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References Balaban, M. Part I: Fresh tuna. Food Prod. Cashon, R. Chow, C. Food Drug Anal. Daniels, F. Outlines of Physical Chemistry, 1st edn. Wiley, New York. Danyali, N. MS thesis. University of Florida, Gainesville. Demir, N. Garner, K. Haard, N. Martin, R. Ory, and G. Flick eds. Technomic Publ.

Hsieh, P. Hultin, H. Shahidi and J. Botta eds. Blackie Academic, Glasgow, pp. Huo, L. IFT Abstract 88A Ishiwata, H. Food Hyg. Icelandic Fisheries Laboratories, Reykjavik, Iceland, pp 27— Livingston, D. Mantilla, D. Abstract 89A— Miyazaki, H. Moncada, S.

Richards, M. Stryer, L. Biochemistry, 4th edn. Freeman, New York. The red color of the meat is due to the presence of myoglobin. The myoglobin molecule has one heme group associated with the globin protein. The heme is an iron-based subunit. The oxidative state of the iron is responsible for the red color of the protein Kanner et al. When the heme is bound to oxygen, the color is bright red.

Carbon monoxide CO can compete with oxygen O2 for the heme-binding site. Practically this means that carbon monoxide will bind 53 54 Use of CO and Filtered Smokes to more heme molecules, will saturate all the available heme binding sites at low concentrations, displace oxygen, and stay bound for long periods of time El-Badawi et al.

Hence, the CO-bound myoglobin has a similar, yet brighter, red color of oxygen-bound myoglobin. Tasteless smoke and carbon monoxide are used as a preservative in the preparation of tuna and other red meat products for packaging and freezing Hahn The red coloration effect occurs from this preservative process, which is caused by the CO binding with the heme proteins in treated red meat. One of the health risks of eating CO-exposed tuna is the release of CO during mastication and digestion of treated tuna with subsequent CO absorption into the blood.

The mouth and stomach are highly vascularized and carbon monoxide is highly diffusible through body tissues. Carbon monoxide diffuses from the blood into the lung and is present in the exhaled air in a concentration directly proportional to the amount in the blood. Measurement of exhaled CO in human subjects with normal lungs is directly proportional to the CO level in the blood and is a reliable measure of blood CO. Carbon monoxide has some water solubility. The CO must be dissolved to transfer by diffusion to the heme protein.

During human consumption of CO-exposed meat, CO will be released from all three storage pools. Stomach digestion of tuna proteins should break down the cell membranes releasing the ICF-dissolved CO. In addition, exposing myoglobin to pepsin-related protein degradation in the stomach will result in degradation of myoglobin. The break down of the myoglobin will destroy the ability of the myoglobin to bind CO and induce the release of protein-bound CO. Thus, CO from all the three tissue storage pools will lead to the diffusion of CO into the blood where it will bind to blood hemoglobin.

Hence, if CO-exposed meat is consumed, then the CO would be released within a time window of 5—30 min after ingestion of the tuna. The free CO will diffuse into the blood where it is reversibly bound to the hemoglobin. CO would be released into the alveolar space during gas exchange in the lung and released into the atmosphere with exhalation of the alveolar gas.

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It is hypothesized that ingestion of CO-exposed tuna will result in the absorption of CO in adult humans. This hypothesis was tested in human volunteers consuming CO-exposed tuna sushi and unexposed tuna sushi in a repeated measured, double blind study. The tuna sushi was prepared according to restaurant standards and served to nonsmoking subjects experienced in eating sushi.

The subjects had a mean age of The project was reviewed and approved by the Institutional Review Board of the University of Florida. The subjects were informed of the nature of the study and their consent was obtained. The containers were removed from the refrigerator and a needle inserted into the headspace air. The concentration of CO in the headspace air was recorded.

The cooked tuna was weighed and transferred to a new ml container. The cooked tuna sample was refrigerated for 24 h and then the headspace air sampled for CO. The subject initially received a pulmonary function test PFT using impulse oscillometry Sansormedics, Inc. Paired samples of unexposed tuna were obtained from the same tuna steak. The tuna was then cut into slices using federal standards to ensure the quality and health safety standards of the food being prepared. The slices of tuna were approximately 1 in. The tuna slices were grouped into g portions, put into standard resealable plastic bags, and frozen for 24 h before consumption.

This ensured the CO samples would not loose CO in the meat. There were two trials exposed and unexposed with the subjects participating in both the trials. Each subject was randomly assigned to test order. The subjects then consumed the tuna within 10 min. Since the color of tuna was changed due to the exposure of CO, a red light was used in a foodtesting booth to prevent the subjects from detecting the sample type.

The sauces had no effect on CO absorption. The exhaled alveolar gas sample was then obtained 5 min after the subjects completed consumption of the tuna. Alveolar gas samples were obtained 5, 15, 30, 45, and 60 min after completion of tuna consumption. After the min time point, the subjects were rescheduled for the second crossover experiment. The CO concentration and the change in CO concentration from preconsumption baseline were both recorded.

There was no measurable CO in the headspace gas of the unexposed tuna samples. The concentration of CO in the exhaled air was determined over 60 min. Filled circles represent the absolute CO concentration. Filled squares, delta CO, represent the difference between the preconsumption baseline and the CO measured subsequent to tuna sample consumption.

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CO exposed and unexposed 6 5 4 3 Unexposed Exposed 2 1 0 —1 0 10 20 30 40 50 60 70 Fig. Filled squares represent the change in CO from baseline after the subjects consumed g of CO-exposed tuna. Filled circles represent the change in CO from baseline after the same subjects consumed unexposed tuna.

CO was bound to the myoglobin as indicated by the color change Chow et al. Mastication disrupts the intercellular matrix releasing the ECF into the mouth. The CO is thus available for diffusion to the mouth mucousal membrane where the CO will diffuse into the blood supplying this tissue. It is also likely that some of the cells are also disrupted by mastication and intracellular stores of CO will be released in the mouth. Thus, the primary sources of CO for initial absorption are the extracellular and intracellular dissolved CO stores.

CO is released from within the cell as it is disrupted during mastication. This is due to the rapid transfer of CO across the cell membrane into the blood stream. Heating the tuna to a level that denatures the muscle proteins probably releases the myoglobin-bound CO. However, the cooked tuna CO level in the headspace measurement was only slightly less than the uncooked tuna CO level. This suggests that the headspace CO concentration is a function of the CO dissolved in the ECF, which is unaffected by the cooking and cooling process used in this experiment.

In addition, this suggests that cooking CO-exposed tuna may reduce the total CO in the sample by decreasing the myoglobin-bound and hemoglobin-bound CO concentration, but the tuna retains CO in the dissolved form even with cooking. Thus the uptake of CO by humans eating CO-exposed meats should be directly related to the treatment concentration and the amount of the product consumed. The parts per million ppm reading that is given from the CO analyzer can be translated into percent CO in the blood or percent CO bound Table 4.

The CO in the expired air reaches a peak and then declines toward baseline. The mouth is highly vascularized and the CO absorbed into the mouth mucousal venous circulation will be transported directly to the right atrium and right ventricle of the heart and then immediately pumped into the pulmonary circulation.

This delivers the blood to the lungs where CO will diffuse into the alveolar gas and then exhaled. This initial rise is then sustained for several minutes by the masticated tuna reaching the highly vascularized stomach. The protein digestive enzymes in the stomach will fully disrupt the tuna tissue structure releasing all protein-bound CO into the chyme of the stomach.

The liquid chyme will allow the CO to diffuse to the vascularized stomach mucousal wall and the CO will be absorbed into the portal venous blood. This blood supply goes through the liver and then into the systemic venous circulation.

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This systemic venous blood is then delivered to the right atrium of the heart and follows the same delivery path as the venous blood coming from the mouth. Again, CO will be delivered to the lung where the CO is released and eliminated from the body. The absorption of CO from the stomach requires a greater time than mouth absorption and is probably the source of the elevated CO from the 15—60 time periods.

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Secondly, this study demonstrates that CO absorbed from eating CO-exposed tuna sushi is rapidly removed from the blood by exhalation of the CO. With the low level increase in CO in the body, any CO that is introduced into the body has the potential of removing additional hemoglobin from oxygen transport. The increase of CO by consuming CO-exposed meats is possible because of CO bound to the oxygen binding proteins in muscle. Myoglobin is one of the main oxygen-binding proteins found in meats Kanner et al. The CO is maintained on the myoglobin until an external factor elicits CO release.

Conformational changes to the myoglobin occur during the digestion process when myoglobin is subjected to the low pH of the stomach and proteases, which hydrolyze myoglobin into small nonfunctional units. Released CO will then diffuse across the stomach lining into the blood stream.

The introduction of CO into the blood by consumption of CO-exposed food products can occur without the knowledge of the consumer. The absorption of CO has the potential of decreasing the oxygen-carrying capacity of the blood hemoglobin. However, with the controlled environmental baseline CO exposure of the remaining subjects, it is clear that CO levels in the blood and subsequent expired air is due to the absorption of CO from exposed tuna. The transfer of CO to the consumer is predicted to be directly related to the concentration of CO in the product. With the increased availability of CO-exposed meats in the market, consumer risk factors such as environmental exposure and health conditions, which increase Human Absorption of CO 63 sensitivity to CO, warrant further investigation into the uptake of CO from CO-containing meat products.

Human consumption of CO-exposed tuna results in a rapid and transient increase of exhaled CO. The origin of the exhaled CO is blood absorption from the mouth and stomach mucousal membranes. The magnitude of the CO increase remained well below blood CO safety limits.

This absorbed CO is rapidly removed from the body by exhalation from the lungs. Further investigation is needed to compare the CO absorbed from CO treatment and traditional hot and cold smoking. References Chow, C. Hahn, M. Kalin, J. Habben ed. Kanner, J. Accessed Feb. Sorheim, O. These include harvest methods, handling, level and type of processing, temperature, muscle pH, microbial type and load, amount and type of prooxidants e.

The shelf life extensions that result from vacuum packaging and MAP is primarily due to the retardation of aerobic microorganism growth as well as minimization of oxidative chemical reactions e. On the other hand, lactic acid bacteria can become important spoiling agents under low-oxygen conditions. Another major drawback may be consumer acceptance related to color change of muscle due to deoxygenation and also autoxidation of heme proteins Meischen et al. This is particularly true for species rich in dark muscle i. This color change is especially accelerated when the muscle is frozen.

On the other hand, potential problems also exist. One can also potentially convert poor products into visually appealing products. Furthermore, it is possible that an appealing product treated with CO or FS may have experienced abuse, leading to food safety problems. Several quality improvement claims have been made for products treated with CO and FS.

In the late s, the Aquatic Foods Program at the University of Florida began a modest research program into the effects of CO on aquatic food quality and safety. In major resources of the program were devoted to investigating the effect of both CO and FS on a large variety of commercially important species. This work included a comprehensive investigation on many different species and a variety of different treatment methods.

Studies involving brief exposures of bacteria to pure CO showed little effect on Staphylococcus aureus, Clostridium botulinum, or Escherichia coli Kaffegakis et al. Francisco and Silvery showed that CO could inhibit the growth of an aquatic streptomycete. Clark et al.

The effect of CO varied between species of bacteria tested. A recent study by Hunt et al. However, no untreated control was included. A study by Rozbeh et al. Several studies do however show that CO may retard microbial growth in meats. Brewer et al. This system supposedly contained no oxygen, but it could not be determined whether inhibition was due to CO or exclusion of oxygen. The studies done on meats have either demonstrated an inhibitory effect of CO on microorganisms or no effect.

However, some of the studies on meat were conducted with very low levels of CO and from many of these studies it is hard to decipher if CO is exerting an effect or just merely the exclusion of oxygen or presence of carbon dioxide in some of the gases studied e. Until recently, very little was known about effects of CO on survival and growth of microorganisms in aquatic foods.

Figure 5. A study by Balaban et al. No treatment represents samples left in oxygen-permeable bags for 48 h prior to freezing. It is very likely that the effectiveness of the CO and FS treatments is a combination of effects and is not simply explained. Work with another species, mahimahi, has also demonstrated a reduction in aerobic microorganisms during CO or FS treatment Fig.

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Freezing is known to reduce the level of bacteria in tuna as a function of time Eitenmiler et al. No treatment represents samples left in oxygen-permeable bags for 24 or 48 h. Pivarnik and coworkers Leydon et al. The study did however compare a fresh control with a previously frozen FS product, from two different sources, which makes it hard to conclusively say that the FS had an antimicrobial effect. Interestingly, the FS-treated products in the study, although having lower aerobic microbial levels, had a lower level of acceptance as judged by a sensory panel.

Aquatic Foods Treated with CO 71 that of fresh untreated tuna. This demonstrates one of the potential problems that exist with the use of this technology. This suggests a possible direct action of the CO molecule, which was at higher levels in this tuna muscle than in the muscle from the other treatments. It is well known that CO has a dramatic effect on respiration mechanisms Chalmers Aerobic bacteria contain a number of respiratory enzymes making up its electron transport chain, which is involved in oxidative phosphorylation.

These enzymes, such as cytochromes, have heme groups very similar to that of hemoglobin and myoglobin, and CO can bind to these heme groups and inhibit the oxidative phosporylation mechanisms and thus inhibit aerobic respiration of these microorganisms and affect their survival Prescott et al. The results shown in Fig. However, the untreated tuna in the study by Ross was fresh, which makes comparison with the CO treatments questionable.

Kristinsson et al. Garner et al. The results demonstrated in Fig. It is possible that both these gases work in combination to reduce and suppress microbial growth. More research is needed in this area. No treatment represents samples left in oxygen-permeable bags for 48 h prior to aerobic storage. Aquatic Foods Treated with CO 73 5. This reaction is particularly rapid at high ambient temperatures.

Fish may contain toxic levels of histamine before appearing spoiled or organoleptically unacceptable Lopez-Sabater et al. If the processes are employed correctly, including a freezing step after treatment, there is little reason for concern. This demonstrates how effective freezing is in reducing the formation of histamine.

Histamine-forming bacteria are able to grow and produce histamine over a wide range of temperature, but growth is more rapid at higher temperatures and even moderately abusive conditions promote their growth FDA The most effective way to minimize histamine formation is proper temperature control, particularly very low temperatures or frozen storage, which may kill or injure the histamine-forming bacteria Arnold et al. However, histidine decarboxylase may remain stable even during frozen storage and can be active soon after thawing.

Some results indicate that there may even be a suppressive effect on histamine formation, directly or indirectly, when products are treated with CO or FS. Fish muscle is especially susceptible to lipid oxidation due to relatively high proportions of polyunsaturated fatty acids. Furthermore, unsaturated aldehydes, which are secondary products of lipid oxidation, such as 2-heptenal, 2nonenal, and 4-hydroxynonenal, have been shown to promote heme protein oxidation Faustman et al.

Dark muscle has been successfully stabilized by antioxidant treatments Kelleher et al. Stabilization of heme proteins to oxidation is thus expected to reduce the oxidation of lipids. When hemoglobin and myoglobin bind to carbon monoxide they are very effectively stabilized and remain in the reduced state and do not easily oxidize, even when subjected to relatively abusive conditions Kristinsson et al.

Several studies support this postulation. Gases containing CO and FS reduced oxidation in mackerel dark muscle to some extent. Gases containing CO were highly effective in reducing oxidation in mackerel white muscle less in red muscle , while those containing FS were less effective Fig. Carbon monoxide stabilizes heme proteins and provides protection from heme oxidation. This stabilization very possibly reduces Aquatic Foods Treated with CO 79 the prooxidative activity of the heme proteins.

The increase in CO percentage was also correlated with reduced metMb formation Luno et al. There is therefore strong evidence that CO in muscle may retard lipid oxidation. Filtered wood smoke is reported to contain phenolic compounds Hawaii International among a number of other chemical compounds derived from smoking.

Some phenolic compounds can function as antioxidants. It is well known that some antioxidants may under certain circumstances be prooxidative. More research is needed on this area. Oxidation of heme proteins has been connected to textural changes in muscle Rowe et al. The direct prooxidative action of heme proteins and oxidation products formed from their action on lipids can lead to oxidation of muscle proteins, which subsequently can cross-link and aggregate i. Cross-linking of muscle proteins 80 Use of CO and Filtered Smokes and reduction in their solubility has been connected to textural problems in muscle Parkington et al.

Firmness and elasticity decreased for the treated and untreated tuna with freezing and during subsequent cold storage, but no differences were found between any of the treatments. This decrease is in line with previous studies, where decreased cohesiveness has been demonstrated with frozen and thawed seafood Gill et al. Results for expressible moisture and drip loss were in line with the compression results, i. All of the samples had a large increase in expressible moisture and drip loss on thawing, which was expected.

References Ahmed, F. In: Seafood Safety. Arnold, S. Balaban, M. Benjakul, S. Brewer, M. Food Qual. Chalmers, A. Clingman, C. Abstract 68—9. Abstract 68— Eitenmiler, R.

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Martin, G. Flick, C. Hebard, and D. Ward eds. Avi Publ. Everse, J. Faustman, C. Francisco, D. Gill, T. Hawaii International Seafood, Inc. Kaffegakis, J. Kelleher, S. Le Blanc, E. Leydon, N. Abstract 89A Lopez-Sabater, E. Food Prot. Luno, M. Munasinghe, D. Offer, G. Lawrie ed. Elsevier Applied Science, London, pp. Parkington, J. Prescott, L. Microbiology, 3rd edn. Brown, Dubuque, IA. Ramirez-Suarez, J. Muscle Foods, — Rawles, D. Food Nutr. Rowe, L. Rozbeh, M. Food Safety, — Samson, A. Food Biochem.

Skinner, G. Smith, J. Part 2: Storage aspects. Srinivasan, S. Food Agric. Undeland, I. Van Laack, M. Xiong, C. Ho, and F. Shahidi eds. As a result, CO will displace oxygen on hemoglobin, even at very low partial pressure, and will prevent transport of oxygen by the blood OSHA Low concentrations of CO, well below the levels considered to be hazardous, will produce a very stable, bright red meat color that is visually indistinguishable from oxymyoglobin.

Oxymyoglobin provides the cherry red color that is preferred for marketing of fresh red meat products. The development and stability of CObased color has its greatest impact on meat products with the highest myoglobin content, such as beef or lamb. Research investigating the use of carbon monoxide for meat color dates back to at least the s when CO was demonstrated to preserve color of freeze-dried beef by the United States Quartermaster Corp Tappel et al.

Tappel subsequently reported that cooked beef exposed to CO developed red color if reducing conditions were present. A patent for the use of CO for meat color preservation was issued in Williams No doubt the concept of using CO for color development and maintenance in red meat originated from the knowledge that bright red hemoglobin and myoglobin provided presumptive diagnostic evidence of carbon monoxide poisoning, but the origins of the original observations of CO effects on heme color are not clear.

Early research on meat products investigated a range of CO concentrations. El-Badawi et al. They reported that CO resulted in a day color life compared with 5 days for aerobically packaged samples. Other researchers have studied CO concentrations ranging from 0. The use of high concentrations of CO is extremely effective for color preservation of red meat. On the other hand, low concentrations 0. They reported that CO at 0. The current consensus of research reports and commercial applications seems to be that 0. As indicated earlier, research has made it clear that less than 1.

Most industrial applications have used 0. The recent approvals in the United States permit use of 0. While the direct advantages of CO for fresh meat color development and stability are well established, there are several other color-related aspects of CO use that are not as obvious. Consequently, use of CO directly enhances color shelf life and indirectly enhances microbial shelf life.

The color effects of CO also offer a means to prevent the discoloration often observed following irradiation of beef. Nanke et al. Kusmider et al. An interesting sidelight to the color changes induced by irradiation of beef is the pinkening or reddening observed in irradiated pork and turkey.

Nam and Ahn found that irradiation resulted in production of CO in both aerobic and vacuum-packaged turkey breast muscle. The amounts of CO produced were dose-dependent but were as high as and ppm for aerobic and vacuum-packaged products, respectively, following a 5. Consequently, it is believed that generation of CO as a result of irradiation processing results in some CO-myoglobin formation.

In meat with low myoglobin concentration, the amount of CO-myoglobin is enough to cause pinkening. Premature browning is considered a potential food safety problem because consumers may assume a product to be fully cooked at temperatures where pathogens survive Lyon et al. John et al. While premature browning in cooked beef can be prevented by CO, the use of CO atmospheres may also result in a greater retention of pinkness following cooking. The reason that CO atmospheres result in internal color changes in red meat is because CO slowly penetrates meat cuts from the surface to eventually form CO-myoglobin throughout the products, if the products are held in a CO atmosphere.

Oxygen, on the other hand, in fresh meat is metabolized as it penetrates from the surface and is depleted at some depth below the surface. Consequently, red oxymyoglobin color is a surface color in red meat, whereas CO-myoglobin begins as a Use of CO for Red Meats 91 surface color but eventually becomes continuous throughout the product when under a CO atmosphere.

Jayasingh et al. Ground beef in a 0. Krause et al. Removal of the CO atmosphere will stop the penetration of color change in red meat, but not immediately. Consequently, it appears doubtful that CO alone at concentrations most commonly used for red meat 0. Higher concentrations of CO, however, even on a short-term basis, may help extend microbial shelf life. If, however, bacteria have already entered the logarithmic phase of growth, the effects of carbon dioxide are greatly reduced.

Thus, carbon monoxide offers the opportunity to utilize increased concentrations of carbon dioxide for packaging of red meat and increased shelf life, but low initial microbial numbers are very important to the success of this approach. Because increased concentrations of carbon dioxide offer the potential for improved microbial control, researchers have studied carbon dioxide concentrations as high as Research with very high carbon dioxide Preliminary results suggest that the very high carbon dioxide Use of CO for Red Meats 93 atmospheres contribute to improved inhibition of growth of these pathogens J.

Sebranek, unpublished data. One of the limitations to using very high carbon dioxide atmospheres for red meat has been carbon dioxide absorption by meat products. Carbon dioxide is highly soluble in meat, and packaged products will absorb a large proportion of this gas from a package atmosphere. When the product is cooked, absorbed gas can quickly expand and result in physical disruption of the tissue Bruce et al. Research with atmospheres containing Ground beef patties stored in Consequently, the amount of carbon dioxide that can be successfully utilized in MAP applications for microbial control will be limited by the amount of physical and textural change that occurs from release of absorbed gas in products following cooking or reheating.

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Please make the prior-learning F identified with your catalog. Odor evaluation of shrimp treated with different chemicals using an electronic nose and a sensory panel Journal of Aquatic Food Product Technology. Inactivation of polyphenol oxidase in muscadine grape juice by dense phase-CO2 processing Food Research International. Enhancing the retention of phytochemicals and organoleptic attributes in muscadine grape juice through a combined approach between dense phase CO2 processing and copigmentation.

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