Sensory impact of chemical and natural antimicrobials on poultry ...

Sensory impact of chemical and natural antimicrobials on poultry products: a review Shilpa S. Samant,∗ Philip G. Crandall,∗,† Corliss O’Bryan,∗ Jody M. Lingbeck,† Elizabeth M. Martin,‡ and Han-Seok Seo∗,1 ∗

Department of Food Science, University of Arkansas, 2650 North Young Avenue, Fayetteville, AR 72704, U.S.A; † Sea Star International, LLC., 2138 East Revere Place, Fayetteville, AR 72701, U.S.A.; and ‡ Department of Biological and Agricultural Engineering, University of Arkansas, 203 Engineering Hall, University of Arkansas, Fayetteville, AR 72701

Key words: antimicrobials, natural, chemical, sensory characteristics, consumer 2015 Poultry Science 00:1–12 http://dx.doi.org/10.3382/ps/pev134

INTRODUCTION

Treatment of processed poultry products with antimicrobials is one of the most effective strategies for minimizing consumers’ risks associated with consuming poultry products. Antimicrobials used in food products are classified under the broader heading of “preservatives” (Davidson and Branen, 2005). The United States Food and Drug Administration (FDA) defines antimicrobial agents as “substances used to preserve food by preventing growth of microorganisms and subsequent spoilage, including fungistats, mold and rope inhibitors, and the effects listed by the National Academy of Sciences/National Research Council under “preservatives””. The term ‘antibiotics’ is often used as a synonym to an antimicrobial drug. However, antibiotics are used to treat live poultry before slaughter in order to maintain the health of the animal during growth (Grugel and Wallmann, 2004). For the purpose of this review, we will restrict the antimicrobials discussed in this paper to compounds typically used in the processing of poultry in order to delay the outgrowth of pathogens and microbial spoilage post slaughter. Antimicrobial activity of a treatment agent against target microorganisms varies with the concentration of the agent. In many cases, high concentrations are needed to achieve the desired antimicrobial effect. However, it is well known that the higher concentrations of antimicrobials might adversely affect the product in terms of its sensory attributes (Davidson and Branen, 2005). It is worth noting that the sensory attributes may play a major role in determining the

There has been an increase in per capita consumption of poultry. During the period 1980 to 2012, per capita poultry meat consumption (strictly speaking, the amount of poultry meat available for human consumption in the United States) increased from 26.4 to 54.1 pounds per year, whereas red meat consumption decreased by almost an identical amount from 96.3 to 71.2 pounds per year (United States Department of Agriculture, Economic Research Service, 2014). However, this increased consumption of poultry products may increase consumers’ risks of acquiring foodborne illnesses. Among all types of food items associated with foodborne illness, poultry products (e.g., chicken, turkey, etc.) rank number one in terms of the annual estimated cost of illness ($2.4 billion) and loss of quality adjusted life year (QALY; a measure of health-related quality of life) (Batz et al., 2012). To reverse this trend, recently the USDA announced additional regulations for poultry processors to further reduce Salmonella and Campylobacter in poultry products (United States Department of Agriculture, Food Safety and Inspection Service, 2014).

C 2015 Poultry Science Association Inc. Received December 2, 2014. Accepted April 7, 2015. 1 Corresponding author: hanseok@uark.edu

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use in poultry processing, it is vital to consider the antimicrobial-induced changes in sensory aspects from the consumers’ perspectives. In spite of its importance, there has been no systematic review on the influences of antimicrobials on sensory aspects of poultry products. This paper reviews the major antimicrobial agents used in the poultry processing industry and their effects on sensory aspects of the poultry products.

ABSTRACT Antimicrobial agents are added to poultry products after slaughter to prevent the growth of pathogenic and spoilage microorganisms and to extend the shelf-life of these products. Antimicrobials can be either natural or chemical, which may affect the sensory attributes at elevated concentrations, such as surface color, odor, flavor, taste, and texture of the poultry products. Thus, when selecting antimicrobials for

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SAMANT ET AL.

commercial success of the product. Many consumers evaluate the quality of poultry meat based on their sensory attributes and acceptability (Van Loo et al., 2010). Surprisingly, there is no systematic review on the effects of antimicrobials on the sensory aspects of poultry products. This review highlights the influences of the most common antimicrobials on sensory characteristics such as: surface color, taste, odor, flavor, and texture of poultry products.

TYPES OF ANTIMICROBIALS USED IN POULTRY PROCESSING

EFFECT OF ANTIMICROBIALS ON SENSORY ASPECTS OF POULTRY PRODUCTS When choosing either a natural or chemical antimicrobial, it is absolutely critical to know how they influence the sensory characteristics of the poultry products to which they are applied while ensuring that the selected antimicrobial is active against the target

Effect of Antimicrobials on Appearance of Poultry Products Appearance, typically surface color, is probably the sensory parameter that is most affected by the addition of antimicrobials. Visual characteristics are important because they create the first impression of any product and play a pivotal role in consumers’ perception of the product quality. For instance, off-colors, i.e., anything other than the typical visual appearance, are considered a sign of poor quality. One way to evaluate the color characteristics of poultry products is to perform a visual inspection, carried out by trained or untrained panelists. However sensory evaluation, especially descriptive sensory analysis, requires panelists with some degree of training, as well as a controlled testing environment (Murray et al., 2001). Thus in most studies, the effect of antimicrobials on the surface color characteristics of poultry products has usually been assessed instrumentally, using a colorimeter. Instrumental analysis and visual inspection results have not however always been well correlated (Kim and Marshall, 2000; Bauermeister et al., 2008; Keokamnerd et al., 2008). It is worth conducting sensory evaluation tests to determine whether differences in color characteristics can be detected by trained or consumer panelists. In an effort to extend the shelf-life of poultry products, weak organic acids such as citric acid, lactic acid, and malic acid have been shown to have varied effects on the appearance of treated, raw poultry products. For example, chicken legs treated with citric acid by directly adding (2% w/v; Del R´ıo et al. 2007) or dipping (0.052 to 0.156M solution; Gonz´ alez-Fandos et al., 2009) were found to improve the color acceptability during a shelflife study when compared with the untreated control. However, in some cases, chicken legs treated with lactic acid solutions were found to decrease the appearance acceptability when compared to the control samples (Kolsarici and Candogan, 1995). Treatment of chicken legs with succinic acid at 3% (w/v) and 5% (w/v) was shown to develop a greyish appearance with reduced yellowness of skin color (Cox et al., 1974). In addition, other organic acids such as malic acid and benzoic


Antimicrobials used in poultry processing are characterized in numerous ways. One way to classify them is to divide them according to whether they are ‘natural’ or ‘traditional’. Naturally occurring antimicrobials are those derived from plants, animals or microorganisms, whereas traditional ones consist of organic acids and other chemicals that have been used for a long time (Davidson and Branen, 2005). Many consumers are concerned about the use of synthetic chemicals in their food (Crandall et al., 2011; Rainey et al., 2011) and as a result, many companies in the poultry industry have started to use more natural antimicrobials rather than synthetic antimicrobial chemicals in an effort to have a “clean label” on their products. Natural antimicrobials have a plant, animal, and/or microbial origin. Essential oils are the most popular natural antimicrobials (Chouliara et al., 2007; Goni et al., 2009). Oils of oregano, rosemary, clove, and citrus have shown good microbial inhibition in this regard (O’Bryan et al., 2008; Nannapaneni et al., 2009; Thanissery and Smith, 2014). Also, chitosan (Giatrakou et al., 2010; Petrou et al., 2012) and lysozyme (Hughey and Johnson, 1987), which are of animal origin, have been found to have significant antimicrobial activity. Liquid smoke extracts are approved as Generally Recognized as Safe (GRAS) and were found to be an effective antimicrobial for processed meat products such as frankfurters (Gedela et al., 2007; Martin et al., 2010; Lingbeck et al., 2014). Furthermore, some microorganisms themselves have a potential to act as antimicrobial agents. For instance, Koo et al. (2012) showed that lactic acid bacteria, which contained lactate/diacetate, functioned as an antimicrobial agent against Listeria monocytogenes on frankfurters .

microorganism. However, in spite of their importance and long-term use, surprisingly little is known about how antimicrobials influence taste, odor/flavor, appearance, and texture of the poultry products. In previous studies, many researchers have demonstrated little or no impact on the sensory attributes of poultry products resulting from the specific antimicrobials used in their studies. However, since some consumers do raise concerns about the sensory impact of antimicrobials on poultry products, poultry processors need to better understand how antimicrobials can affect consumer acceptability of poultry products.

SENSORY IMPACT OF ANTIMICROBIALS ON POULTRY PRODUCTS

Effect of Antimicrobials on Odor/Flavor of Poultry Products Much of earlier research associated with the sensory impacts of antimicrobials considered odor (referred to as orthonasal olfaction) and flavor (referred to as retronasal olfaction) as a single quality, although they are perceived by different pathways, namely via the nose and mouth, respectively (Rozin, 1982). Because of this historical perspective, in this review the effects of antimicrobials on odor and flavor characteristics will be addressed together (Table 2). In many previous studies, odor and flavor characteristics (especially off-odors) of poultry products were used as parameters indicating the preservative activity of antimicrobials in poultry products. For example, Mastromatteo et al. (2009) reported poultry patties treated with thymol and carvacol essential oils (up to 300 ppm) retarded the off-odors associated with poultry meat over time. Based on how these offodors developed, researchers could assess the effect of specific antimicrobials on the shelf-life of poultry products. Another major focus of previous research has been to test the impact of an antimicrobials’ own distinct odors/flavors on consumer acceptability, as well as the odor profiles of poultry products. Some natural antimicrobials, especially essential oils, have their own distinct odors/flavors which may affect the overall odor/flavor profile of the final product, potentially reducing consumer acceptability of the product. Poultry processors and sensory professionals want to retain the expected poultry odors/flavors (e.g., cooked chicken odor) of poultry products even when odorous antimicrobials are

added. For example, 0.2% (v/w) thyme oil was found to retain the odor of cooked chicken kebabs even though it imparted a distinct yet organoleptically appealing odor of its own (Giatrakou et al. 2010). Chicken noodles treated with peppermint oil (1g/100g sample) were found however to be less liked by the panelists because of the strong mint flavor (Khare et al., 2014). As another example, Sallam et al. (2004) studied the effect of garlic in fresh and powdered form in chicken sausages and illustrated that fresh garlic (50 g/kg) produced a distinct, strong, garlic odor in the sausages that was perceived as unacceptable. By contrast, it has been also found that adding antimicrobials can in fact increase panelists’ acceptance of the odors of poultry products (Petrou et al., 2012; Khare et al., 2014). The addition of oregano oil at 0.25% (v/w) was observed to impart a pleasant odor to chicken breast meat at the beginning of its storage life (Petrou et al., 2012). Khare et al. (2014) demonstrated that the addition of eugenol to chicken noodles (0.1 g/100g) resulted in a more acceptable odor during storage compared to the untreated control. Similarly, a study by Giatrakou et al. (2010) highlighted that a more pleasant odor was observed in prepared readyto-cook products until the 12th day of storage due to the addition of 1.5% (w/v) chitosan when compared to untreated control. Among the organic acids, citric acid treatments have been observed to have varying results on the odor/flavor characteristics of raw, cut-up poultry (Table 2). Treatment with 1% lactic acid solution was considered to be ‘very much acceptable’ when evaluated for odor acceptability by untrained sensory panelists in chicken meat in both raw and grilled states (Okolocha and Ellerbroek, 2005). Another study by Gonz´ alez-Fandos and Dominguez (2006) demonstrated that samples treated with lactic acid produced weaker off-odors when compared to an untreated control. Other organic acids such as peracetic acid, peroxy acids, and sorbic acid, have also shown potential to retain and actually improve the flavor profile of cooked chicken products (Kolsarici and Candogan, 1995; Del R´ıo et al., 2007; Bauermeister et al., 2008). Phosphates are another category of chemical antimicrobial that have been extensively studied, especially TSP. The effect of TSP addition on odor retention and acceptability varied depending on the concentration level. No significant difference was found between cut-up chicken drumsticks dipped in 14% (w/v) TSP and untreated controls (Meredith et al., 2013). Samples treated with 100g/L solution of STPP were found to spoil later than the untreated control due to the development of a putrid flavor in the latter (Vareltzis et al., 1997). Along similar lines, Del R´ıo et al. (2007) highlighted that the pleasant odor characteristics of chicken legs persisted for a longer time for samples treated with 12% TSP when compared to an untreated control.


acid have been found to have no significant changes in appearance acceptability of raw chicken breast fillet with respect to the control fillets (Skrˇrivanov´ a et al., 2011). Chemical agents such as phosphates, particularly trisodium phosphate (TSP), have been studied to a great extent to validate their potency as antimicrobials. Whole chicken carcasses treated with TSP dodecahydrate were found to be pinker in appearance compared to the untreated controls and were preferred by the untrained panelists even after the 8th day of storage (Hollender et al., 1993). Similarly, Vareltzis et al. (1997) observed that whole chickens treated with sodium tripolyphosphate (STPP) did not develop surface slime until the 8th day of storage at 4◦ C, whereas the untreated control samples had slimy surfaces from the 5th day. Details on the effect of antimicrobials on the appearance of a wide range of poultry products, raw, cut-up, cooked and otherwise processed poultry are given in Table 1.

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SAMANT ET AL. Table 1. Effect of antimicrobials on visual characteristics/appearance of poultry products Antimicrobials

Source

Quantity added

Eugenol

natural

0.1 g/100g

chicken noodles descriptive analysis untrained (QDA) (experienced)

8-pt desirability color, scale appearance

increased (desirability)

Khare et al. (2014)

Peppermint oil

natural

1 g/100g



decreased (desirability)

Khare et al. (2014)

Rosemary oil natural

1%

ground chicken thigh meat

8-pt hedonic scale

n.s.

Keokamnerd et al. (2008)

Chitosan

natural

1 g/100g



n.s.

Khare et al. (2014)

Acetic acid

chemical

1% (v/v)

chicken wings

Type of product Type of test

affective test

Type of panel

trained

Type of scale

Attributes tested

color

Sensory impact Reference

affective test

untrained

9-pt hedonic scale

appearance

n.s.

Kim and Marshall (2000)

0.1—5 mg/L chicken breast meat with skin

affective test

untrained

7-pt hedonic scale

appearance

n.s.

Skrˇrivanov´ a et al. (2011)

Citric acid & chemical salts


affective test

untrained

7-pt hedonic scale

appearance

n.s.



2% (w/v)

chicken legs

affective test

untrained

9-pt hedonic scale

color

acceptable

Del R´ıo et al. (2007)


1, 2, & 3% (w/v)

chicken legs

affective test

untrained

7-pt hedonic scale

appearance

n.s. (1%), decreased (2, 3%)

Gonz´ alezFandos et al. (2009)


1% (w/v)

chicken wings

affective test

untrained

9-pt hedonic scale

appearance

n.s.



10% (w/v)

chicken meat & affective test skin

trained

7-pt hedonic scale

appearance

n.s.

Doleˇzalová et al. (2010)


1 and 5% (w/v)

chicken drumstick and fillet

descriptive analysis trained

line scale (100 mm)

flesh color, skin thickness, meat shininess

n.s.

Meredith et al. (2013)

Lactic acid & salts

chemical

1% (v/v)

chicken wings

affective test

untrained

9-point hedonic appearance scale

n.s.


Lactic acid & salts

chemical

1% (v/v)

whole chicken meat

affective test

untrained

7-pt hedonic scale

appearance

acceptable

Okolocha and Ellerbroek (2005)

Lactic acid & salts

chemical

0.11–0.55 mol/L

chicken legs

affective test

untrained

7-pt hedonic scale

color, appearance

decreased (0.55 mol/L)

Gonz´ alezFandos and Dominguez (2006)

Lactic acid & salts

chemical

0.5% lactic acid (with 0.05% sodium benzoate)

whole chicken affective test (raw), breast & thigh (fried)

untrained

9-pt hedonic scale

color

n.s.

Hathcox et al. (1995)

Lactic acid & salts

chemical

3% (v/v)

chicken breast & leg meat

affective test

untrained

9-pt hedonic scale

color, appearance

decreased

Kolsarici and Candogan (1995)

Malic acid & chemical salts


affective test

untrained

7-pt hedonic scale

Appearance of mean & skin

n.s.


Peracetic acid

chemical

0.01, 0.015, & 0.02%

chicken breast fillets

affective test

untrained

8-pt hedonic scale

appearance

decreased (0.01%), acceptable (0.015, 0.02%)

Bauermeister et al. (2008)

Peroxyacids

chemical

220 ppm

chicken legs

affective test

untrained

9-pt hedonic scale

color

acceptable


Propionic acid

chemical

1 & 2% (v/v)

chicken legs

affective test

untrained

7-pt hedonic scale

color, appearance

n.s.

Gonz´ alezFandos and Herrera (2013)

Sorbic acid and salts

chemical

5% (w/v)


affective test

untrained

9-pt hedonic scale

color, appearance

increased

Kolsarici and Candogan (1995)

Succinic acid chemical

1, 3, & 5% (w/v)

chicken legs

quality test

untrained

‘good’, ‘fair’ or ‘poor’ (with additional comments)

appearance

decreased

Cox et al. (1974)

Chlorine and chemical salts

1,200 ppm

chicken legs

affective test

untrained

9-pt hedonic scale

color

acceptable



Benzoic acid chemical & salts

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SENSORY IMPACT OF ANTIMICROBIALS ON POULTRY PRODUCTS Table 1. continued Antimicrobials

Source

Quantity added

EDTA

chemical

35 mg/kg



n.s.

Khare et al. (2014)

Phosphates

chemical

12% (w/v)

chicken legs

affective test

untrained

9-pt hedonic scale

color

decreased


Phosphates

chemical

10% (w/v)

whole chicken meat

affective test

untrained

7-pt hedonic scale

appearance

acceptable


Phosphates

chemical

10 & 14% (w/v)

chicken drumstick & fillet


line scale (100 mm)

flesh color, skin thickness, meat shininess

n.s.

Meredith et al. (2013)

Phosphates

chemical

8,10, & 12% chicken thighs (w/v)

affective test

untrained

9-pt hedonic scale

color

decreased

Capita et al. (2000)

Phosphates

chemical

12% (w/v)

whole chicken affective test (raw), breast & thigh (fried)

untrained

9-pt hedonic scale

color

n.s.

Hathcox et al. (1995)

Phosphates

chemical

5, 10, & 15% chicken legs (w/v)

affective test

untrained

9-pt hedonic scale

appearance

decreased


Phosphates

chemical

12% (w/v)

whole chicken affective test (raw), breast & thigh (cooked)

untrained

9-pt hedonic scale

surface appearance

increased

Hollender et al. (1993)

Phosphates

chemical

100 g/L

whole chicken

affective test

trained

5-pt hedonic scale

appearance (slime)

increased (less slime)

Vareltzis et al. (1997)

Glutamal with lactic acid activator

combined

1% formulation

whole chicken meat

affective test

untrained

7-pt hedonic scale

appearance

increased


Nisin & EDTA

combined

500 & 1,500 chicken fillets IU/g nisin, (without skin) 10 & 50 mM EDTA

affective test

trained

9-pt hedonic scale

appearance

increased

Economou et al. (2009)

0–300 ppm (each)

affective test

untrained

5-pt hedonic scale

color

n.s.

Mastromatteo et al. (2009)

poultry patties

Type of panel

Type of scale

Attributes tested


EDTA = Ethylenediaminetetraacetic acid; Glutamal: sugars, foodstuff phosphates, ascorbic/iso-ascorbic acid or their inorganic salts; QDA = quantitative descriptive analysis; n.s. = no significant difference

Effect of Antimicrobials on Taste of Poultry Products People often refer to the perception of volatile compounds via the oral cavity (i.e., “retronasal olfaction”) as “taste” and this phenomenon is called “smell-taste confusion” (Murphy et al., 1977; Murphy and Cain, 1980; Rozin, 1982). Smell-taste confusion may occur because flavor and taste perception commonly occur in the mouth. It is known that there are only 5 basic qualities of taste: sweetness, sourness, bitterness, saltiness, and umami. The sense of “taste”, along with sense of “smell”, is closely related to food consumption, and it is one of the basic sensory modalities used in assessing the quality of food (Seo and Hummel, 2012). As with the odor/flavor characteristics, earlier research has concentrated on the development of an offtaste in poultry products treated with/without antimicrobials (Table 3). An off-taste is often used as an indicator of microbial spoilage in poultry products, typically occuring during storage (Petrou et al., 2012). Natural antimicrobials of animal origin (e.g., chitosan) have

been reported to retain the typical taste characteristics and delay the onset of an off-taste in processed products such as chicken noodles (Khare et al., 2014), breast meat (Petrou et al., 2012), and chicken kebabs (Giatrakou et al., 2010). However, in many previous studies, an off-odor/flavor has been confused with an off-taste. Again, it should be noted that as opposed to the off-odor perceived by sniffing, the off-taste is experienced by ingestion. Thus more caution is necessary when considering how panelists rate off-taste characteristics, especially in shelf-life studies. Previous research has also focused on the influence of antimicrobials’ own distinct taste on acceptability to consumers, as well as the taste profiles of poultry products. Natural antimicrobials, especially essential oils, tend to have a characteristic taste associated with the source of the essential oil. Essential oils appear to add their own taste-related characteristics into the overall taste attributes of the final product, which may alter taste acceptability. The addition of 1.5% (v/w) chitosan to ready-to-cook (RTC) chicken-pepper kebabs (prepared by the incorporation of fresh chicken pieces and


Thymol & combined carvacol essential oils


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SAMANT ET AL. Table 2. Effect of antimicrobials on odor/flavor profile of poultry products Antimicrobials

Source

Quantity added

Eugenol

natural

0.1 g/100g

Fresh garlic natural (FG), garlic powder (GP) and garlic oil (GO) natural

Oregano oil

natural

Oregano oil

natural

Thyme essential oil

natural

Chitosan

natural

Chitosan

natural

Acetic acid

natural

Benzoic acid natural & salts Citric acid & natural salts Citric acid & natural salts Citric acid & natural salts Citric acid & natural salts Citric acid & natural salts Citric acid & natural salts

Lactic acid & salts Lactic acid & salts

Type of panel

chicken noodles descriptive analysis untrained (QDA) (experienced) chicken sausage sensory intensity untrained test

FG: 20—50 g/ kg GP: 6—15 g/ kg GO: 0.06–0.15 g/kg 0.25% (v/w) chicken breast affective test meat 0.1% (w/w) chicken breast affective test meat 1 g/100 g chicken noodles descriptive analysis (QDA) 0.2% (v/w) RTC cook affective test chicken-pepper kebab 1.5% (v/w) RTC affective test chicken-pepper kebab 1.5% (w/v) chicken breast affective test meat 1% (v/v) chicken wings affective test

Type of scale

increased (desirability) increased (FG)

Khare et al. (2014) Sallam et al. (2004)

9-pt hedonic scale 5-pt hedonic scale 8-pt desirability scale 9-pt hedonic scale

odor

n.s.

odor

acceptable

meat flavor odor

decreased (desirability) acceptable

Petrou et al. (2012) Chouliara et al. (2007) Khare et al. (2014) Giatrakou et al. (2010)

untrained

9-pt hedonic scale

odor

acceptable

Giatrakou et al. (2010)

trained

9-pt hedonic scale 9-pt hedonic scale 7-pt hedonic scale

odor

n.s.

odor

n.s.

odor, flavor

n.s.

Petrou et al. (2012) Kim and Marshall (2000) Skrˇrivanov´ a et al. (2011)

odor, overall n.s. (odor), flavor decreased (flavor) odor n.s.

trained untrained untrained (experienced) untrained

untrained

affective test

untrained

affective test

untrained

7-pt hedonic scale

affective test

untrained

0.052–0.156 M (w/v)

chicken legs

affective test

untrained

9-pt hedonic scale 7-pt hedonic scale

1% (w/v)

chicken wings

affective test

untrained

10% (w/v)

chicken meat & affective test trained skin chicken descriptive analysis trained drumstick & fillet

chicken wings

affective test

untrained

9-pt hedonic scale 7-pt hedonic scale line scale (100 mm)


1% (v/v)

natural

2% (v/v) chicken meat & affective test lactic acid & skin 0.2% (w/v) potassium sorbate 1% (v/v) whole chicken affective test meat

trained

untrained

7-pt hedonic scale

smell

Lactic acid & salts

natural

Lactic acid & salts

natural

0.11–0.55 mol/L

chicken legs

affective test

untrained

7-pt hedonic scale

odor

Lactic acid & salts

natural

3% (v/v)


affective test

untrained

9-pt hedonic scale

flavor

0.1—5 mg/L chicken breast meat (with skin) 0.01, 0.015, chicken breast & 0.02% fillets

affective test

untrained

7-pt hedonic scale

odor, flavor

affective test

untrained

8-pt hedonic scale

flavor

Peracetic acid

natural


Del R´ıo et al. (2007) odor increased Gonz´ alezFandos et al. (2009) odor decreased Kim and Marshall (2000) odor, decreased Doleˇzalová off-flavor (cooked skin) et al. (2010) raw poultry increased Meredith et al. odor, off (cooked chicken (2013) odor, cooked odor) chicken odor, & tainted odor odor decreased Kim and Marshall (2000) odor, increased Doleˇzalov´ a off-flavor et al. (2010)

natural

Malic acid & natural salts


8-pt desirability meat flavor scale 8-pt intensity garlic flavor scale

0.1—5 mg/L chicken breast meat (with skin) 0.1—5 mg/L chicken breast meat (with skin) 2% (w/v) chicken legs

1 & 5% (w/v)

Attributes tested

acceptable

Okolocha and Ellerbroek (2005) increased Gonz´ alezFandos and Dominguez (2006) n.s. Kolsarici and Candogan (1995) n.s.(uncooked Skrˇrivanov´ a odor), decreased et al. (2011) (cooked flavor) decreased Bauermeister (0.01%), et al. (2008) acceptable (0.015, 0.02%)


Oregano oil


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SENSORY IMPACT OF ANTIMICROBIALS ON POULTRY PRODUCTS Table 2. continued Source

Quantity added


Type of panel

Type of scale

Peroxyacids

natural

220 ppm

chicken legs

affective test

untrained

Sorbic acid & salts

natural

5% (w/v)


affective test

untrained


Chlorine & salts Phosphates

chemical

1,200 ppm

chicken legs

affective test

untrained

chemical

12% (w/v)

chicken legs

affective test

untrained

Phosphates

chemical

10%

whole chicken meat

affective test

untrained

Phosphates

chemical

10 & 14% (w/v)

chicken drumstick & fillet


line scale (100 mm)

Phosphates

chemical

affective test

untrained

Phosphates

chemical

8,10, & 12% chicken thighs (w/v) 5, 10, & 15% chicken legs (w/v)

affective test

untrained


Phosphates

chemical

8% (w/v)

untrained

9-pt hedonic scale

flavor

Phosphates

chemical

100 g/L

whole chicken affective test (raw), breast & thigh (cooked) whole chicken affective test

trained

odor

Propionic acid

chemical

1 & 2% (v/v)

chicken legs

affective test

untrained


Chitosan & oregano oil

combined

chicken breast meat

affective test

trained

Chitosan & Thyme essential oil

combined

1.5% (w/v) chitosan & 0.25% (v/w) oregano oil 1.5% (v/w) chitosan & 0.2% (v/w) thyme oil 0.2% (v/w) rosemary & 1.5% (w/w) EDTAlysozyme solution 0.2% (v/w) oregano & 1.5% (w/w) EDTAlysozyme solution 0.1–0.3% (v/w) 1% formulation

RTC chicken-pepper kebab

affective test

cooked chicken fillets

EDTAcombined lysozyme & rosemary oil

EDTAlysozyme & oregano oil

combined

EDTA & oregano oil Glutamal with lactic acid activator Nisin & EDTA

combined combined

combined

Thymol & combined carvacrol essential oils

9-pt hedonic scale 9-pt hedonic scale 7-pt hedonic scale

Attributes tested


smell

n.s.

flavor

n.s.

smell

n.s.

smell

n.s.

smell

acceptable

raw poultry n.s. odor, raw off-odor, cooked chicken odor, & tainted odor odor n.s. odor

Del R´ıo et al. (2007) Kolsarici and Candogan (1995) Del R´ıo et al. (2007) Del R´ıo et al. (2007) Okolocha and Ellerbroek (2005) Meredith et al. (2013)

Capita et al. (2000) n.s. (5%) Kim and decreased (10 & Marshall (1999) 15%) n.s. Hollender et al. (1993)

odor

increased (less putrid odor) increased

9-pt hedonic scale

odor

acceptable

untrained

9-pt hedonic scale

odor

acceptable


affective test

trained

9-pt hedonic scale

aroma

acceptable

Ntzimani et al. (2010)


affective test

trained

9-pt hedonic scale

aroma

n.s.


chicken liver meat whole chicken meat

affective test

untrained

acceptable

affective test

untrained

9-point hedonic odor scale 7-pt hedonic smell scale

Hasapidou and Savvaidis (2011) Okolocha and Ellerbroek (2005)

affective test

trained

9-pt hedonic scale

odor

increased


affective test

untrained

5-pt hedonic scale

odor

increased

Mastromatteo et al. (2009)

500 & 1,500 chicken fillets IU/g nisin, (without skin) 10 & 50 mM EDTA 0–300 ppm poultry patties (each)

acceptable

Vareltzis et al. (1997) Gonz´ alezFandos and Herrera (2013) Petrou et al. (2012)

EDTA = Ethylenediaminetetraacetic acid; Glutamal: sugars, foodstuff phosphates, ascorbic/iso-ascorbic acid or their inorganic salts; RTC = ready to cook; QDA = quantitative descriptive analysis; n.s. = no significant difference


Antimicrobials

8

SAMANT ET AL. Table 3. Effect of antimicrobials on taste characteristics of poultry products Antimicrobials

Source

Clove oil

natural

Oregano oil

natural

Oregano oil

natural

Chitosan

natural

Chitosan

natural

Citric acid & chemical salts Citric acid & chemical salts

1 & 2% chicken (v/w) frankfurters 0.25% (v/w) chicken breast meat 0.1% (w/w) chicken breast meat 1.5% (v/w) RTC chicken-pepper kebab 1.5% (w/v) chicken breast meat 2% (v/v) chicken meat & skin 1 & 5% chicken (w/v) drumstick & fillet 2% (v/v) chicken meat & lactic acid & skin 0.2% (w/v) potassium sorbate 10% (w/v) whole chicken meat

Phosphates

chemical

Phosphates

chemical

10 & 14% (w/v)

Chitosan & oregano oil

combined

Chitosan & thyme essential oil

combined

1.5% (w/v) chitosan & 0.25% (v/w) oregano oil 1.5% (v/w) chitosan & 0.2% (v/w) thyme oil 0.2% (v/w) rosemary & 1.5% (w/w) EDTAlysozyme solution 0.2% (v/w) oregano & 1.5% (w/w) EDTAlysozyme solution 0.1–0.3% (v/w) 1% formulation

EDTAcombined lysozyme solution & rosemary oil

EDTAcombined lysozyme solution & rosemary oil

EDTA & oregano oil Glutamal with lactic acid activator Nisin & EDTA

combined combined

combined


Attributes tested

Type of panel

Type of scale

affective test

untrained

taste

affective test

trained

affective test

untrained

affective test

untrained

5-pt hedonic scale 9-pt hedonic scale 5-pt hedonic scale 9-pt hedonic scale

affective test

trained

affective test

trained

9-pt hedonic scale 7-pt hedonic scale line scale (100 mm)



taste

n.s. (1%), decreased (2%) increased

taste

acceptable

taste

increased

taste

increased

taste

decreased

sweet, sour, salty, bitter

saltier

Mytle et al. (2006) Petrou et al. (2012) Chouliara et al. (2007) Giatrakou et al. (2010) Petrou et al. (2012) Doleˇzalov´ a et al. (2010) Meredith et al. (2013)

affective test

trained

7-pt hedonic scale

taste

increased

Doleˇzalov´ a et al. (2010)

affective test

untrained

7-pt hedonic scale

taste

acceptable


line scale (100 mm)

sweet, sour, salty, bitter

n.s.

Okolocha and Ellerbroek (2005) Meredith et al. (2013)

affective test

trained

9-pt hedonic scale

taste

acceptable

Petrou et al. (2012)

RTC chicken-pepper kebab

affective test

untrained

9-pt hedonic scale

taste

acceptable



affective test

trained

9-pt hedonic scale

taste

acceptable



affective test

trained

9-pt hedonic scale

taste

unacceptable


chicken liver meat whole chicken meat

affective test

untrained

taste

acceptable

affective test

untrained


taste

acceptable

Hasapidou and Savvaidis (2011) Okolocha and Ellerbroek (2005)

affective test

trained

taste

acceptable

chicken drumstick & fillet chicken breast meat

500 & 1,500 chicken fillets IU/g nisin, (without skin) 10 & 50 mM EDTA

9-pt hedonic scale


EDTA = Ethylenediaminetetraacetic acid; Glutamal: sugars, foodstuff phosphates, ascorbic/iso-ascorbic acid or their inorganic salts; RTC = ready to cook; n.s. = no significant difference

chopped bell peppers fixed manually on skewers) was observed to contribute to pleasant taste characteristics and enhanced freshness (Giatrakou et al., 2010). Similarly, Chouliara et al. (2007) reported that 1% (w/w) oregano oil in chicken breast meat produced a characteristic desirable taste which went well with the cooked chicken flavor. On the other hand, Mytle et al. (2006) found that higher concentrations of clove oil (around

2% v/w) produced a sharp taste in meat products, such as chicken frankfurters, which was not well accepted by sensory panelists. Earlier research involving combinations of natural antimicrobials has shown that a combination of essential oils with an ethylenediaminetetraacetic acid (EDTA)lysozyme solution seems to be a good approach to increasing the safety of the poultry product whilst



Quantity added


maintaining its preferred taste characteristics. This combination results in a lemon-like taste in chicken fillets which was much appreciated by the panelists (Ntzimani et al., 2010). Hasapidou and Savvaidis (2011) studied the combination of EDTA and oregano oil and found that oregano oil imparted a distinct yet desirable taste to chicken meat. In addition, a combination of EDTA and nisin has proven to be a good option to extend shelf-life in chicken fillets (Economou et al., 2009). Details on the effect of antimicrobials on the taste characteristics of several different types of poultry products are given in Table 3.

Effect of Antimicrobials on Texture of Poultry Products

FURTHER CONSIDERATIONS FOR SENSORY IMPACT OF ANTIMICROBIALS In this review, we have summarized more than 20 years of research on the sensory impact of both chemical and natural antimicrobials on poultry products, and have found numerous gaps in the literature where additional studies need to be conducted to improve our understanding of this vitally important area: r Further studies are needed to answer general and

specific questions as to how the range of commercially used concentrations and combinations of individual antimicrobials impact sensory parameters such as sight, taste, and odor across the major demographics of poultry consumers. r As summarized, the effects of antimicrobials on sensory aspects of poultry products displayed wide variation among previous studies. Since the source of the poultry and the methodologies differed among the studies, it is difficult to directly compare their results. Thus, to provide a better understanding of the sensory impact of individual antimi-

crobials, research should be conducted under controlled conditions so that major sensory attributes of poultry products can be evaluated for both the control (no antimicrobial treatment) and treated cases, with antimicrobials used at commercial concentrations. r When researchers conduct consumer and descriptive sensory analysis to test sensory impacts of antimicrobials on further processed poultry products, they should put more effort into panel training, sample preparation, and lexicon development. In studies where panel training and sample preparation are not well controlled, there might be extraneous influences on the results of sensory analysis. The main purpose of descriptive sensory analysis is to develop a thumbprint of the products sensory profile, which gives researchers a better idea of the various characteristics of their products (Meilgaard et al., 2006). Reliability of the results is based on the consistency and efficiency of carrying out descriptive analysis. Unfortunately, in most of the published studies, sensory analysis was not regarded as the main focus. Accordingly, researchers’ misusage of sensory analysis was often observed. r Major demographic groups of consumers vary in their individual sensory perception and preference. For accurate results, these individual differences should be considered when the type and concentration of antimicrobials are chosen for poultry products. Consumer preferences for poultry products are affected by many factors such as gender, age, and cultural background. Generally, females outperformed males in terms of olfactory performance in odor sensitivity, identification, discrimination, and memory of specific odors (Larsson et al., 2000; Hummel et al., 2007). Also, compared to males, females are more dependent on their sense of smell for daily decision-making because females consider olfaction to be more important attribute (Seo et al., 2011, 2013). A study by Haugaard et al. (2014) evaluating the acceptance of herbs and berries as novel antimicrobials found that female participants were less accepting of newer antimicrobial technologies compared to male participants. Therefore sensory researchers would need to be aware of such expected differences when choosing panelists not only in the sensory perception and acceptability of poultry products treated with antimicrobials, but also in attitudes towards the antimicrobial treated products, especially for all natural antimicrobial products. In addition, based on the findings that older subjects are less capable of discriminating among taste qualities in a product compared to younger subjects (Mojet et al., 2004), there is a high likelihood of age-related bias in the sensory perception and acceptability of poultry products treated with antimicrobials. Furthermore, culturerelated differences in sensory perception and


The impact of antimicrobials on the texture characteristics of poultry meat products has not been studied as extensively as other sensory aspects. A summary of antimicrobial effects on poultry product texture is given in Table 4. Addition of antimicrobials such as garlic, chitosan, vinegar, peppermint oil, and clove oil has not shown to significantly affect the textural quality of chicken in products including noodles and sausages (Sallam et al., 2004; Khare et al., 2014). Kolsarici and Candogan (1995) demonstrated that the addition of 5% (w/v) potassium sorbate solution produced no major difference in texture characteristics when compared to the control with chicken breast and leg meats. However, treatment of chicken breast meat with peracetic acid was found to produce a breast that was more tender in terms of texture than a chlorine control sample at the beginning of a shelf-life study (Bauermeister et al., 2008).

9

10

SAMANT ET AL.

Table 4. Effect of antimicrobials on texture characteristics of poultry products Antimicrobials

Source

Quantity added

Eugenol

natural

0.1g/100g

Fresh garlic natural (FG), garlic powder (GP) and garlic oil (GO)

Peppermint oil Chitosan

FG: 20—50 g/kg GP: 6—15 g/kg GO: 0.06–0.15 g/kg 1 g/100g 1 g/100g


Type of panel

Attributes tested

Type of scale


chicken noodles descriptive analysis untrained (QDA) (experienced) chicken sausage sensory intensity untrained test

8-pt desirability desirability scale of texture 8-pt intensity tenderness scale

n.s.

chicken noodles descriptive analysis untrained (QDA) (experienced) chicken noodles descriptive analysis untrained (QDA) (experienced) chicken descriptive analysis trained drumstick & fillet

8-pt desirability scale 8-pt desirability scale line scale (100 mm)

decreased

Citric acid

chemical

1 & 5% (w/v)

Lactic acid & salts

chemical

3% (v/v)

chicken breast & legs

affective test

untrained

9-pt hedonic scale

Peracetic acid

chemical

0.01, 0.015, & 0.02%

chicken breast fillets

affective test

untrained

8-pt hedonic scale

tenderness

Sorbic acid & salt

chemical

5% (w/v)

chicken breast & legs

affective test

untrained

9-pt hedonic scale

tenderness

EDTA

chemical

35 mg/kg

Phosphates

chemical

8% (w/v)

untrained (experienced) untrained

8-pt desirability desirability scale of texture 9-pt hedonic texture scale

Phosphates

chemical

10 & 14% (w/v)

chicken noodles descriptive analysis (QDA) whole chicken affective test (raw), breast & thigh (cooked) chicken descriptive analysis drumstick & fillet

trained

line scale (100 mm)

n.s. n.s.

n.s.

decreased (0.01%), acceptable (0.015, 0.02%) n.s.

n.s. n.s.

firmness, n.s. moist, dry, chewy, & sticky/gluey

Khare et al. (2014) Khare et al. (2014) Meredith et al. (2013)

Kolsarici and Candogan (1995) Bauermeister et al. (2008)

Kolsarici and Candogan (1995) Khare et al. (2014) Hollender et al. (1993) Meredith et al. (2013)

EDTA = Ethylenediaminetetraacetic acid; QDA = quantitative descriptive analysis; n.s. = no significant difference

acceptability of food products should be considered (Jantathai et al., 2014). For instance, a majority of consumers from Northern Ireland commented that they would never buy chicken with a yellow skin color as they associated it with poor quality. In contrast, consumers in the United States have been reported to actually prefer a yellow color of broiler skin as they consider it to be a sign of freshness and superior quality (Sunde, 1992; Kennedy et al., 2005). This is one example of different consumer concepts on broiler carcasses due to geographical location. Considering the above findings, food processors, sensory professionals, and market managers can design specific antimicrobials which are well fitted to a target consumer group in terms of sensory acceptability. As an example, a higher concentration of some essential oils is appreciated by the elderly in the United States because they may suffer age-related sensitivity loss for odor. However, a high intensity of essential oils could reduce acceptability for young adults who still have a high sensitivity to odor.

CONCLUSION Extensive research has been conducted on maximizing the effects of selected antimicrobials in inhibiting the growth of pathogenic and spoilage microorganisms. There are instances when a very high concentration of antimicrobial needs to be used to achieve the desired effect against a target organism. However, these elevated concentrations might negatively affect the sensory acceptability of the poultry products, ultimately restricting their commercial success. Despite its importance, relatively little attention has been paid to the influence of antimicrobials on the sensory characteristics of further-processed poultry products. However, since sensory acceptability plays an important role in modulating consumers’ willingness to purchase poultry products, it is vital to analyze the sensory impacts of particular antimicrobials on poultry products. It is possible that the added antimicrobial makes the product safe but not commercially acceptable due to a resulting poor sensory quality. It is also possible that antimicrobials can inhibit the necessary sensory perception of spoilage.


desirability of texture desirability of texture firmness, moist, dry, chewy, & sticky/gluey tenderness

n.s.

Khare et al. (2014) Sallam et al. (2004)


Therefore, it is essential to ensure that the poultry product is safe as well as acceptable to consumers and conducting a systematic sensory analysis is extremely important in this regard. Along with effective testing, an analytical approach using descriptive analysis should be also considered for a better understanding of the sensory impact of antimicrobials on poultry meat products. Furthermore, due to consumers’ variation in sensory perception and acceptability, consumer testing should be conducted not only with a wide background of consumers, but also with specific target groups.

ACKNOWLEDGMENTS This study was partially supported by a grant from the USDA SBIR program (USDA-NIFA-SBIR-201233610-20048).

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