噬菌體保鮮技術(shù)在預制菜中的應用研究進展

馮珊紅，鐘樂，程萍，肖乃玉，張雪琴，肖更生，周錦賢

噬菌體保鮮技術(shù)在預制菜中的應用研究進展

馮珊紅，鐘樂，程萍，肖乃玉，張雪琴，肖更生，周錦賢

（1.仲愷農(nóng)業(yè)工程學院 輕工食品學院，廣州 510225；2.廣東省高校中央廚房綠色制造開發(fā)中心，廣州 510225；3.農(nóng)業(yè)農(nóng)村部嶺南特色食品綠色加工與智能制造重點實驗室，廣州 510225）

綜述噬菌體保鮮技術(shù)在預制菜中的應用研究，為預制菜的食品安全保障和噬菌體的應用研究提供依據(jù)。本文以預制菜的食品安全為出發(fā)點，就預制菜進行分類，重點對動植物源食材的噬菌體生物防控的應用研究進行討論。分析表明，噬菌體在預制菜中的應用具有廣泛的應用前景和價值。噬菌體可以有效地控制預制菜中的食源性細菌污染、保持食品品質(zhì)并延長貨架期。為提高噬菌體的抗菌效果，可以從噬菌體的濃度、穩(wěn)定性及其與物理保鮮方法或生物、化學保鮮劑結(jié)合等方面考慮。為實現(xiàn)噬菌體在預制菜中的廣泛應用，還需提高噬菌體的篩選效率和穩(wěn)定性，并制定相應的標準和規(guī)范，以提高消費者的可接受程度，促進噬菌體在國內(nèi)市場的推廣和應用。因此，使用噬菌體保鮮技術(shù)不僅能夠延長預制菜的貨架期、提高食品安全性，還能為食品行業(yè)帶來更多的發(fā)展機遇。

噬菌體；預制菜；食源性細菌；生物防控

預制菜是以畜禽、水產(chǎn)品、果蔬等農(nóng)產(chǎn)品為原料，配以各種輔料，經(jīng)預加工而成的成品或半成品菜肴，分為即食、即熱、即烹、即配[1]。隨著經(jīng)濟社會發(fā)展，對食品工業(yè)提出了新的要求，餐飲行業(yè)的連鎖化和規(guī)?；l(fā)展趨勢顯著，外賣市場和團餐業(yè)務需求強勁，為預制菜行業(yè)帶來了快速發(fā)展的機遇，預制菜因保質(zhì)期長、食用方便等特點廣受青睞[2]。但預制菜對食品的新鮮度和安全性要求高[3]，例如，肉類食品富含蛋白質(zhì)、脂肪等營養(yǎng)成分，易受微生物的侵染，造成食品腐??；果蔬經(jīng)過去皮、切分等加工手段會導致組織細胞損傷、代謝反應急劇活化及微生物污染，造成褐變、萎蔫、黃化、腐爛等品質(zhì)劣變現(xiàn)象[4-5]。食源性細菌污染一直是食品加工過程中需要注重的關鍵問題之一。據(jù)數(shù)據(jù)顯示，美國居民因食用感染產(chǎn)志賀毒素的大腸桿菌的生菜和李斯特菌的金針菇分別導致240人和36人患病[6-7]，以致大量新鮮農(nóng)產(chǎn)品被召回，造成重大糧食損失。因此預制菜的加工、儲運環(huán)節(jié)需要嚴格把控，以抑制食源性細菌并保證食品安全。

為延長預制菜的貨架期，需要從生產(chǎn)端消除食源性細菌的影響，常用的保鮮技術(shù)有：物理方法，即超高壓、輻照、冰溫冷藏、氣調(diào)包裝等[8-12]；化學方法，即無機鹽、有機酸及其鹽類等[13-16]；生物方法，即殼聚糖、植物精油、乳酸鏈球菌素（Nisin From，Nisin）、納他霉素、溶菌酶等[17-22]。這些常規(guī)方法已在食品保鮮中長期實施，其中生物保鮮技術(shù)有很大的發(fā)展空間，被認為是一種可持續(xù)、安全和環(huán)保的選擇，具有天然、無毒、可降解的特點。為提高預制菜的質(zhì)量，減少殺菌帶來的品質(zhì)下降，噬菌體殺滅食源性細菌的方式受到國內(nèi)外研究學者的廣泛關注[23]。噬菌體具有特異性強、裂解效果好、可持續(xù)發(fā)揮作用等優(yōu)點，雖然噬菌體與宿主菌共進化會降低噬菌體的有效性，但也會導致噬菌體在不同宿主細胞中有更廣泛、更針對性的遺傳多樣性，從而提高了噬菌體在不同環(huán)境下的適應性和生存能力[24]。

本文圍繞預制菜，將其分為生鮮肉制品、熟肉制品以及果蔬類。闡述了在預制菜領域中噬菌體控制食源性細菌的研究應用進展，涵蓋了噬菌體在食品檢測領域的應用。為保障預制菜的食品安全和噬菌體制劑的研發(fā)提供依據(jù)。

1 噬菌體特性

噬菌體是地球上最多樣化的生命形式，其數(shù)量是細菌的104倍，在環(huán)境中無處不在，能夠裂解目標細菌，對食品中的病原菌具有高效的殺滅作用，并且是一種非化學性的殺菌，對人體健康無不良影響[25-27]。作為細菌的天敵，噬菌體可以通過裂解復制循環(huán)或溶源循環(huán)在宿主細菌內(nèi)裂解或溶源化，分別稱為裂解性噬菌體和溫和性噬菌體（圖1）[28]。早在20世紀20年代就已提出噬菌體療法[29]，但抗生素的出現(xiàn)導致人們忽略對噬菌體治療的深入研究，隨著抗生素耐藥性的上升，噬菌體療法再次成為人們關注的焦點，被認為是預防或治療耐藥細菌感染的潛在工具。噬菌體治療已得到世界各地的認可，在動植物治療、食品、醫(yī)藥等領域研究廣泛，并已有獲得美國食品藥監(jiān)局認證的噬菌體產(chǎn)品，用于控制肉類及家禽產(chǎn)品的食源性細菌[30]。

噬菌體的發(fā)現(xiàn)及其在食品中的應用，為抑菌劑的種類增添了新的選擇，提供了一種安全、高效且具有強大靶向性的生物抑菌劑[31]?？偨Y(jié)起來，不同的保鮮技術(shù)有不同的特點，歸納見表1。

圖1 噬菌體的裂解和溶源循環(huán)

2 噬菌體在生鮮肉制品的應用研究

生鮮肉類營養(yǎng)豐富，自由水含量較高，pH為5.7～6.5，這些條件都有利于微生物的生長繁殖[32]。最常見的是細菌感染，例如沙門氏菌、霍亂弧菌等，這些細菌可能會導致食物中毒和腸道感染等疾病。有研究證實噬菌體可用于抑制碎牛肉、牛肉片、豬肉、雞肉的大腸桿菌、沙門氏菌以及單核增生李斯特桿菌的污染[33-40]，均有顯著的抑菌效果。

表1 噬菌體保鮮技術(shù)與常規(guī)保鮮技術(shù)的對比

Tab.1 Comparison between phage preservation technology and conventional preservation technology

預制菜生鮮肉的冷鏈貯藏過程中引入特定的噬菌體可以抑制細菌的生長，從而減少細菌污染的風險。Abhisingha等[41]將噬菌體雞尾酒用于減少冷藏期間雞肉上的沙門氏菌，在?20 ℃仍有一定的抑制效果；錢蓓蕾等[42]在0、4 ℃條件下將噬菌體作用于感染李斯特氏菌的蝦仁24 h后，發(fā)現(xiàn)細菌死亡率均可達到99.9%；Xu等[43]將噬菌體作用于受污染的三文魚片和扇貝，在4 ℃貯藏7 d后可將鼠傷寒沙門氏菌的數(shù)量降低至檢測限以下。為了最大限度地發(fā)揮噬菌體的作用，可采用協(xié)同應用的方式。比如，在有氧、真空或氣調(diào)（CO2和O2的體積分數(shù)分別為95%和5%）環(huán)境下，可以增強噬菌體制劑對牛肉、雞胸肉中的大腸桿菌和沙門氏菌的抑制效果[44-45]。將噬菌體與Nisin、山梨酸鉀組合處理污染沙門氏菌的冷鮮豬肉[46]，與有機酸結(jié)合處理雞肉中的腸炎沙門氏菌[47]，與月桂酸精氨酸乙酯（Lauroyl Arginate Ethyl Ester，LAE）聯(lián)合抑制雞胸肉中的單核增生李斯特菌[48]，均能提高整體的抑菌效果。

在食品保鮮中，噬菌體與材料結(jié)合可賦予食品包裝材料抑菌性能，但噬菌體在應用過程中受到環(huán)境因素的影響，其活性容易降低，Cui等[49]研發(fā)了脂質(zhì)體包裹噬菌體的殼聚糖膜，增加噬菌體的穩(wěn)定性和成活率，其包封率可達（57.66±0.12）%。包裹噬菌體的脂質(zhì)體應用于人工污染的牛肉，帶正電荷的脂質(zhì)體與帶負電荷的細菌結(jié)合，噬菌體通過脂質(zhì)體的緩釋性進入牛肉表面，吸附裂解大腸桿菌O157:H7；為提高噬菌體的感染效果，噬菌體還可以固定于聚己內(nèi)酯膜（Polycaprolactone，PCL）、乳清蛋白膜（Whey Protein Concentrate，WPC）上抑制生鮮肉上大腸桿菌O157:H7的生長[50-51]，使噬菌體更容易與目標細菌接觸。亦有將幾種噬菌體制成噬菌體雞尾酒用于生鮮肉托盤吸水襯墊，有效解決微生物污染和水分流失的問題[52]，保持生鮮肉的滋味和質(zhì)量。

噬菌體作為生物保鮮劑，通過其對細菌的特異性感染，可廣泛應用于防控豬肉、牛肉、羊肉及海鮮等預制菜生鮮肉制品中的食源性細菌。此外，噬菌體還可噴涂或清洗生鮮肉加工設備，如切塊機、切片機、絞肉機等，以抑制食源性細菌的生長繁殖，從而減少加工設備的微生物污染。

3 噬菌體在熟肉制品的應用研究

熟肉制品富含脂肪、蛋白質(zhì)等營養(yǎng)物質(zhì)，極易在加工、運輸、銷售等環(huán)節(jié)受到微生物（單核增生李斯特菌、大腸桿菌、沙門氏菌等）的污染[53]。例如低溫肉制品的熱處理溫度低，可能殘留一些耐熱微生物[54]，或在貯藏、銷售期間因微生物存在而將蛋白質(zhì)分解為生物胺[55]，導致肉制品品質(zhì)下降、貨架期縮短。從預制菜熟肉制品的加工流程來看，噬菌體可用于原料、操作空間減菌化，以及包裝、保鮮、殺菌等加工過程的細菌防控。

在食品保鮮時，噬菌體的濃度是影響抑菌效果的重要因素，如果濃度太低，可能無法控制細菌的數(shù)量。Soffer等[56]將不同劑量的ShigaShield?噬菌體制劑用于去除腌牛肉熟食、煙熏三文魚、預煮雞肉等食物中的志賀菌，發(fā)現(xiàn)最大劑量的（2×107或9×107PFU/g）噬菌體制劑可使細菌總數(shù)減少90%。Perera等[57]以不同濃度的ListShield噬菌體處理煙熏鮭魚中的單核增生李斯特氏菌，較高濃度的噬菌體使細菌數(shù)減少了90%。Sirdesai等[58]將濃度為107PFU/cm2和5×107PFU/cm2的PhageGuard S噬菌體用于抑制培根中的沙門氏菌，細菌減少量分別為1.3 lg(CFU/cm2)和0.8 lg(CFU/cm2)。除了使用適量的噬菌體外，還可在使用噬菌體時采取額外的控制措施，如真空包裝、添加抗氧化劑等，以確保食品的安全性。Devlieghere等[59]研究了噬菌體P100對冷藏真空包裝的熟火腿中單核細胞增生李斯特菌生長的影響，熟火腿經(jīng)過噬菌體處理后的28 d和42 d將細菌數(shù)保持在低于或等于1 CFU/g。Radford等[60]在聚乳酸膜上添加含A511噬菌體的黃原膠涂層，研究對預烹飪的火雞胸脯肉片上的沙門氏菌和李斯特菌的抑制效果，其細菌數(shù)減少量可分別達到1.30、6.31 lg(CFU/cm2)。Figueiredo等[61]將噬菌體P100與Nisin用于抑制豬肉火腿片的李斯特菌，72 h后細菌數(shù)減少了3 lg(CFU/cm2)。Khashayar等[62]將6種噬菌體制成新型噬菌體雞尾酒用于熟雞胸肉中抑制志賀菌，與對照樣品相比，7 d后的細菌減少數(shù)達到99%。除此之外，Park等[63]將篩選出的耐熱噬菌體在66 ℃雞胸肉加工條件下，經(jīng)過30 min處理，其噬菌體依然保持100%的存活率，證明了耐熱噬菌體可用于低溫肉制品的微生物防治。研究表明，噬菌體在實際加工中具有顯著的效果，Perera等[57]將噬菌體應用于實際的煙熏三文魚加工廠，發(fā)現(xiàn)ListShield噬菌體處理的魚片均未檢出單核細胞增生李斯特氏菌。由此可見，噬菌體在預制菜熟肉制品的食源性細菌防控中具有潛在價值，對目標細菌進行抑制的同時并不會對食品原有的口感和質(zhì)量產(chǎn)生不良影響。

4 噬菌體在果蔬制品的應用研究

預制菜產(chǎn)品種類豐富，大多為肉類預制菜，而果蔬類預制食品種類很少，其中的原因包括果蔬深加工技術(shù)和開發(fā)新產(chǎn)品思路的受限。為保證果蔬類預制菜的新鮮度和營養(yǎng)性，鮮切產(chǎn)品將成為果蔬市場的新趨勢[64]，給人們帶來更佳的消費體驗。預制菜的鮮切果蔬從采摘、加工、包裝、運輸?shù)戒N售過程中都可能被微生物污染，導致果蔬的微生物種群發(fā)生變化，從而產(chǎn)生腐敗、變質(zhì)等現(xiàn)象[65]。為提高消費者對鮮切果蔬產(chǎn)品的信任度，迫切需要一種新型生物控制劑，抑制鮮切果蔬上的食源性細菌生長并延長貨架期，提供健康安全的產(chǎn)品[66-67]。噬菌體作用于鮮切果蔬后不會改變其營養(yǎng)特性或風味，但能夠增強果蔬制品的抗微生物效果，有利于提高其貯運和銷售過程的安全性[68]。

預制菜的鮮切果蔬種類豐富，直接制成涼拌沙拉或生食會增加感染食源性致病菌的風險。為有效降低食物中毒的風險，可以采用措施減少鮮切果蔬的微生物污染[69]。表2列舉了不同途徑篩選出的噬菌體應用于鮮切果蔬的案例。

表2 篩出的噬菌體在鮮切果蔬的應用

Tab.2 Application of screened phage in fresh-cut fruits and vegetables

噬菌體在鮮切果蔬上的應用仍存在一些局限性。首先是pH值的影響，柑橘、西瓜等的pH通常在4.0左右，而噬菌體的pH穩(wěn)定范圍為6.0～9.0，這種環(huán)境下，噬菌體可能會失去活性；其次，果蔬表面通常會形成微生物生物被膜，這種生物被膜通常由多種微生物組成，能夠增強細菌在果蔬表面的黏附能力和生長速率，降低噬菌體的抑菌效果。

許多研究表明，將噬菌體與其他抑菌劑結(jié)合使用，可以有效抑制鮮切果蔬中微生物的生長。Oladunjoye等[79]將噬菌體和蔗糖單月桂酸酯用于抑制鮮切胡蘿卜上的單核增生李斯特氏菌，儲存6 d后細菌數(shù)減少2.17～4.00 lg(CFU/cm2)。Boyacioglu等[80]將噬菌體與氣調(diào)（O2、CO2、N2的體積分數(shù)分別為5%、35%、60%）結(jié)合用于抑制綠葉蔬菜（菠菜、綠葉萵苣、長葉萵苣）的細菌感染，其細菌減少量分別為3.08、3.89和4.34 lg(CFU/cm2)。Hong等[81]則是將噬菌體與細菌拮抗劑G. asaii聯(lián)合使用測試對哈密瓜片上的李斯特氏菌的抑制效果，發(fā)現(xiàn)兩者混合使用將李斯特氏菌數(shù)減少了6 lg(CFU/cm2)。Oladunjoye等[82]將噬菌體和磷酸三鈉（Tri-Sodium Phosphate，TSP）應用于感染單核細胞增多性李斯特菌的鮮切番茄和西瓜上，噬菌體–TSP使番茄、甜瓜的細菌減少數(shù)分別為1～2 lg(CFU/cm2)、2～5 lg(CFU/cm2)。Oliveira等[83]將包裹噬菌體的食用乳清分離蛋白（Whey Protein Isolation，WPI）涂層用于感染了大腸桿菌的圣女果和切片蘋果，發(fā)現(xiàn)相比于對照組，含有噬菌體的WPI涂層減少的活菌數(shù)為1～3 lg(CFU/cm2)。Cui等[84]用噬菌體和冷氮等離子體處理生菜、黃瓜和胡蘿卜上的大腸桿菌O157:H7生物被膜，冷氮等離子體可以破壞細菌生物被膜的結(jié)構(gòu)，使其失去生物黏附的能力，加上噬菌體的殺菌效果，可以將大腸桿菌的數(shù)量降低到不可檢出的水平?？傮w而言，噬菌體與物理、化學方法結(jié)合應用于鮮切果蔬，可以達到保證果蔬衛(wèi)生安全和延長果蔬保鮮期的雙重效果，具有廣闊的應用前景和發(fā)展?jié)摿Α?/p>

5 結(jié)語

預制菜行業(yè)正處于發(fā)展期，面臨著食品安全方面的挑戰(zhàn)。一方面，預制菜的食材原料存在微生物污染的風險；另一方面，預制菜在運輸、貯藏過程由于冷鏈運輸、配送速度不達標而導致菜品腐敗變質(zhì)、口味不佳等。噬菌體用于預制菜保鮮時，與化學、物理殺菌方式不同，噬菌體能夠在被污染的食品中快速繁殖和擴散，并裂解宿主菌，從而達到殺菌的目的。其殺菌過程不會釋放化學物質(zhì)或能量，因此噬菌體不會對食品的質(zhì)量、味道和營養(yǎng)產(chǎn)生負面影響。

雖然噬菌體保鮮技術(shù)在預制菜方面有顯著優(yōu)勢，但是在工業(yè)化應用上仍存在局限。首先，噬菌體易受外界環(huán)境（高溫、酸性環(huán)境、低水分活度）干擾失去活性、特異性強導致宿主譜窄；其次，噬菌體的應用多為噴灑、浸泡和涂層，與包裝材料結(jié)合的研究較少；最后，若噬菌體進行工業(yè)化生產(chǎn)，必須在監(jiān)管機構(gòu)批準的良好生產(chǎn)規(guī)范（Good Manufacturing Practice，GMP）下制定具體的生產(chǎn)指南，為噬菌體產(chǎn)品制定質(zhì)量和安全標準。

整體而言，噬菌體在預制菜行業(yè)有很大的應用前景，并且其在肉類、果蔬等食品中的研究應用都取得了良好效果。噬菌體生物控制不應該被認為是其他保鮮技術(shù)的替代品，而是作為一種提高食品安全性的額外工具。提高噬菌體的穩(wěn)定性、安全性和消費者的接受度，進而推動我國噬菌體產(chǎn)品的研發(fā)進程，促進噬菌體制劑工業(yè)化生產(chǎn)。

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Research Progress on Application of Phage Preservation Technology in Prepared Vegetables

FENG Shan-hong, ZHONG Le, CHENG Ping, XIAO Nai-yu, ZHANG Xue-qin, XIAO Geng-sheng,ZHOU Jin-xian

(1. College of Light Industry and Food Engineering, Zhongkai University of Agriculture and Engineering, Guangzhou 510225, China; 2. Guangdong Province University Central Kitchen Green Manufacturing Development Center, Guangzhou 510225, China; 3. Lingnan Special Food Green Processing and Intelligent Manufacturing Key Laboratory, Ministry of Agriculture and Rural Affairs, Guangzhou 510225, China)

The work aims to summarize the application of phage preservation technology in prepared vegetables, and to provide a basis for food safety protection of prepared vegetables and application research of phage. Based on the food safety of prepared vegetables, the prepared vegetables were classified, and the application of phage biological prevention and control of animal and plant-derived ingredients was mainly discussed. The analysis showed that the application of phage in prepared vegetables had a wide application prospect and value. Phage could effectively control food-borne bacterial contamination in prepared vegetables, maintain food quality and extend shelf life. In order to improve the antibacterial effect of phage, it could be considered from the concentration and stability of phage and its combination with physical preservation methods or biological and chemical preservatives. To realize the wide application of phage in prepared vegetables, it is necessary to improve the screening efficiency and stability of phage, and formulate corresponding standards and norms to improve the acceptability of consumers and promote the popularization and application of phage in the domestic market. Therefore, the use of phage preservation technology can not only extend the shelf life of prepared vegetables and improve food safety, but also bring more development opportunities for the food industry.

phage; prepared vegetables; food-borne bacteria; biological prevention and control

TS201.6

A

1001-3563(2023)09-0028-09

10.19554/j.cnki.1001-3563.2023.09.004

2023?03?02

2021年“廣東省科技大專項”河源市科技計劃項目（2021006）

馮珊紅（1999—），女，碩士生，主攻抗菌保鮮。

鐘樂（1984—），男，博士，副教授，主要研究方向為功能包裝材料。

責任編輯：曾鈺嬋