Korean Traditional Fermented Fish Products: Jeotgal

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55 Contents lists available at ScienceDirect 56 57 Journal of Ethnic Foods 58 59 60 journal homepage: http://journalofethnicfoods.net 61 62 63 Review article 64 65 1 Q1 Korean traditional fermented fish products: jeotgal 66 2 67 3 a, * b c d d 68 Q16 Ok Kyung Koo , Soo Jung Lee , Kyung Rhan Chung , Dai Ja Jang , Hye Jung Yang , 4 * Dae Young Kwon d, 69 5 70 6 a Department of Food and Nutrition, Gyeongsang National University, Jinju, Republic of Korea 71 b 7 Institute of Agriculture and Life Science, Gyeongsang National University, Jinju, Republic of Korea 72 c 8 The Academy of Korean Studies, Songnam, Republic of Korea 73 d Food Safety Research Group, Korea Food Research Institute, Songnam, Republic of Korea 9 74 10 75 11 article info abstract 76 12 77 13 Article history: 醢 78 14 Jeotgal ( ) is a traditional Korean fermented food with thousands years of history with kimchi and other Available online xxx jang (fermented soybean products, 醬). The history was proved by research from historical literature and 79 15 antique architecture. Jeotgal was developed along with jang (豆醬), fish jang (魚醬), meat jang (肉醬)asa 80 16 Keywords: part of jang (醬) up to the Chosun Dynasty and it was always offered during the ancestral rites or cer- 81 fi 17 fermented sh emonies. According to antique documents written by women, jeotgal had been used as seasonings or 82 fi 18 sh products condiments that were popular especially for women rather than as food served for ancestral rites. In 83 jeot 19 Southeast Asia and other countries, jeotgal uses varieties of fish and seafoods to provide rich and varied jeotgal (젓갈) 84 fl 20 Korea traditional fermented fish avors, and thanks to the next generation sequencing technology, we can identify microorganisms that 85 21 are involved in the fermentation process. Major microorganisms in jeotgal are Bacillus, Brevibacterium, 86 22 Micrococcus, Pediococcus, Pseudomonas, Lactobacillus, Leuconostoc, and Halobacterium. Recently, much 87 research on various health function of jeotgal has been conducted, reflecting increasing interest in the 23 88 safety and the functionality of jeotgal. Many reports on functionalities of jeotgal such as supplying 24 89 25 essential amino acids, and having antioxidant and antitumorgenic have been published recently. Because of the diverse flavor, types, and their function, jeotgal is expected to continue to develop as an important 90 26 seasoning in the world sauce market. 91 27 © 2016, Korea Food Research Institute. Published by Elsevier B.V. This is an open access article under the 92 28 CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). 93 29 94 30 95 31 96 32 97 33 1. Introduction fermentation does not lead to any health issues, people would have 98 34 continued to consume fermented foods even if they had never 99 35 Much of the food technology development in food products has come to understand how fermentation changes food. In the Orient, 100 fi 36 been motivated by the desire to preserve food in good condition for fermented foods have been produced using beans, sh, and meat, 101 醬 37 future consumption [1]. Each country has developed unique ways and the general term for these products is jang ( ) [2,3]. Jang made 102 fi 豆醬 fi 38 of preserving food, especially meat and sh. The most prevalent from beans is referred to as dujang ( , soy jang), from sh as 103 魚醬 fi 肉醬 39 method of preservation is through reducing water activity by eojang ( , sh jang), and from meat as yukjang ( , meat jang) 104 40 adding salt or drying, which protects against microbial spoilage by [3]. Dujang, a representative type of jang in Korea, has been dis- 105 41 inhibiting the growth of harmful microorganisms. Fish, for cussed previously in this journal [4]. At present times, the variation 106 肉醬 42 example, was usually salted down immediately in order to prevent in yukjang ( ) such as this was limited, although jang-jorim, beef 107 43 spoilage. It is presumed that food would ferment during this salted in soy sauce, was widely enjoyed, [1,5]. The most preferred 108 fi 魚醬 44 preservation process by bene cial microorganisms. As type of salted and fermented food in Korea is eojang ( ), which is 109 fi fi 45 made with salted sh and is referred to as jeotgal. Fermented sh 110 46 products have developed into other unique forms across East Asia, 111 47 Southeast Asia, and Europe. 112 * Corresponding authors. Ok Kyung Koo, Department of Food and Nutrition, fi fi 48 Fermented sh products have been consumed as the sh itself, 113 Gyeongsang National University, Jinju, Republic of Korea. Dae Young Kwon, Korea fi fi 49 Food Research Institute, 62 Anyangpankyo-ro 1201-bunkil, Songnam, Kyongki-do, sh sauce, sh paste, and other types of food throughout the world. 114 fi 50 Q2 463-746, South Korea. some of the examples of sh sauces are jeotkal in Korea [6], shott- 115 51 E-mail addresses: [email protected] (O.K. Koo), [email protected] suru from Japan [7], nuoc-man from Vietnam [3], various fermented 116 (D.Y. Kwon). 52 117 53 http://dx.doi.org/10.1016/j.jef.2016.06.004 118 54 2352-6181/© 2016, Korea Food Research Institute. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/ 119 licenses/by-nc-nd/4.0/).

Please cite this article in press as: Koo OK, et al., Korean traditional fermented ﬁsh products: jeotgal, Journal of Ethnic Foods (2016), http:// dx.doi.org/10.1016/j.jef.2016.06.004 JEF69_proof ■ 23 June 2016 ■ 2/10

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1 fish products in India [8], hakarl in northern Europe [9], and Wor- 66 2 cestershire sauce in England, which is mostly manufactured from 67 3 anchovies; these are liquid type of sauces [10]. Fish pastes, which 68 4 are made with minced or blended fish or shellfish include padaek 69 5 from Laos, prahok from Cambodia, and shrimp paste from China 70 6 [10]. These types of food are consumed as proteinaceous staples or 71 7 condiments in Southeast Asia while northern Europeans consume 72 8 them as condiments [8]. Korean jeotgal refers to both liquid and Q4 73 9 paste types of fermented fish foods. 74 10 Jeotgal is a traditional fermented fish food in Korea that is pro- 75 11 duced from the whole meat (Fig. 1) and/or internal organs of fish 76 12 and shellfish (Fig. 2), salted and fermented for inhibition of 77 13 spoilage, for autolysis, and for decomposing the main ingredients 78 14 by microbial activities [11,12]. Unlike salted food to minimize the 79 15 decomposition of the meat by harmful microorganisms, jeotgal 80 16 produces a unique flavor during the protein decomposition of raw 81 17 materials by beneficial organisms. As jeotgal has thousands of years 82 18 of history, it has its own unique and many different characters 83 19 [2,13]. Not only does proteolysis proceed during fermentation, but 84 20 also carbohydrates, lipids, and organic acids are broken down to 85 21 enhance the flavor, so that jeotgal is one of the important subing- 86 22 redients or seasonings in kimchi and other Korean foods [14]. 87 23 Traditionally, fish products have been a great source of protein in 88 24 the Korean diet, but have varied in how they are consumed. For 89 25 example, hongeo (fermented skate) [15] (Fig. 3A) is prepared with 90 26 strong fermentation while gulbi (salted yellow corvina) [15] 91 27 (Fig. 3B) is preserved by salting and drying without additional 92 28 fermentation. In preparations such as myeongtae (dried pollock) 93 29 and hwangtae (dried, aged pollock), another fish product for protein 94 30 source, fish are frozen first and then dried to prevent spoilage 95 31 without adding salt [16]. 96 32 Jeotgal has great nutritional value with additional function to 97 33 our health including appetite, digestion, and beneficial microor- 98 34 ganisms. Many reports have focused on the production of Korean 99 35 fermented fish products [11,17]. However, there are a few papers on 100 36 the historical/cultural background and value added and beneficial 101 37 effects of Korean fermented fishery products. Moreover, jeotgal has 102 38 been underestimated as a food with high sodium content. There- 103 39 fore, we have evaluated this high-added value food, jeotgal, from 104 40 the history to the scientific data analysis in this article. We will 105 41 discuss the origin and history of jeotgal, characterize and classify 106 42 different types of jeotgal and provide the microbial community and 107 43 health functional information of jeotgal. 108 44 109 45 110 46 2. History of jeotgal 111 47 112 48 Hae (醢; Fig. 4) is the Chinese character that generally represents 113 49 jeotgal. Written references to this character are found in historical 114 50 Chinese literature, including the Sigyung (詩經; BCE 551e477) [18] 115 51 and Lyeki (禮記) [19], a book that details the courtesy observed Q5 116 52 during the Zhou (周) dynasty (BCE 1046e256), although written Q6 117 53 later, in the Han (漢) dynasty (BCE 202eCE 220). Although the ref- 118 54 erences mainly discuss yukjang (肉醬), salted or fermented meat 119 55 products, the use of term ranhae (卵䱺) suggests that eojang (魚醬) 120 56 might have existed as a type of jeotgal. Ja (鮓), the Chinese character 121 57 referring to jeotgal made with fish, first appeared in the Chem- 122 58 inyosul (齊民要術; CE 532), written by Ka (賈思勰) of the Sandong 123 59 peninsula (山東半島) in China. At that time, the Yodong peninsula 124 60 (遼東半島) was under Kokuryu (高句麗, BCE 37eCE 668) rule, and 125 61 there were many interactions among Kokuryu, Baekje (百濟, BCE 126 62 127 63 128 Fig. 1. Jeotgal prepared with whole fish by adding salt. (A) Saeu-jeot (small shrimp 64 jeot), (B) myeolchi-jeot (anchovy jeot), (C) whangseokeojeot (yellow corvina jeot), and 129 65 (D) ojingeojeot (squid jeot). (See Table 1.) 130

ﬁ O.K. Koo et al / Korean traditional fermented sh products: jeotgal 3 Q3

1 66 2 67 3 68 4 69 5 70 6 71 7 72 8 73 9 74 10 75 11 76 12 77 13 78 14 79 15 80 16 81 17 82 18 83 19 84 20 85 21 86 22 87 23 88 24 89 25 90 26 Fig. 2. Jeotgal fermented with internal parts of fish products. Myeongranjeot (jeot with roe from pollock), (B) changnanjeot (jeot from intestine of pollock), (C) kalchisokjeot (jeot from 91 27 intestine of cutlass), and (D) chogejeot (geot with clam). 92 28 93 29 94 18eCE 660), and Sandong peninsula. Therefore, it is presumed that kimchi prior to the Chosun period. In those periods, the meaning of 30 95 customs discussed in the Cheminyosul were related to the customs jeotgal was different from that now. Currently jeotgal generally 31 96 of Kokuryu or Baekje rather than those of Southern China. More- refers to fermented food products made with fish. Q7 32 97 over, the Cheminyosul introduced preserved fish food products that A great number of references to jeotgal can be found within 33 98 were salted or wrapped in lotus leaves and resembled fish jeotgal in literature from the Chosun dynasty. The Koryosa (History of Koryo 34 99 Korea [20]. Dynasty, 高麗史) [28] and the Koryosajeolyo (Brief History of Koryo 35 100 In Korea, in addition to hae (醢), hye (醯), which is another Dynasty, 高麗史節要) [29], history books written during the Chosun 36 101 Chinese character for jeotgal, is mentioned in other literary works. dynasty and covering the Koryo dynasty, used the expression “to 37 102 For example, this character can be found in the Samkuksaki (三國史 make a person into jeotgal” to describe cruel execution methods 38 103 記) [22] and on a wooden tablet excavated in Anapji (雁鴨池)[23], used on criminals (Fig. 5). A similar expression is also found in the 39 104 Kyungju in Korea, which described the dietary aspect of royal life in Mokeunjip (牧隱集) [30], written in 1404 by Lee (李穡)2. This 40 105 the Shilla (新羅) dynasty [23,24]. The Samkuksaki mentioned that expression, which drew a parallel between tearing kimchi into 41 106 jeotgal (醯) was served at the royal wedding for King Sinmun (神文 pieces and hacking people into pieces, was described in a previous 42 107 王, CE 681e692) [22]. It is presumed that the jeotgal (醯) introduced paper [31]. These references suggest that poki-kimchi (kimchi made 43 108 on the wooden tablet is the same eojang (魚鮓) as found in the from whole cabbage) and jeotgal have both existed for a long period 44 109 Cheminyosul in Sandong peninsula. The jeotgal (醯)1 from the of time. From this position, the claim that the history of kimchi has 45 110 wooden tablet, along with the one that appeared in the Samkuksaki, spanned less than 100 years, based on Joo’s [32] erroneous argu- 46 111 suggests that the history of jeotgal can be traced back hundreds of ment that gochu pepper came from Japan during the Imjin War (CE 47 112 years. It also suggests that the unique categories of fermented food 1592), cannot be substantiated. 48 113 products established after the Shilla dynasty are different from the Various sources, including the Chosunwangjosilrok, a book 49 114 traditional Chinese references [2]. Fermented food products made written during the Chosun dynasty, introduce jeotgal that was 50 115 with fish were referred to as hae (醢, 醯; jeotgal), meat as damhae made with a variety of seafood products, such as saeujeot (紫蝦醢, 51 116 (醓醢; fermented pork), tohae (兎醢; fermented rabbit), or nokhae shrimp jeot), taegu-aljeot (卵醢, cod roe jeot), dwaejikogijeot (醓醢, 52 117 (鹿醢, fermented venison), and bean as jang (醬) [25]. According to pork jeot), dalpaengijeot (蝸醢, snail jeot), kajamisikhae (食醢, flatfish 53 118 the The Annals of King Sejong and Geography (Sejongsilrokjiriji, 世 shikhae), jogijeot (黃魚醢, yellow corvina jeot), and songeo-aljeot (松 54 119 宗實錄地理志) [26] and The Annals of the Chosun Dynasty (Cho- 魚醢, trout roe jeot) [33,34]. Records of having upset stomachs after 55 120 sunwangjosilrok, 朝鮮王祖實錄) [27], jeotgal was made with not only eating jeotgal are also commonly found in the literature. Books that 56 121 fish but also pork, rabbit, or venison, and was also consumed with contain recipes for jeotgal were published beginning in the 17th 57 122 century, both by male and female authors. The Sallimkyongje (山林 58 123 經濟), a book written by a male author, Hong [35] (洪萬選), intro- 59 124 duced a recipe for saeujeot (紫蝦醢, shrimp jeot) and recommended 60 1 醯 125 There has been an issue with , the Chinese character for jeotgal written on adding it to kuk made with meat, fish, or tofu. In the Jungbo 61 the wooden tablet. Some have claimed that the character on the wooden tablet is 126 62 not the same word the 醢 or 醯 (jeotgal) that was used in the Hunmongjahoe (訓蒙 127 字會 63 ) [18] (Fig. 4). However, the character on the wooden tablet is the same word as 128 醯, but with a different way of writing 酉 or 皿. It is regrettable that same character 64 on the wooden tablet cannot be expressed in Microsoft Word (Microsoft Corpo- 2 “Who would resolve the chagrin of Hanpaeng (韓彭) after he was teared out like 129 65 ration, Redmond, WA, USA). kimchi and jeotgal?” / 韓彭葅醢冤誰雪 / 韓彭葅醢冤誰雪 130

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1 This recipe is similar to the current kanjang-gejang recipe, showing 66 2 that kanjang-gejang has been enjoyed among Koreans for quite 67 3 some time. 68 4 The Siuijonseo (是議全書) [41], another cookbook written by a 69 5 female author in the late 1890s, exclusively explained the types of 70 6 fermented fish products (魚醢) and their recipes. This was 71 7 different from previous books that discussed fermented meat 72 8 products (肉醢) as well. In the Siuijonseo, almost all types of fish 73 9 jeotgal were mentioned, including jeotgal consumed today, such as 74 10 jokijeot, myeolchijeot (anchovy jeot), saeujeot, jogaejeot (clam jeot), 75 11 ojingeojeot (squid jeot), cheongeojeot, guljeot (oyster jeot), and 76 12 aljeot (roe jeot). Jeotgal mentioned in cookbooks published in the 77 13 20th century showed great similarity to contemporary jeotgal. 78 14 References to fermented meat products (肉醢), which were 79 15 generally served during royal ancestral rituals and other rites, 80 16 cannot be found in literature published after the 17th century, 81 17 other than in the Cheminyosul [2]. Cookbooks written by female 82 18 writers mainly discussed fermented fish products. While the 83 19 Eumsikdimibang [39] briefly introduced chamsae-jeot (sparrow 84 20 jeot), which was made with poultry, both the Kyuhapchongseo and 85 21 the Siuijonseo were exclusively concerned with fermented prod- 86 22 ucts made with fish. 87 23 It is presumed that these female authors wrote the books based 88 24 on their own experience of making jeotgal. Thus, in daily life, 89 25 common people would have enjoyed fermented fish products more 90 26 than other fermented meat products. The term jeotgal currently 91 27 refers to fermented fish products only. Fermented fish products 92 28 were served as the main source of foods for common people, while 93 29 fermented meat products were used as a food served at royal 94 30 ancestral ritual or others. Therefore, this paper will focus on the 95 31 current view of jeotgal, which involves only fermented fish prod- 96 32 ucts, rather than the traditional definition of jeot (醢). 97 33 98 34 3. Modern classification of jeotgal 99 35 100 36 Seafood is highly perishable food due to the high moisture 101 37 content and highly nutritive in protein and fat for the growth of 102 38 103 Fig. 3. (A) Fermented hongeo (hongeo from Heuksando: 黑山島, Black Mountain Island) spoilage microorganisms [42]. Jeotgal was a very brilliant process to 39 with rice straw for a couple of days after fishing. (B) Gulbi (croaker from Yeongkwang: maximize the use of seafood in ancient to avoid deterioration. 104 40 Yeongkwang gulbi), which is prepared by drying after saline treatment [15]. Namely, jeotgal is processed by conversion of the deterioration, Q8 105 41 resulting in a unique flavor and a preserved food product [1,17]. 106 42 Jeotgal has been an important condiment in kimchi and not only as 107 增補山林經濟柳重臨 43 Sallimkyongje ( ) [36],Yu( ) discussed recipes condiment, but also as dipping sauce for broiled pig's feet (jokbal), 108 44 that used salt, rice wine lees, alcohol, soy sauce, pepper, green blood/noodle sausage (sundae). Jeotgal has also been added as 109 45 onions, glutinous rice, and malt in various jeotgal, such as cheon- seasoning to substitute salt or soy sauce in Korean style stews, 110 46 geojeot (herring jeot), saeujeot, daehapjeot (clam jeot), saengkuljeot chigae [1], and kuk and tang [43]. Saeujeot (shrimp jeot) is the most 111 47 (raw oyster jeot), and gejeot (crab jeot), or kanjang-gejang (crab commonly used salt substitutive seasoning [17]. More than 150 112 48 marinated in soy sauce) [12,36]. On special occasions, including types of jeotgal have been reported and they can be classified by the 113 49 royal court ceremonies, ancestral rites, and parties, fermented meat main ingredients, processing method and processing region. 114 fi 兔醢鹿 50 and sh products such as tokkijeot ( , rabbit jeot), saseumjeot ( 115 醢醓醢魚醢 51 , venison jeot), dwaejijeot ( , pork jeot), and mulgokijeot ( , 3.1. Classification by main ingredients 116 fi 52 sh jeot) were served [37,38]. These records demonstrate that a 117 53 wide range of ingredients was used in making jeotgal, while only Whole fish: Any fresh fish, crustaceans, and mollusks can be used 118 fi 54 salt and sh products are the main ingredients today. to make jeotgal and each jeotgal is named after the main fish in- 119 55 As opposed to the works of male writers, books written by fe- gredients. In most cases, whole fish, shellfish, or crustaceans are 120 56 male authors described recipes for jeotgal in Hangul. For example, used to produce jeotgal. However, a specific part of fish such as gills, 121 張 57 Jang [39] (Andong- ) discussed recipes for cheongeojeot (herring intestine, or roe can be used. Therefore, jeotgal is classified based on 122 58 jeot), gejeot, yeoneo-aljeot (salmon roe jeot), and chamsaejeot the type of main ingredients (Table 1). 123 閨壼是 59 (sparrow jeot) in her book Food-dimibang (Eumsikdimibang, Myeolchi-jeot (anchovy jeot): Produced from anchovy and 124 議方 60 ) using Hangul (Fig. 6). She also gave detailed information on saeujeot, which is made with shrimp, are the most popular jeot- 125 61 gejeot, which was later developed into kanjang-gejang. In the Kyu- gals in Korea. Depending on the harvesting season, both jeotgals 126 閨閤叢書李 62 hapchongso ( ), published by Lee [40] (Bingheogak )in are often called choonjeot (春醢) from anchovy harvested in spring 127 63 1809, recipes for gejeot were introduced. Gejeot was salted with not and chujeot (秋醢) in autumn [44]. Fresh anchovies, harvested 128 64 only sodium but also soy sauce, alcohol, and vinegar. It was also from the south coast of Korea, are washed, drained, and salted by 129 65 seasoned with green onions and Korea red peppers without seeds. layering with anchovy and salt, alternately. The salt concentration 130

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1 66 2 67 3 68 4 69 5 70 6 71 7 72 8 73 9 74 10 75 11 76 12 77 13 78 14 79 15 80 16 81 17 82 18 83 19 84 20 85 21 86 22 87 23 88 24 89 25 Fig. 4. Chinese characters (鮓 and 醢), which represent jeot or jeotgal in Hunmongjahoe (訓蒙字會) by Choi (崔世珍) [18]. Ja (鮓) and hae (醢) represent jeotgal (fermented fish 90 26 product) in Cheminyosul (齊民要術) and others literature (醢). 91 27 92 28 93 29 94 30 95 31 96 32 97 33 98 34 99 35 100 36 101 37 102 38 103 39 104 40 105 41 106 42 107 43 108 44 109 45 110 46 111 47 112 48 113 49 114 50 115 51 116 52 117 53 118 54 Fig. 5. Expression about cruel way to kill people by tearing the body as kimchi and jeotgal. tearing. Korosajeolyo (高麗史節要) (1173). Many commanders say that if you did not tell Jin 119 55 (金) dynasty (1115e1234) about what happened in 1170 (庚寅年), we would have been executed and our body would have been teared out like as jeot or kimchi and salted (諸將曰,庚 120 56 寅之事,微公告奏,吾屬,葅醢矣). 121 57 122 58 123 is ~20e30% w/w and qualified refined salt is used. The fermen- quality refined salt is added and stored for 4e5 months at 59 124 tation period is ~2e3 months depending on the salt concentration 13e20C [42]. 60 125 and temperature [45]. Fresh shrimp for saeujeot are harvested Other parts or intestines: Jeotgal that is made with gills (agami in 61 126 from Yellow Sea, the west and southwest coast of Korea. Since the Korean) is rich in calcium. About 15e20% of refined salt is added to 62 127 shell is hard for salt infusion into the meat, a higher concentration the washed gills and it is fermented for up to 3 months with the 63 128 of salt is necessary, by 35e40% in summer and ~30% in winter. addition of seasonings. Since salt infusion rate is slow in gills, it is 64 129 Fresh shrimp is washed with sea water or 3e4% salted water then important to incorporate with salt and other ingredients [46]. Other 65 130

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1 66 2 67 3 68 4 69 5 70 6 71 7 72 8 73 9 74 10 75 11 76 12 77 13 78 14 79 15 80 16 81 17 82 18 83 19 84 20 85 21 86 22 87 23 88 24 89 25 90 26 91 27 92 28 93 29 94 30 95 31 96 32 97 33 98 34 99 35 100 36 101 37 102 38 103 39 104 40 105 41 106 42 107 43 108 44 109 45 110 46 111 47 112 48 113 49 114 50 115 51 116 52 117 53 118 Fig. 6. Eumsikdimibang (閨壼是議方, one book of recipe for Korean food described in Hangul) describes the preparing method for chongeojeot (herring jeot) in detail. 54 119 55 120 56 121 57 parts of the fish or shellfish such as intestine and roe (al in Korean) included in Table 1. Skate contains high protein with low fat and glu- 122 58 are used to produce special jeotgal. In order to provide their unique tamic acid (14.7%) aspartic acid (9.59%) and it also contains 22.8% of 123 59 texture and flavor, it is important to remove the whole intestine or essential fatty acids such as linoleic acid, linolenic acid and arachidonic 124 60 roe without cut. acid [15]. It has a very strong pungent order and taste due to the 125 61 Hongeo: Averyspecialfish, skate has a completely different flavor ammonia in the skate. In order to control the osmotic pressure, skate 126 62 from other fermented fish products, and can be classified as hongeo- contains 100 times more urea than humans and the urea is conversed 127 63 jeot.However,unlikeotherjeotgal, hongeo is not named as hongeojeot to ammonium during fermentation. It is often said, “Do not discuss on 128 64 because it was recognized as nutritious main dish rather than Korean foods or tastes until you taste hongeo”. Because of the ammonia, 129 65 seasoning or condiment [15].Thisisthereasonforhongeo not being microorganisms cannot grow to be highly preservative. Skate is Q9 130

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1 Table 1 66 2 Classification of jeotgals based on the main ingredients. 67 3 Type of main ingredients Food products (main ingredients) 68 4 69 Whole fish & shellfish 5 Fish Order Clupeiformes: myeolchijeot (anchovy), baendaengijeot (herring), 70 6 jeoneojeot (gizzard shad), jeongeorijeot (sardine), junchijeot (Chinese 71 7 herring), euneojeot (Coilia nasus), yeobsakjeot (gizzard shad), duiporijeot 72 8 (herring) 73 Order Perciformes: kalchijeot (cutlass fish), chokijeot (croaker), 9 whangseokeojeot (yellow corvina), godeungeo jeot (mackerel), kanari jeot 74 10 (sand eel), mineo jeot (croacker), nungsungeo jeot (convict grouper), domi 75 11 jeot (sea bream), maegari jeot (horse mackerel), byungeo jeot (pomfret) 76 12 Others: bollackjeot (rockfish), kajamijeot (flatfish), kongchi jeot (saury), 77 taegu jeot (cod), baemjangeo jeot (eel), dongtae jeot (frozen pollock), 13 78 bangeo jeot (icefish) 14 Crustaceans Shrimps: saeujeot (small shrimp), gonjangiijeot (mysidacea), kaetgajae jeot 79 15 (squilla), daeha jeot (jumbo shrimp) 80 16 Crabs: tulge jeot (hairy crab), bangke jeot (3-spined shore crab), kotge jang 81 17 (blue crab), dolge jang (stone crab), chamge jeot (Chinese mitten crab) 82 Mollusks Class Cephalopoda: ojingeojeot (squid), koltukijeot (small squid), nakji jeot 18 (small octopus), hanchi jeot (cuttlefish) 83 19 Class Bivalvia: kuljeot (oyster), eorikul jeot (oyster with hot pepper), bajirak 84 20 jeot (clam), dongjuk jeot (surf clam), daehap jeot (clam), matjeot (razor 85 21 clam), moshijogae jeot (short-necked clam), baekhap jeot (large clam), 86 pijogae jeot (ark clam), honghap jeot (mussel) 22 87 Others: obunjaki jeot (supertexta), sora jeot (conch) 23 Internal parts of seafood 88 24 Gills (agami) Taegu-agami jeot (cod), mineo-agami jeot (croaker), myeongtae-agami jeot 89 25 (pollack), jogi-agami jeot (yellow corvina) 90 26 Intestine Chang-nan jeot (pollack), haesam-changja jeot (sea cucumber), 91 kodeungeo-changja jeot (mackerel), kalchi-sok jeot (cutlass fish), 27 chuneobam jeot (gizzard shad), jogi-sok jeot (yellow corvina), 92 28 chunboknae-jang jeot (abalone), baemjangeo-chang jeot (eel) 93 29 Roe (al) Myeong-ran jeot (pollack), gealjeot (crab), godeungeo-al jeot (mackerel), 94 30 taegu-al jeot (cod), saeu-al jeot (small shrimp), sungke-al jeot (sea urchin), 95 sungeo-al jeot (mullet), yuneo-al jeot (salmon) 31 96 32 97 33 98 fi 34 3.2. Classi cation by seasoning similar procedure was recorded in the methods of old literature 99 e 35 [39 41]. Changnanjeot is manufactured using intestine and eggs of 100 36 Jeotgal: Most traditional jeotgal was simply prepared by adding pollock, which provides unique chewy texture to the jeotgal.Itis 101 37 salt and fermenting and maturing for a certain period by based on usually consumed with addition of seasoning including red pepper, 102 齊民要術 e 38 documents in Cheminyosul ( ) [2,39 41] or other old liter- ginger, and sesame. The roe of pollock is also used for the pro- 103 > 39 ature for 1,000 years. duction of jeotgal, named myeongranjeot. Natural coloring agents 104 b 40 Seasoned jeotgal: However, as shown in Table 2, other jeotgals such as monad red, annatto, -carotene, and beet red are added in 105 41 were fermented with Korea red peppers [47], cooked grains, soy the roe with other additives, lactic acid, succinic acid, glycine, and 106 42 sauce (kanjang) [4], and/or malted rice, in addition of salt. Some spices such as hot pepper, garlic, ginger, and sesame, sugar [11]. 107 fl fi 43 others spices are also added to provide additional avor to jeotgal. Aekjeot: Fermented sh sauce, aekjeot (liquid jeot), can be made 108 44 This method is almost similar to the procedure of an old book, by most of seafood ingredients. The main principal of 109 閨閤叢書 45 Kyuhapchongseo ( ) [40]. Oyster is easy to ferment due to manufacturing process is very similar to jeotgal; however, 110 46 the high content of glycogen, so that only 10% of salt is added and fermentation period is much longer than jeotgal. For example, an- 111 e 47 fermented for ~1 week for low salted oyster product. Regular oyster chovy aekjeot is fermented for 6 7 months and the liquid formed 112 48 jeotgal (kuljeot) adds ~20% of salt with a 1-month fermentation during the fermentation is called sangjeot-kuk. 113 食醢 49 period. Eorikuljeot is famous for the addition of Korean red pepper Sikhae ( ): Sikhae was written in an old book, Cheminyosul [2] 114 朝鮮王朝實錄 50 and other spices such as garlic, ginger, relish, and scallion [48]. Most and many books of The Annals of the Chosun Dynasty ( ) 115 fi 51 mollusks including squids and octopuses are processed by [33,34] as a favorite fermented sh product, and is a cured fer- 116 fi 52 removing internal organs and bones and are fermented with mented sh with cooked grains. Cooked grain, malt, hot pepper, 117 53 Korean red pepper, garlic, ginger, syrup, and other seasonings. A and others are mixed with the salted seafood and fermented. There 118 54 are different varieties of sikhae by the type of grains or the com- 119 55 bination of the ingredients, depending on the region. For example, 120 Table 2 56 eight different combinations of cooked grains (rice, glutinous rice, 121 Classification and characteristics of jeotgals by manufacture process. fl 57 our, millet), salt, seasonings (Korean red pepper or malt), and 122 58 Type Main ingredients Spices radish (presence or absent) are known [49]. Any decomposed 123 fl 59 Jeotgal Fish, shellfish, intestine Salt byproducts from the subingredients enhance the avor of salted 124 fi fi 60 Seasoned jeotgal Fish, shell sh, intestine Salt, seasoning (hot seafood. As for fermented sh sauce, any seafood for jeotgal can be 125 pepper, garlic, ginger, 61 used for sikhae and the jeotgal itself can also be used [6]. Kajami- 126 green onions) fl fi 62 sikhae ( at sh sikhae) is the most popular sikhae, especially in 127 Aekjeot Fish, crustaceans, residual Salt fl 63 products North Korea before the Korean War (1950), which is made with at 128 fi e fi 64 Sikhae Fish, mollusks, roe Salt, cooked grains, sh and ~5 10% of re ned salt is added. After ~1 day of salting, 129 e 65 seasoning, malt, radish other subingredients are added with 20 50% w/w and cured for ~2 130

8 J Ethn Foods 2016; -:1e10

1 weeks. Because preservation period is limited by 1e2weeks,itis (shellfish) was dominated by Gammaproteobacteria (mostly Sali- 66 2 produced during autumn and winter [42]. nivibrio), while oyster contained genus Lactobacillus followed by 67 3 family Alphaproteobacteria (Rhizobiales), Gammaproteobacteria, 68 4 4. Microbial community of jeotgal and then Weissella [49]. 69 5 The microbial population in ojingeo jeot (squid) was also 70 6 Microorganisms naturally come from the main ingredients such investigated by pyrosequencing method and it was predominated 71 7 as seafood, spices, and vegetables depending on the type of jeotgal, by genera Leuconostoc (Leuconostoc citreum and Leuconostoc hol- 72 8 and also from the environments such as seawater, marine mud, and zapfelii), Bacillus, Staphylococcus, Psychrobacter, Paracoccus, Kocuria, 73 9 even from the handlers [50]. Because of the high sodium content in and Micobacterium. Along with the microbial community analysis, 74 10 jeotgal, growth of most harmful microorganisms is inhibited due to this group also tested the prevalence of osmotic stress-related 75 11 the increasing osmotic pressure and decrease in water activity for genes. While Leuconostoc did not possess genes homologous to 76 12 the preservation. However, the ripening of jeotgal is not only by the osmotic stress-related genes, all other genomes showed the 77 13 autolysis of the meat and offal of fish but also the microbial activity presence of the genes [55]. 78 14 during fermentation. The microorganisms that survive and are The microbial community of sikhae was also tested by number of 79 15 involved in fermentation are halophilic or halotolerant. As there are researchers. Sikhae showed totally different microbial community 80 16 hundred types of jeotgal depending on the ingredients and compared to jeotgal, potentially due to the subingredients and the 81 17 fermentation methods, microbial communities also differ by the manufacture process. In myeongtae sikhae (Alaska pollock), Lacto- 82 18 ingredients and duration of the fermentation. bacillus sakei was only 2% before the fermentation, but L. sakei was 83 19 Most commonly, Bacillus, Brevibacterium, Flavobacterium, dominated by 74% at 10C and 90% at 20C. L. sakei is psychro- 84 20 Micrococcus, Pediococcus, Pseudomonas, and Staphylococcus are trophic, salt tolerant, and bacteriocin producer, which could be 85 21 frequently isolated from various jeotgal products along with halo- critical for decrease of unpreferred bacterial species during 86 22 philic and halotolerant bacteria such as Halobacterium and Hal- fermentation [56]. Kajami-sikhae was also shown to contain L. sakei 87 23 omonas [51e53]. During fermentation, bacterial community as the most abundant species. Others such as Lactobacillus graminis, 88 24 succession from Proteobacteria to Firmicutes has been monitored Lactobacillus alimentarius, Lactobacillus fructivorans, and Weissella 89 25 and is considered to be a common indicator for jeotgal [50]. thailandensis were also observed. Overall, over 90% were domi- 90 26 The microbial community in myeolchijeot (anchovy) was nated by Leuconostocaceae and Lactobacillaceae families in kajami- 91 27 monitored during fermentation periods and in the early part of sikhae [57]. Sikhae is produced by cooked grains, hot peppers, and 92 28 fermentation, Pseudomonas, Acinetobacter, Flavobacterium, and other spices. White radish is also added to sikhae and interestingly, 93 29 Brevibacterium were common. In the intermediate period, Hal- the white radish in kajami sikhae reduced the level of Proteobac- 94 30 obacterium, Pediococcus, Sarcina, and Micrococcus in bacteria and teria from ~10% relative abundance to almost zero rate. When white 95 31 Saccharomyces and Torulopsis in yeast were isolated and especially radish was added to kajami sikhae, Lactobacillus presented 89e91% 96 32 Pediococcus and Saccharomyces were the most dominant microor- relative abundance and the rest was dominated by Weissella [58]. 97 33 ganisms. As the fermentation proceeds, the microbial population Jeotgal is rich in microorganisms that are yet to be cultured or 98 34 decreased, however Halobacterium, Cutirubrum, Micrococcus mor- identified. As jeotgal is produced by different marine animals from 99 35 rhuae, Sarcina litoralis, and Pediococcus cerevisiae were identified different regions and different fermentation conditions, jeotgal can 100 36 throughout the fermentation process of myeolchijeot [45].In contain varieties of microorganisms. Therefore, several novel mi- 101 37 another study, most of the isolates in myeolchijeot belonged to class croorganisms have been also isolated and identified. Jeotgalicoccus 102 38 Bacilli, including genera Bacillus, Rummeliibacillus, Sporosarcina, was the first identified genus and is the most closely related to 103 39 Virgibacillus as well as Halomonas, Kocuria, and Psychrobacter [53]. Salinicoccus [59]. Proteus cibarius sp. nov. [60], Weissella jogae- 104 40 Saeujeot (small shrimp jeot) contained large number of halo- jeotgali sp. nov. [61], Brevibacterium jeotgali sp. nov. [62], Halomonas 105 41 philic bacteria such as Halomonas, Salinicoccus, Salinimicrobium, cibimaris sp. nov. [63], Kocuria atrinae sp. nov. [64], Paenibacillus 106 42 Salinivibrio, and Staphylococcus, and Lactobacillus, Leuconostoc, tyraminigenes sp. nov. [65], Salinicoccus jeotgali sp. nov. [66], and a 107 43 Psychrobacter, and Weissella were also isolated [53]. Ojingeo-jeot number of other novel bacteria have been identified. 108 44 (squid jeot) is dominated by Bacillus, Staphylococcus, and Weissella, With the high prevalence of lactic acid bacteria in jeotgal, the 109 45 and Carnobacterium, Leuconostoc, and Pediococcus, and others were probiotic potential of the isolates had also been studied. Lactic acid 110 46 also isolated [54]. bacteria and yeasts isolated from commercial jeotgals including 111 47 Until recently, culture-dependent methods have been the pri- ojingeojeot (squid), koltugijeot (small squid), and myeolchijeot (an- 112 48 mary tools to investigate the microbial community, however chovy) showed resistance to artificial gastric and bile juice and 113 49 culture-independent methods were developed and are recognized antimicrobial activity to Listeria monocytogenes [67]. Pediococcus 114 50 as an important tool to show more diverse and complex microbial pentosaceus from saeujeot was able to survive at pH 3.0, and 0.3% 115 51 communities. Therefore, recent studies on the microbial commu- bile salts, and adhered to Caco-2 cells [68]. Lactobacillus plantarum 116 52 nities in jeotgals were also performed with molecular methods such NK181 also showed resistance to pH 2.5 and bile salt, adherence to 117 53 Q10 as pyrosequencing analysis with 16S rRNA genes. Roh et al [50] Caco-2 cells, and 1,1-diphenyl-2-picyryl hedrazyl (DPPH) radical- 118 54 investigated archaea and bacterial communities of saeujeot (small scavenging activity and cholesterol reduction activity [69]. Lacto- 119 55 shrimp), jokaejeot (shellfish), kapojingoe jeot (cuttlefish), kuljeot coccus lactis NK34 additionally showed the production of inter- 120 56 (oyster), myeongranjeot (pollock roe), changranjeot (pollock tripe), leukin-1a and inhibition of the formation of preneoplastic lesions 121 57 and kejeot (crab; see above in History). Depending on each jeotgal, [70]. 122 58 the communities were diverse, while mostly composed of halo- 123 59 philic and mesophilic groups. In the family Halobacteriaceae, 5. Functionality of jeotgal 124 60 halophilic archaea such as Halorumbrum and Halalkalicoccus were 125 61 dominant in most jeotgals, while uncultured mesophilic Cren- Enzymatic autolysis of tissue digestive enzymes in the organs 126 62 archaeota were identified in kapojiingoe jeot (cuttlefish). Lactic acid induces the breakdown of complex compounds (such as carbohy- 127 63 bacteria including Lactobacillus and Weissella were over 90% of all drates, fats, and protein) of the tissues to oligomers or monomers 128 64 bacterial sequences in saeujeot (shrimp), changranjeot (pollock such as peptides, free amino acids, glucose, and vitamins. Jeotgal is 129 65 tripe), myeongranjeot (pollock roe), and kejeot (crab). Jogaejeot rich in essential amino acids such as lysine and threonine and also 130

O.K. Koo et al / Korean traditional fermented ﬁsh products: jeotgal 9

1 provides umami flavor by natural glutamic acid, alanine, and decrease in body fat, and immune-boosting activities. Until now, a 66 2 glycine [46]. Jeotgal increases the appetite, protects liver and is a high concentration of salt has been added to jeotgal for preserva- 67 3 great source of vitamin B. In addition, jeotgal can be a good digestion. However, due to the increase in awareness of health and 68 4 tant because of its high protease content. Saeujeot (small shrimp) is change in appetite, demand for low sodium jeotgal is increasing. 69 5 consumed as a dipping sauce for meat products to ease the diges- With the addition of variety of herbs to substitute sodium and 70 6 tion [71]. prolong the storage time, we should be able to increase the quality 71 7 The health benefits of jeotgal increase as the fermentation pro- and functionality. Therefore, the efforts on research and develop- 72 8 ceeds with the conversion of phytochemicals and/or with the in- ment of jeotgal based on the consumers’ demand shows that jeotgal 73 9 crease in functional byproduct. During fermentation of saeujeot has a great potential to be recognized as a nutritious and palatable 74 10 (small shrimp), free amino acid content increased in twice after 72 food product globally. 75 11 days. Essential amino acids such as lysine, glutamic acid, methio- 76 12 nine, alanine, aspartic acid, and leucine showed 1.27e5.79-fold 77 Conflicts of interest 13 increase after 72 days of fermentation [72]. 78 14 Myeolchijeot (anchovy jeot) is one of the important subing- 79 All authors have no conflicts of interest to declare. Q11 15 redients for kimchi [14]. Fermented myeolchijeot can prevent so- 80 16 matic mutation and has anticancer activity while fresh anchovy 81 17 with salt causes mutations in Drosophila. Meyolchijeot fermented Uncited reference 82 18 for 6 months and 12 months shows 26.6% and 43.4% anti- 83 19 mutagenetic activity, respectively [73]. Lim et al [74] evaluated the [21], [75]. Q15 84 20 cell viability of liver hepatocellular carcinoma cell HepG2 among 85 21 86 commercial jeotgal and jeonubamjeot (shad gizzard) resulted in the References 22 strongest activity by 77.6% followed by kajami-sikhae (flat fish), 87 23 ojingeojeot (squid), and koltugijeot (small squid). As shown, sikhae [1] Kim SH, Kim MS, Lee MS, Park YS, Lee HJ, Kang S, Lee HS, Lee KE, Yang HJ, 88 24 showed stronger anticancer activity due to the highly bioactive Kim MJ, Lee YE and Kwon DY. Korean diet: characteristics and historical 89 e 25 grains and other subingredients such as garlic and hot pepper to background. J Ethn Foods 2016;3:26 31. 90 [2] Ka SH (賈思勰). Cheminyosul (齊民要術). China; 532. 26 increase the health function [76]. [3] Choi DK. 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Please cite this article in press as: Koo OK, et al., Korean traditional fermented ﬁsh products: jeotgal, Journal of Ethnic Foods (2016), http:// dx.doi.org/10.1016/j.jef.2016.06.004