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. 2019 Mar 21;56(4):2167–2174. doi: 10.1007/s13197-019-03698-6

Managing the lionfish: influence of high intensity ultrasound and binders on textural and sensory properties of lionfish (Pterois volitans) surimi patties

L Jiménez-Muñoz 1,2,3, M Quintanilla 3, A Filomena 2,3,✉
PMCID: PMC6443756  PMID: 30996450

Abstract

Lionfish (Pterois volitans) is an invasive and predatory species whose proliferation over the Caribbean Sea threatens to cause great damage to coral reefs by negatively affecting the balance of the ecosystem. Control strategies have been the most effective way to reduce the negative impact of the lionfish. The development of diversified food products based on lionfish could support these strategies. The objective of the present study was to investigate the influence of ultrasound and the addition of binders in different concentrations: Egg white liquid (EWL) and corn starch (ST) on texture, microstructure and sensory evaluation properties of patties made of lionfish surimi. Each set of binders was added up to 3% varying proportions. The texture profile, water holding capacity, sensory qualities and fractal dimension of scanning electron microscopy images were analyzed to evaluate the quality of the product based on surimi gel. Results showed that the application of ultrasound and the use of binders enhanced the properties of patties made of lionfish surimi. The addition of EWL (3%) improved the water holding capacity and hardness of the final product. However, the fractal dimension of the images was higher in samples processed using ultrasound and without binder addition.

Electronic supplementary material

The online version of this article (10.1007/s13197-019-03698-6) contains supplementary material, which is available to authorized users.

Keywords: Fractal dimension, Lionfish, Patties, Surimi, Ultrasound

Introduction

Invasion of predatory lionfish species (Pterois volitans) poses a threat to the coral ecosystems of the western Atlantic Ocean. Lionfish have the capacity to spread rapidly to new marine environments, drastically reducing the population of species present in the reefs (Morris et al. 2011). This species has established in an area that encompasses the eastern coast of the United States, Bermuda, Gulf of Mexico and the Caribbean region. To mitigate the negative impact that this species represents, control strategies such as removal and consumption at a local scale have been performed (Morris et al. 2011). The diversification of lionfish consumption could lead to increasing the effectiveness of these strategies.

Surimi gel has earned great acceptance in the global market due to its characteristics: high myofibrillar proteins concentration which have an excellent gel-forming ability, low-fat content, ready-to-eat product and a unique texture (Fan et al. 2017a, b). To obtain surimi, a process of washing cycles must be carried out, which removes sarcoplasmic proteins, nitrogen compounds, fat, blood, aromatic compounds and other impurities. This improves the quality of the myofibrils (Athaillah and Park 2016) resulting in a product with better texture, color and smell (Park et al. 2013). However, each washing cycle requires large amounts of water (Martín-Sánchez et al. 2009), some alternatives evaluated for surimi production showed a decrease in water usage. Power ultrasound (20 kHz; 10–1000 W) is an emerging technology able to replace a washing cycle in surimi processing (Filomena et al. 2012) which is usually used to achieve physical or chemical modifications of food properties (Kentish and Ashokkumar 2011). Generally, ultrasound increases the efficiency of the diffusion of components, and cavitation generates high shear forces and microbubbles that enhance surface erosion, fragmentation and mass transfer. Ultrasound has been shown to improve the hardness and WHC of the gel (Zhang et al. 2011). When high-quality surimi is the main component of a product, the predominant texture tends to be gummy (Tabilo-Munizaga and Barbosa-Cánovas 2005). To adapt the product to the textural preferences of consumers, it is necessary to add ingredients to the surimi to improve the textural properties and water holding capacity (WHC) (Park et al. 2013). Sodium Citrate was used as a cryoprotectant, a food additive used to prevent denaturation in surimi during frozen storage (Pavathy and Sajan 2014).

Starch is an additive used as a thickener or gelling agent that adds stability and replaces expensive ingredients. According to Park et al. (2013) starch is used to maintain the hardness of the gel and those with high amylopectin content form cohesive and adhesive gels. The egg white is also a common additive in the production of surimi. These binders are the ingredients used to improve the functional, textural and sensory properties of surimi-type products (Park et al. 2013).

Considering lionfish is a new species introduced in the human diet, there are few reports on the sensory acceptance of its derived products. Sensory attributes, texture properties, and consumer acceptance should be studied (Morris et al. 2011). The objective of this research was to evaluate the influence of ultrasound and different percentages of binders on the textural properties and sensory acceptability of lionfish surimi patties.

Materials and methods

Lionfish acquired in local markets of Cartagena (10º 23′58 “N; 75º 30′51″W) (Colombia), was transported and stored at a temperature of − 20 °C for a term of less than a week before processing surimi patties.

Surimi preparation process

Sixteen samples of surimi patties were studied (Table 1). The samples were prepared using two methods: conventional (CN) and ultrasound (US). These variables are reported to affect the texture of surimi (Hunt et al. 2010; Zhang et al. 2011; Filomena-Ambrosio et al. 2015).

Table 1.

Coding for different treatments studied

Treatment Method Concentration of corn starch % (w/w) Concentration of egg white % (w/w)
CN_CTRL Conventional 0 0
CN_3EW Conventional 0 3
CN_3ST Conventional 3 0
CN_1.5EW Conventional 1.5 1.5
CN_2.01EW Conventional 0.99 2.01
CN_0.99EW Conventional 2.01 0.99
CN_2.25EW Conventional 0.75 2.25
CN_0.75EW Conventional 2.25 0.75
US_CTRL Ultrasound 0 0
US_3EW Ultrasound 0 3
US_3ST Ultrasound 3 0
US_1.5EW Ultrasound 1.5 1.5
US_2.01EW Ultrasound 0.99 2.01
US_0.99EW Ultrasound 2.01 0.99
US_2.25EW Ultrasound 0.75 2.25
US_0.75EW Ultrasound 2.25 0.75
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CN conventional, US ultrasound, EW egg white, ST corn starch

Conventional method: Sliced lionfish fillets (2 × 2 × 2 cm), were leached with water at 4 °C in a ratio p/p 1:3 (fillet: water), for three washing cycles (15 min), pressed and homogenized with salt (0.1–0.2%), sugar (0.2–0.3%) and sodium citrate (0.3–0.4%).

Ultrasound method: Sliced lionfish fillets (2 × 2 × 2 cm), were leached with water at 4 °C in a ratio p/p 1:3 (fillet: water), for two washing cycles (15 min), then placed in an ultrasound bath (ELMA, Singen, Germany), at 37 kHz; 150 W, 15–20 (min), pressed and homogenized with salt (0.1–0.2%), sugar (0.2–0.3%) and sodium citrate (0.3–0.4%).

To obtain a set of surimi patties with ranges of different textural characteristics 16 different sample formulations were selected. Each patty weighed 80 ± 2.0 g. The patties were prepared by adding 3% (2.4 g) salt, 2% (1.6 g) sugar and 0.3% (0.24 g) sodium citrate. The rest of the formulation consisted of a different concentration of binders (cornstarch maizena® (ST) and liquid egg white (EW) up to 3% as shown in Table 1.

Surimi patties preparation process

The patties prepared from surimi using two treatments, CN and US, were mixed in a ratio of 3:1 w/w, seasoned with spices in a semi-fat medium, called guiso. The preparation of the stew used tomato (62%), onion (33%) and garlic (5%) cut in small pieces, previously homogenized and fried over low heat, without the addition of salt.

Lionfish patty is presented in Fig. 1. The patties were prepared following the method suggested by Dreeling (Ramadhan et al. 2012). Each patty was cooked on both sides on a flat surface grill until the minimum internal temperature of 80 °C was reached. Subsequently, it was coated with wheat flour, egg yolk, and breadcrumb, then cooked a second time during six min.

Fig. 1.

Fig. 1

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Patty elaborated from lionfish surimi

Water holding capacity

This parameter was measured using the modified method of Jauregui et al. (1981). Samples of 1.500 ± 0.100 g were placed on pre-weighed filter paper (a piece of #3 Whatman filter paper n.50º). The samples were centrifuged at 4 °C for 20 min (Universal 32R Hettich Zentrifuguen), and the filter paper was weighed again to determine the WHC by the weight difference (Filomena-Ambrosio et al. 2015). The measurements were made in triplicate.

Moisture

Samples of 5.0 g ± 0.1 g were dried during 4 h at 102 °C ± 0.1 °C using the stove drying method (985.14 AOAC).

Texture profile analysis

A texture profile analysis (TPA) was performed on a TA.XT Plus Texture Analyzer (Stable Micro Systems, UK) with a 25 mm aluminum test tube and a strain distance of 10 mm. The software used for the analysis was Texture Exponent. The attributes evaluated were hardness, cohesiveness and gumminess (Texture technologies 2003).

Sensory analysis

Four of the sixteen samples were selected to perform the sensory analysis. The selection was made according to the desirability level of the product based on their WHC (the samples reporting the highest and lowest). The treatments with lowest values were CN_CTRL, CN_1.5EW and with highest values were US_CTRL and US_3ST. The descriptive analysis of texture, taste, flavor, saltiness, and sweetness was evaluated by the panelists using a nine-point scale, in which 9 represented the highest score for the attribute and 1 represented the lowest (Stone et al. 2012). The samples were presented to each participant in a sequential monadic manner. The sample presentation was randomized. Thirty-two gastronomy students from Universidad de La Sabana who were currently studying sensory analysis participated in the test as panelists.

Scanning electron microscopy

To perform scanning electron microscopy, the samples were lyophilized using the equipment Labconco, model FreeZone 12L, USA. The process consisted of three steps: Freezing (− 40 °C for 3 h), sublimation (0 and − 10 °C for a period of 24 h) and finally desorption (20 °C and vacuum pressure of 4 mbar).

Fractal dimension analysis obtained from SEM images

The dried samples were placed on carbon tape (Ted 57, Pella, Inc., Mountain Lakes Blvd, Redding, US) and observed by scanning electron microscope (SEM, Phenom G2 Pro®, Belgium). To appreciate the difference in the microstructure of the patties, photos were taken at a magnification of 5000× and 5 kV. The samples were cut into 5 mm portions. The microscope images were analyzed with ImageJ and SDBC Image J plugin. The fractal dimension values (Df) indicate the degree of gel surface irregularity since protein aggregate formation can be characterized as a kind of fractal. Df was calculated using the box count method (Zhu et al. 2016).

Statistical analysis

A categorical multifactorial experimental design with two factors (method and binder) was employed. A two-way analysis of variance was carried out. The effects of the method and mixture of binders (egg white and starch) were evaluated. In all the models, normal distribution of residuals and homogeneous variances were detected. The Tukey HSD test was performed to identify the difference in means between treatments. All experimental runs were performed in triplicate. Four treatments were selected according to the desirability of the product based on their WHC (the two highest and the two lowest). For the sensory test, an ANOVA was carried out. The frequencies were used to calculate the Chi square value. The statistical software used were Design expert v10 and Statgraphics XVII.

Results and discussion

Surimi patties analysis

The values for WHC, texture parameters and fractal dimension (Df) are presented in Table 2.

Table 2.

Water holding capacity, texture profile analysis and fractal dimension of surimi patties processed by conventional and ultrasound method with different binder concentrations

Treatment Water holding capacity (g of held water/g of sample) Hardness (N) Cohesiveness Gumminess (N) Fractal dimension
CN_CTRL 29.45 ± 1.62ª 16.76 ± 3.09ª 0.60 ± 0.07d 10.05 ± 2.07abcd 2.44 ± 0.01ª
CN_3EW 36.59 ± 2.79bc 29.26 ± 1.59cde 0.35 ± 0.07abc 10.29 ± 2.67abcd 2.50 ± 0.01c
CN_3ST 38.55 ± 1.44bc 24.36 ± 1.52bc 0.41 ± 0.09bc 10.13 ± 2.82abcd 2.51 ± 0.01cd
CN_1.5EW 37.53 ± 2.47b 28.11 ± 4.18bcd 0.36 ± 0.07abc 10.43 ± 3.40abcd 2.50 ± 0.01c
CN_2.01EW 38.44 ± 3.12bc 27.32 ± 3.86bcd 0.35 ± 0.04abc 9.48 ± 1.31abc 2.46 ± 0.01b
CN_0.99EW 37.97 ± 0.50bc 33.64 ± 0.85de 0.44 ± 0.05c 15.02 ± 1.90def 2.54 ± 0.01e
CN_2.25EW 38.87 ± 2.58bc 22.54 ± 4.01c 0.30 ± 0.03ab 6.84 ± 2.10ab 2.52 ± 0.01cd
CN_0.75EW 39.21 ± 2.60bcd 22.02 ± 0.50ab 0.29 ± 0.06ª 6.37 ± 1.27ª 2.51 ± 0.01cd
US_CTRL 36.21 ± 1.60bc 22.63 ± 2.75bc 0.36 ± 0.06abc 7.13 ± 1.32abc 2.60 ± 0.01f
US_3EW 43.10 ± 1.25de 31.30 ± 3.39de 0.39 ± 0.07abc 12.12 ± 1.07cde 2.52 ± 0.01d
US_3ST 45.93 ± 1.29e 27.23 ± 1.65bcd 0.39 ± 0.01abc 10.62 ± 0.54abcd 2.50 ± 0.01c
US_1.5EW 39.63 ± 2.82cd 32.27 ± 4.73de 0.34 ± 0.07abc 11.44 ± 3.85bcd 2.51 ± 0.01cd
US_2.01EW 39.82 ± 2.35cd 35.36 ± 6.47e 0.45 ± 0.12c 16.73 ± 7.18ef 2.46 ± 0.01b
US_0.99EW 39.47 ± 3.63bcd 42.20 ± 6.86f 0.46 ± 0.03c 19.29 ± 3.08f 2.59 ± 0.02f
US_2.25EW 38.96 ± 2.80bc 29.04 ± 2.61cde 0.42 ± 0.08c 12.32 ± 2.86cde 2.52 ± 0.01d
US_0.75EW 40.00 ± 1.31cd 25.43 ± 5.48bc 0.39 ± 0.01abc 9.89 ± 1.90abc 2.45 ± 0.01ab
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Data are given as mean ± standard deviation. Different letters indicate statistically significant differences (p < 0.05)

Water holding capacity (WHC)

The statistical analysis of the results indicated that the two factors (method and binder) had an effect on WHC and that there was also an interaction between factors (p < 0.05). The treatments that had higher values for WHC were US_3ST and US_3EW. Starch is used primarily for its high water-holding capacity and its ability to replace a portion of fish protein while maintaining ideal gel properties (Park et al. 2013). The strengthening effect of cornstarch on the surimi gel induced by cooking heat is probably due to the starch granules embedded in the matrix and exerting pressure on it, resulting in a more compact and hard gel (Kim and Lee 1987). Authors such as Alvarez et al. (1997) reported that waxy maize starch had a boosting effect on WHC in cooked surimi gels and the mixed network of surimi-starch retained the added water during the gel preparation. The starch granules absorb and retain water during the formation of the gel (Paker and Matak 2017), when applying high temperatures they interact with the protein and gelatinize, increasing the hardness of the gel (Hunt et al. 2010). Hema et al. (2016) mentioned that to increase the WHC of products made from surimi gel with addition of cornstarch, it is necessary to process them at high temperatures (> 80 °C). Since the gelatinization temperature is influenced by the presence of myofibrillar proteins and the available hydrodynamic water for gelation. However, in their experiments, the WHC of the surimi prepared with cornstarch was lower than that of the control. This was probably due to the fact that the starch granules are more thermostable and start to gel after the protein groups (Kong et al. 1999). Both the protein and the starch compete for the water available in the gel. As the proteins form crosslinks more quickly, the gelation of the starch is partially prevented by the lack of water or because the granules are trapped in the protein network (Hunt et al. 2010). According to Paker and Matak (2017), it is also possible that the high water absorption and retention capacity of the starch granules increase the thermal stability of the protein fraction without competing with protein groups for the absorption of water. Protein gelation can physically and chemically bind water in the gel matrix, which limits the availability of water for starch gelation (Chung and Lee 1991). When there is enough water in the system to hydrate and gelatinize the starch there is no competition between starch and protein that affects the gelling of its components, thus starch would have the ability to gel properly (Alvarez et al. 1997). It is possible that in US_3ST surimi patties, the added stew “guiso” provided enough water for both starch and protein to properly gel, which increased WHC values.

In the research conducted by Hema et al. (2016), it was reported that surimi gels prepared with EW had higher moisture content than other treatments. Egg white forms stabilizing foam with proteins at neutral pH, which are more stable due to the lack of repulsive interactions. This promotes interactions between fish proteins-egg white proteins and the formation of the viscofilm at the interface, which adsorbs more protein. Subsequently, the heating coagulates the egg white protein, leaving cracks and crevices that have non-polar groups increasing the WHC in the gel matrix. In mixed gels, egg white, starch, and fish proteins compete for available water, which prevents the starch from obtaining the water necessary for its swelling and gelatinization (Tabilo-Munizaga and Barbosa-Cánovas 2005). This phenomenon explains why the WHC of mixed gel treatments did not present the highest value.

Treatments processed with US obtained higher values for WHC than gels processed by CN. These data coincide with those reported by McClements (1995) and Turantas et al. (2015). Ultrasound works by generating wave frequencies that act on the matrix as pulsations that affect the spaces formed between the myofibrils (Zhang et al. 2011). The wave frequencies modify the structure of the sarcolemma containing the sarcoplasmic proteins, which are removed during the washing stages due to their low molecular weight, thus creating a structure that retains a greater amount of water (Filomena-Ambrosio et al. 2015).

Texture profile analysis (TPA)

Hardness

The values obtained for the hardness of patties are presented in Table 2. Method and binder had an effect on hardness (p < 0.05). However, there is no interaction between the factors. The patties processed with US showed higher values for hardness than the ones processed with CN (p < 0.05). According to Fan et al. (2017), high acoustic intensities generated by ultrasound can develop greater hardness in the surimi gel. This is due to the mechanical effect of the ultrasound, which improves the packing compactness of the molecules of protein, as well as the degree of interaction between them. The ultrasound treatment US_0.99EW had higher hardness values than that of the control. According to Suklim et al. (2003) and Hunt et al. (2009), starch increases the hardness of surimi more effectively at low concentrations (3%) than higher concentrations (6–9%). However, US_3EW treatment had a greater hardness than US_3ST, probably due to the coagulant capacity of ovalbumin present in egg white (Hema et al. 2016). Iso et al. (1985) suggested that egg white absorbs water within the structural network without increasing the number of protein cross-links in the gel.

Cohesiveness

The addition of binders did not improve the cohesiveness of treatments processed with CN (p < 0.05). The addition of binders in surimi patties processed with CN showed a decrease in cohesiveness compared to the control. Ultrasound has been shown to increase water holding capacity and cohesiveness in meat and meat products (McClements 1995; Turantas, et al. 2015). The cohesiveness of treatments US_2.01EW, US_2.25EW and US_0.75EW were greater than those processed with the same addition of binders but obtained by CN. According to Suklim et al. (2003) the addition of albumin up to 2% can improve the cohesiveness of meat products such as squid patties. The addition of starch in a gel matrix (e.g., surimi) also increases the hardness of the gel and the cohesiveness due to its ability to increase its size, absorb and bind the surrounding water in the gel once gelatinized (Suklim et al. 2003). Consequently, the gel becomes more compact and firm.

Gumminess

Both factors had an effect on the gumminess of surimi patties (p < 0.05). There was no interaction between them. The addition of binders increased the gumminess values for US treatments compared to the controls. The surimi patties made with US showed higher values than those made with CN because the gumminess was calculated by multiplying hardness and cohesiveness (Tabilo-Munizaga and Barbosa-Cánovas 2005).

Scanning electron microscopy (SEM)

The SEM images of the treatments are presented in Fig. 2. The Df values indicate uniformly distributed porosity level around the centroid of the total image (Zhu et al. 2016). According to the values obtained for the different treatments, the Df can vary according to the processing method and the concentration of the binder present in the structure, these vary from 2.44 to 2.60. In addition, interaction between the two factors was found (p < 0.05). The value of Df for surimi patties made with ultrasound and no addition of binder (US_CTRL) obtained the highest value (2.60) while the value obtained by CN_CTRL had the lowest value (2.44). The treatments processed with CN showed higher values than its control when the binders were added. The addition of binders favors a high degree of complexity and the formation of a more ordered microstructure (Marangoni, et al. 2000). However, this behavior is not observed on the patties processed with US, probably due to a reorganization of the three-dimensional protein structure when adding the binders. Surimi patties obtained by the US method exhibit a higher interconnected protein network than those obtained by CN.

Fig. 2.

Fig. 2

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Scanning electron microscopy of surimi patties at 5000×

In the SEM image of US_1.5EW, corn starch granules (15 μm) can be observed (Izidoro et al. 2007; Park et al. 2013; Alcázar-Alay and Meireles 2015). On the contrary, in none of the samples obtained by the US method these granules are appreciated. This could be related to the molecular structure of the starch that allows it to pass through different stages, from the absorption of water up to the disintegration of the granule. The absorption of water and consequent swelling of the starch granule contributes to the separation of amylose-amylopectin phase and loss of crystallinity, which in turn promotes leaching of amylose in the inter-granular space (Alcázar-Alay and Meireles 2015). It is possible that in the surimi patties elaborated by CN the starch granule did not reach the disintegration phase.

Sensory analysis

The sensory attributes hardness and gumminess showed significant differences between treatments (p < 0.05). The sample US3_EW was perceived by panelists as the patty with hardest texture. Montero & Gómez-Guill (1996) found that the egg had a positive effect on the hardness of sardine surimi (Sardina pilchardus). Egg white absorbs water within the network structure without increasing the number of protein crosslinks in the gel (Suklim et al. 2003). According to Hema et al. (2016) the egg white provides strength to the gel due to the coagulation capacity of ovalbumin and it is suited for surimi based products. The sample US_3ST was perceived as the gummiest patty, starch can improve gel strength which might increase gumminess (hardness*cohesiveness) values (Sariçoban et al. 2009). There were no significant differences for the attributes saltiness, sweetness and overall flavor (p > 0.05). The mean of the sensory attributes are shown in Table 3.

Table 3.

Mean of scores and standard deviations

Attributes Samples
CN_CTRL CN_1.5EW US_3ST US_3EW
Hardness 5.4 ± 2.2a 5.6 ± 1.8a 5.8 ± 2.5a 6.8 ± 1.8b
Gumminess 5.6 ± 2.5a 4.8 ± 2.2a 6.7 ± 1.8b 5.8 ± 2.3a
Overall flavor 6.6 ± 2.1a 6.5 ± 1.8a 6.2 ± 2.1a 6.8 ± 2.5a
Saltiness 5.0 ± 2.3a 4.8 ± 1.5a 4.8 ± 1.9a 4.8 ± 2.0a
Sweetness 3.9 ± 2.4a 3.5 ± 2.6a 3.2 ± 2.4a 3.2 ± 2.2a
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Data are given as mean ± standard deviation. Different letters indicate statistically significant differences (p < 0.05)

CN conventional, US ultrasound, EW egg white, ST corn starch

In the sensory test only the texture parameter showed significant differences (p < 0.05) with an X2 = 12.25. In which the patty US3_EW was marked more frequently as the product with better texture. According to Chang-Lee et al. (1990) and Sun and Holley (2011) protein additives such as egg white can improve the characteristics of the gel by providing greater gel hardness.

Conclusion

The use of new raw materials as lionfish and emerging technologies as ultrasound proved to be a successful approach to understand the effect on textural, microstructure and sensory parameters of novel products. The ultrasound treatment could be an ideal method because of its technological and sensory advantages, in line with consumer preference of the final products. Binders provide an improvement in texture for hardness and gumminess which evidence that ultrasound and binders could be used together to develop lionfish surimi derived products of good quality. The sample processed with US and addition of 2.01% starch and 0.99% egg white (w/w) showed the best performance for hardness, gumminess and fractal dimension.

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Acknowledgements

Authors would like to thank the University of La Sabana and COLCIENCIAS for funding the development of research within the framework of Project EICEA-98-2015., Project 761-2016 of COLCIENCIAS.

Footnotes

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