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Hyperspectral imaging for one-step growth simulation of Brochothrix thermosphacta in chilled beef during storage

Xiaohua LiuaBinjing ZhouaJin SongbKang TuaJing PengaWeijie Lana()Jing XucJie WucJuqing Wua()Leiqing Pana()
College of Food Science and Technology, Nanjing Agricultural University, Nanjing 210095, China
College of Artificial Intelligence, Nanjing Agricultural University, Nanjing 210095, China
School of Food and Biological Engineering, Bengbu University, Bengbu 233030, China

Peer review under responsibility of Beijing Academy of Food Sciences.

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Highlights

• One-step growth simulation of B. thermosphacta in beef was performed using HSI.

• Three methods for simulating B. thermosphacta growth by HSI were compared.

• Model Ⅰ using PLSR was best to simulate B. thermosphacta growth (R2 = 0.971).

• HSI and plate count methods were highly consistent in growth simulation.

Abstract

In this work, one-step growth models using hyperspectral imaging (HSI) (400–1000 nm) were successfully developed in order to estimate the microbial loads, minimum growth temperature (Tmin) and maximum specific growth rate (μmax) of Brochothrix thermosphacta in chilled beef at isothermal temperatures (4–25 ℃). Three different methods were compared for model development, particularly using (Model Ⅰ) the predicted microbial loads from partial least squares regression of the whole spectral variables; (Model Ⅱ) the selected spectral variables related to microbial loads; and (Model Ⅲ) the first principal scores of HSI spectra by principal component analysis. Consequently, Model Ⅰ showed the best ability to predict the microbial loads of B. thermosphacta, with the coefficient of determination (Rv2) and root mean square error in internal validation (RMSEV) of 0.921 and 0.498 (lg (CFU/g)). The Tmin (–12.32 ℃) and μmax can be well estimated with R2 and root mean square error (RMSE) of 0.971 and 0.276 (lg (CFU/g)), respectively. The upward trend of μmax with temperature was similar to that of the plate count method. HSI technique thus can be used as a simple method for one-step growth simulation of B. thermosphacta in chilled beef during storage.

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References

[1]

J. Han, Y. Liu, L. Zhu, et al., Effects of spraying lactic acid and peroxyacetic acid on the quality and microbial community dynamics of vacuum skin-packaged chilled beef during storage, Food Res. Int. 142 (2021) 110205. https://doi.org/10.1016/j.foodres.2021.110205.

[2]

F. Russo, D. Ercolini, G. Mauriello, et al., Behaviour of Brochothrix thermosphacta in presence of other meat spoilage microbial groups, Food Microbiol. 23 (2006) 797-802. https://doi.org/10.1016/j.fm.2006.02.004.

[3]

X. Yang, L. Zhu, Y. Zhang, et al., Microbial community dynamics analysis by high-throughput sequencing in chilled beef longissimus steaks packaged under modified atmospheres, Meat Sci. 141 (2018) 94-102. https://doi.org/10.1016/j.meatsci.2018.03.010.

[4]

A. Nowak, A. Rygala, E. Oltuszak-Walczak, et al., The prevalence and some metabolic traits of Brochothrix thermosphacta in meat and meat products packaged in different ways, J. Sci. Food Agric. 92 (2012) 1304-1310. https://doi.org/10.1002/jsfa.4701.

[5]

T. Stanborough, N. Fegan, S.M. Powell, et al., Insight into the genome of Brochothrix thermosphacta, a problematic meat spoilage bacterium, Appl. Environ. Microbiol. 83 (2017) e02786-16. https://doi.org/10.1128/AEM.02786-16.

[6]

J. Fang, L. Feng, H. Lu, et al., Metabolomics reveals spoilage characteristics and interaction of Pseudomonas lundensis and Brochothrix thermosphacta in refrigerated beef, Food Res. Int. 156 (2022) 111139. https://doi.org/10.1016/j.foodres.2022.111139.

[7]

N. Illikoud, R. Gohier, D. Werner, et al., Transcriptome and volatilome analysis during growth of Brochothrix thermosphacta in food: role of food substrate and strain specificity for the expression of spoilage functions, Front. Microbiol. 10 (2019) 2527. https://doi.org/10.3389/fmicb.2019.02527.

[8]

L.D.A. Gonçalves, R.H. Piccoli, A.P. Peres A, et al., Primary and secondary modeling of Brochothrix thermosphacta growth under different temperature and pH values, Food Sci. Technol. 38 (2018) 37-43. https://doi.org/10.1590/fst.13317.

[9]

F. Tarlak, K. Khosravi-Darani, Development and validation of growth models using one-step modelling approach for determination of chicken meat shelf-life under isothermal and non-isothermal storage conditions, J. Food Nutr. Res. 60 (2021) 76-86. https://doi.org/10.1177/10820132211049616.

[10]

L. Huang, IPMP Global Fit: a one-step direct data analysis tool for predictive microbiology, Int. J. Food Microbiol. 262 (2017) 38-48. https://doi.org/10.1016/j.ijfoodmicro.2017.09.010.

[11]

L. Huang, C.A. Hwang, Dynamic analysis of growth of Salmonella enteritidis in liquid egg whites, Food Control 80 (2017) 125-130. https://doi.org/10.1016/j.foodcont.2017.04.044.

[12]

Z. Jia, Y. Peng, X. Yan, et al., One-step kinetic analysis of competitive growth of Salmonella spp. and background flora in ground chicken, Food Control 117 (2020) 107103. https://doi.org/10.1016/j.foodcont.2020.107103.

[13]

L. Huang, C. Li, Growth of Clostridium perfringens in cooked chicken during cooling: one-step dynamic inverse analysis, sensitivity analysis, and Markov Chain Monte Carlo simulation, Food Microbiol. 85 (2020) 103285. https://doi.org/10.1016/j.fm.2019.103285.

[14]

S.M. Yoo, S.Y. Lee, Optical biosensors for the detection of pathogenic microorganisms, Trends Biotechnol. 34 (2016) 7-25. https://doi.org/10.1016/j.tibtech.2015.09.012.

[15]

M. Zhu, D. Huang, X.J. Hu, et al., Application of hyperspectral technology in detection of agricultural products and food: a review, Food Sci. Nutr. 8 (2020) 5206-5214. https://doi.org/10.1002/fsn3.1852.

[16]

J.H. Cheng, D.W. Sun, Recent applications of spectroscopic and hyperspectral imaging techniques with chemometric analysis for rapid inspection of microbial spoilage in muscle foods, Compr. Rev. Food Sci. Food Saf. 14 (2015) 478-490. https://doi.org/10.1111/1541-4337.12141.

[17]

J. Guo, W. Wang, H. Zhao, et al., A new PMA-qPCR method for rapid and accurate detection of viable bacteria and spores of marine-derived Bacillus velezensis B-9987, J. Microbiol. Methods 199 (2022) 106537. https://doi.org/10.1016/j.mimet.2022.106537.

[18]

S. Hameed, L. Xie, Y. Ying, Conventional and emerging detection techniques for pathogenic bacteria in food science: a review, Trends Food Sci. Technol. 81 (2018) 61-73. https://doi.org/10.1016/j.tifs.2018.05.020.

[19]

W. Lan, B. Jaillais, A. Leca, et al., A new application of NIR spectroscopy to describe and predict purees quality from the non-destructive apple measurements, Food Chem. 310 (2020) 125944. https://doi.org/10.1016/j.foodchem.2019.125944.

[20]

W.H. Su, H.J. He, D.W. Sun, Non-destructive and rapid evaluation of staple foods quality by using spectroscopic techniques: a review, Crit. Rev. Food Sci. Nutr. 57 (2017) 1039-1051. https://doi.org/10.1080/10408398.2015.1082966.

[21]

Q. Wei, X. Wang, D.W. Sun, et al., Rapid detection and control of psychrotrophic microorganisms in cold storage foods: a review, Trends Food Sci. Technol. 86 (2019) 453-464. https://doi.org/10.1016/j.tifs.2019.02.009.

[22]

E. Bonah, X. Huang, J.H. Aheto, et al., Application of hyperspectral imaging as a nondestructive technique for foodborne pathogen detection and characterization, Foodborne Pathog. Dis. 16 (2019) 712-722. https://doi.org/10.1089/fpd.2018.2617.

[23]

W. Lan, B. Jaillais, S. Chen, et al., Fruit variability impacts puree quality: assessment on individually processed apples using the visible and near infrared spectroscopy, Food Chem. 390 (2022) 133088. https://doi.org/10.1016/j.foodchem.2022.133088.

[24]

F. Tao, Y. Peng, C.L. Gomes, et al., A comparative study for improving prediction of total viable count in beef based on hyperspectral scattering characteristics, J. Food Eng. 162 (2015) 38-47. https://doi.org/10.1016/j.jfoodeng.2015.04.008.

[25]

X. Zheng, Y. Peng, W. Wang, A nondestructive real-time detection method of total viable count in pork by hyperspectral imaging technique, Appl. Sci. 7 (2017) 213. https://doi.org/10.3390/app7030213.

[26]

K. Wang, H. Pu, D.W. Sun, Emerging spectroscopic and spectral imaging techniques for the rapid detection of microorganisms: an overview, Compr. Rev. Food Sci. Food Saf. 17 (2018) 256-273. https://doi.org/10.1111/1541-4337.12323.

[27]

C.H. Feng, Y. Makino, S. Oshita, et al., Hyperspectral imaging and multispectral imaging as the novel techniques for detecting defects in raw and processed meat products: current state-of-the-art research advances, Food Control 84 (2018) 165-176. https://doi.org/10.1016/j.foodcont.2017.07.013.

[28]

R. Vejarano, R. Siche, W. Tesfaye, Evaluation of biological contaminants in foods by hyperspectral imaging: a review, Int. J. Food Prop. 20 (2017) 1264-1297. https://doi.org/10.1080/10942912.2017.1338729.

[29]

Y. Sun, X. Gu, Z. Wang, et al., Growth simulation and discrimination of Botrytis cinerea, Rhizopus stolonifer and Colletotrichum acutatum using hyperspectral reflectance imaging, PLoS One 10 (2015) e0143400. https://doi.org/10.1371/journal.pone.0143400.

[30]

L. Huang, Optimization of a new mathematical model for bacterial growth, Food Control 32 (2013) 283-288. https://doi.org/10.1016/j.foodcont.2012.11.019.

[31]

L. Huang, C.A. Hwang, J. Phillips, Evaluating the effect of temperature on microbial growth rate: the Ratkowsky and a Bělehrádek-Type models, J. Food Sci. 76 (2011) M547-M557. https://doi.org/10.1111/j.1750-3841.2011.02345.x.

[32]

B. Zhou, X. Fan, J. Song, et al., Growth simulation of Pseudomonas fluorescens in pork using hyperspectral imaging, Meat Sci. 188 (2022) 108767. https://doi.org/10.1016/j.meatsci.2022.108767.

[33]

C. Wang, S. Wang, X. He, et al., Combination of spectra and texture data of hyperspectral imaging for prediction and visualization of palmitic acid and oleic acid contents in lamb meat, Meat Sci. 169 (2020) 108194. https://doi.org/10.1016/j.meatsci.2020.108194.

[34]

J. Chen, T. Bai, N. Zhang, et al., Hyperspectral detection of sugar content for sugar-sweetened apples based on sample grouping and SPA feature selecting methods, Infrared Phys. Technol. 125 (2022) 104240. https://doi.org/10.1016/j.infrared.2022.104240.

[35]

L. Zhou, T. Mu, M. Ma, et al., Nutritional evaluation of different cultivars of potatoes (Solanum tuberosum L.) from China by grey relational analysis (GRA) and its application in potato steamed bread making, J. Integr. Agric. 18 (2019) 231-245. https://doi.org/10.1016/S2095-3119(18)62137-9.

[36]

B.M. Nicolaï, K. Beullens, E. Bobelyn, et al., Nondestructive measurement of fruit and vegetable quality by means of NIR spectroscopy: a review, Postharvest Biol. Technol. 46 (2007) 99-118. https://doi.org/10.1016/j.postharvbio.2007.06.024.

[37]

S. López, M. Prieto, J. Dijkstra, et al., Statistical evaluation of mathematical models for microbial growth, Int. J. Food Microbiol. 96 (2004) 289-300. https://doi.org/10.1016/j.ijfoodmicro.2004.03.026.

[38]

T. Ross, Indices for performance evaluation of predictive models in food microbiology, J. Appl. Bacteriol. 81 (1996) 501-508. https://doi.org/10.1111/j.1365-2672.1996.tb03539.x.

[39]

F. Leroi, P.A. Fall, M.F. Pilet, et al., Influence of temperature, pH and NaCl concentration on the maximal growth rate of Brochothrix thermosphacta and a bioprotective bacteria Lactococcus piscium CNCM I-4031, Food Microbiol. 31 (2012) 222-228. https://doi.org/10.1016/j.fm.2012.02.014.

[40]

K. Zhou, P. Fu, P. Li, et al., Predictive modeling and validation of growth at different temperatures of Brochothrix thermosphacta, J. Food Saf. 29 (2009) 460-473. https://doi.org/10.1111/j.1745-4565.2009.00169.x.

[41]

R.C. McKellar, X. Lu, Modeling microbial responses in food, Boca Raton: CRC Press, 2003, pp. 129-135. https://doi.org/10.1201/9780203503942.

[42]

D. Dave, A.E. Ghaly, Meat spoilage mechanisms and preservation techniques: a critical review, Am. J. Agric. Biol. Sci. 6 (2011) 486-510. https://doi.org/10.3844/ajabssp.2011.486.510.

[43]

J. Ma, D.W. Sun, H. Pu, et al., Advanced techniques for hyperspectral imaging in the food industry: principles and recent applications, Annu. Rev. Food Sci. Technol. 10 (2019) 197-220. https://doi.org/10.1146/annurev-food-032818-121155.

[44]

J.H. Cheng, D.W. Sun, Rapid and non-invasive detection of fish microbial spoilage by visible and near infrared hyperspectral imaging and multivariate analysis, LWT-Food Sci. Technol. 62 (2015) 1060-1068. https://doi.org/10.1016/j.lwt.2015.01.021.

[45]

A. Rady, A. Adedeji, Assessing different processed meats for adulterants using visible-near-infrared spectroscopy, Meat Sci. 136 (2018) 59-67. https://doi.org/10.1016/j.meatsci.2017.10.014.

[46]

X. Zheng, Y. Li, W. Wei, et al., Detection of adulteration with duck meat in minced lamb meat by using visible near-infrared hyperspectral imaging, Meat Sci. 149 (2019) 55-62. https://doi.org/10.1016/j.meatsci.2018.11.005.

[47]

R.J. Jackson, K.T. Elvers, L.J. Lee, et al., Oxygen reactivity of both respiratory oxidases in Campylobacter jejuni: the cydAB genes encode a cyanide-resistant, low-affinity oxidase that is not of the cytochrome bd type, J. Bacteriol. 189 (2007) 1604-1615. https://doi.org/10.1128/JB.00897-06.

[48]

W. Chen, Y.Z. Feng, G.F. Jia, et al., Application of artificial fish swarm algorithm for synchronous selection of wavelengths and spectral pretreatment methods in spectrometric analysis of beef adulteration, Food Anal. Methods. 11 (2018) 2229-2236. https://doi.org/10.1007/s12161-018-1204-3.

[49]

S. Weng, B. Guo, P. Tang, et al., Rapid detection of adulteration of minced beef using Vis/NIR reflectance spectroscopy with multivariate methods, Spectrochim. Acta. A. Mol. Biomol. Spectrosc. 230 (2020) 118005. https://doi.org/10.1016/j.saa.2019.118005.

[50]

Y. Ren, D.W. Sun, Monitoring of moisture contents and rehydration rates of microwave vacuum and hot air dehydrated beef slices and splits using hyperspectral imaging, Food Chem. 382 (2022) 132346. https://doi.org/10.1016/j.foodchem.2022.132346.

[51]

X. Gu, Y. Sun, K. Tu, et al., Predicting the growth situation of Pseudomonas aeruginosa on agar plates and meat stuffs using gas sensors, Sci. Rep. 6 (2016) 1-12. https://doi.org/10.1038/srep38721.

[52]

Z. Saleem, M.H. Khan, M. Ahmad, et al., Prediction of microbial spoilage and shelf-life of bakery products through hyperspectral imaging, IEEE Access 8 (2020) 176986-176996. https://doi.org/10.1109/ACCESS.2020.3026925.

[53]

E. Bonah, X. Huang, J.H. Aheto, et al., Comparison of variable selection algorithms on vis-NIR hyperspectral imaging spectra for quantitative monitoring and visualization of bacterial foodborne pathogens in fresh pork muscles, Infrared Phys. Technol. 107 (2020) 103327. https://doi.org/10.1016/j.infrared.2020.103327.

[54]

H. Wang, H. He, H. Ma, et al., LW-NIR hyperspectral imaging for rapid prediction of TVC in chicken flesh, Int. J. Agric. Biol. Eng. 12 (2019) 180-186. https://doi.org/10.25165/ijabe.v12i3.4444.

[55]

X. Yu, X. Yu, S. Wen, et al., Using deep learning and hyperspectral imaging to predict total viable count (TVC) in peeled Pacific white shrimp, J. Food Meas. Charact. 13 (2019) 2082-2094. https://doi.org/10.1007/s11694-019-00129-0.

[56]

L.C. Fengou, A. Lianou, P. Tsakanikas, et al., Evaluation of Fourier transform infrared spectroscopy and multispectral imaging as means of estimating the microbiological spoilage of farmed sea bream, Food Microbiol. 79 (2019) 27-34. https://doi.org/10.1016/j.fm.2018.10.020.

[57]

S. Griffin, M. Magro, J. Farrugia, et al., Towards the development of a sterile model cheese for assessing the potential of hyperspectral imaging as a non-destructive fungal detection method, J. Food Eng. 306 (2021) 110639. https://doi.org/10.1016/j.jfoodeng.2021.110639.

[58]

X. Yin, Y. Zhang, S. Tu, et al., Model for the effect of carbon dioxide on Listeria monocytogenes in fresh-cut iceberg lettuce packaged under modified atmosphere, Food Sci. Technol. Res. 24 (2018) 1021-1027. https://doi.org/10.3136/fstr.24.1021.

Food Science and Human Wellness
Article number: 9250016
Cite this article:
Liu X, Zhou B, Song J, et al. Hyperspectral imaging for one-step growth simulation of Brochothrix thermosphacta in chilled beef during storage. Food Science and Human Wellness, 2025, 14(1): 9250016. https://doi.org/10.26599/FSHW.2024.9250016
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