J. Anim Sci. 2006. 84:3251-3258. doi:10.2527/jas.2006-187
© 2006 American Society of Animal Science
ANIMAL GROWTH, PHYSIOLOGY, AND REPRODUCTION |
Computer image analysis of intramuscular adipocytes and marbling in the longissimus muscle of cattle1
X. J. Yang*,
E. Albrecht
,
K. Ender,
R. Q. Zhao* and
J. Wegner,2
* Nanjing Agricultural University, Nanjing 210095, China; and
and
Research Institute for the Biology of Farm Animals, D-18196 Dummerstorf, Germany
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Abstract
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The deposition of fat in muscle, recognized by the consumer as marbling, is an important meat quality trait. The objective of the study was to provide additional insights into the quantitative extent of marbling by means of computer image analysis. Fifty-one F2 generation German Holstein and Charolais crossbreed cattle, 18 mo of age, were used to determine relationships among marbling traits, adipocyte size, and the amount of adipose tissue in different depots. Differences were recorded among the size of i.m. adipocytes in different groups of marbling flecks, divided according to the location in the muscle cross-section and to the size of the marbling flecks. The results showed positive correlation between i.m. adipocyte size and the weight of s.c. fat, intestinal fat, omental fat, and perirenal fat (r = 0.50, 0.61, 0.70, and 0.63, respectively, P < 0.001). The i.m. adipocyte size was correlated with i.m. fat content, number of marbling flecks, proportion of marbling fleck area, and total length of marbling flecks (r = 0.71, 0.44, 0.62, and 0.55, respectively, P < 0.01). The number of marbling flecks was also correlated with i.m. fat content, proportion of marbling fleck area, and total length of marbling flecks (r = 0.58, 0.62, and 0.91, P < 0.01, respectively). The ventral marbling flecks had a 5-fold larger fleck area, 4-fold more adipocytes, and larger adipocytes (P < 0.001). Larger marbling flecks contained larger adipocytes (P < 0.001). Moreover, compared with the small marbling flecks, there was a 48-fold larger fleck area and 26-fold more adipocytes in the large marbling flecks. The results indicate that i.m. fat deposition increases concurrently with the other fat depots but is still independent. Furthermore, the i.m. fat is preferentially deposited in the ventral area of LM. Although the i.m. adipocyte size has an important effect on the traits of marbling flecks, cell number plays a greater role in i.m. fat deposition than cell size.
Key Words: adipocyte • cattle • computer image analysis • longissimus muscle • marbling
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INTRODUCTION
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The deposition of i.m. fat or marbling is an important meat quality trait. Taste, juiciness, and tenderness, particularly in cattle, are influenced by i.m. fat deposition and are therefore appreciated by the consumer (Platter et al., 2005
). In the last decades, marbling has been the focus of many studies on meat animals. Although some exciting results have been acquired, the mechanism of marbling development is still not well understood. The contribution of hypertrophy (increased cell size) and hyperplasia (increased cell number) to intramuscular fat deposition is controversial, and the description of cellularity in different marbling flecks in a muscle cross-section is still lacking. The recent development of computer technologies and color image processing techniques have made the measuring of marbling by computer image analysis (CIA) more efficient (Albrecht et al., 1996; Basset et al., 2000). Therefore, a reevaluation of i.m. adipose tissue cellularity was warranted.
For the i.m. adipocyte size, most of the studies show differences in adipocyte size between i.m. fat and other fat depots (May et al., 1995; Gilbert et al., 2003; Schoonmaker et al., 2004) or among animals with different marbling scores (Moody and Cassens, 1968; Cianzio et al., 1985). But within the same muscle cross-section, the marbling flecks still exhibit different sizes and are located at different positions. Does the adipocyte size differ between large and small marbling flecks or among the marbling flecks located at different positions? How is the i.m. adipocyte size related to marbling fleck characteristics, or how does the i.m. adipocyte size affect marbling fleck traits?
The objective of the current study was to investigate the i.m. adipocyte and marbling traits, detected by CIA, and the relationships among i.m. adipocytes, marbling, and the weights of other fat depots. The study should contribute to a better understanding of fat deposition in muscle on a cellular level.
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MATERIALS AND METHODS
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Animals
All animals were cared for and killed according to German rules and regulations for animal care. The experiment was approved by the institutional authorities and by the responsible office of the County of Mecklenburg-Vorpommern, Germany.
Fifty-one F2 generation German Holstein and Charolais crossbreed bulls were used in the study. The bulls were raised using a tethering system with individual feeding. Calves were fed with a milk replacer diet up to 4 mo of age. After weaning, the bulls received a diet ad libitum consisting of concentrates (6 kg of DM) based on barley, beet pulp, soybean extraction meal (92.8% OM, 15% CP, and 9% crude fiber), and roughage (2 kg of DM). Any unconsumed feed was removed, weighed, and recorded daily. The cattle were slaughtered at the research institute’s experimental slaughterhouse at 18 mo of age.
Carcass and Meat Quality Measurements
After slaughter, chilling at 6°C for 24 h, and carcass dressing, samples were removed from the left side of the carcass. The i.m. fat content of LM samples was obtained in triplicate via the Soxhlet extraction method using petroleum ether as the solvent and was determined gravimetrically after evaporating the solvent (Association of Official Agricultural Chemists, 2000). The weights of different fat depots, including s.c. fat, intestinal fat, omental fat, and perirenal fat, were individually determined.
Computer Image Analysis of Marbling
A 2-cm thick slice of LM was removed 24 h after slaughter at the level of the 12th rib. For CIA, muscle slices were fixed in 5% formaldehyde, cut into smaller slices (2-mm thick), and stained with oil red O, as described in detail by Albrecht et al. (1996). The stained slices provided a good contrast between fat (red), connective tissue (white), and muscle (pink). The CIA system was composed of a digital camera (Coolpix 8700, Nikon, Düsseldorf, Germany; camera resolution = 3,264 x 2,448 pixels) and a PC with the image analysis software ImageC (Aquinto, Berlin, Germany). Marbling traits were calculated as described by Faucitano et al. (2005). The measurement was performed after conversion of the color image to gray scale and application of a threshold function. The program allowed for interactive adjustment of the threshold to account for minor differences between samples. To be designated as a marbling fleck, the size of the fat area had at least 4 pixels. The following group of marbling characteristics was determined: number of marbling flecks, proportion of marbling fleck areas, proportion of the 3 largest marbling fleck areas, total length of marbling flecks, largest marbling fleck area, and length of the longest marbling fleck. The length of a continuous marbling fleck was determined as fiber length, which is provided by the program.
The area of single marbling flecks used for determination of adipocyte size was measured after interactive detection (freehand mask) of the fleck in a magnified image (100 and 200x for large and small marbling flecks, respectively). The system was calibrated with a ruler according to the software requirements. To eliminate subjective operator-to-operator differences, measurement was performed by only one experienced operator.
Intramuscular Adipocyte Size Determination
The size of an i.m. adipocyte was measured as cross-sectional area. For adipocyte area determination, the muscle slice next to the slice for CIA of marbling was used. Transverse sections of marbling flecks, 30-µm thick, were cut using a cryostat microtome (CM 3050 S, Leica, Bensheim, Germany). The sections were stained with eosin. The muscle fibers around the marbling flecks were pink, and the adipocytes in the marbling fleck were unstained and clearly visible. The adipocyte area of each animal was determined as an average of adipocytes in 6 to 9 randomly selected marbling flecks (at least 200 and on average 700 adipocytes) in 1 muscle cross-section.
To measure the adipocytes, the CIA system was composed of a black and white video camera (XC-77 CE, Sony, Berlin, Germany) and a microscope Axiolab (Zeiss, Jena, Germany). The microscopic pictures of adipocytes were analyzed by AMBA software (IBSB, Berlin, Germany). For calibration, a micrometer was used according to the software requirements (1 pixel = 1.0554 µm). The apparent adipocyte number in a marbling fleck was calculated from the area of the marbling fleck and the adipocyte area.
For measuring the adipocyte area in marbling flecks at different locations, the muscle cross-sections were divided into 2 parts by the midline (along the frontal plane; Figure 1). If the fleck was located above this line, it was considered as a dorsal marbling fleck, and a fleck below this line was considered as a ventral marbling fleck. If the fleck was located around this line, it was ignored. For the different sizes, marbling flecks were divided into 3 groups: small, <2.5 mm2; middle, 2.5 to 15 mm2; and large, >15 mm2. Each group contained at least 100 marbling flecks.
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Figure 1. Example of a black and white-rendered image of an LM cross-section with marbling flecks detected and grouped as follows: A, B = marbling flecks belonging to the dorsal marbling group; C, D = marbling flecks belonging to the ventral marbling group; A, D = marbling flecks belonging to the large marbling group; C = marbling fleck belonging to the middle marbling group; B = marbling fleck belonging to the small marbling group; and M = middle line.
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Statistical Analysis
The results were expressed as means, SD, minimum, and maximum (Table 1), and means ± SE (Table 4). The relationships among the fat-related traits were analyzed as Pearson’s correlation coefficients by SPSS (Release 11.0.1, SPSS Inc., Chicago, IL). The GLM procedure of SPSS for Windows (2001) was used to test differences among groups of marbling flecks. The sources of variation included in the model were animal, marbling group, and animal x marbling group interaction. To further characterize the adipocyte size differences between the small, middle, and large marbling flecks, adipocyte size frequency distributions were calculated. In total, 8,000 adipocytes were included for each group.
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RESULTS AND DISCUSSION
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In Table 1
, traits of adipose tissue depots in body and muscle of F2 bulls at 18 mo of age are presented. In general, these traits are in-between the traits of German Holstein and Charolais breeds (unpublished data) which were used to generate the F2 population in this study. The proportion of marbling flecks measured by CIA is greater than the intramuscular fat content measured via the Soxhlet extraction. These are 2 different techniques. The chemical intramuscular fat content is weight dependent, but the proportion of marbling flecks is area dependent. The same weight of fat occupies more area compared with muscle. Furthermore, the fat is stored in cells which are surrounded by connective tissue, so the stained areas also include areas of connective tissue, blood vessels, and others (Figure 2B).
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Figure 2. Macroscopic and microscopic image of stained marbling flecks. (A) Macroscopic image of large and small marbling flecks. Muscle fiber bundles are grayish; marbling flecks are dark; connective tissue is whitish; and blood vessels are indicated by the arrows. Scale bar = 6 mm. (B) Microscopic image of small marbling flecks; muscle fibers are grayish but well outlined; adipocytes are whitish; connective tissue is grayish; and blood vessels are indicated by the arrows. Scale bar = 100 µm.
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Table 2 presents correlation coefficients among traits of adipose tissue depots in body and muscle. It was unexpected that the BW at slaughter was not related to i.m. fat content and i.m. adipocyte area. Most studies showed that the BW in cattle had linear response with the marbling scores (Miller et al., 1987; May et al., 1992; Bruns et al., 2004). Breed and age influenced this relationship. In our study, F2 crossbred bulls originated from German Holstein and Charolais, which is a very lean beef breed, were used. The bulls were already slaughtered at 18 mo of age before they developed a relationship between BW and fat deposition. Interestingly, the BW at birth in the current study was negatively correlated with i.m. fat content and i.m. adipocyte area (r = –0.29 and –0.34, respectively). Reports of direct correlations between the i.m. fat or i.m. adipocyte size and birth weight in cattle were not found in the literature. However, it is well known that the double-muscled Belgian Blue bulls have very great birth weights and a very low i.m. fat content compared with other breeds. The greater birth weight is related to the doubled muscle fiber number, emphasizing a more extensive hyperplasia of muscle fibers during embryonic development in double-muscled Belgian Blue bulls (Wegner et al., 2000). Casas et al. (2004) investigated the association of an inactive myostatin allele with early calf mortality and found low birth weight related to great backfat thickness and great marbling. In pigs, Gondret et al. (2006) recently showed that animals with low birth weights exhibited greater back fat depth and greater adipocyte diameter in semitendinosus muscle and back fat. Our results show that in cattle the prenatal life is also related to the later fatness. In further adipogenesis research the prenatal interactions between myogenesis and adipogenesis should be considered.
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Table 2. Correlation coefficients among traits of adipose tissue depots in body and muscle of F2 bulls at 18 mo of age (n = 51)1
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The i.m. adipocyte area was moderately correlated with the weight of s.c. fat, intestinal fat, omental fat, and perirenal fat. The correlation coefficients between i.m. fat content and the weight of the other fat depots were also moderate but lower. In agreement, Riley et al. (2002) reported a moderate correlation between the 12th rib backfat thickness and marbling score (rp = 0.3; rg = 0.56, respectively) in Brahman cattle. Conversely, Pitchford et al. (2002) found low phenotypic correlation (r = 0.15) between i.m. fat content and backfat depth in crossbred cattle, and indicated an ample potential to select animals within breeds for improvements in both s.c. (not desirable) and i.m. (highly desirable) fat. In Brangus cattle, Stelzleni et al. (2002) also showed low correlation (r = 0.17) between ultrasonically determined backfat thickness and ultrasonically percent intramuscular fat. In Angus steers, Brethour (2000) found low correlation between s.c. fat and marbling score and concluded that these depots accumulate lipid stores independently rather than sequentially. Nevertheless, the cattle used in studies of Stelzleni and Brethour were very young (from 320 d to 410 d and 8 mo old, respectively). The CIA of macroscopic marbling traits: number, proportion, and the total length of marbling flecks also were moderately correlated with the weights of other fat depots (Table 2). The presented results at 18 mo showed that the i.m. fat traits exhibited a relatively high consistency with the other fat depots.
In Table 3, the relationships among adipocyte area and CIA marbling traits in a same muscle cross-section are shown. The i.m. adipocyte area was moderately correlated with the i.m. fat content, number of marbling flecks, proportion of marbling fleck area, and total length of marbling flecks (r = 0.71, 0.44, 0.62, and 0.55, P < 0.01, respectively). The number of marbling flecks was also moderately correlated with i.m. fat content, proportion of marbling fleck area, and total length of marbling flecks (r = 0.58, 0.62, and 0.91, P < 0.01, respectively). During growth new marbling flecks appear after preadipocyte hyperplasia and lipid filling (Albrecht et al., 2006). Some animals did not show very large marbling flecks, but they still had a great i.m. fat content because they contained more marbling flecks. From the present results, it can be concluded that i.m adipocyte area and number of marbling flecks play an important role in determination of the marbling characteristics.
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Table 3. Correlation coefficients among i.m. adipocytes and marbling traits in F2 bulls at 18 mo of age (n = 51)1
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The large marbling flecks always considerably influence the marbling score, but the current study showed that the proportion of the 3 largest marbling flecks was not correlated with the i.m. fat content. Moreover, the area of the largest and the length of the longest marbling fleck were slightly correlated with i.m. fat content. No correlation was found between the largest or the longest marbling fleck and the number of marbling flecks. The largest marbling fleck area had the strongest relationship with the longest marbling fleck (r = 0.95, P < 0.001). This relationship shows the general pattern of the i.m. fat deposition. The shape of marbling flecks follows the muscle bundle structure and becomes longer with increasing size (Figure 2).
On cellular level, marbling appears in clusters of adipocytes, embedded in a connective tissue matrix, and grouped in close proximity to blood vessels (Harper and Pethick, 2004). Figure 2 shows a macroscopic and a microscopic image of marbling flecks surrounding blood vessels. We measured adipocyte areas in marbling flecks of different size and at different locations. To quantify these differences, marbling flecks were divided according to their location in the muscle and according to their size into groups. The adipocytes in each group were measured (Table 4). The results showed clear differences (P < 0.001) among groups. Animal and animal x marbling group interaction had no influence on the results.
The ventral marbling flecks had a 5-fold larger fleck area, 4-fold more adipocytes, and also larger (P < 0.001) adipocytes. The ventral muscle layer is closer to the intercostal arteries. Blood provides the nutrients for adipocyte hypertrophy and i.m. preadipocytes coming from stromal-vascular cells (Hausman et al., 1993; Hausman and Richardson, 2004). Many marbling flecks seem to grow from the ventral part of the muscle cross-section and spread out to dorsal direction in a treelike shape. Concerning the reason for the ventral and dorsal adipocyte area differences, we hypothesized this difference may be influenced by the outside fat depots very close to muscle [they may share the same blood flow or basal nerve stimulation, so we also compared the adipocyte size outside the epimysium of LM (subcutaneous and intermuscular fat; Figure 3)]. The adipocyte area in the subcutaneous fat was larger than the adipocyte area of the intermuscular fat (7,820 ± 672 vs. 5,977 ± 315 µm2, respectively, P < 0.01). Both depots outside the muscle have larger adipocytes compared with the adipocytes in the marbling flecks (intramuscular fat). It is well known that the i.m. adipocyte diameter is smaller than the adipocyte diameter in other fat depots (Cianzio et al., 1985; Miller et al., 1991; Lee et al., 2000). This was confirmed in the current study for depots very close to the muscle. The larger adipocyte size in the ventral marbling flecks (Table 4) is not influenced by the intermuscular fat outside the epimysium; likewise, the large adipocyte size of subcutaneous fat has no influence on the adipocyte size of dorsal marbling flecks. That means though the different fat depots grow concurrently, shown by correlations between i.m. fat content and the weight of other fat depots, the i.m. fat deposition is still independent.
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Figure 3. Image of an LM cross-section with marbling flecks detected and fat depots outside the epimysium. A = subcutaneous fat; B = intermuscular fat.
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Furthermore, we divided the marbling flecks in a muscle cross-section into 3 groups by the size. For the small, middle, and large group we found differences (P < 0.001) in adipocyte area. Small marbling flecks contained smaller adipocytes (P < 0.001) than middle, and middle marbling flecks contained smaller adipocytes (P < 0.001) than large marbling flecks. Previously, Moody and Cassens (1968) also divided the i.m. fat depot into 3 groups according to the adipocyte number. In their study, 5 to 10, 11 to 20, and >20 adipocytes in one marbling fleck were the grouping standard for 3 groups. In comparison to our study this would correspond to a division within the smallest group of marbling flecks into 3 further groups because the small marbling flecks in our study contained more than 30 adipocytes. The results of both studies agreed that i.m. adipocyte size increased with increasing marbling fleck size. In Figure 4, adipocyte size frequency distributions are shown to further characterize the adipocyte size differences between the small, middle, and large marbling flecks. Adipocyte areas distribution was monophasic in all 3 size groups of marbling flecks. The distribution in the large marbling flecks compared with the other marbling fleck groups showed an increased range of adipocyte areas. Also, very small adipocytes were found, which means there is still recruitment of preadipocytes also in large marbling flecks. Additionally, the apparent number of adipocytes in the 3 different size groups was calculated. Although the adipocyte area was larger (P < 0.001) in the middle and large marbling flecks compared with the small one, this enlargement of adipocytes was not the main reason for the larger marbling flecks. Compared with the small marbling flecks, there were a 48-fold larger fleck area and 26-fold more adipocytes in the large marbling flecks, but only 1.5-fold larger adipocyte area. Cianzio et al. (1985) and Robelin (1986) stated for cattle fat depots except for i.m. fat that the growth of adipose tissue is mainly due to hypertrophy of adipocytes. For i.m. fat, adipocyte hyperplasia is also very important (Hood and Allen, 1973; Cianzio et al., 1985; May et al., 1994). The presented study and the results from Albrecht et al. (2006) show that hyperplasia plays a greater role in i.m. fat deposition than hypertrophy. The adipocyte size showed large differences between different marbling flecks within the same muscle. Whether this difference is determined by the local muscle environment of the i.m. adipocyte, including the nutrient diffusion from blood vessels, or by its genetically determined growth potential needs further investigation.
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Figure 4. Frequency distribution of adipocyte areas in small (A), middle (B), and large (C) marbling flecks (8,000 each). Number of animals was 48, 37, and 35 for small, middle, and large marbling flecks, respectively.
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Footnotes
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1 This study was supported by the Federal Ministry of Food, Agriculture, and Consumer Protection of Germany and The Agricultural Ministry of China (grant no. 26/2005–2006 "Adipogenesis"). The authors thank Karola Marquardt for excellent technical assistance. 
2 Corresponding author: wegner{at}fbn-dummerstorf.de
Received for publication March 28, 2006.
Accepted for publication July 10, 2006.
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Abstract
INTRODUCTION
