Introduction
Flavor and tenderness are two significant drivers of consumer eating satisfaction of beef (Savell et al., 1987; Miller et al., 2001; Killinger et al., 2004; Behrends et al., 2005a, 2005b). Although the National Beef Tenderness Surveys have reported no significant increase in the tenderness of beef steaks after 2006, inconsistent tenderness has been identified as a major quality issue by purveyors, restaurateurs, and supermarkets (Smith et al., 2006; Voges et al., 2007; Igo et al., 2015; Martinez et al., 2017).
Electrical stimulation (ES) is one of the postharvest intervention strategies that can improve tenderness in beef (Savell et al., 1978a; McKeith et al., 1981; Roeber et al., 2000). ES also enhances lean color, texture, and lean maturity of beef carcasses (Savell et al., 1978a; Cross, 1979; Roeber et al., 2000). Improvement in tenderness with ES has been attributed to increased adenosine triphosphate (ATP) metabolism and prevention of sarcomere shortening during carcass chilling (Gilbert and Davey, 1976; Agbeniga and Webb, 2021). Moreover, the contractile forces during ES can damage cellular integrity and liberate calcium from the sarcoplasmic reticulum, which can activate the calpain system to enhance the postmortem tenderization process (Ducastaing et al., 1985; Uytterhaegen et al., 1992).
The voltage used for ES can vary among different commercial beef processing facilities ranging from voltage as high as 450 to 500 V to very low voltages (40 to 45 V). In general, most large-scale commercial beef processing facilities in the United States utilize low- to medium-voltage ES. Previous research has reported that either high- or low-voltage ES can improve beef tenderness, with the greatest improvement observed in high-voltage ES carcasses (Savell, 1985). However, the effect of commercially implemented ES voltages on beef quality has not been evaluated yet. Therefore, the objective of the current study was to evaluate the effect of different voltage levels of ES on beef longissimus muscle (LM) tenderness.
Materials and Methods
Experimental design and treatments
Beef carcasses (N = 270) were selected from 3 commercial plants located in Nebraska, Colorado, and Texas (90 beef carcasses per plant) at the time of slaughter. Within a carcass, paired sides were assigned to one of 3 treatment combinations, resulting in 180 replicates per treatment: (1) control and ES level 1 (ES1); (2) control and ES level 2 (ES2); or (3) ES1 and ES2. For this study, controls had no ES; ES1 had voltages of 16, 20, 24, and 28 V for 17 s each; and ES2 had voltages of 25, 35, 45, and 55 V for 17 s each immediately following the carcass hot water wash, approximately 30 min postmortem, just before carcass chilling. All carcasses traveled through these 4 zones (17 s in each zone) of 60-Hz ES in the commercial processing facilities, immediately after which the carcasses were spray-chilled for the first 8 h of the chill period.
Temperature and pH measurement
Internal temperature and pH of the LM were measured immediately following ES, at 3 h postmortem, and at the time of grading (between 36 and 48 h postmortem depending on the standard practice for the plant) using a Type K thermocouple (Model 34040, Atkins Technical, Inc., Gainesville, FL) and a portable pH meter (Model HI 99161, Hanna Instruments, Woonsocket, RI). Temperature and pH of LM were measured at the approximate geometric center of the LM, immediately posterior to the lumbar vertebra of the 13th rib.
Carcass yield grade and color data
Upon the conclusion of 36- to 48-h chilling, the carcasses were ribbed and graded. Marbling score, skeletal maturity, and lean maturity were determined by a USDA grader. Preliminary yield grade (PYG), adjusted PYG, and LM area (LMA) were determined by trained Colorado State University personnel. In addition, adjusted hot carcass weight (HCW) and percentage kidney, pelvic, and heart (KPH) fat were also recorded. The LM lean and external fat color were measured at the 12th and 13th rib interface for each side following proper bloom time, using a portable spectrophotometer equipped with a 6-mm aperture (MiniScan XE; Hunter Associates Laboratory, Reston, VA) following the standardization procedures outlined for the spectrophotometer (illuminant A and 10° standard observer). Three individual color measurements were averaged to obtain a single value for instrumental lightness (L*), redness (a*), and yellowness (b*).
Sample collection and tenderness measurement
LM sections (5.08 cm) removed from the anterior end of the strip loins (Institutional Meat Purchase Specifications #180) were vacuum packaged and transported on ice to the Colorado State University Meat Laboratory, after which they were aged for 14 d (−1°C). After aging (never frozen), samples were fabricated to 2.54-cm-thick steaks for slice shear force (SSF) measurement. The steaks were stored at 2°C to ensure that precooking internal temperatures were between 1°C and 5°C. Steaks were cooked on electric grills (George Forman Grilling Machine GRP90WGP, Salton Inc., Lake Forest, IL) to an internal temperature of 70°C. Peak internal temperature measurements were recorded from the geometric center of each steak using a Type K thermocouple (model 34040, Atkins Technical, Inc.).
SSF measurement was conducted immediately after the postcooking measurements were complete using the shear force protocol by Shackelford et al. (1999). Briefly, a 1-cm-thick, 5-cm-long slice was removed from each cooked steak parallel to the longitudinal orientation of the muscle fibers and then sheared perpendicular to the muscle fiber orientation using a universal testing machine (model 4443, Instron, Norwood, MA) equipped with a flat, blunt-end blade. A single peak SSF measurement was recorded for each steak.
Statistical analysis
A balanced incomplete block design was utilized to determine the effect of differing voltages of ES on beef LM tenderness, postmortem temperature and pH decline, and carcass quality with individual carcass serving as the block.
Data for SSF values, carcass characteristics, and temperature and pH decline rate were analyzed using the MIXED procedure of SAS (SAS Institute, Cary, NC) with the individual side serving as the experimental unit. Data for pH and temperature were analyzed as repeated measures using the SAS MIXED procedure. Carcass identification was included as a random variable for one-time measurements. Whole carcass identification and side identification within the whole carcass were included as a random variable for repeated measures (pH and temperature data). For all analyses, the Kenward-Roger approximation was used to calculate denominator degrees of freedom, and least-squares means were separated using the PDIFF option at a significance level of P < 0.05.
Results
Carcass characteristics, longissimus muscle color, and subcutaneous fat color
There was no treatment × plant interaction (P > 0.05) for carcass characteristics. Furthermore, the voltage setting of ES did not influence (P > 0.05) HCW, PYG, LMA, KPH, fat L*, or fat a* measurements (Table 1). However, lean a* measurements were affected by the treatment, with ES carcass sides (both ES1 and ES2) having greater redness compared with controls (Table 1; P > 0.05).
Least-squares means and standard error of the mean (SEM) for carcass characteristics corresponding to the main effect of electrical stimulation (ES) treatment1
| ES Treatment | |||||
|---|---|---|---|---|---|
| Trait | Control1 | ES1 | ES2 | SEM | P Value |
| Hot Carcass Weight, kg | 357 | 360 | 360 | 53 | 0.326 |
| Adjusted Preliminary Yield Grade | 3.24 | 3.26 | 3.26 | 0.03 | 0.440 |
| Longissimus Muscle Area, in2 | 13.30 | 13.36 | 13.30 | 0.10 | 0.574 |
| Kidney, Pelvic, and Heart Fat % | 2.20 | 2.20 | 2.20 | 0.02 | 0.804 |
| Lean CIE Redness (a*) | 10.71b | 11.06a | 11.27a | 0.16 | <0.001 |
| Fat CIE Lightness (L*) | 68.46 | 68.21 | 67.96 | 0.30 | 0.312 |
| Fat CIE Redness (a*) | 0.14 | 0.14 | −0.01 | 0.10 | 0.184 |
Control = no ES; ES1 = 16, 20, 24, and 28 V for 17 s each; ES2 = 25, 35, 45, and 55 V for 17 s each.
ES treatment × plant interaction is presented in Table 3 for lean Commission Internationale de l´Eclairage (CIE) L* and b* and fat CIE b*.
Means in the same row without a common superscript differ (P < 0.05).
Least-squares means summarizing the effect of the plant on carcass characteristics are presented in Table 2. There was no difference in HCW among the plants (P > 0.05). Carcasses in Plants A and C were not different in adjusted PYG estimates (P > 0.05), whereas carcasses in Plant B were leaner (P < 0.05). Carcasses in Plant C had greater (P < 0.05) LMA than carcasses in Plant B, whereas carcasses in Plant A were intermediary, having similar (P > 0.05) LMA to both Plants B and C. Carcasses from Plant C had the least (P < 0.05) KPH, whereas carcasses from Plants A and B were not different (P > 0.05) in KPH percentages.
Least-squares means and standard error of the mean (SEM) for carcass characteristics corresponding to the main effect of plant
| Plant | |||||
|---|---|---|---|---|---|
| Trait | A | B | C | SEM | P Value |
| Hot Carcass Weight, kg | 363 | 363 | 361 | 34 | 0.362 |
| Adjusted Preliminary Yield Grade | 3.30a | 3.15b | 3.32a | 0.05 | 0.011 |
| Longissimus Muscle Area, in1 | 13.44ab | 13.01b | 13.52a | 0.16 | 0.048 |
| Kidney, Pelvic, and Heart Fat % | 2.23a | 2.31a | 2.05b | 0.05 | <0.001 |
| Lean CIE Redness (a*) | 11.52a | 10.81b | 10.73b | 0.24 | 0.039 |
| Fat CIE Lightness (L*) | 68.44b | 69.81a | 66.37c | 0.41 | <0.001 |
| Fat CIE Redness (a*) | 0.61a | −0.59b | 0.25a | 0.14 | <0.001 |
Electrical stimulation treatment × plant interaction is presented in Table 3 for lean Commission Internationale de l´Eclairage (CIE) L* and b* and fat CIE b*.
Means in the same row without a common superscript differ (P < 0.05).
There was a treatment × plant interaction for marbling scores, overall maturity, lean Commission Internationale de l´Eclairage (CIE) L*, lean CIE b*, and fat CIE b* (Table 3). ES did not influence (P > 0.05) marbling scores in Plants A and B, whereas in Plant C, carcasses receiving ES2 had higher (P < 0.05) mean marbling scores compared with controls. There was also a difference (P < 0.05) in marbling scores in Plant C, where carcasses treated with ES2 had greater (P < 0.05) marbling scores compared with control carcasses. Carcasses treated with ES1 were not different (P > 0.05) from both control and ES2 carcasses for marbling scores in Plant C. Both Plants A and B were not different in marbling scores (P > 0.05) across ES treatments. Additionally, Plants A and B showed no differences (P > 0.05) between ES treatments for overall maturity, whereas control carcasses in Plant C had greater (P < 0.05) maturity scores than both ES treatments.
Least-squares means and standard error of the mean (SEM) for carcass characteristics corresponding to the electrical stimulation (ES) treatment1 × plant interaction
| Plant A | Plant B | Plant C | |||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|
| Trait | Control1 | ES11 | ES21 | Control1 | ES11 | ES21 | Control1 | ES11 | ES21 | SEM | P Value |
| Marbling Score2 | 399 | 406 | 406 | 456 | 451 | 449 | 336b | 346ab | 352a | 9.39 | 0.043 |
| Overall Maturity3 | 174 | 173 | 172 | 166 | 165 | 168 | 172a | 169b | 167b | 2.65 | 0.026 |
| Lean CIE L* | 35.55b | 37.27a | 37.04a | 37.85b | 39.01a | 37.35b | 36.24 | 36.74 | 36.44 | 0.45 | 0.027 |
| Lean CIE b* | 11.51b | 12.24a | 12.61a | 11.56 | 12.16 | 11.84 | 10.75b | 11.39a | 11.01ab | 0.26 | 0.015 |
| Fat CIE b* | 6.87 | 6.94 | 6.63 | 6.75b | 7.53a | 6.31c | 5.88 | 5.77 | 5.77 | 0.23 | 0.002 |
Control = no ES; ES1 = 16, 20, 24, and 28 V for 17 s each; ES2 = 25, 35, 45, and 55 V for 17 s each.
Slight = 300 to 399; small = 400 to 499; modest = 500 to 599.
“A” maturity = 100 to 199.
Means in the same row, within a plant, without a common superscript differ (P < 0.05).
CIE = Commission Internationale de l´Eclairage.
In Plant A, carcasses receiving ES1 and ES2 had higher (P < 0.05) lean L* values than controls (Table 3). In Plant B, carcasses receiving ES1 produced the highest (P < 0.05) lean L* values. The ES did not affect (P > 0.05) lean L* values in the Plant C facility. Carcasses from Plant A, regardless of ES stimulation level, had greater (P > 0.05) b* values than control carcasses. Additionally, carcasses from Plant C that received ES1 had greater (P < 0.05) lean b* values than control carcasses, with ES2 carcasses being similar (P > 0.05) to both. There were no differences (P > 0.05) in fat b* values between ES treatments for Plants A and C. Carcasses treated with ES1 in Plant B had the greatest (P < 0.05) fat b* values, with ES2 carcasses’ fat b* values being the least (P < 0.05).
Temperature and pH
There was a treatment × plant × time interaction (P < 0.0001) for temperature, pH, and the rate of pH decline (Table 4). Control carcasses had greater pH (P < 0.05) than ES2 carcasses in all 3 plants immediately following ES. At 3 h postmortem, the effect of ES on pH was evident (P < 0.05) in Plants A and B, where the pH of control carcasses was greater (P < 0.05) than both ES carcass treatments. However, there was no difference (P > 0.05) in pH between the treatments at 3 h in Plant C. The ultimate pH collected at the time of grading was not affected by ES (P > 0.05) in any of the plants. In Plants A and B, control carcasses had slower (P < 0.05) rates of pH decline than carcasses receiving ES1 and ES2 treatments. However, this difference was not observed (P > 0.05) in Plant C, where control and ES2 exhibited a similar (P < 0.05) rate of pH decline. Additionally, the temperature at ES, at 3 h postmortem, and at grading was not influenced (P > 0.05) by the treatments or plants.
Least-squares means for pH and temperature of carcass at each time point, and rate of pH decline (pH units/h) of carcass corresponding to the electrical stimulation (ES) treatment1 × plant × time interaction (P < 0.0001)
| Plant A | Plant B | Plant C | ||||||||
|---|---|---|---|---|---|---|---|---|---|---|
| Time | Control1 | ES11 | ES21 | Control1 | ES11 | ES21 | Control1 | ES11 | ES21 | |
| pH | ES2 | 6.82a | 6.75ab | 6.72b | 6.93a | 6.73b | 6.73b | 6.70a | 6.73a | 6.59b |
| 3 h3 | 6.38a | 6.14b | 6.15b | 6.32a | 6.02b | 5.88c | 6.02 | 5.93 | 5.98 | |
| Grade4 | 5.34 | 5.31 | 5.31 | 5.27a | 5.24b | 5.25ab | 5.35 | 5.35 | 5.35 | |
| pH Decline Rate | ES to 3 h | −0.134a | −0.201b | −0.185b | −0.195a | −0.225b | −0.271c | −0.207a | −0.250b | −0.181a |
| 3 h to grade | −0.018 | −0.008 | −0.013 | −0.026 | −0.017 | −0.010 | −0.011 | −0.007 | −0.008 | |
| ES to grade | −0.025 | −0.010 | −0.023 | −0.040 | −0.034 | −0.032 | −0.024 | −0.024 | −0.020 | |
| Temperature, °C | ES | 41.4 | 41.0 | 41.3 | 40.1 | 40.5 | 40.6 | 41.4 | 41.2 | 40.8 |
| 3 h | 31.5 | 31.6 | 32.0 | 29.8 | 29.6 | 30.1 | 30.0 | 29.8 | 29.7 | |
| Grade | 1.2 | 1.2 | 1.2 | 3.0 | 3.0 | 2.8 | 0.2 | 0.3 | 0.3 | |
Control = no ES; ES1 = 16, 20, 24, and 28 V for 17 s each; ES2 = 25, 35, 45, and 55 V for 17 s each.
Time “ES” is immediately following application of ES.
Time “3 h” is 3 h ± 10 min postmortem.
Time “Grade” is at the time of grading (between 36 and 48 h postmortem).
Means in the same row, within a plant, without a common superscript differ (P < 0.05).
Longissimus tenderness
There was no ES × plant interaction for SSF values (P > 0.05). However, tenderness was influenced by the ES and the processing plant (P < 0.05). Irrespective of the voltage setting, ES decreased (P < 0.05) the SSF values compared with the controls (Table 5). Additionally, Plant C had the greatest (P < 0.05) SSF values (Table 6).
Least-squares means and standard error of the mean (SEM) for the effect of electrical stimulation (ES) treatment on slice shear force (SSF)
| Treatments1 | |||||
|---|---|---|---|---|---|
| Control | ES11 | ES21 | SEM | P Value | |
| SSF, kg | 22.88a | 20.60b | 20.13b | 0.47 | <0.001 |
Control = no ES; ES1 = 16, 20, 24, and 28 V for 17 s each; ES2 = 25, 35, 45, and 55 V for 17 s each.
Means in the same row without a common superscript differ (P < 0.05).
Discussion
Carcass quality characteristics
In the current study, there was no difference in marbling score between the control and ES carcasses at 36 to 48 h postmortem in 2 of the 3 plants. However, in Plant C, there was an increase in marbling score as ES increased. The results from Plant C are supported by Savell et al. (1978a, 1978b), who reported that ES could affect marbling scores because of the earlier “setting up” of the intramuscular fat in LM. In addition, Calkins et al. (1980) also reported higher-quality grades associated with ES carcasses. On the other hand, results from Plants A and B are supported by a later study by Savell (1985), in which the differences in marbling scores between ES and non-ES sides were negligible after chilling for more than 48 h postmortem. The variation among plants could be associated with the 12-h spread in chilling times prior to grading among the plants.
Lean color is one of the quality attributes associated with fresh beef and plays a key role in consumer purchasing decisions and USDA quality grades (Killinger et al., 2004; Ramanathan et al., 2020). In addition to marbling, lean color accounts for a portion of the overall quality grade in the United States. Lean maturity of beef is determined in part by anterior LM color (Wulf and Wise, 1999). Therefore, objective color measurement (L*, a*, and b*) of LM served as a more consistent indicator of actual differences among treatments and plants. Previous studies reported that application of ES resulted in the appearance of more youthfulness of lean, more desirability of overall maturity scores, and improved CIE L*, a*, and b* values of lean color compared with the controls (McKeith et al., 1981; Tatum et al., 1999; Roeber et al., 2000; McKenna et al., 2004; Nazli et al., 2010; Agbeniga and Webb, 2021). This is relatively consistent with the findings of this study, as carcasses receiving ES had a redder lean color compared with control carcasses. This reinforces the hypothesis that ES can improve the color of beef steaks, and, more notably, this is still demonstrated at lower voltages used in this study.
Temperature and pH
In the current study, the treatment × plant × time interaction for temperature, pH, and their rate of decline indicated that the 3 ES treatments produced differing effects on these parameters depending on the plant in which the carcass was processed and the time of measurement. Control carcasses had a higher pH compared with carcasses treated with ES2 immediately after stimulation, but there was no difference in final pH among treatments in 2 of the 3 plants in the study. ES causes the acceleration of glycolysis, which leads to a more rapid pH decline. Similar results were reported in multiple prior studies in which a more rapid pH decline with varying voltage settings was observed (Uytterhaegen et al., 1992; Hwang and Thompson, 2001; Zhang et al., 2019; Ji et al., 2021). Unlike other studies (Uytterhaegen et al., 1992; Hwang and Thompson, 2001), which reported an initial increase in temperature after ES as glycolysis began to accelerate, there was no temperature difference at any of the time points measured in this study regardless of plant. This lack of difference in temperature could be attributed to different applications and voltages used in each study. Hwang and Thompson (2001) used a similar voltage to the current study (45 V, 10 ms on and 12 ms off at 36 pulses per second), but Uytterhaegen et al. (1992) used a much higher voltage for a much longer period of time (600 V for 120 s).
Longissimus tenderness
ES is employed in the beef industry to help reduce the incidence of cold shortening, which can negatively impact tenderness. Cold shortening occurs when the muscles are rapidly chilled prior to the onset of rigor mortis. ES prevents cold shortening by accelerated glycolysis and pH decline, ultimately causing an early onset of rigor mortis (Swatland, 1981). In addition to accelerating the glycolysis, ES could cause damage to the ultrastructure of the muscle, aiding in the further breakdown of the muscle during aging, ultimately increasing tenderness (Dransfield, 1994; Zhang et al., 2019).
Our results are in agreement with previous studies that also reported that ES improved tenderness of beef steaks (Savell et al., 1978a; Tatum et al., 1999; Roeber et al., 2000; Simmons et al., 2008; Aalhus et al., 2011; Zhang et al., 2019). However, our results indicated that voltage settings (ES1 vs. ES2) used in this study did not impact tenderness. Additionally, the SSF values varied among plants from which the LM steaks were collected. Steaks from Plant C had the greatest toughness, whereas steaks from Plants A and B exhibited similar SSF values. The tenderness difference among plants could be due to biological variation in cattle sourced for different plants as well as the minor variations in the chilling practices. In partial support, there were minor variations in the pH decline rates among the plants. The rapid pH decline along with slow chilling could adversely affect tenderness because of potential heat shortening of sarcomeres (Takahashi et al., 1987).
Conclusions
Regardless of the voltage settings, ES steaks had lower SSF values compared with control steaks. However, the lack of difference in postmortem tenderness between the voltage settings used in this study indicated that there was no additional value in increasing the ES voltage at low levels. Moreover, the variation in tenderness among plants indicated that the ES setting might need to be standardized for each plant depending on the cattle source and chiller settings in order to achieve consistent quality improvements.
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