Encyclopedia of Marine Biotechnology

Editor(s): Professor Se‐Kwon Kim

First published:11 August 2020

Print ISBN:9781119143772 Online ISBN:9781119143802 DOI:10.1002/9781119143802

© 2020 John Wiley & Sons Ltd.

Table of Contents

Volume V : Encyclopedia of Marine Biotechnology Front Matter (Pages: i-xlv)

Section IX : Pharmaceutical Development CHAPTER 120 Marine Algal‐derived Pharmaceuticals: Potential Anticancer Agents (Pages: 2691-2724) Sanith Cheriyamundath, V.L. Sirisha

CHAPTER 121 Marine Source‐derived Anti‐HIV Therapeutics (Pages: 2725-2753) Amit G. Mirani, Tanvi K. Shah, Vandana B. Patravale

CHAPTER 122 Marine Biopharmaceuticals – A Retrospective of Molecular Mechanisms (Pages: 2755-2772) Samiha Tabassum Ghori, Vishaalini Kamali Raja, Uthira Muralitharan, Aathira Maikkara, Ayyavu Mahesh

CHAPTER 123 Chitosan and Trimethyl Chitosan (TMC) as Drug Absorption Enhancers: Moving Forward toward Clinical Acceptance (Pages: 2773-2795) Berglind Eva Benediktsdóttir

Section X : Science CHAPTER 124 Application of Local Proteases to Produce Fish Protein Hydrolysate (FPH) in (Pages: 2797-2812) Yusro Nuri Fawzya, Ekowati Chasanah

CHAPTER 125 Allergic Risks Associated with Seafood (Pages: 2813-2843) Samanta S. Khora

CHAPTER 126 Applications of Biotechnology in Seafood Production and Processing (Pages: 2845-2865) C.S. Ranadheera, P.H.P. Prasanna, J.K. Vidanarachchi

CHAPTER 127 Dielectric Properties of Selected Seafood and their Products (Pages: 2867-2880) L.T. Nguyen, I. Ahmad, N.Y. Jayanath

CHAPTER 128 Health Risk Assessment for Radionuclide Contamination in Seafood (Pages: 2881-2894) P. Sivaperumal, P. Kumar, K. Kamala, Ajit. A. Ambekar, K. Ponnusamy, R. Rajaram, A.K. Pal

CHAPTER 129 Indonesian Traditional Fermented Fish Ikan Peda: Processing, Quality, and Utilization Improvements (Pages: 2895-2911) Giyatmi, Hari Eko Irianto

CHAPTER 130 Improvements in Seafood Products through Recent Technological Advancements in Seafood Processing (Pages: 2913-2938) Upani Pinnaduwa, Eresha Mendis, Se‐Kwon Kim

CHAPTER 131 Seafood in the Human Diet for Better Nutrition and Health (Pages: 2939-2959) Chathurika Jayasekara, Eresha Mendis, Se‐Kwon Kim

CHAPTER 132 Seafood By‐products: A New Way from Waste to High Added Value in Pharmaceuticals and Cosmetics (Pages: 2961-2986) Ngo Dang Nghia

CHAPTER 133 Seafood as Source of Protein‐based Functional Foods (Pages: 2987-2997) Rahmi Nurdiani, Asep Awaludin Prihanto, Muhamad Firdaus

CHAPTER 134 Stress in Fish and Application of Carotenoid for Aquafeed as an Antistress Supplement (Pages: 2999-3019) Toshiki Nakano

CHAPTER 135 Recovery of Bioactive Components from Seafood By‐products toward Zero‐waste Processing (Pages: 3021-3039) Trang Si Trung, Nguyen Van Hoa, Pham Thi Dan Phuong, Nguyen Cong Minh, Nguyen Thi Hong Mai, Hoang Ngoc Cuong, Phan Thanh Loc, Willem Frans Stevens

CHAPTER 136 Traditional and Novel Seafood Processing Techniques Targeting Human Health Promotion (Pages: 3041-3084) Harshani Nadeeshani, Niranjan Rajapakse, Se‐Kwon Kim

CHAPTER 137 The Potential of Developing Additives from Marine Bioresources for the Food Industry (Pages: 3085-3107) Shachini Karunarathne, Eresha Mendis, Se‐Kwon Kim

CHAPTER 138 Applications of Flow Cytometry in Marine Biotechnology (Pages: 3109-3118) Teresa Lopes da Silva, Alberto Reis

Section XI : Tools for Marine Biotechnology CHAPTER 139 Bioremediation of Marine Effluents and Environments (Pages: 3119-3137) J. Paniagua‐Michel

CHAPTER 140 Bioremediation: A Promising Xenobiotics Cleanup Technique (Pages: 3139-3172) Thandapani Gomathi, M. Saranya, E. Radha, K. Vijayalakshmi, P. Supriya Prasad, P.N. Sudha

CHAPTER 141 Future of Mariculture with the Advent of Modern Biotechnology Tools (Pages: 3173-3194) Dr. T. Charles John Bhaskar

CHAPTER 142 In Silico Techniques Used in Marine Biology Research: An Overview (Pages: 3195-3211) Jitendra Narayan, Rahul Agarwal

CHAPTER 143 Innovative Alternative Technology for Fucoxanthin Recovery (Pages: 3213-3227) Evi Amelia Siahaan, Byung Soo Chun

CHAPTER 144 Marine : Tools for Radionuclide Bioremediation (Pages: 3229-3244) P. Sivaperumal, K. Kamala, S. Manjunath Kamath, P. Kumar, R. Rajaram, W. Richard Thilagaraj

CHAPTER 145 Transgenic Fish Technology: Principle and Application (Pages: 3245-3282) Thomas T. Chen, Maria J. Chen

CHAPTER 146 Reproductive Processes of Marine Animals as Biomarker for Environmental Stress Impact (Pages: 3283-3298) Alessandra Gallo, Elisabetta Tosti

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129

Indonesian Traditional Fermented Fish Ikan Peda Processing, Quality, and Utilization Improvements Giyatmi1 and Hari Eko Irianto1,2

1 Food Technology Department, Sahid University, Jakarta Selatan, 12870, Indonesia 2 Research and Development Center for Marine and Fisheries Product Processing and Biotechnology, Jakarta Pusat, 10260, Indonesia

129.1 Introduction process occurred during transportation or shipment and generates changes chemically As an archipelagic country, Indonesia is not and microbiologically to , transform- only abundant with fisheries resources, but ing the product into fermented fish which is also rich in various types of fish‐processing then called ikan peda. The product can be kept methods, including traditional processing for a few weeks or a couple of months at most, practices. One of the traditional fish process- depending on the quality. ing methods is , and there are Ikan peda is a very popular product in Java many kinds of fermented fish products which Island, especially in West Java. Physically and can be found in many parts of Indonesia. The in flavor, this product is quite different from most popular fermented fish products in other fermented fish products and even from Indonesia are ikan peda (moist salted fish), other traditional fish products such as ikan terasi (fermented fish or ), kecap asin (dried salted fish), pindang (boiled salted ikan (), and ikan jambal roti (moist fish) or ikan asap (). For most salted split fish). Some other fermented fish Indonesians consuming , the flavor of ikan products are bekasang (fermented fish entrails) peda is able to raise their appetite. Due to the from North Sulawesi, bekasam (fermented high salt content, ikan peda is normally con- rice‐fish) from South Sumatera, cincalok (fer- sumed in limited portions. Consumers of this mented rice shrimp mixture) from West product come from almost all strata of society, Kalimantan and Riau, and wadi (fermented ranging from low to high income. ) from South Kalimantan. These Ikan peda manufactured through the fer- products have special consumers in Indonesia, mentation process is a way to preserve the fish since they provide unique characteristics catch. Ikan peda is produced by processors including specific flavor and texture. which can be found along the coast of Sumatera Van Veen (1953) described the history of and Java islands with uncomplicated technol- ikan peda, in which the product was originally ogy and using simple equipment. Basically, the salted fish exported from Thailand to method of ikan peda processing is a salting and Indonesia. That product arrived in process with two salting steps, in which each Indonesia in very large bamboo crates where it salting step is carried out for a certain period. could be held for months. The fermentation The first salting is normally performed for

Encyclopedia of Marine Biotechnology: Five Volume Set, First Edition. Edited by Se-Kwon Kim. © 2020 John Wiley & Sons Ltd. Published 2020 by John Wiley & Sons Ltd. 2896 129 Indonesian Traditional Fermented Fish Ikan Peda

­several days and known as the first fermenta- which it undergoes a maturing or ripening tion. The second salting takes several weeks to process which takes a number of weeks or develop flavor and texture, and this step is months. Sjachri and Nur (1977) said that ikan called the second fermentation (Irianto, 1990). peda in Central Java and East Java is made to This type of salting process makes ikan peda preserve the fish during the peak season to pre- different from ordinary salted fish, particularly vent spoilage and to avoid the low price obtain- in terms of flavor and texture, making it more able at that time in the market. Processors suitable to be classified as a fermented fish make ikan peda by soaking the fish in satu- product than salted fish. rated brine in concrete tanks for an indefinite period until the price in the marketplace rises. In general, the processing method of ikan 129.2 ­Processing of Ikan Peda peda is divided into two stages: the first and the second fermentation (Winarno et al., 1973; So far there is no a standard prescribed method Hanafiah, 1987; and Irianto, 1990). The first of ikan peda processing, but some methods fermentation is to develop the characteristic which are employed by traditional processors flavor and texture of ikan peda, while the sec- have been described by Winarno et al. (1973), ond fermentation is principally a maturation Sjachri and Nur (1977, 1979), Hedrawan phase (Irianto and Irianto, 1998). The basic (1981), Irianto (1990), Huda (2012), and Hakim method of ikan peda processing is outlined in (2016). In fact, processing methods might be Figure 129.1. Firstly, the fish are cleaned by different from one place to another or even washing with fresh water and then drained. from one processor to another. Subsequently the fish are soaked for three days Van Veen (1965) noted that in ikan peda in salt (about 25% of the total fish weight) in a making, the fish are salted, kept for 12–24 salting tank. This process is known as the first hours, washed, and then dried superficially. fermentation. After this, the fish are washed Sometimes more fresh salt is added and the with fresh water and drained. The drained fish mixture is carefully packed in large crates, in are then put in a wooden box, arranged in

FISH Salt addition; about 30% of total sh weight SECOND FERMENTATION FOR A WEEK CLEANING AND Water WASHING CLEANING Salt Salt addition about 25% DRAINING of total sh weight AERATION

FIRST FERMENTATION FOR 3 DAYS IKAN PEDA

WASHING Water

DRAINING

Figure 129.1 Process flow of ikan peda (Adapted from Irianto, 1990). 129.2 ­Processing of Ika Ped 2897

­layers between dry banana leaves. Salt is sprin- at higher salt concentration. The salt dissolves kled between layers until the total amount of in the extracted water and forms a highly con- salt is around 30% of the fish weight. The box is centrated solution at the surface of the fish then covered with banana leaves and the fish is (Irianto, 1990; Horner, 1997). Irianto (1994) allowed to ferment for one week or more, until found that salt content of fish increased during the specific aroma of ikan peda is obtained. the first fermentation, while moisture content, This process is called the second fermentation. water activity (aW) value, and pH decreased. The last step of the process is to remove the salt Those changes occurred rapidly during the from the fish and subsequently the fish are first two days of fermentation and significant ­aerated to get the desired moisture content. changes continued until the fifth day of fer- Ikan peda is described as a fatty, partly dried mentation. A longer fermentation period salty fish with reddish‐brown color, and as tended to exhibit insignificant changes. At the being moist and slightly pasty with a flabby end of the first fermentation, aW of fish texture and a specific flavor which is cheesy, achieved 0.764 which was suitable for halo- tasty, salty, and often mixed with a mild rancid philic growth. flavor (Putro, 1993). Texture developments in The salt amount used in the first fermenta- ikan peda is affected by fat content and the tion affects the success of the fermentation presence of proteolytic enzymes in which their process. Winarno et al. (1973) noted the use of activities contribute to the changes in fish, salt at around 25% of the total fish weight for resulting in the specific unique texture of ikan the first fermentation, while Hedrawan (1981) peda called masir (Paparang, 2013). reported the use of salt as 20–25% of fish weight. Sukarsa (1979) and Hanafiah (1987) used about 30% of the total fish weight of salt 129.2.1 First Fermentation in the first fermentation for their experiments. The first fermentation is a salting process as On the other hand, Menajang (1988) and Eva employed in the manufacture of dried salted and Untari (2014) used 10% salt in ikan peda fish. During salting, water from inside the fish made from mackerel and failed to produce sat- is drawn out into the strong salt solution out- isfactory ikan peda, because the fish became side the fish. As the water moves out, the salt rotten. moves in, penetrating deeply into the flesh of the fish (Tuara, 1997). Therefore, the main fea- 129.2.2 Second Fermentation ture of salting is basically the removal of some water from the fish flesh and its partial replace- The second fermentation in the processing of ment with salt. The salt penetrates the fish ikan peda is also known as the “maturation flesh because of the osmotic pressure differ- process” or “ripening process” (Hanafiah, ences in the fish and the salt surrounding the 1987; Menajang, 1988). Theoretically, the rip- fish and at the same time the water is pushed ening process can be described by three out to be released from the fish. The water hypotheses: (1) microbiological theory; (2) dilutes the coarse salt and forms pickled brine autolytic theory; and (3) enzyme theory. In which covers the fish at the end of the first fer- microbiology theory, the microbes produce the mentation. The loss of a large portion of water essential active enzymes and these penetrate results in the weight loss and shrinkage of the into the flesh and contribute to its ripening. fish and the salt which has passed in can coag- The autolytic theory explains that ripening is a ulate the protein. The salt concentration out- result of the activity of enzymes of the muscles side the fish is an important factor affecting the or other tissues, or of the gastrointestinal tract. rate of salt penetration, in which more rapid The last theory, the enzyme theory, describes osmolysis and removal of moisture take place the ripening of salted fish as taking place under 2898 129 Indonesian Traditional Fermented Fish Ikan Peda

the influence of certain enzymes, namely those value, and pH of ikan peda during the second contained in the muscle tissue and in the fermentation occurred over an eight‐week ­intestinal body organs of the fish, together ­fermentation period and further fermentation with those produced by microorganisms process would give relatively constant values (Voskresensky, 1965). A certain degree of ran- for those parameters. cidity is both necessary and desirable for suffi- cient ripening of the product. The rancidity process can be classified into two types, namely 129.3 Microbiology and the enzymatic process and non‐enzymatic Enzymes of Ikan Peda ­process. Enzymatic rancidity can occur in fish, but the levels of lipolytic enzymes in the Bacteria play an important role in the fermen- ­muscle are low in lean types of fish. The non‐­ tation process of ikan peda. The qualitative enzymatic rancidity is auto‐catalytic and is microbiological analysis of fish during salting most significant during the storage of fish revealed that the genus Micrococcus is predomi- product (Βjοrkevoll et al., 2008). nant and that its ratio increases gradually from Basically, the ripening process is the sum of 40% to approximately 90% of total number. biochemical processes that cause the changes Simultaneously an appreciable reduction is in chemical and physiochemical characteris- observed in the other genera which are named tics of the tissue typical of the product. These in the following order of importance: changes are induced by enzymes which break Flavobacterium, Achromobacter, Pseudomonas, down both protein and fats into simpler com- Bacillus, and Sarcina (Dussault, 1958). The salt- pounds. The rate of ripening of salted fish ing treatment reduces the water activity of fish depends upon type, quality and original chem- from about 0.98 to about 0.70–0.75. At this ical composition of the raw fish; the salt water activity range, the only possibility is the ­composition, salting method and condition growth of halophilic bacteria, xerophilic mold, employed; and the amount of salt in the fish and osmophilic yeast (Smith, 1989). Fortunately, tissue (Suwandi, 1988; Irianto, 2012; Βjørkevoll most pathogenic bacteria are not salt tolerant, et al., 2008). so they can be destroyed during salting (Weiser Farid et al. (2016) revealed from their study and Mountney, 1971). Andriyani (2005) using three different sizes of freshwater fish, obtained 28 halophilic bacteria isolated from namely shol (Channa striatus), taki (Channa salted fish, and identified them as the genera of punctatus), and tengra (Mystus tengra), that Pseudomonas, Chromohalobacter, Halobacter, ripening of the dry‐salting process had a posi- Deleya, Bacillus, Salinococcus, Marinococcus, tive significant role on the biochemical and and Kurthia. mineral composition of the fish and reduced The role of microorganisms in the fermenta- bacterial load as well as made them nutrition- tion process of fish is different from that in ally suitable for all. After the ripening period, ­fermented vegetable products. The high salt the values of moisture (%) and pH were content of these products allows only salt‐­ decreased whereas protein (%), fat (%), ash (%), tolerant microorganisms to survive (Rose, salt (%), TVB‐N, FFA (%) and mineral content 1982); for example, ikan peda has 9–35% salt (Ca, Mg, Fe, Cu, Zn, Mn) increased signifi- (Syachri and Nur, 1977). cantly in these three fish. The decrease in total Fermentation in ikan peda is carried out bacterial count may be due to the presence of mainly by halophilic bacteria (Winarno, 1973). high salt concentration, so the pathogenic Halophilic bacteria in ikan peda have various growth can probably be con- responses to the salt level as noted by Suwandi trolled. Irianto and Brooks (1994) reported that (1988), in which isolated halophilic bacteria changes in salt content, moisture content, aW show optimal growth in media containing 129.3 ­Microbiornggy an Engyyms of Ika Ped 2899

0–15% salt. Hanafiah (1987) reported that suspected of being responsible for the forma- Gram‐positive bacteria are predominant in the tion of specific flavor in ikan peda. Indriati processing of fermented fish ikan peda and et al. (2006) obtained four isolates of lactic acid some were identified as . bacteria from commercial ikan peda, in which Suwandi (1988) isolated halotolerant bacteria those isolates were demonstrated to have anti- from ikan peda purchased from the market bacterial activities against Escherichia coli, and revealed that bacteria growth in ikan peda Bacillus cereus, Pseudomonas aeruginosa, and was characterized as the Gram‐positive cocci, Staphylococcus aureus. In a previous study, which were non‐motile, aerobic or faculta- Indriati et al. (1999) isolated tively aerobic, catalase positive, non‐idole ­vitulinus and damnosus from ikan ­producers, and oxidase negative. They can uti- peda. lize citrate as the only carbon source, ferment Sarnianto et al. (1984) reported that the num- glucose, and show proteolytic activity, and ber of total plate count (TPC), Lactobacillus, some of them are able to reduce nitrate. These and Staphylococcus of ikan peda were 3 – 10 × bacteria can be classified as mesophiles and 105, 0.08 – 0.2 × 102, and 0 – 2 × 102 cfu g–1 require the pH of the medium to be around respectively. In addition, Syafii (1988) revealed 6–8. They show variation in salt tolerance and from commercial ikan peda that the number of they can be divided based on salt tolerance as TPC, halophilic bacteria, proteolytic bacteria, weak, moderate, and halotolerant bacteria. lipolytic bacteria, acid‐forming bacteria, and Idawati (1996) obtained seven isolates of yeast or mold were present at 4.8 – 4.48, ­lactic acid bacteria from ikan peda made in the 3.08 – 5.26, 4.11 – 5.50, 3.93 – 5.54, 3.99 – 4.93, laboratory. Identification showed that those and 1.00 – 3.00 log cfu g–1, respectively. isolates were two isolates heterofermentative The gut has a significant contribution in the Lactobacillus sp., one isolate homofermentative fermentation of ikan peda, since most micro- Lactobacillus sp., three isolates Leuconostocs biological and enzymatic activities take place sp., and one isolate Streptococci from entero- in the gut. Most of the lipolysis and proteolysis cocci group. Those bacteria demonstrated their activities in the processing of ikan peda occur antibacterial effects of being able to inhibit the in the gut, especially at the beginning of the growth of Pediococcus fluorescens, Alkaligenes fermentation process (Irianto and Giyatmi, sp., Staphylococcus aureus, Listeria monocy- 2002). Hasan (2015) reported that activities of togenes, Vibrio parahaemolyticus, Escherichia protease and lipase extracted from short‐bod- coli, and Salmonella typhii. Heterofermentative ied mackerel guts varied with pH value and and homofermentative Lactobacillus were salt concentration. Protease activity at pH 11 able to inhibit the growth of those bacteria. (1.610 μmol ml–1) and salt concentration 6% Heterofermentative Lactobacillus showed (0.869 μmol ml–1) showed the highest activity; higher inhibiting activity to the growth of P. and pH 10 (0.031 μmol ml–1) and salt concen- fluorescens, but homofermentative Lactobacillus tration 15% (0.073 μmol ml–1) was the lowest had more inhibiting effect on the growth of activity. Lipase activity at pH 4 (2.428 μmol –1 Alcaligenes. H2O2 is suspected as a main anti- ml ) and salt concentration 3% (4.131 μmol microbial compound produced by Lactobacillus ml–1) was the highest activity; and pH 11 (0.042 for inhibiting the growth of P. fluorescens and μmol ml–1) and salt concentration 15% (2.237 Alcaligenes. μmol ml–1) was the lowest activity. The pro- Savitri (2006) harvested six isolates of halo- tease and lipase activity decreased with the tolerant bacteria from ikan peda made of increase in salt concentration. This indication short‐bodied mackerel (Rastrelliger negletus). was also observed by Irianto (1990) in his study Those isolates were characterized as non‐­ that the enzyme activities in the guts of ikan pathogenic Staphylococcus sp. The bacteria are peda fell rapidly during the process, which 2900 129 Indonesian Traditional Fermented Fish Ikan Peda

may be due to increasing salt content in the in the flesh and in the gut, while Staphylococcus gut. The enzyme activity in the flesh was rela- spp seemed to be contaminant during tively more stable than in the gut, and was processing. probably maintained by the enzyme released by bacteria and enzymes moving from the gut. The proteolytic, lipolytic, and lactic acid bacte- 129.4 ­Chemical and Nutritional ria probably contribute significantly only at Properties of Ikan Peda the beginning of the fermentation, since their number tended to decrease, some disappearing The proximate composition of ikan peda completely after a period. The lipolytic bacteria according to Poernomo et al. (1984) is 50.35% seemed to predominate in both the flesh and moisture, 26.67% protein, 6.36% fat, 2.9% car- the gut after the sixth day of second fermenta- bohydrate, and 18.89% ash. Sjachri and Nur tion. Both lipolytic enzymes and proteolytic (1977) noted that chemical composition of enzymes were still active until the end of the ikan peda obtained from several places in second fermentation. It is suggested that the Indonesia is 41.16–61.68% protein, 3.45–8.56% lipolysis process occurs microbiologically and fat, 42.39–52.12% moisture, 14.02–18.41% ash, enzymatically, that the proteolysis is mainly and 9.13–34.80 % salt. While nutritional com- the result of leakage of gut enzymes. This fur- position of ikan peda as described by Soedarmo ther suggests that probably the lipolysis pro- and Sediaoetama (1984) is 46% moisture, 28% cess plays the main role in developing the protein, 4% protein, 156 calorie/100 g, 174 flavor of ikan peda. Therefore, leaving the gut mg/100 g calcium, 316 mg/100 g phosphor, 3.1 is desirable to produce ikan peda with a mg/100 g iron and 110 IU/100g vitamin A. stronger flavor. Syafii (1988) reported that the moisture and Yeni (2005) has successfully identified hista- salt contents of commercial peda were 44.02%– mine‐producing bacteria from ikan peda made 53.12% and 18.03%–21.95%, respectively. of short‐bodied mackerel; those are 19 types of Sarnianto et al. (1984) informed that the mois- bacteria which are 8 types of Gram‐positive rod ture and salt contents of ikan peda purchased bacteria (Bacillus spp., Brevibacterium mcbrell- from the market were 49.42%–56.78% and neri, Brevibacterium otitidis, Clostridium spp., 10.99%–14.41%, respectively. In addition, the Carnobacterium alterfunditum, Corynebacterium salt content of ikan peda is also informed by nitrilophilus, Corynebacterium spp., and Murdinah et al. (1983), Savitri (2006) and Microbacterium testaceum), 7 types of Gram‐ Poernomo et al. (1984), i.e. 5.16%, 11.4% and negative rod bacteria (Aeromonas spp., 13.72% respectively. The above data demon- Brevundimonas vesicularis, Enterobacter spp., strate that ikan peda found in the market have Routella terrigena, Serratia rubidae, Vibrio algi- a very diverse salt content which may induce noluticus, and Vibrio aestuarium), and 4 types of differences of microorganisms growing in ikan Gram‐positive cocci bacteria (Micrococcus diver- peda from one product to another as well as sus, Staphylococcus spp., Staphylococcus lentus, salty taste levels of the product. and Streptococcus spp.). There are more types of Hanafiah (1987) noted that relative amounts histamine‐producing bacteria in the flesh than of omega‐3 fatty acids C20:5 (eicosapentaenoic in the stomach contents, namely 15 and acid/EPA) and C22:6 (docosahexaenoic acid/ 11 species, respectively. Indriati et al. (2006) DHA) of ikan peda were 10.51 and 24.81% fatty reported that the predominant histamine‐­ acids respectively. The fatty acid profile of raw producing bacteria during the period of inten- fish seemed to be retained in the ikan peda sive histamine production in ikan peda were after the process, although some were Enterobacter spp and Staphylococcus spp. ­significantly changed in terms of percentage. Enterobacter spp originated from raw fish, both The profile of fresh fish compared to that after 129.5 ­Processingg, Qualigyg, kief Uiiain Improvement 2901 salting in the first fermentation, pronouncedly rial quality improvement, diversification, and reduced the polyunsaturated fatty acids evisceration, as well as introduction of suitable (PUFA), particularly the omega‐3 highly packaging materials. More utilization of ikan unsaturated fatty acids, namely C22:6 and peda can be performed by developing culinary C22:5. However, C20:5 fatty acid was more or new food products which will be able to ­stable during the first fermentation than other ­provide more variety of products to purchase omega‐3 fatty acids. The maturation process in and consume by consumers. the second fermentation induced reduction of two fatty acids of PUFA group, i.e. C20:4 and 129.5.1 Diversification of Raw Material C22:5. Ikan peda is commonly processed from marine fish, particularly mackerel from the 129.5 Processing, Quality, species of Rastrelliger brachisoma and and Utilization Improvements Rastrelliger negletus (Sjachri and Nur, 1979; Tedja and Nur, 1979). In general, ikan peda is Upgrading of the quality of ikan peda through better prepared from fatty fish. Fatty fish will improvements in the processing method produce ikan peda that is better than fish hav- should be carried out with regard to the ing low fat content. During the fermentation assumptions of the criteria of good quality process, fats undergo chemical changes that ikan peda as follows (Hendrawan, 1981): produce a unique flavor. Therefore, fatty fish will produce ikan peda with strong flavor as 1) Tasty taste and aroma are suspected due to the result of chemical reactions involving fat. the presence of methyl ketone compounds The surface of ikan peda made from fatty fish and volatile fatty acids. is brown, while ikan peda processed from 2) The taste is not too salty, but if the salt is low‐fat fish have tangibly less brown color used in small quantities may lead ikan (Irianto, 2012). peda being quickly spoiled. The presence Diversification of raw materials from of lactic acid will help to keep the product marine fish used for manufacturing ikan peda longer. has been performed by utilizing sardines 3) Besides salty taste, ikan peda also has a (Sardinella sp.), scads (Decapterus sp.), bigeye slightly sour taste, and the right mixture of scads (Caranx sp) (Rahayu et al., 1992), mul- sour taste and salty taste will result in deli- let (Aldricetta forsteri) (Irianto, 1990), and cious taste of ikan peda. indian scad (Decapterus russelii) (Paparang, 4) The texture of ikan peda is solid but not eas- 2013). Besides the size being similar to mack- ily broken and the product has a good erel, is also suitable as a raw material enough shelf life. in the processing of ikan peda. This is because Efforts which have been made to improve of mullet has a fairly high fat content, which the traditional processing method of ikan peda is 4.47% (Irianto, 1992), while the fat content are aimed at optimizing processing efficiency of short‐bodied mackerel was 2.68% and obtaining better quality products, espe- (Menajang, 1988). Freshwater fish which cially in terms of product sensory acceptability have been used as raw materials in the pro- by consumers. Processing efficiency improve- cessing of ikan peda are (Tilapia mos- ments are concentrated to modify the first and sambica), common (Cyprinus carpio), second fermentation steps of the method and kissing gourami (Pontius javanicus). which were usually applied by processors. However the quality of ikan peda produced is Product acceptability improvements of ikan not like ikan peda that is processed from peda can also be conducted through raw mate- marine fish (Sukarsa, 1979). 2902 129 Indonesian Traditional Fermented Fish Ikan Peda

129.5.2 Use of High-quality Raw flavor, and texture compared to those pro- Material cessed from uneviscerated ones. Syafii (1988) also showed that the evisceration treatment Striped mackerel and short‐bodied mackerel improves the quality of ikan peda. Hanafiah are raw materials mostly used to produce ikan (1987) also noted that ikan peda processed peda. Those fish are classified in the scromboid using eviscerated fish which have been treated fish families, related to scromboid poisoning with antioxidants had a better acceptability, due to the high amount of free histidine in the particularly in terms of flavor and texture. The fish flesh which usually occurs in fish that product is clean and more attractive. The fried have deteriorated or declined in the quality of product is described as slightly flaky but moist, freshness. Heruwati et al. (2004) reported that salty, and tasty, having a slightly rancid flavor, delaying processing of the fish kept in ice but without the strong smell of ikan peda. increased histamine content in fish. The hista- However, Hasan et al. (2013) obtained from mine contents of fresh fish, moderately fresh their study that the best ikan peda can be pro- fish, and unfresh fish were 2.4 mg, 4.8 mg, and cessed from uneviscerated fish. In addition, 6.1 mg% respectively. Ikan peda processed Hasan et al. (2014) introduced ikan peda pro- from those fish through the 3‐week maturation cessed using fillets of short‐bodied mackerel, period had histamine contents of 4.4 mg, 12.4 but organoleptically the product was worse mg, and 18.7 mg% correspondingly. Therefore, than ikan peda made from whole fish and to produce a good‐quality ikan peda that is safe ­gutted fish. for consumers there is no other way except to use fresh raw materials or high‐quality fish. 129.5.4 Use of Better Quality Salt

129.5.3 Evisceration of the Fish Salt which is generally used by processors for manufacturing ikan peda is “garam rakyat,” a The raw materials used in the processing of salt produced traditionally by evaporating ikan peda are traditionally uneviscerated. This ­seawater. Impurities are still found in that salt. fact brings the notion that the guts provide a Impurities in the salt affect the quality of ikan specific role in the formation of the unique fla- peda. Impurities in raw salt also known as vor of ikan peda. As previously mentioned, the “garam krosok” are CaSO4, MgSO4, MgCl2, and guts are a source of bacteria and proteolytic others (Rositawati et al., 2013). The use of salt enzymes which make an important contribu- containing impurities will inhibit the penetrat- tion in the process of fermentation, particu- ing process of salt into fish flesh. Mathias larly in the formation of this flavor (Irianto. (2015) investigated the effect of salt quality on 2012). Menajang (1988) noted that gut removal the quality of ikan peda. This study revealed can decrease total bacterial, halophilic bacte- that the better quality of salt used for the pro- rial, and microaerophilic bacterial counts in duction of ikan peda, the better the quality of ikan peda. Irianto (2012) revealed that the the product. The salt level used in this study presence of stomach contents has a real effect was 30% of fish weight. on the ability of the product to retain water, stimulates the formation of carbonyl com- 129.5.5 Optimization of the First pounds which give the specific odor and flavor Fermentation of ikan peda, and increases the pH and micro- bial population of ikan peda. However, Nur Efforts to optimize the first fermentation in and Sjachri (1979) informed that ikan peda order to improve the quality of ikan peda have prepared from eviscerated short‐bodied mack- been explored in various ways, namely by erel had a better sensory acceptability of color, ­optimizing salt amount and fermentation 129.5 ­Processingg, Qualigyg, kief Uiiain Improvement 2903 period, as well as carbohydrate usage. The characterized as follows: (a) a three‐day first amount of salt used in the fermentation of fermentation: moisture content 58.28% (w/w), ikan peda determines the quality of the prod- salt content 14.84% (w.b.), water activity 0.83, uct and affects the types of microbes that play and pH 6.60; and (b) a seven‐day first fermen- a role in fermentation. If the amount of salt tation: moisture content 53.77% (w/w), salt used is too high, it will result in too salty a content 18.66% (w.b.), water activity 0.76, and product. The salty taste will limit the quantity pH 6.46 (Irianto, 1990). The salt content of the of ikan peda to be consumed. sample fermented for three days in the first fer- Desniar et al. (2009) processed ikan peda by mentation was nearly the same as the result employing various salt amounts, namely 30, obtained by Hanafiah (1987) from Indian 40, and 50%, in which 90% of those salt levels mackerel fermented for seven days, i.e. 14.1% were used in the first fermentation and the (w.b.). The sample fermented for seven days in remaining was for the second fermentation. the first fermentation had a salt content in the Sensory evaluation suggested that the best range reported using short‐bodied mackerel ikan peda should be processed with 30% salt. fermented for seven days by Sjachri and Nur Paparang (2013) made ikan peda from indian (1977), i.e. 16.98–20.63% (w.b.). The differences scad with 10–20% salt, in which the more salt of fish performances between the one under- used in the first fermentation the more accept- going the first fermentation for three days and able taste of the product will be. The best ikan seven days probably selects for differences in peda was obtained from the first fermentation the bacterial growth. employing 20% salt. Increasing the length of the first fermenta- Determination of the first fermentation tion from three‐ to seven‐day fermentation duration required for ikan peda processing period had undesirable effects on the appear- using mullet as raw material was conducted by ance of ikan peda. The high salt and low mois- comparing the fermentation periods of three ture contents obtained from a seven‐day first days and seven days. Products fermented for fermentation brought about shrinkage of fish three days were organoleptically more accept- and this condition was actually unexpected. able than those fermented for seven days. This The longer first fermentation may have caused may be related to the release of oil during the more oil separation from the fish and this first fermentation. The end of the first fermen- reduced fat content resulted in ikan peda with tation process found a thin layer of oil on the a less‐intense brown colour (Irianto, 1990). top of the salt solution. The longer the first fer- Therefore, this result suggested that the first mentation process, the more oil is released fermentation should not be run for more than from the fish. Consequently, the product pro- three days. This first fermentation period has duced with seven days of fermentation has a been applied by several researchers, such as weaker brown color than the one fermented Winarno et al. (1973), Sjachri and Nur (1979), for three days. The high salt content and low and Sukarsa (1979). moisture content of ikan peda that has under- Eva and Haslina (2012) modified processing gone 7 days of fermentation resulted in the method of ikan peda by introducing the use of wrinkling of the fish. This makes the product rice washing water which has been added with less acceptable organoleptically (Irianto, 1990). 15–25% salt as the fermentation media of Therefore, the first fermentation is suggested short‐bodied mackerel. Rice washing water not to exceed three days (Irianto and Brooks, was used as the source of carbohydrate to facil- 1994). The first fermentation is actually to pre- itate the growth of lactic acid bacteria during pare the fish for the maturation process in the three‐day fermentation. The most preferred second fermentation. The performance of product was fermented using rice washing the fish after the first fermentation could be water with 25% salt addition, and the product 2904 129 Indonesian Traditional Fermented Fish Ikan Peda

resulting from this process had 21.03% salt remove. Sensory evaluation indicated that ikan content, 11.67% moisture content, and 21.99% peda fermented for three days in the first fer- acid content. mentation and without salt addition in second Tedja and Nur (1979) conducted a study on fermentation was the best product. In order to ikan peda made from short‐bodied mackerel implement this finding, the fish which has using various salt and glucose concentrations in been fermented for three days in the first fer- a five day first fermentation. Faster pH reduction mentation is just continued into the second occurred at lower concentration of salt and the fermentation without further salt addition fastest reduction was found at 10% salt, while the but the brine which has formed on the fish effect of glucose concentration on ikan peda was is drained. This recommended processing not revealed until the end of study. method can be used as the basic information in Employing visceral enzymes prior to salting the improvement of the process and of the in the first fermentation of ikan peda was car- ­finished product itself. With regard to the fer- ried out by Hasan et al. (2014). The fish was mentation period, Hasan et al. (2013) revealed smeared with visceral enzymes and then that maturation at 35°C for a 30‐day period underwent first fermentation with 20% salt for ­produced a better ikan peda compared to one a day. After removal of the remaining salt, the fermented at 30°C, in terms of sensory, micro- fish was kept for four weeks at the second fer- biological, and chemical parameters. mentation. Ikan peda made involving enzymes Based on the sensory evaluation of ikan peda are better than ones processed without enzyme processed using mullet, the second fermenta- treatment. tion was recommended not to be conducted for more than four weeks (Irianto and Brooks, 1994), since after this period the appearance 129.5.6 Optimization of the Second and taste of ikan peda got worse. Fermentation

Modifications have been made to optimize the 129.5.7 Use of Bacterial Starter Culture role of the second fermentation to obtain ­better quality ikan peda and faster process through Bacterial starter cultures are used to accelerate optimization of the salt addition level and the fermentation process of ikan peda, which ­fermentation period. normally takes a long time. By employing the Irianto (1990) investigated the effect of the starter cultures in several ways, as well as vari- salt addition in the second fermentation com- ous starter forms, the fermentation process is pared to the one without salt addition and the guaranteed to achieve ikan peda with the optimum second fermentation period. The use desired quality faster. of salt in the second fermentation produced a Eva and Untari (2014) used solution from higher salt content, lower moisture content, fermented chicory as the media for the fermen- and lower water activity in ikan peda. This fact tation process of ikan peda, where the fermen- suggests that some salt penetration actually tation took place for three days. The solution still occurs during the second fermentation. expected as the source of lactic acid bacteria However, the salt addition in the second fer- was prepared by placing chicory into rice mentation is actually unnecessary, since the washing water with 10–20% salt added, then product obtained without salt addition was crushed by hand and undergoing the fermen- organoleptically indistinguishable from the tation process for three days. Ikan peda manu- product with salt addition. The salt addition factured from the solution of fermented could even make the appearance of ikan peda chicory processed by using rice washing water less acceptable, because the remaining salt on with 15 and 20% salt addition showed better the surface of ikan peda was difficult to taste compared with a commercial ikan peda. 129.5 ­Processingg, Qualigyg, kief Uiiain Improvement 2905

A solution of fermented shrimp paste, also conducted by Kamil et al. (1975) and terasi, has been used as the source of lactic Irawadi (1979). Kamil et al. (1975) used starter acid bacteria to be employed in the processing made by mixing ikan peda flesh and mung- of ikan peda (Fajri et al., 2014). The solution bean flour. The amount of ikan peda flesh was made by dissolving fermented shrimp added was around 10% of the formula. Irawadi paste in 20% salt brine. Mackerel (Rastrelliger (1979) processed ikan peda by adding glucose sp.) were soaked in the solution for 3 hours, as carbohydrate source and Lactobacillus spp. followed by the first fermentation with obtained from sauerkraut as starter culture. 15–25% salt for 7 days, and a second fermen- Eva (2011) inoculated Lactobacillus plantarum tation with 15–25% salt for 21 days. FNCC 0364 culture isolated from fermented Organoleptically, ikan peda processed by shrimp by soaking the fish into 24 hours old introducing lactic acid bacteria from fermented culture for 15 minutes. After that the fish was shrimp paste was more acceptable, especially drained, washed, and underwent second fer- the one fermented using 25% salt. mentation for 8 weeks. The study exhibited Pediococcus acidilactici F‐11 was employed that L plantarum was able to inhibit the growth by Rinto (2010) as starter culture in the first of coliform and accelerated the growth of ­lactic fermentation of ikan peda with different salt acid bacteria shown by increasing its total concentrations, i.e. 20, 25, and 30%. The use count. of P. acidilactici F‐11 as a biocontrol of micro- flora during ikan peda fermentation was 129.5.8 Use of Antimycotic effectively employed at a low salt concentra- and Antioxidants tion of 20%. This is shown by the inhibition of the growth of coliform and histamine‐forming Growing mold and oxidation attack are the bacteria during the first fermentation process, most common problems encountered in ikan in which the coliform number decreased up peda during storage and marketing. Sjachri to 2 log cycles from 1.3 x 106 to 1.7 x 104CFU and Nur (1979) investigated the use of sorbic and histamine‐forming bacteria number acid as antimycotic and butylated hydroxyl reduced up to 3 log cycle from 1.2 x 106 to 3.8 anisole (BHA) as antioxidant in the second x 103 CFU. However, P. acidilactici F‐11 was fermentation and found that they pronounc- not effectively used to suppress the growth of edly improved the quality of ikan peda with coliform and histamine‐forming bacteria if regard to peroxide and total volatile base val- the salt concentration employed was more ues. Employing 0.1% sorbic acid and 0.02% than 25%. BHA can reduce the production of volatile The bacterial starter prepared from ikan bases, in which total volatile base contents of peda in an anaerobic environment was intro- ikan peda with and without adding those duced by Nur and Sjachri (1979) in the second additives were 54.20 mgN% and 61.55 mgN%, fermentation of ikan peda. The use of starter respectively, while peroxide values of ikan culture can make the fermentation process peda with and without using sorbic acid and more intensive and leads to the quality BHA were 1.6 meq kg–1 and 2.0 meq kg–1 cor- improvement of ikan peda, especially in the respondingly. Hanafiah (1987) observed that formation of reddish‐brown color that signifies erythrobat used as antioxidant and added as a good‐quality ikan peda. Starter cultures can much as 1% did not effectively penetrate or be made from the reddish‐colored meat of ikan become absorbed by the fish to prevent from peda by drying at 40°C and pounding into oxidation attack, indicated by the ikan peda powder. having higher non‐protein nitrogen (NPN), The process improvement of the second fer- total volatile bases (TVB), and free fatty mentation by introducing microorganisms was acids contents. 2906 129 Indonesian Traditional Fermented Fish Ikan Peda

129.5.9 Use of Packaging water content, pH, and microorganism popu- lation of ikan peda (Irianto, 2012). A condition which should be taken into con- sideration for ikan peda during storage, trans- portation, and display in the markets is that 129.5.10 Use of Proper Storage the fermentation process or maturation pro- Methods cess still occurs, inducing microbiological Proper storage methods for ikan peda can and chemical changes in the product. Ikan extend its shelf life and also ensure the safety peda is normally sold in traditional market of the product to be consumed, especially unwrapped, but the ones displayed in modern those processed from mackerel due to hista- supermarkets are packed in plastic bags. The mine formation. Indriati et al. (2005) com- use of packaging for ikan peda is to facilitate pared three treatments of ikan peda made consumers in bringing the products home from short‐bodied mackerel for storage study: conveniently and to protect the products from drying followed by storage at ambient temper- the unfavorable effects of the environment, ature; without ­drying directly stored at ambi- including providing certain favorable envi- ent temperature; and without drying directly ronmental conditions for the products being stored at chilled temperature (5–10°C). In packed, such as vacuum conditions. The use terms of histamine content, chilled tempera- of polyethylene bags, bamboo baskets lined ture is recommended for storage of ikan peda with banana leaves, and crocks of clay for due to the lowest histamine formation, while packing ikan peda did not show any signifi- the highest histamine content was found in cantly different effect on the product quality ikan peda being directly stored at ambient (Sjachri and Nur, 1979), thus any types of temperature. packaging material can actually be used for packing ikan peda. In order to control the 129.5.11 New Developed Products maturation process, vacuum packing is sug- from Ikan Peda gested for ikan peda (Hanafiah, 1987). Employing vacuum packing inhibits the pro- Mahendradatta et al. (2010) introduced a duction of NPN and TVB as well as retains newly developed product of seasoning pow- more water in ikan peda. Due to consumers der made from ikan peda. Ikan peda was pro- preferring not to consume ikan peda with cessed through a 6‐day first fermentation very strong flavor, the best ikan peda are sug- using 20% salt and clove and cinnamon were gested to use eviscerated raw material and to added. After fermentation, the fish was then conduct second ­fermentation in ­vacuum con- milled into paste, put into a container, closed dition, even though the process requires a tightly, and allowed to ferment for 14 days. longer ­fermentation period. After that onion and garlic were added to the The results of the study showed that anaero- paste and the mixture was then dried, milled, bic fermentation leads to higher production of and sieved into powder. The salt used for the amine compounds, resulting in products that fermentation process was 20% of the fish have higher water holding capacity and better weight of the material. Drying was carried out texture. The amines can hold water molecules. at 60°C for about 8 hours (Anas, 2012). The Anaerobic fermentation seems to accelerate seasoning powder can be stored in aluminum the formation of reddish brown color from foil wrap for up to 10 weeks at ambient tem- meat, inhibit oxidative rancidity, facilitate perature and still accepted organoleptically the degradation of proteins into carbonyl until 8 weeks, except for its odor. Meanwhile, ­compounds, and have a marked effect on the total microbe as well as histamine and 129.6 Cnldn Remark 2907

­moisture content increased ­during storage 129.6 ­Concluding Remarks (Mahendradatta et al., 2010). The above facts indicate that there is still room to improve the quality of ikan peda through 129.5.12 Culinary Products from optimization and modification of existing tra- Ikan Peda ditional processing practices, as well as appli- Strong salty taste limits the amount of ikan cation of new findings and knowledge related peda consumption as a part of the daily diet of directly or indirectly to ikan peda processing. Indonesians. In recent years, culinary or food Other things which should still be considered products that use ikan peda as the main ingre- for both consumer satisfaction and consumer dients have been widely developed, and there protection are to upgrade sanitation and are even products that are claimed as unique hygiene levels of processing practices and per- culinary products originating from a particu- sons involved in production activities, and to lar city, province, and ethnicity. Those ­culinary provide acceptable quality raw materials of products include pepes ikan peda, tumis ikan ikan peda. peda, tim ikan peda, and sambal ikan peda. Mostly, traditional fishery products in Pepes ikan peda is processed firstly by pouring Indonesia are produced in processing units ikan peda with all spices thoroughly, and then which have not implemented sanitary and arranging on a banana leaf lined with pump- hygiene practices yet, including ikan peda kin leaves, bay leaves, and basil leaves. Green ­production. Due to lack of information and onions are spread over spiced ikan peda and knowledge, processors neglect those practices. then tomato is added. The banana leaf is Therefore, processors have to be made aware folded and wrapped, and the wrapped ikan of the importance of sanitation and hygiene to peda is steamed until cooked for around two be implemented in processing activities of ikan hours and then grilled (Anonymous, 2015). peda. In order to guarantee the safety of the Tumis ikan peda is made by cooking without product, the processors of ikan peda have to extra salt addition because ikan peda already pay serious attention and to control the envi- has salty taste. Tumis ikan peda can be made ronments of processing units and equipments with extra chili to add spicy flavor and a more to assure that sanitary and hygiene principles delicious taste for those who like spicy foods have been applied properly. (Anonymous, 2014). Tim ikan peda is pre- Ikan peda should be processed using good‐ pared by steaming ikan peda with seasonings quality fish, especially ones processed using consisting of shallot, garlic, chili, tomato, mackerel as raw material. The supply of fresh, sugar, salt, bay leaf, lemongrass, and lemon for quality mackerel is a must to avoid excessive 20 minutes (Permatasari, 2017). Sambal ikan histamine in ikan peda. Sarnianto et al. (1984) peda is made by steaming ikan peda until reported that the histamine content of ikan cooked and then shredded. Big green chili, peda is the highest among Indonesian fer- green curly chili, green chili pepper, tomatoes, mented fish products. The histamine content and shallot are steamed together and then of commercial ikan peda noted is approxi- pounded. Cooking oil is heated. The pounded mately 107.32–133.43 mg%, which is over the cooked ingredients are poured into hot oil limit of 50 mg% regulated in Indonesia. This until aroma appears, and then shredded ikan fact indicates that utilization of fresh fish, as peda and sugar are added. That mixture is well as sanitary and hygienic practices during stirred and heated until cooked (Anonymous, processing, is necessary to produce ikan peda 2017). that is good quality and safe to be consumed. 2908 129 Indonesian Traditional Fermented Fish Ikan Peda

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CONTRIBUTORSHIP STATEMENT

The undersigned below:

No. Name Institution 1. Giyatmi Sahid University, Jakarta, Indonesia

2. Hari Eko Irianto Research and Development Center for Marine and Fisheries Product Processing and Biotechnology, Ministry of Marine Affairs and Fisheries, Indonesia

Hereby declare that all authors have made important contributions for published paper:

Title : Indonesian Traditional Fermented Fish Ikan Peda - Processing, Quality, and Utilization Improvements Authors : Giyatmi (main-author) Hari Eko Irianto (main-author)

Book : Encyclopedia of Marine Biotechnology: Five Volume Set, First Edition. Edited by Se-Kwon Kim  Online ISBN: 9781119143802, Print ISBN: 9781119143772 https://doi.org/10.1002/9781119143802.ch129

Giyatmi Hari Eko Irianto