Effects of Superheated Steam Pretreatment on Muscle Release and Meat Quality of Shucked Tropical Oyster (Crassostrea iredalei)

doi:10.21203/rs.3.rs-3108218/v1

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Research Article

Effects of Superheated Steam Pretreatment on Muscle Release and Meat Quality of Shucked Tropical Oyster (Crassostrea iredalei)

https://doi.org/10.21203/rs.3.rs-3108218/v1

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Superheated steam (SS) is promising for thermal shucking application of oysters due to its high energy. Tropical oysters Crassostrea iredalei was probed with K-type thermocouples connected to a datalogger to monitor and record process temperatures during superheated steam pretreatment at different temperatures (170, 210, and 250 °C) and holding time (4, 5, 6 min) followed by rapid ice immersion. The combination of heating and rapid chilling on the release of oyster meat during shucking were evaluated for muscle relaxation, muscle release, meat quality, texture profile analysis, and color and optimized for maximum muscle release and meat quality. The thermal profiles of SS reveled rapid temperature increment of both muscle and oyster shell compared to conventional steam, resulting in increased relaxation of adductor muscles and degree of meat release with increase in temperature and time Texture of the oyster meat retained hardness, gumminess and chewiness of the fresh oyster at low superheated steam temperature and short exposure time. Sufficient meat detachment of more than 85% was achieved at 170 °C and 5 min with minimum meat quality changes which also lower in microbial load (4.1 x 10³ CFU/g), TVB-N (11.7 mg/100 g) and final pH reduction (0.3) compared to untreated [microbial load (5.2 x 10³ CFU/g), TVB-N (15.7 mg/100 g), pH reduction (0.6)] and microwave treated [microbial load (4.3 x 10³ CFU/g), TVB-N (21.0 mg/100 g), pH reduction (0.5)] samples. In sum, SS is potential to minimize oysters shucking time and prolonged shelf life of shucked oysters without compromising meat quality.

superheated steam

shucking

muscle release

meat detachments

protein oxidation

tropical oysters

Oyster (family Ostreidae) is one of the highly valued salt-water bivalve mollusks harvested intensively as a seafood delicacy. Not only are they appetizing to many, but they are also important sources of protein, vitamins, and minerals (Yoda et al., 2021). In 2018, the estimated global production of tropical oysters was around 5.7 million tons, valued at approximately 6,800 million USD, indicating a highly lucrative aquaculture market (FAO, 2019). In Malaysia, Crassostrea iredalei and Crassostrea belcheri are the predominant culture species, and they are usually sold fresh as whole shell or shucked meat, both fresh or packaged and refrigerated in the local market (Tan et al., 2014). The warm tropical climate encourages the growth of bacteria such as Vibrio spp., Escherichia coli, and Salmonella spp., which raises the risk of foodborne illnesses from consuming raw oysters. Some pathogenic strains in tropical oysters have been shown to have an adaptive cold shock response to survive and grow at low temperatures (Alarcón Elvira et al., 2020), which necessitates critical post-harvest care to assure the safety and quality of the oysters and extend their shelf life.

The shucking operation is the bottleneck of oyster processing chain. Oyster shucking is labor intensive, require skilled labor to cut adductor muscle attachments from the shell and can introduce risks, such as cross-contamination by foodborne pathogens due to temperature control failure, contaminated utensils, human carrier, and contaminated water during processing (Intarakul et al., 2011; Kadariya et al., 2014). Oysters contain two different types of adductor muscles, slow acting smooth (opaque) and fast acting striated fibers (translucent), which enable sustained and quick shell closing and aid in removing pseudofaecal material from the mantel. The opaque muscle's strength enables the oysters to close for a long period causing it hard to open (Martin, 2006). The adductor muscle can be detached at the muscle–shell bond area by heating the attachment layer or alternatively, using high pressure processing (Ma et al., 2021). The translucent muscle releases at a lower temperature than the opaque counterpart at about 71°C to detach it, but changes in the meat's flavor and texture can occur at temperatures as low as 54°C when held for extended periods (Wheaton, 2007). High temperature short time method of thermal shucking able to release muscle from the shell without cooking the oyster. Thermal treatments such as high-pressure steam, steam, flame, infrared radiation, microwave, and laser have been studied to relax the opaque muscle (Martin, 2006). Rapid heating and cooling of Crassostrea virginica increased success rate of shucking depending on heating and cooling combinations (Martin, 2003).

Superheated steam produced when steam is heated above the boiling temperature of water that changes properties of steam into transparent hot-dry gas with greater energy compared to steam (Alfy et al., 2016; Fang et al., 2022). Thus, more efficient heat transfer can retain raw-like quality of shucked oysters since the consumers perceive whole raw oysters as high-quality product from minimal processing. Superheated steam treatment of pen shell minimized lipid oxidation and preserved nutritional and sensory quality (Mohibbullah et al., 2018; Negara et al., 2021). Nevertheless, no information is available on the effect of superheated steam to raw shucked oyster. The present study aimed to investigate the effects of superheated steam treatment on its capability to release adductor muscles, asses the consequent impact on raw-like oyster quality, texture, microbial reduction. The thermal response of the oysters during thermal treatments were also evaluated. Finally, the effects of superheated steam on the shelf-life and texture changes of shucked oysters during refrigerated storage were also compared with untreated and microwave treatment.

Materials

Tropical oysters (Crassostrea iredalei) (about 280 pieces of about 100 g each) were collected in January at Bakau Hijau oyster farm, Sungai Merbok estuary, Kedah, Malaysia with recorded water salinity at 21± 3 ppt. The tropical oysters were cleaned and scrubbed under the high-pressure water tap using brush to eliminate fouling materials. The harvested oysters were kept cool at 10°C during transport and prior to treatment and tested within 2 days of harvest. The harvested oysters were tested and found to be absent of Escherichia coli and Vibrio parahaemolyticus. The total coliform and fecal coliform of the harvesting area were recorded at 41 MPN/100 mL water. Based on the US National Shellfish Sanitation Programme, the tropical oysters in this study can be categorized under approved area while under EU shellfish harvesting area classification criteria, it belonged to the harvesting area A, where mollusks can be directly harvested for human consumption (Su & Liu, 2014).

Buffered peptone water, plate count agar (HiMedia, Mumbai, India), magnesium oxide (R & M Chemicals, Essex, United Kingdom), boric acid (Systerm®, Selangor, Malaysia) and all other chemicals were of analytical grade.

Thermal shucking methods

Superheated steam shucking

Shell density and thickness of the oyster can influence the heat transfer and effectiveness of the thermal shucking treatment. Thus, 10 oysters were standardized in size to within 3” in length and 1” in height with 100 ± 5 g of weight. Selected oysters shell was drilled to make small hole to probed with two K-type thermocouples inside the center of the oyster, inside, and outside the shell to measure meat and shell temperatures profiles during the thermal shucking process according to Martin et al. (2007) using 8-channel datalogger (Omega Engineering, Norwalk, CT, USA) to collect and record the temperature outputs. The thermocouples were secured in place with clay plug and banded them on the oysters shell using rubber bands as shown in Fig. 1b. The superheated steam treatment was conducted in a preheated superheated steam oven (Healsio, AV-1500V, Sharp, Japan) at different temperatures (100, 175 and 250°C) and time (2, 4 and 6 min). The treated samples were immersed immediately in ice for 2 min. After cooling, the oysters were shucked and analyzed within 2 hours. Each batch consisted of eight oysters.

Experimental design

Face-centered (α = 1) central composite design (CCD) was employed to model the effects of thermal shucking treatment parameters using superheated steam treatment. Two factors were temperature (100, 175 and 250°C) and time (2, 4 and 6 min) that results in 11 experimental runs with three center points. The response variables were statistically analyzed using Design Expert version 12.0.10 (State Ease, Inc., Minneapolis, MN, USA) for ANOVA, regression analysis with hierarchical backward elimination at a 95% significance level (p < 0.05) and fitted to second-order model polynomial equation by multiple regression. The adequacy of the models was evaluated by the overall predictive capability of the model and explained by the coefficient of determination R². The developed models were overlaid and optimized for maximum relaxation values, degree of release for the ease of oyster shucking and maximum meat quality, chewiness, and lightness, L* for the quality characteristics of shucked oyster.

Microwave treatment

Or comparison, 10 oysters were microwaved (Healsio, AV-1500V, Sharp) each time at high power (800 W) for 60 s and held for 60 s which showed raw-like meat quality and high degree of release. The treated samples were immersed immediately in ice for 2 min. After cooling, the oysters were shucked and analyzed within 2 hours.

Determination of relaxation, degree of release and meat quality

The effectiveness of thermal shucking was evaluated based on the degree of relaxation, degree of release and oyster meat quality according to Martin et al. (2007). For the degree of relaxation, each oyster’s shell was pressed closely using hand and grade based on any movement of the shells. No movement after pressing was given with score 0. Score 1, 2, or 3 indicated that the degree of relaxation of the abductor muscle becoming more relaxed with a value of 3 demonstrated as a fully gaped oyster.

Analysis on degree of release was carried out by snooping the open of the oyster shell to examine the attachment of the adductor muscle (translucent and opaque) to the muscle scar. A value of zero was given if there was no muscle release from the scar. The increment of values (1, 2, and 3) were given based on how much muscles were still attached where a value of 3 denoted that the adductor muscle fully released from the muscle scars. Meat quality was analyzed visually through the comparison with raw tropical oysters. A value of 1 was given if cooking level of the treated oysters was intolerable and value of 2 or below was assigned if the oysters showed less than 10% cooking while a value of 3 was given if the oyster looked alike with the raw oysters. An untreated oyster was shucked and used for visual comparison.

Quality evaluation of shucked oysters

Texture profile analysis

The texture analysis of the tropical oysters was measured using a texture analyzer (TA.XTplusC, Stable Micro Systems, Surrey, UK) with a Software (Exponent, Stable Micro Systems) at room temperature in triplicate readings according to Wang (2015). Double compression was carried out with 50% of the original height of the tropical oysters using aluminum probe P/75 with a 5 kg load cell applied at a cross-head speed of at the speed of 2 mm/s. There was 5 s elapse between two compression cycles. The result of hardness, gumminess, and chewiness were recorded to reflect the eating quality of the raw oysters.

Color measurement

The color of the shucked oysters was measured at the central body using a CM-700d Konica Minolta (Tokyo, Japan) instrument. Calibration was carried out using blank and white reference. The readings of each sample were recorded with a Hunter system values such as L* (lightness), a* (redness), b* (yellowness) as described in a previous study (Bashir et al., 2018; Chen et al., 2015; Mohibbullah et al., 2018).

Storage study of refrigerated shucked oysters

The microbial analysis was carried out on fresh and treated tropical oysters. The tropical oysters’ shells were rub with a scrubber to remove dirt, washed and dried using a pad. To secure oyster meat and liquor in aseptic conditions, the shells were then sprayed with alcohol. Total plate count was carried out in triplicates using shucked oyster meat and oyster liquor for both fresh and treated tropical oysters.

Total plate count (TPC)

Shucked oyster meat and oyster liquor (10 g) from composite samples of 5 oysters were added to 90 mL of buffered peptone water (BPW) and transferred into stomacher bag. The mixture was blended at 250 rpm for 2 minutes using Stomacher® 400 Circulator Paddle Blender (Seward Laboratory System Inc., West Sussex, UK). The aliquot was used for serial dilution with dilution factors of 10^− 2 and 10^− 3 using BPW. The aliquots from each dilution (0.1 ml) were spread on plate count agar (PCA) using spread plate technique and incubated at 37°C for 24 hours.

pH analysis

The oyster meat and liquor (5 g) from composite samples of 5 oysters were homogenized with 50 mL of distilled water using homogenizer. The pH of the homogenized oysters was measured using a pH meter (Mettler Toledo, InLab Expert Pro, UK) in triplicates.

Total volatile basic nitrogen (TVB-N)

The determination of TVB-N was carried out via both the sample hyperspectral image and the semi-micro Kjeldahl method according to Chen et al. (2019) with some modification. Oyster meat (8 g) from composite samples of 5 oysters was homogenized at 13000 rpm/min for 1 min and centrifuged at 3000 rpm for 20 min. The supernatant (10 mL) was transferred to a distillation tube with the addition of 10 mL of 10 g/L magnesium oxide solution. Boric acid (30 mL, 10 g/L) and 5 drops of methylene red and methylene blue indicator were added to a conical flask. Steam distillation was carried out using Kjeldahl nitrogen distillation system (Vapodest 200–450, Gerhardt, Germany) for 5 minutes. The distillate was titrated using 0.01 mol/L hydrochloric acid solution. TVB-N content was calculated using equation as follow:

(1)

where, V₁ is the titration volume of the test sample (mL), V₂ is the titration volume of the blank (mL), c is the concentration of the HCl solution (mol/L), and M is the mass of the sample (g).

Statistical analysis

Results were expressed as mean ± standard deviations of triplicate analyses for each sample unless otherwise stated. The statistical analyses for physicochemical properties of samples were performed using SPSS (Version 23.0, SPSS Inc., Chicago, IL, USA). A comparison of the means was ascertained by Turkey’s test at 5% level of significance using one-way analysis of variance (ANOVA).

Thermal profile of oysters during superheated steam treatment

Figure 1 shows the temperature profiles of the tropical oyster’s muscle (at the center) and outside shell during the superheated steam (SS) treatment at 170, 210, and 250°C for 6 minutes followed by rapid ice immersion for 2 minutes compared to conventional steam. The insert shows the temperature profile of the inside shell. Increase in SS temperature rapidly increased the muscles and shell’s temperatures before rapidly dropped with ice immersion. The maximum temperature, rate of heating and cooling for the muscle and shell are shown in Table 1. The maximum temperatures of the shell ranged between 75.1 to 92.7°C for the SS and 63.3°C for the steam which were about 3 to 5°C higher compared to the muscle’s temperatures (between 72.2 to 89.0°C for SS and 58.0°C for steam). The rate of heating of the shell (0.91–2.16°C/min) was also higher compared to the muscles (0.13–1.99°C/min) considering higher thermal conductivity of oyster shell (0.9–2.27 W/m.°C) versus oyster meat (Wheaton, 2007).

The heat transfer during thermal shucking is affected by variation in shell density and thickness of the oyster’s shell. The heat capacity, thermal diffusivity, and thermal conductivity of oyster’s shell reported to vary largely in the range of ~ 1 J/g.°C, 3.22–6.89 x 10^− 6 m²/s, and 0.90–2.27 W/m.°C for different species as well as sampling location (Martin et al., 2007). The oysters from Bakau Hijau estuary have flaky and thin shell structure which explains the rapid heat increment during superheated steam treatment. Interestingly, heat loss from the superheated steam treated samples after 2 minutes of ice immersion, ranged between 0.75 to 1.22°C/min were also significantly higher compared to the conventional steam at 0.63°C/min. Superheated steam does not contain moisture which can act as insulation and further increasing its thermal conductivity. Rapid heating is crucial for the muscle detachment and the rapid cooling can preserve meat quality of the fresh oysters.

Table 1

Maximum temperature, heating and cooling rates of oyster’s muscle and inner shell during superheated steam (SS) treatment at different temperatures compared to conventional steam.
Treatments	Oyster’s meat					Oyster’s shell
Treatments	Max temperature (°C)	Heating rate (°C/min)	R²	Cooling rate (°C/min)	R²	Max temperature (°C)	Heating rate (°C/min)	R²
SS, 170°C	72.2 ± 0.2	1.24 ± 0.02	0.999	0.75 ± 0.05	0.996	75.1 ± 0.3	1.49 ± 0.01	0.986
SS, 210°C	77.9 ± 0.3	1.47 ± 0.01	0.999	1.13 ± 0.04	0.996	86.5 ± 0.1	1.62 ± 0.02	0.996
SS, 250°C	89.0 ± 0.4	2.16 ± 0.01	0.998	1.22 ± 0.05	0.988	92.7 ± 0.2	1.99 ± 0.02	0.987
Steam, 100°C	58.0 ± 0.2	0.91 ± 0.2	0.987	0.63 ± 0.03	0.998	63.3 ± 0.3	1.13 ± 0.02	0.995

Effects of superheated steam for thermal shucking of tropical oyster

The effect of superheated steam temperature and time on the relaxation of the muscles, and degree of meat quality reflecting the effectiveness of thermal shucking were evaluated using response surface methodology. Besides, the meat quality, texture, and color of the shucked oysters were also evaluated to determine the raw-like properties of the treatment. All the responses were most suitably fitted with either a linear, two factor interaction or reduced quadratic model with adequacy and significance of the model evaluated by ANOVA as shown in Table 2. The adequacy and fitness of these final reduced models were sufficiently explained by acceptable correlation coefficient, R², adjusted R² and significant lack-of-fit test.

Table 2

ANOVA, F-value, p-value, lack of fit, and adjusted R²of the final reduced model for nine response variables of the superheated steam treatment.
Responses¹	Shucking quality²			Texture²			Color²
Responses¹	Relaxation	Degree of release	Meat quality	Hardness (N)	Gumminess (N)	Chewiness (mJ)	L*	a*	b*
Model	Quadratic	Quadratic	2FI	2FI	Linear	Quadratic	Quadratic	Linear	2FI
F-value	33.86	17.78	156.32	42.77	18.43	30.60	23.87	189.37	24.04
p-value	0.0003	0.0034	< 0.0001	< 0.0001	0.0010	0.0002	0.0017	< 0.0001	0.0005
A	62.02*	15.81*	80.37*	74.55*	30.46*	28.69*	24.75*	210.08*	16.42*
B	47.78*	44.10*	370.23*	40.89*	6.40*	17.63*	13.24*	168.66*	1.30
AB	5.81*	13.34*	18.36*	12.89*	-	-	56.00*	-	54.40*
A²	-	15.60*	-	-	-	45.49*	16.62*	-	-
B²	20.13*	1.55*	-	-	-	-	15.48*	-	-
Lack of fit	0.0517	0.7215	0.1439	0.1439	0.0663	0.3965	0.4349	0.0593	0.6781
Adjusted R²	0.9293	0.7519	0.9261	0.9261	0.7771	0.8819	0.9196	0.9741	0.7907

¹ Effects are statistically significant *p-value < 0.05.

² A: Temperature; B: Time.

Relaxation, degree of release, and meat quality

Shucking an oyster involves severing the adductor muscle from the valves, thus separating the shells of the oyster. Thermal shucking provides advantage to relax the oyster’s muscle and result in gaping to facilitate meat removal from inside the shells. Figure 2 shows response surface plot of relaxation values, degree of release and meat quality of tropical oysters as function of superheated steam treatment temperature and treatment time. These parameters are important to evaluate the easiness in shucking oysters. The muscle relaxation can be determined by giving score to the gaping between two halves of the tropical oysters. The relaxation value of 0 indicates no gapping and incremental values from 1, 2 or 3 rank the degree of gapping with 3 being fully gapped. Although high in variation, the relaxation values showed increment trend with the increase in the temperature and treatment time with maximum value at 1.5. Martin (2004) reported that heat treatment with 60 s of steam injection with 60 s of holding time on Crassostrea virginica resulted in 0.2 value of relaxation and did not show any trend with different steam injection treatment time and holding time. The superheated steam treatment resulted in higher values but also reflected similar observation of high variation in the values given by low Adjusted R² of the response surface model.

Other important factors that determine the effectiveness of superheated steam for thermal shucking are degree of release. The value of 1 in degree of release indicates a small degree of release of the adductor muscle while the value of 3 indicated the completely release of the adductor muscle. The release of adductor muscle will lead to the ease in shucking the oysters without causing cut or ‘bleeds’ in the oysters. Figure 2b shows the degree of release significantly fitted into quadratic model. By comparing the F-values, the treatment time had the greater impact on degree of release of the adductor muscle from the scars compared to the treatment temperature. Thus, prolong treatment time can resulted in similar degree of release for different superheated steam temperatures. Heat treatment stimulate the abdominal ganglion of oysters to relax the nerves causing the release of adductor muscle from the catch contraction (Namba et al., 1995). Superheated steam can facilitate rapid heating from its higher enthalpy compared to steam which increase heat transfer rate (Fang et al., 2022). The denaturation of protein and connective tissues can take place with heat treatment which leads to disruption of tertiary protein structure and gelatin transition causing the release of adductor muscle (Voisin, 2004).

The meat quality reflects the degree of freshness of the oysters. Based on visual observation, the overall appearance of the treated oyster meat was scored for sign of cooking from 1 to 3 with 1 being unacceptably cooked appearance and 3 being raw in comparison to untreated shucked oysters. The scoring opposite to Martin et al. (2007) was applied which provided better optimization configuration when overlayed. The meat quality significantly fitted into two-factor interaction model with greater effects shown by the treatment time compared to temperature as shown in Fig. 2c. Increase in superheated steam treatment time significantly reduced meat quality with higher effects of temperature at 6 min treatment time. The combination of low temperature (170°C) and time (4 min) resulted in the highest meat quality as expected. The meat quality is a crucial parameter to determine the success of a thermal shucking process as consumer prefer a ‘fresh’ and ‘raw’ oysters in terms of taste, texture and appearance (Martin, 2006).

Texture profile analysis (TPA)

The thermal treatment is expected to impart quality changes to the texture and color of the oyster meat. Figure 3 shows response surface and perturbation plots of three texture parameters recommended as indicators to compare the differences between fresh and treated muscle oysters, which are hardness, gumminess, and chewiness as function of the superheated stream temperature and time. Hardness can be defined as the ability of the oysters to maintain its own shape through the internal binding force which can indicate the firmness of the oyster muscles (Ma et al., 2021; Wang, 2015). Chewiness of oysters represents the tenderness of oysters where it can be defined as the energy required to disintegrate a solid food to a ready state of swallowing (Ma et al., 2021; Wang, 2015). Since oysters are semi-solid food samples, gumminess is also an important parameter where it can be defined as the force required to masticate the oyster muscles (Wang, 2015). The untreated tropical oysters were at 12.26 N, 0.85 N, and 0.07 mJ for hardness gumminess, and chewiness, respectively. These values were significantly lower compared to Crassostrea virginica muscles reported by Wang (2015) at 164.4 N, 88.0 N, and 65.5 J for hardness gumminess, and chewiness, respectively.

The hardness, gumminess, and chewiness were fitted into 2FI, linear, and reduced quadratic models, respectively. All texture parameters showed stronger influence of treatment temperature with one-, five-, and three-fold higher in F-value compared to time for hardness, gumminess, and chewiness, respectively (Table 2). The significant interaction effect between superheated steam treatment temperature and time was observed only on the hardness parameter as response surface shown (Fig. 3a). Increase in superheated steam temperature reduced hardness gumminess and chewiness. However, prolong superheated steam treatment showed opposite effects for these parameters except for hardness. For hardness, increase in time resulted in great reduction at low superheated steam temperature as the hardness were comparably low at high temperature treatments. The change of muscle texture is related to muscle moisture and denaturation of protein such as myofibrillar and sarcoplasmic proteins during heating leading to color and textural changes in oyster muscle (Cruz-Romero et al., 2008). According to Lekjing et al. (2017), higher temperatures caused a higher amount of protein denaturation which will lead to the softer the oyster tissues. A higher temperature of the superheated steam treatment might induce a faster protein denaturation which will lead to a more rapid textural changes where the protein denaturation rate can be increased by 600-fold for every increment of 10°C in the treatment temperature (Anglemer & Montgomery, 1976). On the other hand, the gumminess and chewiness increased significantly with increase in treatment time. This can be explained by the increase of elastic modulus of the muscle with treatment time causing the toughness of oyster meat and hence, the oysters become gummier (Chung et al., 2021; Llave et al., 2018).

Color

Color parameter is an important attribute to identify the freshness of the oysters as it represents the appearance of the oysters. L* values indicate the brightness of the oysters; a* values which is positive indicates the redness while a* values which is negative indicates the greenness of the oysters; b* values which is positive indicates the yellowness and b* values which is negative indicates the blueness of the oysters. The color of the fresh tropical oysters from Bakau Hijau estuary was at 67.03, 2.64, and 23.68, for L*, a* and b* values, respectively. Figure 4 shows the response surface plot of L*, a*, and b* values as function of superheated steam treatment temperature and time which significantly fitted into quadratic, linear, and 2FI models, respectively. The L* and a* values showed stronger influence of treatment temperature compared to time while b* values showed stronger influence of interaction of temperature and time. The F-value of temperature effect was one-fold higher than time for the L* and a* values while the F-value of interaction effect was three-fold higher than temperature and forty-two-fold higher than time for b*values. Increase in temperature and time significantly reduced L* values. Increase in temperature significantly increase a* and b* values. However, prolong superheated steam treatment showed opposite effects for these parameters.

For L* values, increase in time resulted in great reduction at high superheated steam temperature as the L* values were comparably higher at low temperature treatments. The results of L* parameter was in the agreement with the findings of Lekjing et al. (2017) where they had mentioned that the color parameter L* was decreasing with the increment of treatment temperature. The L* values of the oysters are usually improved by protein denaturation where opaque precipitates will be formed to mask the undesirable dark pigments where increasing in temperature could lead to higher rate of protein denaturation (Chung et al., 2021). On the other hand, the a* and b* values increased significantly with increase in treatment temperature. The color changes might be due to the lipid oxidation of the oyster muscles during heat treatment causing the release of free metal ions (Fe and Cu) from the muscles (Cruz-Romero et al., 2008). Lipid oxidation and Maillard reaction can impart negative effect to L* values forming dark color products (Chung et al., 2021; Lekjing et al., 2017). The changes of a* and b* values of the oysters are mainly due to the protein denaturation, especially sarcoplasmic and myofibrillar proteins (Chung et al., 2021; Cruz-Romero et al., 2007).

Numerical optimization and model verification

The superheated steam shucking was optimized with for maximum relaxation values, degree of release, meat quality, hardness, and lightness in color (L*) to obtain product which is easier to shuck but retaining the quality of the raw oysters. Figure 5 shows the graphical optimization demonstrating the overlay plot responses within the desired boundaries with the optimum area shaded in yellow. The optimization condition was selected at 170 °C and 5 minutes with predicted responses and model validation presented in Table 3 showing no significant differences (p > 0.05) between them, implying that the experimental values agreed with the predicted values at a 0.05 level. The shucking effectiveness and quality parameters of the optimized superheated steamed samples were compared against the untreated (control) and microwave treated samples as shown in Table 3.

Table 3

Predicted and experimental values of the responses for optimized superheated steam treatment compared to control and microwave treatment.
Variables	Control	Superheated steam treatment			Microwave treatment
Variables	Control	Predicted	Actual	p-value	Microwave treatment
Degree of relaxation	0 ± 0	0.51	0.5 ± 0.1	0.674	0 ± 0
Degree of release	0 ± 0	1.0	1.0 ± 0.5	1.000	0.6 ± 0.5
Meat quality	3.0 ± 0	2.18	2.3 ± 0.5	0.910	3.0 ± 0
Texture parameters
Hardness (N)	12.3 ± 0.4	13.1	13.1 ± 0.5	0.977	14.1 ± 0.9
Gumminess (N)	0.85 ± 0.3	0.79	0.72 ± 0.2	0.790	0.87 ± 0.4
Chewiness (mJ)	0.07 ± 0.01	0.07	0.06 ± 0.01	0.532	0.07 ± 0.02
Color parameter
L*	67.0 ± 2.3	70.7	69.5 ± 3.0	0.688	64.3 ± 3.5
a*	2.6 ± 0.2	1.1	1.1 ± 0.3	0.994	3.1 ± 0.2
b*	23.7 ± 1.0	20.4	21.4 ± 1.8	0.532	22.9 ± 2.2

The superheated steam treatment showed higher value of relaxation (0.51) and degree of release (1.0) compared to microwave treatment at 0 and 0.60 for relaxation value and degree of release, respectively. Moreover, the L* values of the superheated steam treated oysters (69.5) were higher compared to microwave treated oysters (64.31) which indicated brighter appearance as shown in supplementary Figure S1. However, the microwave treatment (3.00) showed a better meat quality than the superheated steam treatment (2.25) where the hardness of the microwave treated oysters possessed a higher value compared to the superheated steam treated oysters. When comparing with raw oysters, we can see that the superheated steam treatment aided in improving the degree of relaxation and degree of release but loosing on texture and color especially increase in L* values and significant reduction redness (a*) and yellowness (b*) which were better preserved by the microwave treatment.

Quality changes of shucked oysters during refrigerated storage

Total Plate Count

Figure 6a illustrates the effect of SS shucking treatment compared to microwave treatment and untreated oysters on the survival and growth of bacteria during refrigerated storage of the shucked oysters measured by total plate count (TPC). For the initial counts on day zero, both treatments showed equivalent counts with the control at 4.2x10³, 4.3x10³ and 5.1x10³ CFU/g for SS, microwave and control, respectively. The bacterial loads vary depending on the age of the oysters, time and location of the harvest. The TPC of Crassostrea iredalei harvested from the same farm in Sungai Merbok estuary, Kedah, Malaysia throughout different monsoon of the year reported range from 5.2x10³ to 1.3x10⁵ CFU/g and absent of Escherichia coli depending on the tide and raining monsoon.

After five days of storage, the untreated and microwave treated samples already significantly tripled in levels of bacteria (p < 0.05) to 1.5x10⁴ and 1.2x10⁴ CFU/g, respectively while the increment in SS sample was not significant. The TPC of the untreated and microwave treated samples gradually increased along 20 days storage to final count at 2.4x10⁴ and 1.7x10⁴ CFU/g, respectively, which were 2 and 1.3-fold higher than the SS treated samples, although the microwave treated sample was significantly lower compared to the untreated sample. The SS treatment showed lowest TPC among the samples with significant increment showed only after day 14 to 1.1x10⁴ CFU/g which was significantly lower than the bacteria count in the microwave treated samples at day 5. Thus, the SS treatment is more efficient in the reduction of microbial load and extend the shelf life of refrigerated shucked tropical oysters by 10 days.

Mild heat treatments have shown an ability to reduce bacteria in shellfish while maintaining an essentially raw product. Martin et al. (2007) studied the application of high steam injection with and without pre-heating and holding prior to ice water immersion with 85% muscle release of raw like oyster meat reported reduction in TPC not greater than one log difference from the untreated samples after 14 days storage at 2 ⁰C. Andrews et al. (2000) noted that the application of pasteurization at 50 ℃ for 0 to 15 min on the oysters which stored at chilled condition for 14 days had an inconsistent trend on TPC within 2 logs. Chung et al. (2021) reported longer pasteurization (50 ℃) of oysters to 20 min with lower fluctuation of TPC between 50 to 2.3x10⁴ CFU/g for 14 days refrigerated storage. When comparing with other studies, the SS treatment is efficient to reduce the microbial load of the shucked oysters during refrigerated storage up to 20 days.

Total volatile basic nitrogen (TVB-N)

Figure 6b shows the trend of total volatile basic nitrogen (TVB-N) of untreated and treated shucked oysters comparing superheated steam and microwave treatments during 20 days of refrigerated storage. At day 0, the TVB-N were significantly influenced by the thermal treatment with lowest value in SS sample followed by microwave and untreated sample at 11.65, 15.73, and 20.98 mg N/100 g. The TVB-N values gradually increased during storage periods with the SS treated samples remained lowest. Drastic increment in TVB-N values of microwave treated sample can be seen at day 5 which paralleled with the increase in microbial counts which finally reaching beyond acceptable limit of 30 mg N/100 g. TVB-N is a common parameter to measure the post-mortem decomposition on both protein and non-protein nitrogenous compound from the degradation caused by the microbial activity and endogenous proteolytic enzymes (Ruiz-Capillas & Moral, 2005; Tantratian & Kaephen, 2020).

Chung et al. (2021) reported that the Akoya oysters with treatment of pasteurization at 50 ℃ for 5 to 10 min showed TVB-N values below 24 mg N/100 g with elevation of values for 14 storage days. Min et al. (2020) and Songsaeng et al. (2010) showed the same trend of TVB-N values in Crassostrea belcheri and Crassostrea gigas during chilling storage (Chung et al., 2021). A study conducted by Cao et al. (2009) reported that the pacific oyster possessed 53.33 mg N/100 g of TVB-N after 18 storages days at 4 ℃.

pH

Figure 6c shows the pH changes of untreated and treated shucked oysters comparing SS with microwave treatment during 20 days of refrigerated storage. The pH of freshly treated samples was at 6.5 for the control and microwave treatment, which is within the range of pH values for freshly shucked oysters (generally between 6.2 and 6.6) (Chung et al., 2021). The freshly treated SS sample was significantly higher at pH 6.6 at day 0. During heating, protein in oysters unfolds causing the number of acidic groups decrease where it will cause an increase in pH from the changes in free carbonyl and amino groups (Cruz-Romero et al., 2007). Both untreated and microwave treated samples fell between 5.9 and 6.0 in 20 days with significant reduction to pH 6.2 started in day 5 indicating the degradation in the quality of oysters (Cruz-Romero et al., 2007). On the other hand, the SS treated sample showed significant dropped in pH in day 11 and remained at pH 6.4 until day 20 which may explain drastic increase on the TPC value at day 11 (Fig. 6a).

A pH value above 6.0 in oysters is indicative of good quality of fresh oysters while those with pH lower than 5.0 is already decomposed (Cook, 1991). The accumulation of organic acids such as lactic and pyruvic acid as a result of post-mortem glycolysis and the degradation of proteins and nucleotides causing the reduction of pH value (Chung et al., 2021; Songsaeng et al., 2010). This suggests that the SS treatment considered to preserve the quality of shucked tropical oysters during refrigerated storage with minimal organic acids presented. Moreover, inorganic salt in oyster liquor can affect the solubility of myofibrillar protein and provide volatile bases that delay the reduction of pH during storage (Chung et al., 2021).

Texture profile analysis

The changes in texture of oysters were mainly due to the changes of pH and number of bacteria where the degradation of muscles occur due to the autolysis enzymes from spoilage bacteria and oyster tissues (Tantratian & Kaephen, 2020). Figure 7 shows the changes of texture properties of the superheated steam and microwave treated shucked oysters compared to the untreated samples during 20 days of refrigerated storage. The hardness of the oyster meat showed slight reduction but no significant changes during the storage period for all samples as shown in Fig. 7a. On the other hand, the gumminess and chewiness significantly reduced with apparent observation at day 10 for the superheated steam and microwave treated samples. The control sample started showing significant changes at day 5 for chewiness as shown in Fig. 7c.

The decrease in texture might be due to disintegration of connective tissue causing the fragment of muscle occurs (Berthelin et al., 2000; Chung et al., 2021; Hyldig & Nielsen, 2007; Kong et al., 2007). The force required is reduced due to the decomposition structure in the oyster tissues where softening is not a desirable parameter when consuming oysters (Chung et al., 2021; Lekjing et al., 2017). Other studies such as He et al. (2002) and Songsaeng et al. (2010) reported that the oysters possessed softening attributes when there was increment in storage time and this showed the similar trend with the current findings. However, on the contrary, Chung et al. (2021) reported that the firmness of Akoya oyster muscle tissue increased during 14 storage days. The contradict results might be due to the different oyster species where the chemical changes such as pH, interaction with salt, structural changes of macronutrients or effect of treatment methods (Chung et al., 2021).

Color

The changes in color of oysters were mainly due to the changes of TVB-N which is the indication of protein degradation (Tantratian & Kaephen, 2020). Figure 8 shows the changes of color properties (L*, a*, and b*) of the superheated steam and microwave treated shucked oysters compared to the untreated samples during 20 days of refrigerated storage. There was no significant difference in L* values throughout 20 days storage while the a* and b* values increased gradually which indicated increasing in redness and in yellowness, respectively. Drastic increase in a* value of the superheated steam sample on day 10 may reflects the changes observed on the TPC, TVB-N and pH. The increase in a* values was contradicted with the findings of Chung et al. (2021) and Lekjing et al. (2017) where both the findings stated that the a* values showed decreasing trend throughout the storage time. The contradict results is reasonable as the color changes are due to the mixed complex reactions where the chemical reactions would occur at different rate (Chung et al., 2021).

On the other hand, for b* values, it showed the similar result with the other findings where the b* values was in an increasing trend during storage (Chung et al., 2021; Lekjing et al., 2017). However, Plaza and Gabriel (2008) found that the application of mild thermo-treatment on the tropical oysters affect the b* values in decreasing trend. The contradict results of b* values with other studies are reasonable as b* values are normally based on the composition, sugar, amino acid, temperature, pH, and trace minerals (Chung et al., 2021; Lekjing et al., 2017). According to Chung et al. (2021), yellowness indicates the decline in quality of the oysters where the increase in b* values of the oysters showed the decline in quality of oysters during chilled storage. Lipid oxidation will also occur during heating as highly unsaturated carotenoids such as astaxanthin will be degraded which leads to color loss in oyster (Cruz-Romero et al., 2008). The use of superheated steam results in decreased oxidation losses and better product quality in terms of color, shrinkage, and rehydration characteristics (Fang et al., 2022).

This study describes method of thermal shucking of tropical oysters using superheated steam to cause a relaxation of the adductor muscle which facilitates the shucking process. The superheated steam thermal treatment caused rapid temperature increase and heat loss from the muscle and shell, resulting in superior relaxation and degree of release compared to conventional steam. The optimal shucking regimes was identified at 170 ℃ at 5 min that maximize degree of release while maintaining highest meat quality of the shucked tropical oysters. Texture of the superheated steamed oyster meat was firmer, and the appearance was brighter compared to the untreated and microwave treated oysters. Considering minimal change in meat quality, the superheated steam was superior in the preservation towards microbial, chemical and physical changes of the shucked product during refrigerated storage compared to the microwave treatment and untreated samples. Thus, the superheated steam treatment is promising method of thermal shucking of oysters for effectiveness and maintenance of a near raw oyster with modest reduction in microbial content. However, this thermal technique must be replicated for multiple batches of oysters originating from diverse regions or exhibiting significant variations in size and shell thickness, prior to its application in the enhancement of shucking lines for tropical oysters.

Acknowledgments

Authors greatly acknowledge the support by Division of Industry & Community Network, University Sains Malaysia (USM) for the community engagement with local oyster farms for oysters sampling.

Author Contributions

Wei Ping Cheng: investigation, formal analysis, writing–original draft; Azim Patar: writing– review; Yong Foo Wong: writing– review, resources; Siti Balqis Zulfigar: resources, writing–review; Chengchu Liu: conceptualization, writing–review; Musfirah Zulkurnain: conceptualization, writing–review and editing, funding acquisition, resources, supervision.

Funding

The work has been funded by the University Sains Malaysia through APEX ERA Grant [1001/PTEKIND/881001] granted to M.Z. which is gratefully acknowledged.

Data Availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

Compliance with Ethical Standards

Conflicts of Interest

The Authors declare that there is no conflict of interest.

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Competing interest reported. The work has been funded by the University Sains Malaysia through APEX ERA Grant [1001/PTEKIND/881001] granted to Musfirah Zulkurnain which is gratefully acknowledged.

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Effects of Superheated Steam Pretreatment on Muscle Release and Meat Quality of Shucked Tropical Oyster (Crassostrea iredalei)

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Abstract

Figures

Introduction

Materials and Methods

Materials

Thermal shucking methods

Superheated steam shucking

Experimental design

Microwave treatment

Determination of relaxation, degree of release and meat quality

Quality evaluation of shucked oysters

Texture profile analysis

Color measurement

Storage study of refrigerated shucked oysters

Total plate count (TPC)

pH analysis

Total volatile basic nitrogen (TVB-N)

Statistical analysis

Results and Discussion

Thermal profile of oysters during superheated steam treatment

Effects of superheated steam for thermal shucking of tropical oyster

Relaxation, degree of release, and meat quality

Texture profile analysis (TPA)

Color

Numerical optimization and model verification

Quality changes of shucked oysters during refrigerated storage

Total Plate Count

Total volatile basic nitrogen (TVB-N)

pH

Texture profile analysis

Color

Conclusion

Declarations

References

Additional Declarations

Supplementary Files

Status:

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