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Prediction of specific spoilage organisms in smoked chicken legs with modified atmosphere packaging at 4℃ using multivariate statistical analysis

Qiang Wanga, Yubo Zhaoa, Yumeng Suia, Qian Chena, Zhiming Donga, Qian Liua, Baohua Konga(), Ligang Qinb()
College of Food Science, Northeast Agricultural University, Harbin 150030, China
College of Animal Science and Technology, Northeast Agricultural University, Harbin 150030, China

Peer review under responsibility of Beijing Academy of Food Sciences.

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Highlights

• A total of 26 core dominant bacteria were identified during a 25-day storage period.

• Serratia proteamaculans has the highest relative abundance in the spoilage stage.

• A total of 65 key volatile organic compounds (VOCs) were identified during storage.

• A total of four specific spoilage organisms in smoked chicken legs were predicted.

Abstract

The present study monitored bacterial succession, physicochemical properties, and volatile organic compounds (VOCs) changes in smoked chicken legs with modified atmosphere packaging (MAP, 60% CO2 and 40% N2) during a 25-day storage period at 4 ℃. After 15 days of storage, Serratia proteamaculans and Pseudomonas fragi became the predominant bacteria. Furthermore, physicochemical properties changed significantly, as evidenced by an increase in thiobarbituric acid reactive substances and b* (yellowness) value, and a decrease in hardness. A total of 65 VOCs were identified during storage. Correlation between bacterial succession and quality indicators (including VOCs and physicochemical properties) allowed the identification of 26 core dominant bacteria, including S. proteamaculans, Psychrobacter alimentarius, Pseudomonas putida, and Pseudomonas poae, which were positively related to spoilage VOCs (e.g., 1-octen-3-ol, 1-pentanol, and 3-methyl-1-butanol) and could be defined as specific spoilage organisms (SSOs). The results of this study provide a systematic approach to predict SSOs in smoked chicken legs during storage, which can also provide a basis for product safety.

Keywords

Smoked chicken legsModified atmosphere packagingBacterial communityVolatile organic compoundsSpecific spoilage organisms

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Food Science and Human Wellness
Volume 14 Issue 1,
January 2025
Article number: 9250020
DOI: 10.26599/FSHW.2024.9250020
Cite this article:
Wang Q, Zhao Y, Sui Y, et al. Prediction of specific spoilage organisms in smoked chicken legs with modified atmosphere packaging at 4℃ using multivariate statistical analysis. Food Science and Human Wellness, 2025, 14(1): 9250020. https://doi.org/10.26599/FSHW.2024.9250020
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Number of clean reads, observed OTUs, diversity indices (Shannon and Simpson), diversity richness (Chao1 and ACE), and Good’s coverage of amplified 16S rDNA for MAP smoked chicken legs.

Storage time (days) Clean reads OTUs Shannon Simpson Chao1 ACE Good’s coverage
0 9842 69 2.347 0.620 72.438 76.224 0.998
5 13833 124 3.365 0.777 140.714 141.881 0.994
10 21264 131 3.460 0.827 236.056 251.044 0.987
15 10404 91 3.381 0.836 113.895 126.472 0.994
20 15273 50 2.356 0.734 57.091 59.631 0.997
25 14443 34 1.980 0.635 38.546 43.355 0.998

Changes in physicochemical properties of MAP smoked chicken legs during a 25-day storage period at 4℃.

Physicochemical property Storage time (days)
0 5 10 15 20 25
Note: a–e Means within the same row with different lowercase letters differ significantly (P < 0.05).
pH 6.53 ± 0.02d 6.69 ± 0.01c 6.74 ± 0.01b 6.83 ± 0.02a 6.81 ± 0.02a 6.50 ± 0.02d
TBARS (mg/kg) 0.36 ± 0.03e 0.45 ± 0.07de 0.54 ± 0.06cd 0.65 ± 0.05bc 0.75 ± 0.04b 1.04 ± 0.09a
Hardness (N) 5.15 ± 0.60a 4.96 ± 0.58a 4.96 ± 0.40a 4.83 ± 0.35a 4.78 ± 0.21ab 4.24 ± 0.31b
Moisture content (%) 65.30 ± 0.32a 65.63 ± 0.33a 65.33 ± 0.31a 65.81 ± 0.19a 65.54 ± 0.30a 65.62 ± 0.66a
L* 43.25 ± 0.99a 43.95 ± 0.98a 43.16 ± 0.90a 43.86 ± 0.75a 44.09 ± 0.63a 43.20 ± 0.40a
a* 14.89 ± 0.63a 14.73 ± 0.51a 14.43 ± 0.52a 14.05 ± 0.94a 13.44 ± 0.41a 13.38 ± 0.43a
b* 33.57 ± 0.95c 34.02 ± 0.69c 34.53 ± 0.43bc 34.96 ± 0.39bc 36.34 ± 0.46ab 37.48 ± 0.93a

Identification and content (μg/kg) of VOCs in MAP smoked chicken legs during a 25-day storage period at 4 ℃.

VOCs Storage time (days)
0 5 10 15 20 25
Note: a–e Means within the same row with different lowercase letters differ significantly (P < 0.05). n. d.: not detected.
Alcohols (16)
Eucalyptole 4.94 ± 0.31b 3.32 ± 0.22c n. d. n. d. 5.08 ± 0.24b 7.88 ± 0.23a
Ethanol 12.22 ± 0.84e 14.51 ± 1.33e 40.63 ± 0.54d 68.54 ± 1.67c 173.20 ± 3.25b 232.88 ± 2.67a
1-Pentanol 8.09 ± 0.53d 7.45 ± 0.62d 10.03 ± 0.35c 13.75 ± 0.92b 12.69 ± 0.85b 23.75 ± 0.96a
2-Heptenal n. d. 11.11 ± 0.23b n. d. n. d. n. d. 12.65 ± 0.25a
Linalool 22.58 ± 0.34c 12.09 ± 0.37f 18.57 ± 0.31e 20.32 ± 0.23d 32.61 ± 0.34a 25.36 ± 0.26b
1-Hexanol n. d. 6.46 ± 0.22c n. d. 14.11 ± 1.26b 12.81 ± 0.57b 185.26 ± 5.36a
1-Octen-3-ol 88.32 ± 2.35e 81.58 ± 3.24f 129.34 ± 3.54d 157.76 ± 5.26c 218.33 ± 3.24b 231.14 ± 4.39a
1-Heptanol 6.27 ± 0.15a 3.21 ± 0.04b n. d. n. d. n. d. n. d.
Cyclooctanol n. d. 11.07 ± 0.15b 16.94 ± 1.17a 15.89 ± 1.24a n. d. n. d.
trans-2-Octen-1-ol 18.59 ± 0.23b n. d. n. d. n. d. n. d. 20.42 ± 0.32a
Terpinen-4-ol 19.18 ± 0.22b 11.34 ± 0.34e 15.37 ± 0.93c 14.19 ± 1.28c 22.52 ± 0.23a 12.79 ± 0.36d
3-Furanemethanol n. d. n. d. n. d. n. d. n. d. 154.27 ± 3.24a
α-Terpineol n. d. 7.47 ± 0.66b n. d. 9.04 ± 0.55a n. d. 8.34 ± 0.44ab
2,3-Butanediol n. d. n. d. n. d. n. d. 5.24 ± 0.25b 15.01 ± 0.23a
3-Methyl-1-butanol n. d. n. d. n. d. n. d. 5.25 ± 0.31a 5.24 ± 0.24a
1-Dodecanol n. d. 12.31 ± 0.63a 12.97 ± 0.54a n. d. n. d. n. d.
Acids (3)
4-Hydroxybenzenephosphonic acid n. d. n. d. 11.53 ± 0.34b n. d. 13.11 ± 0.15a 4.92 ± 0.09c
Butyric acid n. d. n. d. 1.26 ± 0.31c n. d. 5.67 ± 0.15a 4.67 ± 0.17b
Acetic acid n. d. n. d. n. d. n. d. n. d. 19.18 ± 0.23a
Esters (6)
Ethylcapronate 18.91 ± 0.34d 11.01 ± 0.23e 27.09 ± 0.26c 34.83 ± 1.37b 37.81 ± 0.97a 32.39 ± 1.27b
Hexanoic acid ethenyl ester 38.82 ± 0.54d 30.05 ± 0.28e 46.45 ± 0.54c 73.22 ± 0.55b 81.45 ± 0.23a 24.14 ± 0.21f
Hexylmethanoate 7.27 ± 0.76a n. d. 6.22 ± 0.67a n. d. n. d. n. d.
Heptyl formate n. d. n. d. 3.49 ± 0.05c 5.06 ± 0.22b n. d. 9.07 ± 0.13a
Ethyl caprylate n. d. n. d. n. d. n. d. n. d. 4.26 ± 0.17a
(S)-Menthyl chloroformate 17.13 ± 0.22c 10.99 ± 0.17d 19.99 ± 0.19b n. d. 25.56 ± 0.31a n. d.
Aldehydes (12)
Hexanal 175.49 ± 3.24e 245.02 ± 4.77d 290.38 ± 4.36c 609.11 ± 6.75a 331.19 ± 5.64b 68.65 ± 0.57f
Heptaldehyde 12.04 ± 0.21b 5.46 ± 0.24d n. d. 12.04 ± 0.24b 18.51 ± 0.21a 6.84 ± 0.33c
Benzaldehyde 32.62 ± 1.32b 20.58 ± 0.31c 33.31 ± 1.23b 30.25 ± 1.25b 55.78 ± 0.66a n. d.
(E, E)-2,4-Decanedienal 14.73 ± 1.34c 15.26 ± 0.72c 13.35 ± 0.85c 7.12 ± 0.26d 36.81 ± 0.31a 28.99 ± 0.87b
1-Nonanal 68.99 ± 0.86b 45.96 ± 0.89f 56.34 ± 0.57c 53.95 ± 1.59de 80.57 ± 0.64a 50.28 ± 1.64e
Decyl aldehyde 8.76 ± 0.17b 5.84 ± 0.65c 8.89 ± 0.18b 6.77 ± 0.68c 12.50 ± 0.24a 2.62 ± 0.07d
5-Methyl furfural 369.92 ± 12.65bc 233.54 ± 3.84d 352.44 ± 15.56c 389.62 ± 16.75b 532.66 ± 6.47a 176.18 ± 5.84e
3-Fural dehyde 1423.49 ± 34.22b 823.87 ± 10.74d 1085.02 ± 18.14c 1482.49 ± 24.5b 1697.25 ± 15.57a 335.57 ± 6.57e
Pentadecanal 10.26 ± 0.35b 10.68 ± 0.24b 15.73 ± 0.21a n. d. 4.37 ± 0.25c 4.61 ± 0.29c
Octanal 25.26 ± 0.79b 22.82 ± 0.17c 24.21 ± 0.66b 29.87 ± 0.24a n. d. 15.81 ± 0.23d
p-Anisaldehyde 20.89 ± 0.56b 17.71 ± 0.27c 23.44 ± 0.64b 12.44 ± 0.24d 47.60 ± 0.23a n. d.
trans-Cinnamaldehyde n. d. 16.33 ± 0.44b 22.61 ± 0.22a 5.76 ± 0.21c n. d. n. d.
Ketones (10)
3’-Methylacetophenone 11.93 ± 0.15a 2.46 ± 0.45b 3.15 ± 0.41b n. d. n. d. n. d.
4’-Hydroxyacetophenone n. d. 5.71 ± 0.27b 14.07 ± 0.18a n. d. n. d. 6.21 ± 0.32b
Piperitone 31.64 ± 1.24a 15.21 ± 0.55c 20.28 ± 0.75b 14.43 ± 0.23c 34.63 ± 1.37a 17.31 ± 0.61bc
2-Methyl-3-furanacrolei n. d. 13.34 ± 0.43c 17.81 ± 0.41b 12.26 ± 0.42c 52.89 ± 0.58a 13.39 ± 0.54c
Umbellulon n. d. n. d. n. d. n. d. 31.05 ± 0.24a 5.93 ± 0.21b
Acetophenone 15.97 ± 0.24b 9.87 ± 0.23d 13.82 ± 0.65c 12.84 ± 0.55c 25.83 ± 0.34a 14.08 ± 0.62c
Prenylacetone n. d. n. d. 3.40 ± 0.38b n. d. 6.42 ± 0.08a 2.94 ± 0.32b
1-(3,5-Dimethyl-2-furanyl)-ethanone n. d. 3.09 ± 0.15b 3.25 ± 0.21b n. d. 6.47 ± 0.10a 3.40 ± 0.32b
Acetone n. d. 5.25 ± 0.08e 8.35 ± 0.22d 12.56 ± 0.12c 16.35 ± 0.21b 32.21 ± 0.44a
2,3-Dimethylcyclopent-2-enone 4.64 ± 0.49ab 2.92 ± 0.06c 4.43 ± 0.44ab 4.97 ± 0.35ab 5.99 ± 0.38a 3.39 ± 0.24b
Furans (6)
2-Methyl-5-propionyl-furan n. d. n. d. 7.83 ± 0.31a n. d. n. d. 7.28 ± 0.38a
2-Furfuryl-5-methylfuran n. d. 13.04 ± 0.57a 12.24 ± 0.65a 10.91 ± 0.10b n. d. 13.81 ± 0.61a
2-Methylbenzofuran 21.01 ± 0.23b 14.55 ± 0.54d 19.03 ± 0.25c 11.13 ± 0.19e 29.57 ± 0.16a 15.94 ± 0.75d
5-Methyl-2-acetylfuran 27.06 ± 0.26b 17.36 ± 0.24d 26.76 ± 0.34b 22.51 ± 1.27c 38.25 ± 0.54a 20.46 ± 1.02c
2-Acetylfuran 70.99 ± 0.57c 40.85 ± 0.54e 64.81 ± 0.57d 70.77 ± 0.77c 110.83 ± 1.64a 79.44 ± 0.96b
2,5-Dimethylfuran n. d. n. d. n. d. n. d. 13.08 ± 0.54a 2.94 ± 0.05b
Phenols (2)
Eugenol n. d. 11.93 ± 0.17b n. d. n. d. 22.97 ± 0.27a n. d.
o-Cresol 12.68 ± 0.40c 11.96 ± 0.41c 22.03 ± 0.24b 7.34 ± 0.21d 26.21 ± 0.23a 7.33 ± 0.24d
Alkanes (8)
9-Methyl-octadecane 7.92 ± 0.24a n. d. 5.81 ± 0.48b n. d. 6.33 ± 0.24b n. d.
Tetradecane n. d. n. d. n. d. n. d. 10.96 ± 0.54b 16.91 ± 0.22a
3,8-Dimethyldecane n. d. n. d. n. d. n. d. n. d. 4.90 ± 0.23a
2,2,4,6,6-Pentamethyl-heptan 9.59 ± 0.22c 5.37 ± 0.04d 8.46 ± 0.89c 17.74 ± 0.14b 25.25 ± 0.12a 9.40 ± 0.34c
1-Methyl-2-ethylcyclopentane n. d. n. d. 15.42 ± 0.24b n. d. 26.30 ± 0.54a n. d.
9-Methylnonadecane n. d. 2.97 ± 0.28a 3.41 ± 0.31a n. d. n. d. n. d.
1,2-Epoxyoctadecane n. d. n. d. 6.43 ± 0.21b n. d. 8.95 ± 0.21a n. d.
Heneicosane n. d. n. d. n. d. n. d. 5.56 ± 0.12a 2.49 ± 0.09b
Other compounds (2)
Carbon disulfide n. d. n. d. n. d. 8.58 ± 0.49b 7.99 ± 0.54b 12.94 ± 0.44a
cis-Anethol 40.14 ± 0.94b 22.83 ± 0.14d 34.13 ± 1.14c 31.01 ± 1.26c 67.45 ± 1.14a 30.57 ± 1.04c