Skip to main content
  • Original article
  • Open access
  • Published:

Improving the safety of pindang, a traditional fish product from Indonesia: case study from Palabuhanratu, Sukabumi District, West Java Province, Indonesia

Abstract

Pindang is a popular traditional fish product in Indonesia that has been produced for decades. Scombroid fish such as tuna, mackerel, and scad, which have a naturally high level of histidine, are commonly used to make pindang. Hence, improper handling and processing can lead to the accumulation of histamine, potentially causing health issues. Due to uncertainty or limited availability of fresh fish, many pindang producers use frozen fish as an alternative raw material. Reports implicate pindang as a major causative agent of HFP outbreaks in Indonesia. However, detailed investigation on how histamine is formed during pindang processing needs to be updated based on current processing conditions. This study investigated the existing practices of pindang production in Palabuhanratu, Sukabumi District, West Java Province, Indonesia; evaluated potential critical control points (CCPs) of histamine production; and identified strategies to improve the safety of pindang. Fresh Skipjack tuna (Katsuwonus pelamis) and frozen Eastern Little tuna (Euthynnus sp.) were used as raw materials for pindang processing. Results showed that pindang made from fresh fish generally had lower histamine levels compared to those made from frozen fish. Improper handling, especially abusive temperatures and time delays during fish thawing, was identified as the main causes of histamine formation during pindang processing. Therefore, to reduce the risk of histamine formation, a temperature-controlled circulated thawing system could be used. This finding can help pindang producers improve the safety of their products and ensure compliance with national and international food safety standards.

Introduction

Indonesia is a major global fish producer, processing 6.85 million tonnes in 2019 of which 53% is traditionally processed, followed by frozen (20%) and surimi (14%) [1, 2]. Traditional processing uses simple methods passed between generations in home or micro- and medium-scale industries, and produces the following products: dried fish, dried-salted fish, salted-boiled fish, smoked fish, and fermented fish [3]. From 2014 to 2019, the production volume of processed fish increased 21%, including traditionally processed products [4]. Salting/drying is the most popular method, representing 72% of all traditionally processed fish in 2019, followed by salted-boiling (16%) and smoking (11%) methods [1].

Pindang or salted-boiled fish, a popular traditionally processed fish product, is typically made from Scombroid fish such as tuna, mackerel, and scad, which known for their high level of histidine in the muscle tissue. With the increasing scarcity of fresh fish, frozen fish is now commonly used for pindang production. An additional step of thawing may lead to the increased risk of histamine formation, if not perform properly. Reports implicate pindang as a major causative agent of HFP outbreaks in Indonesia [5,6,7,8,9]. However, detailed investigation on how histamine is formed during pindang processing needs to be updated based on current processing conditions.

The history of salted-boiled fish (pindang)

Salted-boiled fish, locally named pindang, has been produced in Indonesia for more than 50 years, preserving fish with salt and heat [10]. Brined and salted pindang are common processing methods [11], classified as standard methods by the Indonesian National Standard (Standar Nasional Indonesia-SNI) (SNI 2717.3:2009, SNI 2717:2017) [12, 13]. Brined pindang involves soaking fish in brine and then boiling for 30–60 min (Fig. 1); while salted pindang involves adding salt to the fish surface before boiling in water for 1–4 h, followed by low heat for one additional hour (Fig. 2). Similarly, prepared fish products are found in other Southeast Asian countries, such as sinaing na tulingan in the Philippines and pla thu nung in Thailand [14, 15].

Fig. 1
figure 1

Standard brined pindang processing method according to Indonesian National Standard (SNI 2717.3:2009, SNI 2717:2017): a fish preparation; b fish soaking in boiled brine; and c final cooked brined pindang

Fig. 2
figure 2

Standard salted pindang processing method according to Indonesian National Standard (SNI 2717.3:2009, SNI 2717:2017): a fish preparation; b adding salt to the fish surface; c fish boiling; and d final cooked salted pindang

Since the 1980s, pindang has been a preferred substitution for salted-dried fish [11]. The combination of high salt concentration and heat treatment produces a firm textured product, with a desirable flavour, lower salt content, and longer shelf-life compared to fresh fish [11, 15]. In addition, only 0.7–3.9% salt remains in the final product, compared to 12–20% for salted-dried fish [16,17,18]. Unlike dried fish, pindang processing is simpler and does not depend on variable weather conditions for drying [11].

Indonesian pindang processors are distributed across the country (Fig. 3), with total numbers of more than 10,000 in 2019; of these, approximately 5000 were located in West Java [19, 20]. The remaining processors are located in various regions of Java, such as Central Java, East Java, Banten, Jakarta, and Yogyakarta. Fewer processors are found in West Nusa Tenggara, Sulawesi, Bali, and Sumatera [21]. The largest processing centres are in Palabuhanratu—Sukabumi District (West Java Province) and Juwana (Central Java Province) [3].

Fig. 3
figure 3

Geographic distribution of pindang processors in Indonesia (2019). Most of the processors were located in Java Island, including West Java, Central Java, East Java, Banten, Jakarta, and Yogyakarta provinces. Fewer processors were found in West Nusa Tenggara, Sulawesi, Bali, and Sumatera

Regional variations in pindang preparation and flavour result from several factors, such as the choice of raw material, salt concentration, boiling time, and packaging material. These variations are driven by distinct practices and taste preferences in societies throughout the country. As a result, these different approaches yield unique sensory qualities in the end product, affecting its organoleptic appearance and shelf-life [15]. Pindang is also considered a ready-to-eat product, thus enabling subsequent culinary processing and personalised presentations that display distinctive characteristic of each region.

The significance of the economic and societal contributions of pindang, together with the increasing product demand from cities distant to processing centres, led the Indonesian government to elevate pindang processing to an industrial level through Ministerial Regulation PER.27/MEN/2012, regarding general guidelines for marine and fisheries industrialisation.

In the 1980s, family and neighbourhood-based pindang industries in Palabuhanratu (Sukabumi District, West Java Province) were established, utilising basic and traditional processing facilities and techniques passed between generations. Since a decade ago, fish processors were forced to change the raw material from fresh to frozen tuna, due to limited availability of fresh tuna from local catchments. Frozen tuna constitutes 15–20% of total raw material used for the production of pindang [22].

Apart from tuna, pindang can be made from a wide range of raw materials, including freshwater fish species such as milkfish, barb, tilapia, and carp, as well as marine fish species such as scad, mackerel, milkfish, pomfret, herring, and sardines [23]. Amongst these fish species, Scombroid fish including tuna, mackerel, and scad require specific attention during handling and processing, as they are more susceptible to histamine contamination due to naturally high levels of histidine [24,25,26,27,28,29,30,31,32]. Mediated by histidine decarboxylase (hdc) enzyme, free histidine in fish is metabolised by histamine-producing bacteria (HPB) to histamine (Fig. 4) [33, 34], either by hdc produced endogenously in fish muscle and/or exogenously by bacteria (e.g. Enterobacteriaceae) on fish [33, 35,36,37,38]. The formation and accumulation of histamine may lead to histamine fish poisoning (HFP), a foodborne intoxication due to consumption of fish or other foods containing toxic levels of histamine [35, 39,40,41].

Fig. 4
figure 4

Histamine biosynthesis through the histidine decarboxylation pathway. The conversion of histidine into histamine is mediated by histidine decarboxylase (hdc) enzyme, which is produced by histamine-producing bacteria (HPB)

Strategies to reduce or prevent histamine formation, which are applicable in pindang processing facilities, should also be identified. Therefore, this study observes current processing practices for pindang in Palabuhanratu and describes critical control points (CCPs) in processing that can potentially increase safety of pindang.

Materials and methods

Field observation and fish sample collection

Fish samples were collected from traditional fish processors in Palabuhanratu, Sukabumi District, West Java Province, Indonesia. Five pindang processors were selected and observed during processing. Fish temperature during processing was recorded using a four-channel thermocouple data logger (DTM-319 TECPEL, Taiwan). Three replicates of raw and cooked fish were collected for microbiological and histamine analysis.

Microbiological analysis

The viable counts of fish samples were analysed following method by Rachmawati et al. [42]. Five grams of fish flesh was homogenised in 45 ml of phosphate buffer saline (PBS) (pH 7.4). The homogenate was then serially diluted in PBS and spread-plated on tryptone soya broth (Oxoid, CM0129, UK) supplemented with 1.5% agar and 2% NaCl. Incubation was performed aerobically at 30 °C for 24 h. Total viable counts were expressed as log CFU/g.

Histamine analysis

Histamine extraction from fish sample

Histamine was extracted following the methods of Sirochi et al. [43], with some modification. Fish flesh was blended and then 5 g extracted with 15 ml 15% trichloroacetic acid (TCA) (Sigma, USA). The homogenate was centrifuged at 2500 × g for 10 min, and approximately 10 ml of the supernatant transferred to a new tube. After that, 100 µl of 10 µg/ml histamine.2HCl (α, α, β, β-D4, 98%) (Novachem, AU) was added to the supernatant, as internal control for histamine. Sample pH was adjusted by adding 200 µl of 28% NH4OH (Sigma, USA).

Sample clean-up was performed using a SPE STRATA X cartridge 33 µm polymeric reverse-phase (30 mg/3 ml) (Phenomenex, AU). Prior to sample loading, the cartridge was conditioned twice with 2 ml methanol followed by 2 ml Milli-Q water. Two ml of sample was loaded into the cartridge and then rinsed with 2 ml of MeOH/H2O (5/95 v/v). The cartridge was dried under vacuum to remove excess water, and the analyte was eluted twice with 2 ml methanol/acetic acid (99/1 v/v), and then dried with nitrogen gas. Analyte was re-dissolved in 2 ml Milli-Q water prior to chromatographic analysis.

Chromatographic analysis

Chromatographic analysis was performed following a method of Rachmawati et al. [42]. The mobile phase consisted of two solvents: 0.1% (v/v) formic acid in water (solvent A) and acetonitrile (solvent B). The UPLC programme was 100% A to 60% A: 40% B at 3.0 min, which was held for 0.5 min. This was followed by immediate re-equilibration to starting conditions for 3 min. The flow rate was 0.20 ml/min. Sample injection volume was 10 µL. Approximate retention time for histamine was 2.9 min.

Fishbone analysis and CCP determination for histamine formation during pindang processing

Fishbone analysis is a valuable cause-and-effect diagram used to methodically examine issues and possible problematic factors in a food production system [44,45,46,47]. We employed this approach to investigate the causes of histamine formation in each step of pindang processing and identify the factors that contributed to the problem.

To determine the critical control points (CCPs) in pindang processing, we evaluated whether any measures could be implemented during processing to prevent, reduce, or eliminate the histamine formation risk to acceptable levels [48, 49]. We also utilised a decision tree and literature search to identify the CCPs. Control and preventive measures were identified based on the current processing conditions of pindang in Sukabumi District, West Java, Indonesia.

Results

Field observations

We studied two different raw materials used in the production of pindang. Two processors utilised Skipjack tuna (Katsuwonus pelamis) that were caught locally, while three other processors used frozen Eastern Little tuna (Euthynnus sp.) purchased from suppliers. Fresh skipjack, designated pindang type 1, were caught in local waters using a seine net on “payang” vessels that leave fishing ports between 3 and 6 am and return between 4 and 8 pm [50,51,52]. Frozen Little tuna were designated as pindang type 2.

Figure 5 depicts processing flowcharts for both pindang types. The average weight of individual Skipjack tuna was 3–4 kg, while the Eastern Little tuna weighed 300–400 g. The main difference between the two processing types was that pindang type 2 was thawed. In addition, fish for pindang type 1 were wrapped with paper after cooking, while fish used in type 2 were wrapped with paper prior to cooking.

Fig. 5
figure 5

Processing variations of pindang in Palabuhanratu: a pindang type 1 using fresh skipjack and b pindang type 2 using frozen little tuna as raw material. The final products were distributed within 1–2 days

For pindang type 1, the raw Skipjack was maintained at 5–7 °C before processing, washed, arranged, and salted within 30 min, and then cooked immediately. Before cooking, the fish temperature was 17 °C. In contrast, for pindang type 2, the temperature of frozen tuna was approximately − 5 °C. The fish were thawed in 60–90 min, in open air, without water replacement. During thawing, the fish temperature increased from − 5 to 13–20 °C.

To prevent direct contact between the fish and container, wooden wicker was layered between fish and water added to the bottom of containers. The fish were then arranged in layers, and salt was added between and on top of each layer, with 50–60 g of salt applied per kg fish (i.e. 5–6%). The topmost layer of fish was covered with thick plastic or paper. Fish were cooked by steaming for approximately 3–4 h. The cooked fish was cooled at room temperature (25–28 °C) and distributed within 1–2 d.

Microbiological count and histamine content

For both types of pindang, the total viable count (TVC) of raw fish was 3.0–4.5 log CFU/g. For type 2, raw samples were thawed fish. TVC of cooked fish was ≤ 2 log CFU/g, except for processor 2 where TVC ranged from 4.1 to 5.1 log CFU/g (Table 1). Histamine levels of pindang type 1 were 10–100 times lower than type 2. For the latter, increasing levels of histamine were observed from raw to cooked fish for processors 3 and 4. For processor 5, the histamine was lower in cooked compared to raw fish.

Table 1 Average total viable counts and histamine concentration for raw and cooked fish

Causes of histamine formation and identification of CCPs during the processing of pindang

Raw and cooked pindang from processing type 1 had low levels of histamine (< 50 mg/kg), whereas processing type 2 generally had higher levels of histamine. Some raw fish from these processors had histamine levels of more than 100 mg/kg. Generally, histamine levels increased after cooking, except for fish from processor 5. Based on these observations, processing of pindang type 2 was selected for fishbone analysis to determine causes of histamine formation during processing (Fig. 6).

Fig. 6
figure 6

Identified critical control points in pindang type 2 processing, as sources of bacterial contamination and histamine accumulation. The stages include receiving of raw materials, fish preparation, cooking, and post-process handling

The histamine levels in the final product depend on the initial levels in the raw materials and the activity of histamine-producing bacteria (HPB) during processing. Four main sources of HPB and histamine during pindang processing were identified: raw materials, preparation, cooking, and post-process handling (Fig. 6). The preparation steps included thawing, washing, wrapping with paper, arranging in a cooking container, and salting. Inadequate cooling at each step was identified as the main factor that could promote the growth of HPB.

To identify critical control points (CCPs) in pindang type 2 processing, a decision tree recommended by FAO/WHO [33] was used. Four questions were asked and six CCPs identified: raw materials, thawing, washing, salting, cooking, and post-process handling (Table 2). Control and preventive measures for each CCP are presented in Table 3.

Table 2 Decision tree questions to identify CCPs of pindang processing
Table 3 CCPs and control measures to prevent histamine formation in pindang type 2

Discussion

The pindang processing steps used in Palabuhanratu classify the final product as salted pindang (SNI 2717.3:2009). All raw fish, whether fresh and frozen, were tested in this study and had a TVC lower than 5.0 × 105 CFU/g, which meets the requirement set by the Indonesian Standardisation Body for fresh fish (SNI 2729–2013, SNI 2717.1: 2009). Although TVC is not a quantitative indicator of the hygienic and quality for frozen fish, it is still useful as a qualitative measure [53]. The cooked pindang samples from four out of five processors had very low TVC values (< 2 log CFU/ml), with some samples showing no bacterial growth. These results suggest that post-cooking contamination was absent in most of the pindang processing investigated. However, higher TVC values were observed from the cooked pindang of processor 2, which could be due to unhygienic handling when wrapping fish with paper before storage.

The accumulation of histamine in fish depends on both the presence of free histidine and activity of histidine decarboxylase-producing bacteria (HPB) that convert histidine to histamine using the hdc enzyme [33, 54, 55]. Therefore, fish with high levels of free histidine in their muscle are more likely to accumulate histamine than other types of fish. For instance, Skipjack tuna has been found to have histidine levels of 1200–1340 mg/100 g, while Little tuna has histidine levels of 1090 mg/100 g [56, 57]. It is recommended to immediately cool these fish after harvest, particularly for fish caught in tropical countries with warm temperature and high humidity, to prevent bacterial growth and histamine formation [23, 58]. When fish have been exposed to temperatures greater than 83 °F (28.3 °C), the US FDA recommends immediate chilling on ice, refrigerated seawater, ice slurry, or brine (no more than 6 h after fish death) at 40 °F (4.4 °C), to prevent rapid formation of the hdc enzyme and subsequent histamine production [58].

In our study, when fresh Skipjack tuna was used as raw material for pindang type 1, the histamine concentrations of raw and cooked fish were very low, and no sample exceeded 100 mg/kg of histamine. Since the thawing step is not required, the fish could be processed directly, thereby avoiding time delay and abusive temperatures. Similarly, another study conducted on pindang from Skipjack tuna in Palabuhanratu also reported low levels (ranging from 2.03 to 26.89 mg/kg) of histamine in both the raw and cooked products [59].

However, the use of frozen Eastern Little tuna as the raw material for pindang type 2 resulted in some samples of both raw and cooked fish having histamine levels exceeding 100 mg/kg. The frozen fish was purchased from a local supplier, and there was no information available on how the fish was handled prior to purchase. It is possible that the fish came from different fishing vessels, which could have contributed to variations in fish quality, including histamine levels. Thawing the frozen fish during pindang processing could be the most critical step in histamine formation, as this process was carried out under uncontrolled temperatures. The frozen fish was initially thawed in open air, and then, the thawing continued using water in a bucket without recirculation.

To ensure the safety and quality of the fish during thawing, it is recommended to thaw in still or moving air, while maintaining the temperature at or below 18 °C [60]. If thawing in water, it is important to use clean, circulated water with the temperature controlled at or below 20 °C [60]. Unfortunately, meeting these requirements can be challenging for the pindang processors located in rural areas with limited access to cooling facilities [61] and clean water supplies. Thawing fish in uncontrolled conditions also creates a risk for bacterial cross contamination between the fish and the environment. This step, which only took 60–90 min, provides favourable conditions for bacterial growth and might allow HPB to produce high levels of histamine. For example, based on the growth and histamine prediction model of M. morganii in the Food Spoilage and Safety Predictor (FSSP) software (www.fssp.dtu.dk), an initial amount of HPB at 3.5 × 103 CFU/g could multiply by 4.3 × 103 CFU/ml after 90 min of fish thawing at 30 °C.

Although 6% salt (60 g/kg of fish) was added shortly before cooking, it may not be sufficient to prevent the growth of halotolerant histamine-producing bacteria (HPB) during the preparation phase. Studies have suggested that Vibrio, Staphylococcus and Pseudomonas, which are halotolerant HPB, may contribute to histamine formation in fish products. These bacterial genera can grow and produce histamine at salt concentration of up to 10–15% NaCl in histidine broth or 12% NaCl in sardine [62,63,64,65]. To prevent histamine formation in salted fish products, a combination of salt and refrigeration is more effective [33, 66]. Refrigerated brined anchovies (14% salt w/v) showed very low histamine levels (< 0.5 mg/kg), while at room temperature, histamine levels were > 500 mg/kg, inversely related to the salt concentration [67]. This approach might be suitable for cooked pindang. High salt concentration in the final product could prevent the growth of bacteria that might come from post-processing contamination. Storage at a refrigerated temperature could improve the product’s shelf-life. However, it should be noted that pindang processors in rural areas may face challenges in implementing these measures due to limited access to refrigeration facilities and clean water supplies.

HACCP is an effective method to improve food product safety and quality by improving the food production process [48, 49]. This study focused on the likelihood of histamine formation during pindang processing; therefore, the presence of HPB and histamine at different stages of processing were identified as critical control points (CCPs). The previous studies have identified three CCPs in Indonesian pindang processing, i.e. materials receiving, cooking, and post-processing handling [68, 69]. The identification of these CCPs was not only based on the presence of HPB and histamine but also other hazards such as pathogenic bacteria, formaldehyde, heavy metals, and foreign materials. In our study, three additional CCPs were found for processing pindang type 2, i.e. thawing, washing, and salting. The use of fresh fish is recommended as the first preventive measure, as the levels of histamine in raw fish will determine the levels in the final products. Since histamine is heat stable, preformed histamine cannot be eliminated by heating in subsequent processing steps [21, 58]. Additionally, it is crucial to maintain appropriate fish temperature during processing to control the growth and activity of HPB.

Defining CCPs during pindang processing is crucial for improving the practices of processors. To prevent histamine formation and accumulation in the final product, processors must implement the suggested control and preventive measures of CCPs, even if their facilities do not yet have a fully established HACCP system. However, before applying HACCP procedures, it is essential to have several prerequisite programmes in place, such as Good Manufacturing Practice for foods, Good Hygienic Practices (GHP), Codex Codes of Practice, and other food safety requirements determined by competent authorities. In Indonesia, hygiene and sanitation practices of pindang processing are regulated by SNI 2717.2017, which covers not only tuna-based pindang but also pindang made from other non-Scombroid fish. However, this regulation does not explicitly mention HPB and histamine as hazards in the pindang processing. Moreover, it aims to control hazards based on general processing steps such as receiving raw materials, gutting, washing, salting, cooking, cooling, packaging, and storing. Since the use of frozen fish is not common amongst non-Scombroid pindang, the thawing step is not included as a critical step in this regulation.

Conclusion

The study conducted in Palabuhanratu, Sukabumi District, West Java Province, Indonesia, examined two types of pindang processing. The study found that the levels of histamine in pindang were influenced by the quality of raw materials and processing practices. To ensure the safety of pindang produced by traditional fish processors in Indonesia, it is recommended that fresh fish be used as raw material. However, if frozen fish is used, care must be taken during the preparation step, including maintaining low fish temperature during thawing and avoiding time delays. The identified CCPs and their respective control and preventive measures can serve as a valuable guideline for processors to improve their processing practices.

Availability of data and materials

All data and materials have been presented in the paper.

References

  1. Perhitungan volume produksi olahan hasil perikanan skala mikro-kecil tahun 2019 [Production volume of micro-small scale fishery processed products 2019] [Internet]. Directorate General for Product Competitiveness of Marine and Fisheries Product, Indonesian Ministry of Marine Affairs and Fisheries. 2019 [cited 2023 May 23]. Available from: https://kkp.go.id/djpdspkp/artikel/26307-sebaran-upi-skala-mikro-kecil-tahun-2019.

  2. Directorate General of Marine and Fisheries Product Competitiveness. Laporan Kinerja Tahun 2022 Direktorat Jenderal Penguatan Daya Saing Produk Kelautan dan Perikanan [Performance Report 2022 Directorate General of Marine and Fisheries Product Competitiveness]. Jakarta: Ministry of Marine Affairs and Fisheries; 2023

  3. Heruwati ES. Pengolahan ikan secara tradisional: prospek dan peluang pengembangan [Traditional fish processing: prospects and development opportunities]. J Litbang Pertanian. 2002;21(3):92–9.

    Google Scholar 

  4. Center of Data Statistic and Information. Kelautan dan Perikanan dalam Angka tahun 2020 [Marine and Fisheries in Figures year 2020]. Jakarta: Ministry of Marine Affairs and Fisheries; 2021.

  5. Ainun Y. 34 Kepala desa keracunan makanan saat diklat [34 head of villages had food poisoning during training] Malang: Kompas Cyber Media; 2015 [Available from: http://regional.kompas.com/read/2015/04/23/10475371/34.Kepala.Desa.Keracunan.Makanan.Saat.Diklat.

  6. Anonymous. Keracunan pindang, 166 orang masuk RS dan 19 opname [Pindang poisoning, 166 people seek medical treatment and 19 people hospitalized]: Gudeg Net; 2004 [Available from: http://gudeg.net/id/news/2004/02/2236/Keracunan-Pindang-166-Orang-Masuk-RS-dan-19-Opname.html#.VCOj9vmSx2B.

  7. Anonymous. Puluhan karyawan Nikia keracunan pindang [Dozens of Nikia’s workers had pindang poisoning]: Berita Bali; 2008 [Available from: http://www.beritabali.com/index.php/page/berita/gyr/detail/2008/03/16/Puluhan-Karyawan-Nikia-Keracunan-Pindang/200803160010.

  8. Anonymous. Puluhan santri keracunan ikan pindang [Dozens of students had pindang poisoning]: Pos Kota News; 2014 [Available from: http://poskotanews.com/2014/10/21/puluhan-santri-keracunan-ikan-pindang/.

  9. Anonymous. Ratusan buruh PT RPG keracunan [Hundreds of workers at PT RPG had food poisoning] 2014 [Available from: http://www.jabar.polri.go.id/?p=16189.

  10. Fawzya YN, Dewi FR, Wibowo S. Kesiapan usaha pemindangan dalam program industrialisasi perikanan [Readiness of salted-boiled fish business in the fish industrialization program]. In: Irianto HE, Heruwati ES, Poernomo A, Wibowo S, editors. Analisis kebijakan pengembangan industri pengolahan hasil perikanan dan kelautan 2012 [Policy analisis for marine and fisheries industrial development 2012]. Jakarta: Research and Development Centre for Marine and Fisheries Product Processing and Biotechnology; 2012. p. 23-42.

  11. Putro S. Boiled-salted fish (pindang) as a possible substitute for dried-salted fish: problems and prospects. In: James D, editor. The production and storage of dried fish; Serdang, Malaysia: FAO; 1983.

  12. Indonesian National Standardization Agency. Ikan pindang [Salted-boiled fish]. Standar Nasional Indonesia. Jakarta: Badan Standardisasi Nasional; 2017.

  13. Indonesian National Standardization Agency. Ikan pindang - Bagian 3: Penanganan dan pengolahan [Salted-boiled fish - Part 3: Handling and processing]. Standar Nasional Indonesia. Jakarta: Badan Standardisasi Nasional. 2009.

  14. Marine Fisheries Research Development. Maximizing utilization of pelagic fish resources. Singapore: SEAFDEC. 2006.

  15. Wibowo S. Industri pemindangan ikan [Salted-boiled fish industry]. Jakarta: Penebar Swadaya. 1996.

  16. Nitibaskara R, Dollar AM. Quality changes during storage of boiled fish product prepared from pacific herring by an improved method. Bull Japan Soc Sci Fish. 1967;33(11):1028–34.

    Article  Google Scholar 

  17. Ibrahim R. Production and storage of salted-boiled fish (pindang) using Atlantic Mackerel (Scomber scombrus): Loughborough University; 1986.

  18. Indonesian National Standardization Agency. Ikan asin kering [Dried-salted fish]. Standar Nasional Indonesia. Jakarta: Badan Standardisasi Nasional. 2016.

  19. Anonymous. Pindang, sang primadona [Pindang, the favourite food]. Warta Pasar Ikan. 2012. pp. 6–7.

  20. Sebaran UPI Skala Mikro Kecil tahun 2019 [Distribution of Micro and Small-Scale Fish Processing Units in 2019] [Internet]. Directorate General for Product Competitiveness of Marine and Fisheries Product, Indonesian Ministry of Marine Affairs and Fisheries. 2020 [cited 2023/May/23]. Available from: https://kkp.go.id/djpdspkp/artikel/26307-sebaran-upi-skala-mikro-kecil-tahun-2019.

  21. Visciano P, Schirone M, Tofalo R, Suzzi G. Histamine poisoning and control measures in fish and fishery products. Front Microbiol. 2014;5:500.

    Article  Google Scholar 

  22. Anonymous. Ketika pindang terbentur tembok bahan baku [Raw Material Constraints Challenge Traditional Fish of Pindang]. Warta Pasar Ikan. 2012 pp. 8–9.

  23. Putro S, Saleh M. Post harvest handling - Effect of delay icing of Skipjack tuna. In: Pan BS, James D, editors. Histamine in marine products : production by bacteria, measurement and prediction of formation. FAO Fisheries Technical Paper: Food and Agriculture Organization of the United Nations. 1985

  24. Rachmawati N, Triwibowo R. Histamine fish poisoning (HFP) in Indonesia: current status and challenges. E3S Web Conf. 2022 pp. 344

  25. Emborg J, Dalgaard P, Kjølby A, Sørensen ND, Larsen IK. Results of biogenic amine concentrations and microflora in seafood causing histamine fish poisoning (HFP). 2008

  26. Awazu K, Takatori S, Kakimoto S, Nomura C, Masayama A, Yamaguchi M, et al. Detection of Histamine in fish and fishery products in Osaka prefecture (Fiscal 2015 Report). Food Hyg Saf Sci. 2017;58(1):43–8.

    Article  Google Scholar 

  27. Tsai YH, Kung HF, Lee TM, Chen HC, Chou SS, Wei CI, et al. Determination of histamine in canned mackerel implicated in a food borne poisoning. Food Control. 2005;16(7):579–85.

    Article  Google Scholar 

  28. Hwang CC, Tseng PH, Lee YC, Kung HF, Huang CY, Chen HC, et al. Determination of histamine in Japanese Spanish Mackerel (Scomberomorus niphonius) meat implicated in a foodborne poisoning. J Food Prot. 2019;82(10):1643–9.

    Article  Google Scholar 

  29. Chen H-C, Kung H-F, Chen W-C, Lin W-F, Hwang D-F, Lee Y-C, et al. Determination of histamine and histamine-forming bacteria in tuna dumpling implicated in a food-borne poisoning. Food Chem. 2008;106(2):612–8.

    Article  Google Scholar 

  30. Demoncheaux JP, Michel R, Mazenot C, Duflos G, Iacini C, Delaval F, et al. A large outbreak of scombroid fish poisoning associated with eating yellowfin tuna (Thunnus albacares) at a military mass catering in Dakar. Senegal Epidemiol Infect. 2011;140(6):1008–12.

    Article  Google Scholar 

  31. Velut G, Delon F, Merigaud JP, Tong C, Duflos G, Boissan F, et al. Histamine food poisoning: a sudden, large outbreak linked to fresh yellowfin tuna from Reunion Island, France, April 2017. Eurosurveillance. 2019;24(22):26–33.

    Article  Google Scholar 

  32. Kang CR, Kim YY, Lee JI, Joo HD, Jung SW, Cho S-I. An outbreak of scombroid fish poisoning associated with consumption of yellowtail fish in Seoul, Korea. J Korean Med Sci. 2018;33(38):e235.

    Article  Google Scholar 

  33. Lehane L, Olley J. Histamine fish poisoning revisited. Int J Food Microbiol. 2000;58(1–2):1–37.

    Article  Google Scholar 

  34. Rawles DD, Flick GJ, Martin RE. Biogenic amines in fish and shellfish. Adv Food Nutr Res. 1996;39:329–65.

    Article  Google Scholar 

  35. Food and Agriculture Organization of the United Nations, World Health Organization. Public Health Risks of Histamine and Other Biogenic Amines from Fish and Fishery Products. Rome: FAO and WHO. 2013. Available from: https://www.who.int/publications/i/item/9789240691919.

  36. Kimura B, Takahashi H, Hokimoto S, Tanaka Y, Fujii T. Induction of the histidine decarboxylase genes of Photobacterium damselae subsp. damselae (formally P. histaminum) at low pH. J Appl Microbiol. 2009;107(2):485–97.

    Article  Google Scholar 

  37. Takahashi H, Kimura B, Yoshikawa M, Fujii T. Cloning and sequencing of the histidine decarboxylase genes of gram-negative, histamine-producing bacteria and their application in detection and identification of these organisms in fish. Appl Environ Microbiol. 2003;69(5):2568–79.

    Article  Google Scholar 

  38. Visciano P, Schirone M, Tofalo R, Suzzi G. Biogenic amines in raw and processed seafood. Front Microbiol. 2012;3(188):1–10.

    Google Scholar 

  39. Taylor SL. Histamine food poisoning: toxicology and clinical aspects. CRC Crit Rev Toxicol. 1986;17(2):91–128.

    Article  Google Scholar 

  40. Taylor SL, Stratton JE, Nordlee JA. Histamine poisoning (Scombroid fish poisoning): an allergy-like intoxication. J Toxicol Clin Toxicol. 1989;27(4–5):225–40.

    Article  Google Scholar 

  41. Ababouch L, Gram L. Production of biogenic amines. In: Huss HH, Gram L, editors. Assessment and Management of Seafood Safety and Quality. FAO Fisheries Technical Paper. Rome: Food and Agricultural Organization of the United Nations. 2003

  42. Rachmawati N, Powell SM, Triwibowo R, Nichols DS, Ross T, Tamplin ML. Modelling growth and histamine formation of Klebsiella aerogenes TI24 isolated from Indonesian pindang. Int J Food Microbiol. 2022;362: 109459.

    Article  Google Scholar 

  43. Sirocchi V, Caprioli G, Ricciutelli M, Vittori S, Sagratini G. Simultaneous determination of ten underivatized biogenic amines in meat by liquid chromatography-tandem mass spectrometry (HPLC-MS/MS). J Mass Spectrom. 2014;49(9):819–25.

    Article  Google Scholar 

  44. Arvanitoyannis IS, Palaiokostas C, Panagiotaki P. A comparative presentation of implementation of ISO 22000 versus HACCP and FMEA in a small size Greek factory producing smoked trout: a case study. Crit Rev Food Sci Nutr. 2009;49(2):176–201.

    Article  Google Scholar 

  45. Charteris W. Quality function deployment: a quality engineering technology for the food industry. Int J Dairy Technol. 1993;46(1):12–21.

    Article  Google Scholar 

  46. Ishikawa K. Guide to quality control. Tokyo: Asian Productivity Organization. 1976

  47. Luo T, Wu C, Duan L. Fishbone diagram and risk matrix analysis method and its application in safety assessment of natural gas spherical tank. J Clean Prod. 2018;174:296–304.

    Article  Google Scholar 

  48. Food and Agriculture Organization of the United Nations, World Health Organization. Food hygiene, Basic texts. Second ed. Rome: FAO/WHO. 1999

  49. Food and Agriculture Organization of the United Nations, World Health Organization. Food hygiene, Basic texts. Fourth ed. Rome: FAO/WHO. 2009.

  50. Marcille J, Boëly T, Unar M, Merta G, Sadhotomo B, Uktolseja J. Tuna fishing in Indonesia. Paris: ORSTOM; 1984.

    Google Scholar 

  51. Mujib Z, Boesono H, Purnamafitri AD. Pemetaan sebaran ikan tongkol (Euthynnus sp.) dengan data klorofil-α citra modis pada alat tangkap payang (Danish-seine) di perairan Teluk Palabuhanratu, Sukabumi, Jawa Barat [Spatial mapping of bullet tuna (Euthynnus sp.) distribution using chlorophyll-a data derived from MODIS imagery captured by Danish-seine fishing apparatus in the waters of Teluk Palabuhanratu, Sukabumi, West Java]. J Fish Res Utiliz Manag Technol. 2013;2(2):11.

    Google Scholar 

  52. Stequert B, Marsac F. Artisanal tuna fisheries in the Indian Ocean. In: Stequert B, Marsac F, editors. Tropical Tuna-Surface Fisheries in the Indian Ocean. FAO Technical Paper. Rome: FAO. 1989. p. 76–117.

  53. Huss HH. Assurance of seafood quality. Rome: FAO; 1994.

    Google Scholar 

  54. Yoshinaga DH, Frank HA. Histamine producing bacteria in decomposing skipjack tuna (Katsuwonus pelamis). Appl Environ Microbiol. 1982;44(2):447–52.

    Article  Google Scholar 

  55. Kim S, Price R, Morrissey M, Field K, Wei C, An H. Histamine production by Morganella morganii in mackerel, albacore, mahi-mahi, and salmon at various storage temperatures. J Food Sci. 2002;67(4):1522–8.

    Article  Google Scholar 

  56. Silva CCG, Ponte DJB, Dapkevicius MLNE. Storage temperature effect on histamine formation in big eye tuna and skipjack. J Food Sci. 1998;63(4):644–7.

    Article  Google Scholar 

  57. Suyama M, Yoshizawa Y. Free amino acid composition of the skeletal muscle of migratory fish. Nippon Suisan Gakk. 1973;39(12):1339–43.

    Article  Google Scholar 

  58. United States Department of Health Human Services, Food Drug Administration, Center for food safety applied nutrition. fish and fishery products hazards and controls guidance. Fourth ed. Gainsville: Florida Sea Grant. 2011.

  59. Abdillah Z, Afrianto E, Kurniawati N. Evaluasi penerapan sanitasi terhadap risiko keberadaan histamin pada pengolahan pindang cakalang di Pelabuhan Ratu [Assessment of sanitation practices and their impact on the risk of histamine occurrence during the processing of pindang cakalang in Pelabuhan Ratu]. Jurnal Perik Kel. 2015;6(1):61–9.

    Google Scholar 

  60. Jason AC. Thawing frozen fish. Aberdeen: Torry Research Station, Ministry of Agriculture, Fisheries and Food. 1974

  61. Nurhayati A, Purnomo AH. Techno-socio-economic analysis of losses in capture fishery: a case study in Pelabuhan Ratu, Sukabumi, West Java Province. IOP Conf Series: Earth Environ Sci. 2018;139(1): 012034.

    Google Scholar 

  62. Yatsunami K, Echigo T. Occurrence of halotolerant and halophilic histamine-forming bacteria in red meat fish products. Nippon Suisan Gakk. 1992;58(3):515–20.

    Article  Google Scholar 

  63. Hernandez-Herrero MM, Roig-Sagues AX, Rodriguez-Jerez JJ, Mora-Ventura MT. Halotolerant and halophilic histamine-forming bacteria isolated during the ripening of salted anchovies (Engraulis encrasicholus). J Food Prot. 1999;62(5):509–14.

    Article  Google Scholar 

  64. Kung H-F, Lee Y-H, Teng D-F, Hsieh P-C, Wei C-I, Tsai Y-H. Histamine formation by histamine-forming bacteria and yeast in mustard pickle products in Taiwan. Food Chem. 2006;99(3):579–85.

    Article  Google Scholar 

  65. Yatsunami K, Echigo T. Changes in the number of halotolerant histamine-forming bacteria and contents of non-volatile amines in sardine meat with addition of NaCl. Nippon Suisan Gakk. 1993;59(1):123–7.

    Article  Google Scholar 

  66. Rachmawati N. Assessing the Risk of Histamine from the Indonesian Salted-Boiled Fish (Pindang) [Doctoral]. Hobart, Tasmania: University of Tasmania; 2019.

    Google Scholar 

  67. Karaçam H, Kutlu S, Köse S. Effect of salt concentrations and temperature on the quality and shelf-life of brined anchovies. Int J Food Sci Technol. 2002;37(1):19–28.

    Article  Google Scholar 

  68. Purba D. Optimasi usaha pengolahan ikan skala menengah di Kabupaten Sukabumi, Jawa Barat [Optimization enterprises of fish processing medium scale in Sukabumi District, West Java]. Bogor, Indonesia: Bogor Agricultural University; 2010.

    Google Scholar 

  69. Thaheer H, Hasibuan S, Mumpuni FS. Model resiko keamanan pangan produk pindang pada UMKM pengolahan ikan rakyat [Risk assessment model for food safety of pindang products in small and medium-sized enterprises (SMEs) involved in traditional fish processing]. J PASTI. 2010;9(3):275–85.

    Google Scholar 

Download references

Acknowledgements

The authors acknowledge the expert technical assistance of Dr. David S. Nichols from the Central Science Laboratory (CSL), University of Tasmania, in histamine analysis and acknowledge the resources provided by CSL.

Funding

This research is funded by the Australia Awards Scholarship (NR) and the Tasmanian Institute of Agriculture, University of Tasmania.

Author information

Authors and Affiliations

Authors

Contributions

NR designed the research, collected data from field work, performed laboratory analysis, analysed and interpreted data, and wrote the manuscript. RT assisted field work data collection and data interpretation. TR provided suggestion for the experimental design and input for the manuscript. SP provided suggestion for the experimental design and input for the manuscript. MT provided suggestion for the experimental design and input and constructive review of the manuscript.

Corresponding author

Correspondence to Novalia Rachmawati.

Ethics declarations

Ethics approval and consent to participate

Not applicable.

Consent for publication

The authors approve the publication of this manuscript.

Competing interests

The authors declare that they have no competing interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rachmawati, N., Triwibowo, R., Ross, T. et al. Improving the safety of pindang, a traditional fish product from Indonesia: case study from Palabuhanratu, Sukabumi District, West Java Province, Indonesia. J. Ethn. Food 12, 14 (2025). https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s42779-025-00275-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s42779-025-00275-5

Keywords