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276.
S P E C I F I C B I O P H Y S I C A L F E A T U R E S OF POST-MORTEM CHANGES I N P O R C I N E MUSCLE
JOHN D. S I N K
The r a t e and extent of the post-mortem changes t h a t occur i n the transformation of muscle t o meat r e f l e c t many underlying, complex physico- chemic a1 in t e rac t ions/ t en s i on s . influence meat qual i ty and thus contribute t o the acceptance of meat as a food.
The s e b i olog i c al/ph y s iologic a 1 a l t e r at i ons
One of t he major problems t h a t has confronted meat s c i e n t i s t s and technologists i s the var ia t ion i n raw materials. Although various ante-mortem and post-mortem fac to r s have been studied, more def in i t ive information i s needed. phenomena, the e f fec t ive control of meat qua l i ty w i l l indeed be hard t o achieve.
Unti l we f u l l y understand these basic biological
The most important of the post-mortem changes t h a t occur i n muscle t i s s u e a re those associated with the process of r igor mortis. The usual review papers (Bate-Smith, 1948; Whitaker, 1959; Bendall, 1960a; Lawrie, 1962), considering these post-mortem changes and t h e i r subsequent effect on the various muscle properties, have concerned themselves primarily with describing the nature of the underlying biochemical changes.
This paper w i l l attempt t o present specif ic biophysical fea tures of the various post-mortem changes t h a t occur i n muscle t issue-- and more specif ical ly , those t h a t occur i n porcine muscle t i s sue .
The Post-Mortem Biophysical Changes
The general aspects of post-mortem biophysical changes i n muscle t i s s u e a re outlined i n Figure 1. A s a consequence of c i rcu la tory f a i l u r e or exsanguination, t he thermodynamic equilibrium, charac te r i s t ic of t he ac t ive i n -- vivo s t a t e of muscle, i s destroyed. With the depriva- t i o n of oxygen, the oxidation-reduction poten t ia l drops and the aerobic production of energy f o r the various metabolic processes ul t imately ceases. A s a re su l t of t h i s interrupt ion i n the metabolic i n t e g r i t y of muscle, the a b i l i t y t o maintain: (2) an isothermal environment, (3) an osmotic and vapor pressure equilibrium, and (4) the appropriate and necessary ion concentrations, i s rapidly l o s t .
(1) a d i f f e r e n t i a l l y permeable and polarized membrane,
'National Science Foundation Postdoctoral Fellow, 1964-65 a t The University of Wisconsin.
277.
Figure 1. Post-Modem Biophysical Changes in Muscle
Exsanguination
Thermodynamic equilibrium de st royed
Oxidation-Reduction potential drops
Thermal equilibrium
__ equilibrium , destroyed
4;/ , Viscoelasticity <
changes
\I
E x t ensibility/Ekcitabilit y decreases / .
,
278.
Further, ac t in and myosin, normally prevented from associating by relaxing fac tor and e l ec t ros t a t i c forces, now begin t o unite, a s t he muscle contracts, t o form the more insoluble, gel- l ike actomyosin complex. Thus, a l l these changes r e s u l t i n a decrease i n the ex tens ib i l i t y and e x c i t a b i l i t y of muscle t i s s u e which eventually lead t o the charac te r i s t ic r igor mortis condition. O f these many complex biophysical phenomena, four w i l l be discussed i n t h i s paper, namely, ex tens ib i l i ty , exc i tab i l i ty , c o n t r a c t i l i t y and v iscoe las t ic i ty .
Extensibi l i ty Changes. Although the study of the extensible propert ies of matter can be t raced t o the ear ly work of Galileo Ga l i l e i i n i636, it remained f o r Robert Hooke, some 40 years later, t o r e l a t e the amount of deformation i n a material t o the deforming force applied t o it (Westergaard, 1952). however, t h a t serious e f f o r t s were i n i t i a t e d r e l a t ing t h i s c l a s s i c a l law t o the changes i n muscle t i s sue .
It was not u n t i l the twentieth century,
Living skeletal muscle d i f f e r s from most other materials i n t h a t it can recover completely and rapidly from s t re tch deformations up t o approximately 150 percent of i t s rest or noncontracted length. How- ever, when it dies and passes in to r igor mortis, i t s ex tens ib i l i t y t o an applied load f a l l s about 30-40 times, and it i s no longer able t o recover completely from deformations of more than 3 percent of i t s r e s t length. O f the various physical changes which occur i n muscle after death, the most ea s i ly measured i s t h i s loss of ex tens ib i l i ty . This i s because only one parameter i s involved, the s t r e t ch deformation of t he f i b e r s (Bendall , 19 60b ) .
Various manual, mechanical and e l e c t r i c a l devices have been developed t o measure the time course of these ex tens ib i l i t y changes (Ba te -Wth & Bendall, 1949; DeFremery & Pool, 1960; Briskey, Sayre & Cassens, 1962). An excised muscle s t r i p (1 cm2 x 6-8 cm), which i s loaded and unloaded (50-gm weights) at specif ic in te rva ls (2-min), i s used i n these "rigorometers." The read-out i s a pr inted record of ex tens ib i l i t y change with t i m e post-mortem.
Extensibi l i ty changes have been taken as the main c r i t e r i a i n delineating and defining the several "phases" i n the process of r igor mortis (Bate-Smith & Bendall, 1949; Briskey, Sayre & Cassens, 1962):
a- delay phase, v i r t u a l l y no change i n ex tens ib i l i ty
b- onset phase, continuous reduction i n ex tens ib i l i t y
c- completion phase, complete loss of ex tens ib i l i t y
I n the following t ab le (Table l), it can be observed t h a t there i s a wide var ia t ion i n the response of muscle a s it passes i n t o r igor mortis, influenced by such biological f ac to r s as muscle and breed, and possibly body s ize and sex.
279 I
Table 1. Post-Mortem Changes i n the Ektensibi l i ty of Porcine Muscle
Source of var ia t ion
Delay phase h s e t phase Total time duration duration t o completion
k s c l e Longissimus dorsi Light semitendinosus Dark semitendinosus
Breed (1. dors i ) Yorkshire Poland China Hampshire Chester White
Body Size (1. dors i ) 25 kilograms 50 kilograms 90 kilograms
120 kilograms
sex (1. dors i ) Barrows G i l t s
min
115 100
35
90 105 120 130
110 100 145 115
85 80
min
150 50 60
110 140 145 150
120 100 160 115
10 5 75
min
265 150 95
200 24 5 265 280
230 200 30 5 230
190 155
Exci tab i l i ty Changes. The study of t he exc i t ab i l i t y or i r r i t a b i l i t y of muscle t i s s u e has had a ra ther long and in te res t ing h is tory since Luigi Galvani performed h i s c l a s s i c experiments almost two centur ies ago (Loeb, 1905; Opatowski, 1951; Galambos, 1962). The e x c i t a b i l i t y of l i v ing systems depends, t o a la rge extent, on t h e i r metabolic i n t eg r i ty . When this in t eg r i ty i s interrupted ( i . e . , death), there i s a lo s s of exc i t ab i l i t y concomitant with the depletion of energy s tores (Ungar, 1963).
Each muscle f i b e r maintains, i n the res t ing s t a t e , a po ten t ia l (ca.-90 m v ) negative t o the outside. from -90 t o +40 mv (Buchthal, 1957). oxidative enzymatic and thermodynamic processes (Nachmansohn & Wilson, 1955) .
Excitation a l t e r s t h i s d. c. po ten t ia l Repolarization occurs a s a r e s u l t of
The res t ing muscle f i b e r i s excited under the influence of a stimulus (Pay, Goodall & Szent-Gyorgyi, 1953). t ions , e l e c t r i c a l stimulation has been used t o study these exci table proper- t i e s of muscle. evaluated a r e the exc i t ab i l i t y threshold voltage and the loss i n muscle response t o continuous stimulation a t a constant voltage.
In most laboratory investiga-
The two parameters of an e l e c t r i c a l stimulus usually
280.
Using the electromyographic apparatus described by Forrest e t a l . (1965), a preliminary study was conducted at Wisconsin recently t o examine the nature of post-mrtem changes i n the response of muscle t o e l e c t r i c a l stimulation. From the da ta presented i n Table 2, the loss of exc i t ab i l i t y i s evident f romthe increase i n exc i t ab i l i t y threshold voltage necessary t o st imulate the muscle s t r i p i n i t i a l l y , and the decrease i n response t o the reFet i t ive stimulation at a constant voltage (50v) w i t h time Fost-mortem.
Table 2. Post-lrlortem Changes i n t h e Exci tab i l i ty of Porcine Muscle
Source of Exci tab i l i ty Response t o 50-volt stimulationb var ia t ion t h r e sholda
Maximum Total response a force
durat ionc amount
2 V g sec cm O-hr post-mortem
Hampshire 4 750 t 475 145 Chester White 3 7 50 350 80
15-min post-mortem Hampshire 15 5 25 Chester White 20 350
30-min post-mortem Hampshire 25 200 Chester White 50 50
l - h r post-mortem Hampshire 125 --- Chester White 130 -t ---
460 98 335 26
250 19 80 2
dHinimum v o l t a g e required to produce a c o n t r a c t l l e response.
% e p e t l t l v e s t i m u l a t i o n a t a frequency o f 2 cycles / second and a s t imulus duration o r
'Tntal time the e x c i s e d muscle s t r i p (I cm x 6 cm) was a b l e to produce a c o n t r a c t i l e
*Tota l area o r the s t i m u l a t l n n response pattern rrom F = l n l t i a l to F = grams.
0.1 millisecond.
f o r c e o f >10 grams. 2
Contrac t i l i ty Changes. The usual description shows ske le t a l muscle t o be composed of bundles of p a r a l l e l f ibers , the f i b e r s i n tu rn a r e made up of bundles of p a r a l l e l myofibrils, and the myofibrils a r e composed of a hexagonal a r ray of myofilaments containing molecular chains of the cont rac t i le proteins, a c t i n (A) and myosin (M) (Huxley, 1958).
The cross-s t r ia t ions, ch rac t e r i s t i c of ske le t a l muscle, a r i s e from a repeating var ia t ion i n the protein density along the myofibril. However, these do not represent permanent s t ruc tures but ra ther physio- l og ica l s ta tes .
281.
Under a phase contrast microscape (Figure 2) , there i s a regular a l te rna t ion of dense (A-bands) and l i gh te r (I-bands). The central region of the A-band i s less dense than the rest of the band, and i s known as t h e H-band. In the center of t h i s band i s a denser M-line. The I-band i s bisected by a narrow, dense l i n e cal led the Z-line. the next i s usually taken as the repeating uni t of myofibril lar s t ructure and i s designated a sarcomere. approximately 3 A.
From one Z-line t o
I n most ver tebrates t h i s length i s
Since earliest times, the contraction of s t r i a t e d muscle has been re la ted t o changes i n these c ross -s t r ia t ions (Buchthal & Knappeis, 1943; Rorvath, 1952; Gilev, 1962) as wel l as t o changes i n the periodi- c i t y or sarcomere length (Hodge, 1955; Perry, 1956; Huxley, 1957). Even the relat ionship between s t r i a t i o n pa t te rn and sarcomere length has been investigated (Garamvolgyi, Kerner & Cser-Schultz, 1964).
F I G U R E 2. S T R l A T l O N P A T T E R N O F T H E N O N - C O N T R A C T E D M Y O F l B R I L .
Z M Z
'I SARCOrnRF: I'
2 82
Table 3 summarizes the resu l t s of an experiment i n which w e studied the s t r i a t ion pat tern as a function of sarcomere length i n three porcine muscles. It can be observed t h a t each sarcomere type has limit- ing sarcomere lengths. These r e su l t s with porcine muscles are i n good agreement with those reported t o occur post-tcortem i n the muscles of other vertebrates.
Table 3. Distribution of Sarcomere Types i n Post-Mortem Porcine Muscle
Wscle
Sarcomere type* / length range
Trapezius thoracis
Rectus Longissimus femoris dorsi
SS/ > 3 . 5 0 4
RL/Z. 70-3.49,
SC/2 40- 2 69,
NC/l. 90- 2 39 4
HC/l 40-1.89,
EC/( 1.39,
4 0.5
71.5
la .O
8.0
0.5
0.5
$ $
0.0 0 .o
22.5 3.0
21.0 5.0
46.5 64.0
9.5 27 -0
0.5 1.0
Mean sarcomere length 2.77- 2-25, 1.94/y
*Note: SS = s l igh t ly stretched; RL = relaxed or noncontracted; SC = s l igh t ly contracted; NC = normally contracted; HC = highly contracted; EC = extremely contracted.
283.
I n another experiment (Sink -- e t al. , 1965), we demonstrated t h a t the sarcomere shortening i s qui te severe when the delay phase of r igor mortis i s of short duration. mortis i s of long duration, t h e sarcomere shortening t h a t occurs i s much less. Consequently, it can be s ta ted t h a t the amount of sarcomere shortening or contraction, coincident with the r igor mortis onset, i s highly dependent upon the time course of r igor mortis (r = 0.9; P <.Ol).
However, when the delay phase of r igor
Viscoelast ic i ty Changes. The physical change of state from the p l a s t i c condition of f r e sh muscle t o the hard condition of muscle i n a s t a t e of r igor mortis has long been noted. esses of muscle a re disturbed following exsanguination, concomitant changes i n the v iscoe las t ic propert ies begin t o occur (Pryor, 1952). t i s sue i s a co l lo ida l system (protein -t water), it undergoes a phase change from a ra ther l i qu id condition, known a s a sol, t o a so l id or semisolid state, known as a gel , during the development of r igo r mortis (Ferry, 1948). Although various models have been proposed t o explain these v iscoe las t ic propert ies of muscle (Will.de, 1954; Pringle, 1960), none appear t o be qui te sa t i s fac tory . This sol +ge l transformation plays an important r u l e i n post-mortem muscle physiology.
When the thermodynamic proc-
Since muscle
The assumption t h a t the basic physical process of muscular contraction may consis t of a so l + g e l transformation has been advanced (Polissar, 1952). Actually, t h i s transformation occurs a s a r e su l t of the cross-bond formation between ac t in and myosin t o form actomyosin. t he v iscoe las t ic changes i n muscle are not so le ly due t o t h i s actomyosin formation, but a r e due p a r t l y t o the formation of cross l inks and adhesions between other p a r t i c l e s which permit l i t t l e r e l a t ive m t i o n .
All of
The binding of a c t i n and myosin r e s u l t s i n propert ies which a re qui te d i f fe ren t from the propert ies of f r e e A and f r e e M (Hasselbach, 1952). This molecular cross-linking increases the in t e rna l v i scos i ty of muscle and decreases i t s ex tens ib i l i t y and exc i t ab i l i t y . If a c t i n and myosin a re l e f t f o r a suf f ic ien t time i n t h i s associated condition, secondary h i s t e r e t i c changes take place, i n which links t h a t were reversible become i r revers ib le (Szent-Gyorgyi, 1953).
Although other methods (Catton, 1957) a re avai lable f o r deter- mining the post-mortem viscoe las t ic propert ies of muscle, t he lo s s i n so lub i l i t y of the myofibril lar proteins, or the Deuticke-Kamp ef fec t , i s wel l established and can be used as an indication of t he amount of cross- l inking t h a t has occurred. The following table (Table 4) presents some comparative data on the post-mortem so lub i l i t y changes i n the myofibril lar and sarcoplasmic proteins proteins i n two porcine muscles. A greater reduction In the so lub i l i t y of the myofibril lar proteins i s observed.
284.
Table 4. Post-Mortem Changes i n the Protein Solubi l i ty of Porcine Muscle
Muscle
Protein nitrogen solubi l i tya
Myofibrillar Sarcoplasmic
0 - H R 2 4 - H R 0 - H R 2 4 - K R
l$ k Longissimus dors i 49 31
Semitendinosus Dark portion 46 33 Light portion 45 27
% $ 24 21
21 1 7 23 20
aExpressed as percent of t o t a l tissue nitrogen.
The Biophysical Changes and Meat Qual i ty
In the course of t h i s paper, a number of specif ic biophysical fea tures of post-mortem changes i n procine muscle have been presented. The l imi ta t ion of t i m e has made it impossible t o discuss but a small par t of t h e biophysics involved i n the transformation of muscle t o meat (Ernst, 1963). changes a re re la ted t o meat qual i ty .
Finally, w e might ask how these post-mortem biophysical
Any abnormalities i n the usual post-mortem biophysical changes t h a t occur a re associated with the development of the pale, sof t , exudative condition i n porcine muscle, recent ly described i n an extensive review by Briskey (1964). The extent of the v iscoe las t ic changes appears t o play an important par t i n t he fat-emulsifying propert ies of porcine muscle (Trautman, 1964). t o subsequently e f f ec t the cooking charac te r i s t ics of muscle (Sayre, =ernat & Briskey, 1964).
The t i m e course of r igor mortis has been shown
Recent s tudies a t New Zealand (Locker, 1960) and Wisconsin (Herring, Cassens & Briskey, 1965) have investigated the relat ionship between sarcomere length and tenderness. that the r a t e of l o s s of so lub i l i t y i n the myofibril lar protein f rac t ion p a r a l l e l s the rate of development of toughness (Connell, 1960). w e a r e beginning t o
It has a l so been demonstrated
Finally, examine tenderness at the c e l l u l a r and molecular leve l .
While the exact nature of meat qua l i ty i s yet unknown, an understanding of the post-mortem biophysical changes t h a t occur i n muscle can perhaps lead us t o more precisely control i t s development. If an ante-mortem o r ea r ly post-mortem prediction of the ult imate meat qua l i ty can be made by biophysical or other methods (Forrest -- e t a l . , 1965), appropriate control measures could be developed (Briskey, 1963; Hallund & Bendall, 1965) t h a t would eventually lead t o desired degrees of tenderness, texture , juiciness , f lavor and color.
285.
While the post-mortem biophysics of muscle discussed i n t h i s paper may not necessarily r e f l e c t the ac tua l carcass conditions, they represent our knowledge today and of fer us a s t a r t i n g point f o r much needed fur ther invest igat ions.
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Briskey, E. J. 1963. Influence of ante- and post-mortem handling prac t ices on propert ies of muscle which a r e re la ted t o tenderness, -- R o c . Meat Tenderness Sm., Campbell Soup Co., p. 195-221.
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Forrest, J. D., M. D. Judge, J. D. Sink, W. G. Hoekstra and E. J. Briskey, 1965. Prediction of the time course of r igor mortis through response of muscle t i s sue t o e l ec t r i ca l stimulation. - J. -- Food Sci. (submitted).
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288.
G. R. BEECHER: The three speakers t h i s morning have presented reviews and observations on the relat ionship of ante-mortem physiological phenomenon i n the porcine animal a s they may be re la ted t o the ultimate propert ies of the muscle. D r . Zobrisky has indicated the ro l e nu t r i t i on plays i n the development and maturation of muscle t i s sue . He has a l so pre- sented evidence t h a t t he enzyme and substrate concentrations i n muscle t i s sue immediately p r io r t o exsanguination of the animal are very important i n determining the ultimate post-mortem muscle properties.
Mr. Forrest has presented very exci t ing observations on the relat ionship of some ante-mortem physiological measurements t o the ultimate propert ies of the muscle t i s s u e from the same animals. concepts t h a t John presented a re well-known, however they have been applied i n a new manner t o the f i e l d of muscle research.
The physiological
The t h i r d speaker, D r . Sink, has a l so presented an excellent review of a d i f f i c u l t subject and implicated how physical changes may or do a f f ec t the ultimate properties of muscle.
I would l i k e t o expand b r i e f l y on another area t h a t w e f e e l a f f ec t s the f o r a large portion of the muscle-muscle var ia t ion observed i n the porcine carcass. This area i s the red f i b e r content of a muscle.
ult imate propert ies of porcine muscle and cer ta in ly accounts
M r . Norman b r i e f l y touched on t h i s area yesterday. Generally, white muscle f i b e r s are characterized by anaerobic o r glycolytic enzyme a c t i v i t y whereas red fibers have aerobic or Kreb's cycle enzyme ac t iv i ty . Thus, it can be seen t h a t t he proportion of red t o white f i b e r s i n a muscle w i l l predict the general type of metabolic a c t i v i t y ante-mortem and de f in i t e ly predict the amount and r a t e of enzyme a c t i v i t y post-mortem pro- vided suf f ic ien t substrate, i n t h i s case glycogen, i s present.
We have observed ranges i n red fiber content from a low of 19% i n the semitendinosus l i g h t portion t o a high of 47% i n t he trapezius. The seven porcine muscles studied were c l a s s i f i ed a s e i the r red o r white on the basis of t h e i r red fiber content.
It should be pointed out t h a t those muscles i n the porcine carcass which become pale, sof t , and exudative most frequently (longissimus dorsi and gluteus medius) a r e white muscles (less than 30% red f ibe r s ) whereas those muscles characterized by a r e s i s t a n m o t h i s condition a re red muscles (greater than 30% red f i b e r s ) .
From these observations, we f e e l the red f i b e r content of a muscle i s extremely important i n determining the propert ies that a muscle will ultimately a t t a i n post-mortem and adds another fac tor t o the many t h a t contribute t o the ultimate post-mortem propert ies of a muscle.
I believe there i s t i m e f o r a few questions. Although w e a r e running l a t e , I am sure t h a t t h i s a very exci t ing area and we w i l l enter- t a i n questions from the f loor . Dr. Webb?
289.
DR. WEBB: evaluation of these muscles, t he time a f t e r death they were cut, the temperature of the muscle, the l i g h t conditions t i o n a t observation.
I have a question f o r Mr. Forrest concerning the
and the general condi-
J. C. FORRESJ!: These carcasses were cut at 24 hours post There was very mortem.
l i t t l e var ia t ion. We did not measure the ac tua l temperature.
V. R. CAHILL: As we move i n t o t h i s second phase of the pro- gram we are going t o take a look a t those fea tures of both carcass and pork product. We know tha t over t he years a great deal of work has been done on swine improvement. where we've heard much about pioneering i n the last f e w days and w e have ca l led on a man who has pioneered i n the area of pork carcass evaluation and swine improvement. pioneering f o r a year i n a new area, the Armour Pork Company, and without taking fu r the r t i m e , Wilbur, may I tu rn t h i s microphone t o you.
We a re out here i n t h i s State of Kansas
I am re fer r ing t o Wilbur Bmner who i s now
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