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Combination of NMR and MRI Techniques for Non-invasive Assessment of Sea Cucumber (Stichopus japonicas) Tenderization During Low-Temperature Heating Process

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Abstract

The purpose of this study was to develop and test the combination of nuclear magnetic resonance (NMR) and magnetic resonance imaging (MRI) method to assess the proton changes of sea cucumber body wall during low-temperature heating process. NMR relaxometry and MRI measurements indicated a significant proton change in the internal structure for sea cucumber body wall when the heating temperature increased from 45 to 55 °C. Differential scanning calorimetry (DSC) analysis revealed that the denaturation temperature of sea cucumber body wall was in the range of 45–55 °C with an endothermic peak at 51 °C, which is in accordance with the result observed in NMR and MRI. Rheological study showed similar trend to the DSC thermogram. The band change in amide I region of Fourier transform infrared (FTIR) spectra indicated the decrease in α-helix content and possible formation of other secondary structures. Scanning electron microscopy (SEM) further confirmed that the low-temperature heating did induce microstructure changes. The analysis of the Ringerʼs soluble fraction (RSF), enzyme-labile fraction (ELF), and total unaltered fraction (TUF) for sea cucumber body wall during low-temperature heating provided more detailed information on the cause of structure change observed in NMR and MRI. The NMR parameters were highly correlated with the rheology storage modulus (G′), relative enzymatic assay parameters, RSF, ELF, and TUF. All these results demonstrated that it could be possible to use NMR and MRI to assess sea cucumber tenderization during low-temperature heating process.

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References

  • Bertram HC, Wu Z, Berg FVD, Andersen HJ (2006) NMR relaxometry and differential scanning calorimetry during meat cooking. Meat Sci 74:684–689. doi:10.1016/j.meatsci.2006.05.020

    Article  CAS  Google Scholar 

  • Carneiro CDS, Mársico ET, Ribeiro RDOR, Conte Júnior CA, Álvares TS, De Jesus EFO (2013) Quality attributes in shrimp treated with polyphosphate after thawing and cooking: a study using physicochemical analytical methods and low-field1H NMR. J Food Process Eng 36:492–499. doi:10.1111/jfpe.12011

    Article  CAS  Google Scholar 

  • Cui F-X, Xue C-H, Li Z-J, Zhang Y-Q, Dong P, Fu X-Y, Gao X (2007) Characterization and subunit composition of collagen from the body wall of sea cucumber Stichopus japonicus. Food Chem 100:1120–1125. doi:10.1016/j.foodchem.2005.11.019

    Article  CAS  Google Scholar 

  • Dileep A, Shamasundar B, Binsi P, Badii F, Howell N (2005) Effect of ice storage on the physicochemical and dynamic viscoelastic properties of ribbonfish (Trichiurus spp) meat. J Food Sci 70:E537–E545. doi:10.1111/j.1365-2621.2005.tb08316.x

    Article  CAS  Google Scholar 

  • Geng S, Wang H, Wang X, Ma X, Xiao S, Wang J, Tan M (2015) A non-invasive NMR and MRI method to analyze the rehydration of dried sea cucumber. Anal Methods-UK 7:2413–2419. doi:10.1039/C4AY03007A

    Article  CAS  Google Scholar 

  • Goetz J, Koehler P (2005) Study of the thermal denaturation of selected proteins of whey and egg by low resolution NMR. LWT-Food Sci Technol 38:501–512. doi:10.1016/j.lwt.2004.07.009

    Article  CAS  Google Scholar 

  • Han M, Zhang Y, Fei Y, Xu X, Zhou G (2009) Effect of microbial transglutaminase on NMR relaxometry and microstructure of pork myofibrillar protein gel. Eur Food Res Technol 228:665–670. doi:10.1007/s00217-008-0976-x

    Article  CAS  Google Scholar 

  • Herrero AM, Carmona P, García ML, Solas MT, Careche M (2005) Ultrastructural changes and structure and mobility of myowater in frozen-stored hake (Merluccius merluccius L.) muscle: relationship with functionality and texture. J Agric Food Chem 53:2558–2566. doi:10.1021/jf0490706

    Article  CAS  Google Scholar 

  • Hill F (1966) The solubility of intramuscular collagen in meat animals of various ages. J Food Sci 31:161–166. doi:10.1111/j.1365-2621.1966.tb00472.x

    Article  CAS  Google Scholar 

  • Hong Y-S, Cho J-H, Kim N-R, Lee C, Cheong C, Hong KS, Lee C-H (2009) Artifacts in the measurement of water distribution in soybeans using MR imaging. Food Chem 112:267–272. doi:10.1016/j.foodchem.2008.05.109

    Article  CAS  Google Scholar 

  • Kim S-K, Himaya S (2012) Triterpene glycosides from sea cucumbers and their biological activities. Adv Food Nutr Res 65:297–319. doi:10.1016/B978-0-12-416003-3.00020-2

    Article  Google Scholar 

  • Kr S (1986) Vibrational spectroscopy and conformation of peptides, polypeptides, and proteins. Adv Protein Chem 38:181–364

    Article  Google Scholar 

  • Lee DC, Haris PI, Chapman D, Mitchell RC (1990) Determination of protein secondary structure using factor analysis of infrared spectra. Biochemist 29:9185–9193. doi:10.1021/bi00491a012

    Article  CAS  Google Scholar 

  • Leikina E, Mertts M, Kuznetsova N, Leikin S (2002) Type I collagen is thermally unstable at body temperature. P Natl Acad Sci USA 99:1314–1318. doi:10.1073/pnas.032307099

    Article  CAS  Google Scholar 

  • Li C, Liu D, Zhou G, Xu X, Qi J, Shi P, Xia T (2012) Meat quality and cooking attributes of thawed pork with different low field NMR T 21. Meat Sci 92:79–83. doi:10.1016/j.meatsci.2011.11.015

    Article  Google Scholar 

  • Liu J, Zhu K, Ye T, Wan S, Wang Y, Wang D, Li B, Wang C (2013) Influence of konjac glucomannan on gelling properties and water state in egg white protein gel. Food Res Inter 51:437–443. doi:10.1016/j.foodres.2013.01.002

    Article  CAS  Google Scholar 

  • Liu L, Zhang Z, Liu Q, Yang B, Huang J, Gao X (2012) Rheological and structural properties of sea cucumber Stichopus japonicus during different heating temperature. Int J Fish Aquaculture 4:209–216. doi:10.5897/IJFA12.027

    Google Scholar 

  • Liu R, Zhao S-M, Xiong S-B, Xie B-J, Qin L-H (2008) Role of secondary structures in the gelation of porcine myosin at different pH values. Meat Sci 80:632–639. doi:10.1016/j.meatsci.2008.02.014

    Article  CAS  Google Scholar 

  • Lomiwes D, Farouk M, Wu G, Young O (2014) The development of meat tenderness is likely to be compartmentalised by ultimate pH. Meat Sci 96:646–651. doi:10.1016/j.meatsci.2013.08.022

    Article  CAS  Google Scholar 

  • Marcone MF, Wang S, Albabish W, Nie S, Somnarain D, Hill A (2013) Diverse food-based applications of nuclear magnetic resonance (NMR) technology. Food Res Inter 51:729–747. doi:10.1016/j.foodres.2012.12.046

    Article  CAS  Google Scholar 

  • Nagai T, Suzuki N (2000) Isolation of collagen from fish waste material - skin, bone and fins. Food Chem 68:277–281. doi:10.1016/S0308-8146(99)00188-0

    Article  CAS  Google Scholar 

  • Naganathan GK, Grimes LM, Subbiah J, Calkins CR, Samal A, Meyer GE (2008) Visible/near-infrared hyperspectral imaging for beef tenderness prediction. Comput Electron Agr 64:225–233. doi:10.1016/j.compag.2008.05.020

    Article  Google Scholar 

  • Nakano S, Kousaka J, Fujii K, Yorozuya K, Yoshida M, Mouri Y, Akizuki M, Tetsuka R, Ando T, Fukutomi T, Oshima Y, Kimura J, Ishiguchi T, Arai O (2012) Impact of real-time virtual sonography, a coordinated sonography and MRI system that uses an image fusion technique, on the sonographic evaluation of MRI-detected lesions of the breast in second-look sonography. Breast Cancer Res Treat 134:1179–1188. doi:10.1007/s10549-012-2163-9

    Article  Google Scholar 

  • Patel KK, Khan MA, Kar A (2015) Recent developments in applications of MRI techniques for foods and agricultural produce—an overview. J Food Sci Technol MYS 52:1–26. doi:10.1007/s13197-012-0917-3

    Article  CAS  Google Scholar 

  • Powell T, Hunt M, Dikeman M (2000) Enzymatic assay to determine collagen thermal denaturation and solubilization. Meat Sci 54:307–311. doi:10.1016/S0309-1740(99)00092-3

    Article  CAS  Google Scholar 

  • Rabotyagova OS, Cebe P, Kaplan DL (2008) Collagen structural hierarchy and susceptibility to degradation by ultraviolet radiation. Mat Sci Eng C-Mater 28:1420–1429. doi:10.1016/j.msec.2008.03.012

    Article  CAS  Google Scholar 

  • Sánchez-Valencia J, Sánchez-Alonso I, Martinez I, Careche M (2015) Low-field nuclear magnetic resonance of proton (1H LF NMR) relaxometry for monitoring the time and temperature history of frozen hake (Merluccius merluccius L.) muscle. Food Bioprocess Tech 8:2137–2145. doi:10.1007/s11947-015-1569-x

    Article  Google Scholar 

  • Saito M, Kunisaki N, Urano N, Kimura S (2002) Collagen as the major edible component of sea cucumber (Stichopus japonicus). J Food Sci 67:1319–1322. doi:10.1111/j.1365-2621.2002.tb10281.x

    Article  CAS  Google Scholar 

  • Salomonsen T, Sejersen MT, Viereck N, Ipsen R, Engelsen SB (2007) Water mobility in acidified milk drinks studied by low-field 1 H NMR. Intl Dairy J 17:294–301. doi:10.1016/j.idairyj.2006.04.003

    Article  CAS  Google Scholar 

  • Sano T, Ohno T, Otsuka-Fuchino H, Matsumoto JJ, Tsuchiya T (1994) Carp natural actomyosin: thermal denaturation mechanism. J Food Sci 59:1002–1008. doi:10.1111/j.1365-2621.1994.tb08177.x

    Article  CAS  Google Scholar 

  • Santos PM, Corrêa CC, Forato LA, Tullio RR, Cruz GM, Colnago LA (2014) A fast and non-destructive method to discriminate beef samples using TD-NMR. Food Control 38:204–208. doi:10.1016/j.foodcont.2013.10.026

    Article  CAS  Google Scholar 

  • Shaarani SM, Nott KP, Hall LD (2006) Combination of NMR and MRI quantitation of moisture and structure changes for convection cooking of fresh chicken meat. Meat Sci 72:398–403. doi:10.1016/j.meatsci.2005.07.017

    Article  CAS  Google Scholar 

  • Shao X, Li Y (2010) Classification and prediction by LF NMR. Food Bioprocess Tech 5:1817–1823. doi:10.1007/s11947-010-0455-9

    Article  Google Scholar 

  • Susi H, Byler DM (1986) Resolution-enhanced Fourier transform infrared spectroscopy of enzymes. Method Enzymol 130:290–311. doi:10.1016/0076-6879(86)30015-6

    Article  CAS  Google Scholar 

  • Van Laack R, Stevens S, Stalder K (2001) The influence of ultimate pH and intramuscular fat content on pork tenderness and tenderization. J Anim Sci 79:392–397. doi:10.2527/2001.792392x

    Article  CAS  Google Scholar 

  • Yearbook CFS (2009) China fishery statistical yearbook 2008. Fisheries Bureau, Department of Agriculture of China, Beijing (in Chinese)

    Google Scholar 

  • Yogesh K, Ali J (2014) Effect of mung bean and sprouted mung bean (Vigna radiata) powder on chicken breast meat tenderness, microbial and sensory characteristics. J Food Sci Tech 51:1411–1415. doi:10.1007/s13197-012-0650-y

    Article  CAS  Google Scholar 

  • Zhang L, McCarthy MJ (2012) Black heart characterization and detection in pomegranate using NMR relaxometry and MR imaging. Postharvest Biol Tec 67:96–101. doi:10.1016/j.postharvbio.2011.12.018

    Article  CAS  Google Scholar 

  • Zhang L, McCarthy MJ (2013) NMR study of hydration of navy bean during cooking. LWT-Food Sci Technol 53:402-408. doi:10.1016/j.lwt.2013.03.011

  • Zhou D-Y, Chang X-N, Bao S-S, Song L, Zhu B-W, Dong X-P, Zong Y, Li D-M, Zhang M-M, Liu Y-X (2014) Purification and partial characterisation of a cathepsin L-like proteinase from sea cucumber (Stichopus japonicus) and its tissue distribution in body wall. Food Chem 158:192–199. doi:10.1016/j.foodchem.2014.02.105

    Article  CAS  Google Scholar 

  • Zhou Y, Yang H, Liu S, Yuan X, Mao Y, Liu Y, Xu X, Zhang F (2006) Feeding and growth on bivalve biodeposits by the deposit feeder Stichopus japonicus Selenka (Echinodermata: Holothuroidea) co-cultured in lantern nets. Aquaculture 256:510–520. doi:10.1016/j.aquaculture.2006.02.005

    Article  Google Scholar 

  • Zhu J, Wang D, Dong X, Zhu B (2013) Study on tenderization of sea cucumber (StichoPusjaPonicus) by low-temperature heating. In: Abstract of Food Summit in China 2013 & Annual meeting of Chinese Institte of Food Science and Technology (p. 64). Hangzhou China: Chinese Institte of Food Science and Technology

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Authors and Affiliations

  1. School of Food Science and Technology, Dalian Polytechnic University, National Engineering Research Center of Seafood, 1 Qinggongyuan, Ganjingzi District, Dalian, 116034, China

    Xiuping Dong, Yan Li, Yong Li, Liang Song, Shasha Cheng, Dongmei Li, Bei-Wei Zhu, Dayong Zhou & Mingqian Tan

  2. Engineering Research Center of Seafood of Ministry of Education of China, Dalian, 116034, China

    Xiuping Dong, Yan Li, Shasha Cheng, Dongmei Li, Bei-Wei Zhu, Dayong Zhou & Mingqian Tan

  3. Liaoning Key Laboratory of Seafood Science and Technology, Dalian, 116034, China

    Xiuping Dong, Yan Li, Yong Li, Liang Song, Shasha Cheng, Dongmei Li, Bei-Wei Zhu, Dayong Zhou & Mingqian Tan

  4. National Research and Development Branch Center for Shellfish Processing (Dalian), Dalian, 116034, China

    Xiuping Dong, Yan Li, Yong Li, Liang Song, Dongmei Li, Bei-Wei Zhu & Dayong Zhou

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  1. Xiuping Dong
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Correspondence to Mingqian Tan.

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Funding

This work was supported by the National Nature Science Foundation of China (31401520, 31401519), the National Key Scientific Instrument and Equipment Development Project of China (2013YQ17046307), the National Key Technology Research and Development Program of China in 12th Five-Year Plan (2014BAD04B09), the Public Science and Technology Research Funds Project of Ocean (201505029), and Cultivation Plan for Youth Agricultural Science and Technology Innovative Talents of Liaoning Province (2015002).

Conflicts of Interest

Xiuping Dong declares that he has no conflict of interest. Yan Li declares that he has no conflict of interest. Yong Li declares that he has no conflict of interest. Liang Song declares that he has no conflict of interest. Shasha Cheng declares that he has no conflict of interest. Dongmei Li declares that he has no conflict of interest. Wei-bei Zhu declares that he has no conflict of interest. Dayong Zhou declares that he has no conflict of interest. Mingqian Tan declares that he has no conflict of interest.

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Dong, X., Li, Y., Li, Y. et al. Combination of NMR and MRI Techniques for Non-invasive Assessment of Sea Cucumber (Stichopus japonicas) Tenderization During Low-Temperature Heating Process. Food Anal. Methods 10, 2207–2216 (2017). https://doi.org/10.1007/s12161-016-0770-5

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