Bacillus subtilis and Bacillus licheniformis spores can survive processing temperatures used in the thermal processes of high-acid foods. Therefore, this study investigated the thermal inactivation of B. subtilis and B. licheniformis spores in pineapple juice at different temperatures (85–100°C) and soluble solids (SS, 11–30°Brix). The quality of juices and microbial loads after the thermal treatments during storage at 4 °C for 35 days was then checked. A linear decrease in D-value was observed with increasing temperature of treatment. Furthermore, the D-values determined in pineapple juice were: D90°C=13.2 ± 0.5 mins, D95°C = 6.8 ± 0.9 mins and D100°C = 2.1 ± 1.7 mins for B. subtilis spores, and D85°C = 16.6 ± 0.4 mins, D90°C = 7.6 ± 0.5 mins and D95°C = 3.6 ± 1.5 min, for B. licheniformis. Generally, the susceptibility of the bacteria to soluble solid change was affected by the interaction between temperature, SS and strain. In addition, pasteurization processes of ≥95°C for ≥33.8 mins was needed to ensure a recommended 5-log reduction of B. subtilis spores and limit vitamin C degradation of pineapple juice within three-week of storage at 4 °C.
AbabouchLHGrimitLEddafryRBustaFF. (1995).
Thermal inactivation kinetics of Bacillus subtilis spore suspended in buffer and oils. Journal of Applied Bacteriology78(6): 669–676.
2.
AğçamEAkyıldızADündarB. (2018). Thermal pasteurization and microbial inactivation of fruit juices. In: Rajauria G and Tiwari BK (eds) Fruit Juices: Extraction, Composition, Quality and Analysis. London: Academic Press, pp. 309–339.
3.
AziziARangannaS. (1993).
Spoilage organisms of canned acidified mango pulp and their relevance to thermal processing of acid foods. Journal of Food Science and Technologies30(4): 241–245.
4.
BaeYLeeHKimSRheeM. (2009).
Inactivation of Alicyclobacillus acidoterrestris spores in apple juice by supercritical carbon dioxide. International Journal of Food Microbiology136(1): 95–100.
5.
BalasubramanianSBalasubramaniamVM. (2009).
Synergistic effect of pressure, temperature, and pH on the inactivation of Bacillus subtilis spores in buffer and model food systems. Journal of Food Process Engineering33(5): 781–801.
6.
BerendsenEMKoningRABoekhorstJde JongAKuipersOPWells-BennikMHJ. (2015).
High-level heat resistance of spores of Bacillus amyloliquefaciens and Bacillus licheniformis results from the presence of a spoVA operon in a Tn1546 transposon. Frontiers in Microbiology7: 1912.
7.
BeuchatLR. (1988).
Thermal tolerance of Talaromyces flavus ascospores as affected by growth medium and temperature, age and sugar content in the inactivation medium. Transactions of the British Mycological Society90(3): 359–364.
8.
BigelowW. (1921).
The logarithmic nature of thermal death time curves. Journal of Infectious Diseases29(5): 528–536.
9.
BreidtFJrCostilowRN. (2004). Processing and safety. In: Fleming HP (ed.) Acidified Foods: Principles of Handling and Preservation. St. Charles, IL: Pickle Packers International, Inc., pp. 5-1–5–16.
10.
CasasJValverdeMTMarín-IniestaFCalvoL. (2012).
Inactivation of Alicyclobacillus acidoterrestris spores by high pressure CO2 in apple cream. International Journal of Food Microbiology156(1): 18–24.
11.
ChakrabortySRaoPSMishraHN. (2016).
Changes in quality attributes during storage of high-pressure and thermally processed pineapple puree. Food and Bioprocess Technology9(5): 768–791.
12.
ChenJZhengXDongJChenYTianJ. (2015).
Optimization of effective high hydrostatic pressure treatment of Bacillus subtilis in hami melon juice. LWT - Food Science and Technology60(2): 1168–1173.
13.
ChiaSLRosnahSNoranizanMAWan RamliWD. (2012).
The effect of storage on the quality attributes of ultraviolet-irradiated and thermally pasteurised pineapple juices. International Food Research Journal19(3): 1001–1010.
14.
ColemanWHChenDLiYCowanAESetlowP. (2007).
How moist heat kills spores of Bacillus subtilis. Journal of Bacteriology189(23): 8458–8466.
15.
CondónSSalaJF. (1992).
Heat resistance of Bacillus subtilis in buffer and foods of different pH. Journal of Food Protection55(8): 605–608.
16.
CorollerLLeguérinelIMafartP. (2001).
Effect of water activities of heating and recovery media on apparent heat resistance of Bacillus cereus spores. Applied and Environmental Microbiology67(1): 317–322.
17.
DaveyMWMontaguMVInzéDSanmartinMKanellisASmirnoffN, et al. (2000).
Plant L-ascorbic acid: chemistry, function, metabolism, bioavailability and effects of processing. Journal of the Science of Food and Agriculture80(7): 825–860.
18.
De-JongJ. (1989).
Spoilage of an acid food product by Clostridium perfringens, C. barati and C. butyricum. International Journal of Food Microbiology8(2): 121–132.
19.
Evelyn and SilvaFVM. (2016).
High pressure processing pretreatment enhanced the thermosonication inactivation of Alicyclobacillus acidoterrestris spores in orange juice. Food Control62: 365–372.
20.
Evelyn and SilvaFVM. (2019).
Heat assisted HPP for the inactivation of bacteria, moulds and yeasts spores in foods: Log reductions and mathematical model. Trends in Food Science and Technology88: 143–146.
21.
EvelynESilvaFVM. (2015b).
Use of power ultrasound to enhance the thermal inactivation of Clostridium perfringens spores in beef slurry. International Journal of Food Microbiology206: 17–23.
22.
EvelynESilvaFVM. (2015a).
Thermosonication versus thermal processing of skim milk and beef slurry: modeling the inactivation kinetics of psychrotrophic Bacillus cereus spores. Food Research International67: 67–74.
23.
EverisLBettsG. (2001).
pH stress can cause cell elongation in bacillus and clostridium species: a research note. Food Control12(1): 53–56.
24.
FieldsMLZamoraAFBradsherM. (1977).
Microbiological analysis of home-canned tomatoes and green beans. Journal of Food Science42(4): 931–934.
25.
GazeJEBettsGD. (1992). Food Pasteurization Treatments.
Gloucestershire:
Campden Food and Drink Research Association.
26.
GeorgeDSRazaliZSanthirasegaramVSomasundramC. (2015).
Effects of ultraviolet light (UV-C) and heat treatment on the quality of fresh-cut Chokanan mango and Josephine pineapple. Journal of Food Science80(2): S426–S434.
27.
GerhardtPMarquisRE. (1989). Spore thermoresistance mechanisms. In: Smith I, Slepecky RA and Setlow P (eds) Regulation of Prokaryotic Development. Washington, DC: American Society for Microbiology, pp. 43–63.
28.
GibrielAYAbd-ElATH. (1973).
Measurement of heat resistance parameters for spores isolated from canned products. Journal of Applied Microbiology36(2): 321–327.
29.
HajarNZainalSNadzirahKZRohaSAMAtikahOElidaTTZM. (2012).
Physicochemical properties analysis of three indexes pineapple (Ananas comosus) peel extract variety N36. APCBEE Procedia4: 115–121.
30.
HemadyRZaltasMPatonBFosterCSBakerAS. (1990).
Bacillus-induced endophthalmitis: New series of 10 cases and review of the literature. British Journal of Ophthalmology74(1): 26–29.
31.
HoffmanJL. (1986). Growth of Bacillus subtilis and Bacillus licheniformis in tomato juice at selected oxygen partial pressures. PhD Thesis, Purdue University, USA.
32.
IkeyamiYOkayaCSamayamaZMoriDOkuM. (1970).
Gaseous spoilage by butyric anaerobes in canned fruits, I in canned mandarin orange. Canners Journal49(11): 993–996.
33.
Isnawati TrimulyonoG. (2018).
Temperature range and degree of acidity growth of isolate of indigenous bacteria on fermented feed “fermege”. IOP Conference Series: Journal of Physics953: 1–5.
34.
JacobsenMJensenHC. (1975).
Combined effect of water activity and pH on the growth of butyric anaerobes in canned pears. Lebensmittel-Wissenschaft and Technologie8: 158–160.
35.
JagannathATsuchidoTMembreJM. (2005).
Comparison of the thermal inactivation of Bacillus subtilis spores in foods using the modified Weibull and Bigelow equations. Food Microbiology22(2–3): 233–239.
36.
JunejaVKOsoriaMHwangCAMishraATaylorTM. (2020).
Thermal inactivation of Bacillus cereus spores during cooking of rice to ensure later safety of boudin. Lebensmittel-Wissenschaft & Technologie122: 108955.
37.
KortRO'BrienACvan StokkumIHMOomesSJCMCrielaardWHellingwerfKJ, et al. (2005).
Assessment of heat resistance of bacterial spores from food product isolates by fluorescence monitoring of dipicolinic acid release. Applied and Environmental and Microbiology71(7): 3556–3564.
38.
KortRO'BrienACVan StokkumIHMOomes Sjcm CrielaardWHellingwerfKJBrulS. (2005).
Assessment of heat resistance of bacterial spores from food product isolates by fluorescence monitoring of dipicolinic acid release. Applied and Environmental Microbiology71(7): 3556–3564.
39.
LagnikaCAdjoviYCSLagnikaLGogohoungaFODo-SacramentoOKoulonyRK, et al. (2017).
Effect of combining ultrasound and mild heat treatment on physicochemical, nutritional quality and microbiological properties of pineapple juice. Food and Nutrition Sciences08(02): 227–241.,
40.
LeeSDoughertyRHKangD. (2002).
Inhibitory effects of high pressure and heat on Alicyclobacillus acidoterrestris spores in apple juice. Applied Environmental Microbiology68(8): 4158–4161.
41.
LeguerinelICouvertOMafartP. (2000).
Relationship between the apparent heat resistance of Bacillus cereus spores and the pH and NaCl concentration of the recovery medium. International Journal of Food Microbiology55(1–3): 223–227.
42.
LeguérinelICouvertO.Mafart (2006).
Modelling the influence of the incubation temperature upon the estimated heat resistance of heated bacillus spores. Letters in Applied Microbiology43(1): 17–21.
43.
MafartP. (2000).
Taking injuries of surviving bacteria into account for optimising heat treatments. International Journal of Food Microbiology55: 175–179.
44.
MaldonadoMCBelfioreCNavarroAR. (2008).
Temperature, soluble solids and pH effect on Alicyclobacillus acidoterrestris viability in lemon juice concentrate. Journal of Industria Microbiology and Biotechnology35: 141–144.
45.
MallidisCCFrantzeskakisPBalatsourasGKatsaboxakisC. (2007).
Thermal treatment of aseptically processed tomato paste. International Journal of Food Science & Technology25(4): 442–448.
46.
MolinNSnyggBG. (1967).
Effect of lipid materials on heat resistance of bacterial spores. Applied Microbiology15(6): 1422–1426.
47.
MontvilleTJSapersGM. (1981).
Thermal resistance of spores from pH elevating strains of Bacillus licheniformis. Journal of Food Science46(6): 1710–1712.
48.
MtimetNGuéganSDuranLMathotAGLeguérinelICorollerL, et al. (2016).
Effect of pH on Thermoanaerobacterium thermosaccharolyticum DSM 571 growth, spore heat resistance and recovery. Food Microbiology55: 64–72.
49.
MtimetNTrunetCMathotAGVenailleLLeguérinelICorollerL, et al. (2015).
Modelling the behavior of Geobacillus stearothermophilus ATCC 12980 throughout its life cycle as vegetative cells or spores using growth boundaries. Food Microbiology48: 153–162.
50.
MundtJOCollinsJLMcCartyIEBaileyR. (1978).
Description and microbiology of home-canned tomatoes and tomato juice. Journal of Food Protection41: 944–947.
51.
NakajyoMIshizuY. (1985).
Heat-resistance of Bacillus coagulans spores isolated from spoiled canned low-acid foods. Nippon Shokuhin Kogyo Gakkaishi32(10): 725–730.
52.
NakaumaMSaitoKKatayamaTTadaMTodorikiS. (2004).
Radiation-heat synergism for inactivation of Alicyclobacillus acidoterrestris spores in citrus juice. Journal of Food Protection67: 2538–2543.
53.
OladipoICAdelekeDTAdebiyiAO. (2010).
The effect of pH and chemical preservatives on the growth of bacterial isolates from some Nigerian packaged fruit juices. Pakistan Journal of Biological Sciences13(1): 16–21.
OmorotionmwanFOOgwuHIOgwuMC. (2019).
Antibacterial characteristics and bacteria composition of pineapple (Ananas comosus [linn.] merr.) peel and pulp. Food and Health5: 1–11.
56.
PaidhungatMSetlowBDriksASetlowP. (2000).
Characterization of spores of Bacillus subtilis which lack dipicolinic acid. Journal of Bacteriology182: 5505–5512.
57.
PalopARasoJPagánRCondónSSalaFJ. (1996).
Influence of pH on heat resistance of Bacillus licheniformis in buffer and homogenised foods. International Journal of Food Microbiology29: 1–10.
58.
PellouxJRusterucciCMellerowiczEJ. (2007).
New insights into pectin methylesterase structure and function. Trends in Plant Science12(6): 267–277.
59.
PetruzziLCampanielloDSperanzaBCorboMRSinigagliaMBevilacquaA. (2017).
Thermal treatments for fruit and vegetable juices and beverages: a literature overview. Comprehensive Reviews in Food Science and Food Safety16(4): 668–691.
60.
PintoCASantosMDFidalgoLGDelgadilloISaraivaJA. (2018).
Enhanced control of Bacillus subtilis endospores development by hyperbaric storage at variable/uncontrolled room temperature compared to refrigeration. Food Microbiology74: 125–131.
61.
RaatjesGJMSmeltJPPM. (1979).
Clostridium botulinum can grow and form toxin at pH values lower than 4.6. Nature281: 398–399.
62.
RahmanMMKhanMMRHosainMM. (1970).
Analysis of vitamin C (ascorbic acid) contents in various fruits and vegetables by UV spectrophotometry. Bangladesh Journal of Scientific and Industrial Research42(4): 417–424.
63.
RodriguezJHCousinMANelsonPE. (1993a).
Oxygen requirements of Bacillus licheniformis and Bacillus subtilis in tomato juice; Ability to grow in aseptic packages. Journal of Food Protection56(2): 165–168.
64.
RodriguezJHCousinMANelsonPE. (1993b).
Thermal resistance and growth of Bacillus licheniformis and Bacillus subtilis in tomato juice. Journal of Food Protection56(2): 165–168.
65.
Salkinoja-SalonenMSVuorioRAnderssonMAKampferPAnderssonMCHonkanen-BuzalskiT, et al. (1999).
Toxigenic strains of Bacillus licheniformis related to food poisoning. Applied and Environmental Microbiology65(10): 4637–4645.
66.
SandovalAJBarreiroJAMendozaS. (1992).
Thermal resistance of Bacillus coagulans in double concentrated tomato paste. Journal of Food Science57(6): 1369–1370.
67.
Sant’AnaAAlvarengaVPenaW. (2014). Alicyclobacillus in algae see single-cell protein: the algae. In: Batt CA and Tortorello ML (eds) Encyclopedia of Food Microbiology. Amsterdam: Elsevier, pp. 42–53.
68.
SetlowP. (2000). Resistance of bacterial spores. In: Storz G and Hengge‐Aronis R (eds) Bacterial Stress Responses. Washington, DC: American Society for Microbiology, pp. 217–230.
69.
ShawPE. (1992). Shelf life and aging of citrus juice, juice drinks and related soft drinks. In: Redd JB, Shaw Ir PE, Hendrix CM and Hendrix DL (eds) Quality Control Manual for Citrus Processing. Auburndale, FL: AgScience, pp. 173–199.
70.
ShridharPShankhapalKV. (1986).
Bacterial spoilage of canned mango pulp and green garden peas. Indian Journal of Microbiology26(12): 39–42.
71.
SilvaFVM and Evelyn. (2018). High pressure processing effect on microorganisms in fruit and vegetable products. In: Houška M and Silva FVM (eds) High Pressure Processing of Fruit and Vegetable Products. Boca Raton, FL: CRC Press, pp. 3–38.
72.
SilvaFVMGibbsPVieiraMCSilvaCLM. (1999).
Thermal inactivation of Alicyclobacillus acidoterrestris spores under different temperature, soluble solids and pH conditions for the design of fruit processes. International Journal of Food Microbiology51(2): 95–103.
73.
SilvaLPGonzales-BarronUCadavezVSant'AnaAS. (2015).
Modeling the effects of temperature and pH on the resistance of Alicyclobacillus acidoterrestris in conventional heat-treated fruit beverages through a meta-analysis approach. Food Microbiology46: 541–552.
74.
SilvaFVMTanEKFaridM. (2012).
Bacterial spore inactivation at 45–65°C using high pressure processing: Study of Alicyclobacillus acidoterrestris in orange juice. Food Microbiology32(1): 206–211.
75.
SoniAOeyISilcockPBremerP. (2016).
Bacillus spores in the food industry: A review on resistance and response to novel inactivation technologies. Comprehensive Reviews in Food Science and Food Safety15(6): 1139–1148.
76.
SplittstoesserDFChureyJJLeeCY. (1994).
Growth characteristics of aciduric sporeforming bacilli isolated from fruit juices. Journal of Food Protection57(12): 1080–1083.
77.
SpryC. (2008).
Understanding current steam sterilization recommendations and guidelines. AORN Journal88(4): 537–554.
78.
ThurnJRGoodmanJL. (1988).
Post-traumatic ophthalmitis due to Bacillus licheniformis. The American Journal of Medicine85(5): 708–710.
79.
TolaYBRamaswamyHS. (2014).
Thermal destruction kinetics of Bacillus licheniformis spores in carrot juice extract as influenced by pH, type of acidifying agent and heating method. LWT - Food Science and Technology56(1): 131–137.
80.
TrunetCMtimetNMathotAGPostollecFLeguérinelICouvertO, et al. (2020).
Suboptimal Bacillus licheniformis and Bacillus weihenstephanensis spore incubation conditions increase heterogeneity of spore outgrowth time. Applied and Environmental Microbiology86(6): 19. e02061.
81.
TrunetCMtimetNMathotAGPostollecFLeguérinelISohierD, et al. (2015).
Modeling the recovery of heat-treated Bacillus licheniformis Ad978 and Bacillus weihenstephanensis KBAB4 spores at suboptimal temperature and pH using growth limits. Applied and Environmental Microbiology81(2): 562–568.
82.
UchidaRSilvaFVM. (2017).
Alicyclobacillus acidoterrestris spore inactivation by high pressure combined with mild heat: modeling the effects of temperature and soluble solids. Food Control73: 426–432.
83.
UemuraKKobayashiIInoueT. (2010).
Inactivation of Bacillus subtilis spores in orange juice and the quality change by high electric field alternating current. Japan Agricultural Research Quarterly: JARQ44(1): 61–66.
84.
United States Food Drug and Administration. (1998).
Hazard analysis and critical control point (HACCP): Procedures for the safe and sanitary processing and importing of juice. Federal Register63: 20449–20486.
85.
VaughnRHIrvingHKMercerWA. (1952).
Spoilage of canned foods caused by the Bacillus macerans-polymyxa group of bacteria. Journal of Food Science17(1–6): 560–570.
86.
WalkerHWMatchesJR. (1965).
Release of cellular constituents during heat inactivation of endospores of aerobic bacilli. Journal of Food Science30(6): 1029–1036.
87.
WardaAKden BestenHMWShaNAbeeTGrootMNN. (2015).
Influence of food matrix on outgrowth heterogeneity of heat damaged Bacillus cereus spores. International Journal of Food Microbiology201: 27–34.
88.
WardaAKTempelaarsMHAbeeTGrootMNN. (2016).
Recovery of heat treated Bacillus cereus spores is affected by matrix composition and factors with putative functions in damage repair.Frontiers in Microbiology7: 1096.
89.
WarthAD. (1978).
Relationship between the heat resistance of spores and the optimum and maximum growth temperatures of Bacillus species.Journal of Bacteriology134(3): 699–705.
90.
WilksJCKitkoRDCleetonSHLeeGEUgwuCSJonesBD, et al. (2009).
Acid and base stress and transcriptomic responses in Bacillus subtilis.Applied and Environmental Microbiology75(4): 981–990.
91.
YangZMengXBreidtFJrDeanLLArrittFM. (2015).
Effects of acetic acid and arginine on pH elevation and growth of Bacillus licheniformis in an acidified cucumber juice medium. Journal of Food Protection78: 728–773.
92.
ZwieteringMHWijtzesTRomboutsFMRietK. (1993).
A decision support system for prediction of microbial spoilage in foods. Journal of Industrial Microbiology12(3–5): 324–329.
