo (raw meat) 11.7 2.9 5.1 0.2 9

Rice bran oil 29.0–42.0 0.5–0.1 <0.1 11

Soybean oil 52.0–60.0 2.0–8.0 <0.1 11

Coconut oil 1.0–3.0 0.0 11

Groundnut oil 13.0–28.0 0.0 11

Corn oil 34.0–62.0 0.0 11

Palm oil 2.0–11.0 0.0 11

Sunflower oil 55.0–70.0 0.0 11

Note: Data are adopted and modified in order to be expressed as % of total FA; (1) present study; (2) Shirai et al. (2002); (3) Steffens (1997); (4) Rahman et al. (1995); (5)

Karapanagiotidis et al. (2006); (6) Ahlgren et al. (1994); (7) Hasan (2001); (8) Chaijan et al. (2006); (9) USDA (2007); (10) Lien (1992) for mature human milk from mothers on

ad libidum Western diets; (11) FAO (1987); (12) Koch et al. (1968).

I.T. Karapanagiotidis et al. / Journal of Food Composition and Analysis 23 (2010) 1–86

Tocher, 1987). This depends on whether the species is freshwateror marine, while a wide range of factors have been reported toaffect the FA variability, including water temperature, seasonality,reproductive stage, wild or reared in captivity among others(Ackman, 1989). In general, the lipids of freshwater fish species arecomposed by higher proportions of saturated fat and C18 PUFA andlower levels of C20 and C22 PUFA than the lipids of marine fishspecies (Sargent et al., 2002). In addition, the FA composition offreshwater fish is characterized by higher levels of n-6 PUFA,especially C18:2n-6 and C20:4n-6, and their ratio of n-3/n-6 PUFAis lower than that of marine fish, ranging from 0.5 to 4.0(Henderson and Tocher, 1987) with the lowest values generallybeing found in tropical species. This reflects the FA composition oftheir dietary lipids. Freshwater micro-algae, such as blue greenalgae, are rich in C18:2n-6 but PUFA of chain lengths greater thanC18 are not present in large amounts (Ahlgren et al., 1992). Greenleaves of terrestrial plants that constitute a significant input tofreshwater ecosystems are generally rich in C18:3n-3, whileC20:5n-3 is contained in some primitive mosses, liverworts andferns (Kenyon, 1972). Insects and insect larvae that can form alarge part of the diet of many freshwater fish are rich in C18:2n-6and C18:3n-3 with smaller amounts of C20:4n-6 and C20:5n-3,and some C22:6n-3 (Sargent et al., 2002). Good sources of C22:6n-3 in freshwater ecosystems are certain flagellates, such asCryptomonas, Rhodomonas and Peridinium (Ahlgren et al., 1992).Thus, freshwater fish species tend to contain higher proportions ofC18 PUFA and lower levels of C20 and C22 PUFA in their lipidscompared to marine fish species where the food chain is rich in thelatter fatty acids (Henderson and Tocher, 1987). Given that theflora and fauna of the tropics are incredibly diverse, it is not

surprising that there were marked differences in the FA profiles ofthe aquatic animals studied here with those of the literature.

The lipids of the aquatic animals, especially of snakehead,coming from the rice fields in Northeast Thailand were character-ized by relatively high levels of C22:6n-3 and C20:4n-6 concur-rently with substantial contents of C18:2n-6, C18:3n-3 andC20:5n-3. The levels of C22:6n-3 were comparable to those ofmarine fish species (Table 4), but such high levels of C20:4n-6 arenot commonly seen in either marine or freshwater ecosystems.Such elevated levels of C20:4n-6 have been reported in someAustralian and Malaysian marine fish species (Dunstan et al.,1988) and in wild Nile tilapia (Oreochromis niloticus) from Thailand(Karapanagiotidis et al., 2006). The high levels of C22:6n-3 couldhave originated directly from the feeding on food rich in thesenutrients. Flagellated algae are known to contain substantial levelsof C22:6n-3, while certain filamentous fungus, such as Mortierella

alliacea, is known as a rich source of C20:4n-6 (Aki et al., 2001). Thefatty acid profiles of micro-algae and zooplankton from tropicalfreshwater environments are poorly known and further research isrequired to give information on this area. We should also bear inmind that snakehead, in which the levels of C22:6n-3 and C20:4n-6 were found to be the highest, is a piscivore species so that thehigh concentrations of these FA may have occurred up the foodchain. Alternatively, these high levels of C22:6n-3 and C20:4n-6could be the result of chain elongations and desaturations of theirprecursors, viz. C18:3n-3 and C18:2n-6, respectively. It is knownthat freshwater fish species have greater in vivo abilities to convertC18 PUFA to their C20 and C22 analogues, by an alternatingsuccession of desaturation and elongation (reviewed by Turchiniet al., 2009). Perhaps these tropical freshwater animal species have

I.T. Karapanagiotidis et al. / Journal of Food Composition and Analysis 23 (2010) 1–8 7

greater capacities for these bioconversions than marine fish. In thisrespect, more information is needed on how or whether organismsin the tropical freshwater food chains can transform the shorterchain n-3 and n-6 PUFA present in phytoplankton into longerchained PUFA of higher nutritional value. However, studies so farhave shown that such bioconversions by fish cannot achieve thetissue levels of C20 and C22 PUFA found in fish fed diets containingthese PUFA (Bell and Dick, 2004; Karapanagiotidis et al., 2007).

The high levels of C22:6n-3 and C20:4n-6 is of particularimportance for human nutrition. These two FA are found in highconcentrations in membrane structural lipids, particularly exci-table membranes of the central nervous system, in the brain andthe retina (Hoffman et al., 2009). Delayed development of visualacuity has been shown in pre-term and term infants when fedformulas lacking these FA (Uauy et al., 2003). Moreover, a numberof studies have also shown a link between these FA andpsychomotor development and cognitive development (Uauy etal., 2003). There is also evidence that many mental disorders inhuman such as schizophrenia and Alzheimer’s disease areassociated with depressed levels of C22:6n-3 and C20:4n-6 inbrain cells (Florent-Bechard et al., 2009). For human nutrition,since the rate of C18:3n-3 conversion to C22:6n-3 may beinsufficient to meet demand during early development it isrecommended that formula feeds should be supplemented withC22:6n-3 and C20:4n-6 (Hoffman et al., 2009).

The studied species contained considerable levels of total n-3PUFA. Although these levels are comparatively low compared toother fish species of marine and of coldwater-freshwater origin(Table 4), the studied species can also serve as valuable sources ofthe health-related n-3 PUFA to human nutrition. This is of vitalimportance when considering that rural populations in rice-farming regions do not have access to seafood rich in n-3 PUFA(Meusch et al., 2003). Other food products that are commonlyavailable to these traditional communities are poor source of longchained PUFA of both n-3 and n-6 series (Table 4).

4. Conclusions

The freshwater aquatic animals from rice–fish farming systemsin Northeast Thailand are significant components of overall diets tothe local communities, especially to the resource-poor (Morales,2007), contributing not only quantitatively, but also qualitatively,to food security, as a source of essential nutrients. They are goodsources of important nutrients, such as calcium and vitamin D,needed for growth and development especially if eaten whole(Mogensen, 2001; Roos et al., 2003). They are also good sources ofthe essential fatty acids and particularly of 22:6n-3 and 20:4n-6.The latter two fatty acids are important for normal neurodevelop-ment and visual function in pre-term infant nutrition. Their ediblemuscle tissues also contained substantial levels of other fatty acidsof the n-3 series, such as 20:5n-3 and 18:3n-3. Although thestudied species represent low-fat diets, they can contribute to therequirement for essential fatty acids, particularly of n-3, that areabsent in other food sources commonly available to these people.Consumption of these species in rural Northeast Thailand has beenestimated to be about 58–111 g/capita/day (Morales, 2007), whichequals to 19–76 mg of C20:5n-3 + C22:6n-3 per capita per day(assuming that edible muscle portion is 50% of total weight).

Given the inadequacies of local diets and the prevalence ofchronic malnutrition, the role of aquatic resources in rurallivelihoods is vital. In the absence of seafood, freshwater aquaticanimals are not only the main animal protein source in alreadyprotein-poor diets, but they are also a valuable source of thehealth-related n-3 PUFA maintaining people’s health and well-being. The intensification of agriculture, through the excessive useof chemical fertilizers and pesticides, flood control and irrigation,

threatens the status of biodiversity in rice fields (Bambaradeniyaand Amarasinghe, 2003). In this respect, strategies for food securityin Northeast Thailand should pay special attention to sustainableaquatic resources management.

Acknowledgements

The authors wish to thank the farmers from Sisaket Province fortheir assistance with the sampling and the staff from the UdonThani Fisheries Development Center for their contribution to thisresearch.

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