In the United States, both fresh and fermented apple juice may be called “apple cider,” but “cider” here refers to the alcoholic, fermented “hard” cider product. Food safety considerations regarding apple juice or “sweet cider,” the nonalcoholic, unfermented product, is not addressed in this review, as they have been previously reviewed and addressed elsewhere (Vojdani et al., 2008). Cider production is currently a small segment of the alcoholic beverage industry with a national size equaling ≈1.3% of U.S. beer production. In other cider-producing regions, such as the United Kingdom, France, and Spain, the size of the cider industries are 22%, 4.8%, and 2.0%, respectively, relative to beer (Brager and Crompton, 2017). However, despite the relatively small size of the U.S. cider market, this beverage category has experienced significant growth in recent years, with much of the growth in the craft cider markets (Brager and Crompton, 2017).
A wide variety of apple cultivars, including dessert and culinary apples, may be used for cider production, resulting in countless styles and flavor profiles. Cultivars may be selected based on their sugar profile and sugar content, acids, tannins, aroma profiles, or other factors important for sensory evaluation; however, most ciders are made from dessert or culinary apples that may be destined for multiple markets, including fresh consumption and juice production. Traditional, European-style ciders contain cider-specific apple cultivars that have high concentrations of tannins that make them valuable for lending bitter and astringent sensory properties to the cider deemed as “bittersweet” or “bittersharp” (Barker, 1903). Unlike dessert and culinary apples, cider cultivars do not serve alternative purposes and are therefore destined for cider processing via alcoholic fermentation. These cultivars are in relative short supply and, therefore, are more expensive in the United States, so blending with and use of dessert and culinary apples is necessary for cider production.
Although apples in the United States are typically hand-harvested before full ripeness to allow for long-term storage of fresh market apples, it is not uncommon in other countries to allow fruit destined for cider production to fully ripen on the tree. Once fruit is fully ripe, it will drop naturally or by mechanically shaking the tree to encourage fruit drops. The fruit is then mechanically swept up and collected for processing (Lea, 2015). Because of high labor costs and workforce shortages, this “shake and sweep” method is advantageous and may also result in cost savings compared with hand-harvesting.
Despite these advantages, there are some important tradeoffs to consider. Because of the bruising and damage that occurs when fruit is shaken and allowed to drop from the tree, fruit must be processed immediately, as it will rot more rapidly (Alexander et al., 2016; Miles and King, 2014). Furthermore, fruit contact with the orchard floor may raise pathogen-related concerns due to potential contact with contaminated water, animal feces, untreated manure, soil, or airborne contaminants (Brandl, 2006). Although there are inherent risks in any fresh produce operation, several pathogens have been reported in apple juice and sweet (nonalcoholic) cider. From 1995 to 2005, 10 of the 21 juice-related outbreaks in the United States were associated with apple juice and sweet cider. The pathogens associated with these outbreaks included Escherichia coli O157:H7, E. coli O111, Cryptosporidium parvum, and one or more unknown pathogens, and many of these juices were unpasteurized before consumption (Vojdani et al., 2008). More recently, Listeria monocytogenes has become a pathogen of concern in apple products, partially due to its ability to survive during cold storage and its relative resistance to heat treatments and acidic solutions (Barker and Park, 2001; Mak et al., 2001; Sheng et al., 2017). Salmonella species are prolific food pathogens and have appeared in various studies examining food safety processes in apple and other juices. These pathogens, their threat to human health, and their likely contamination sources are outlined in Table 1. Ground-harvested fruit, commonly referred to as “drops,” are also associated with higher levels of patulin, a mycotoxin produced by Penicillium expansum and other molds that can be detrimental to human health (Jackson et al., 2003).
Foodborne pathogens potentially present in apple juice and their potential contamination sources, threats to human health, and infectious doses.
European Union regulatory agencies accept that cider can be made from fruit collected from the ground and washed with the understanding that fermentation is an acceptable means of controlling pathogens (Merwin et al., 2008). However, in the United States, those involved with the production of human food and animal feed must comply with the Food Safety Modernization Act (FSMA), which requires that preventive controls are in place for food safety. FSMA has several parts important for food and beverage producers. One section of FSMA, 21 CFR Part 112: Standards for the Growing, Harvesting, Packing, and Holding of Produce for Human Consumption, or more commonly known as the “Produce Safety Rule,” puts forth mandatory food safety regulations for producers of fresh produce [U.S. Food and Drug Administration (USFDA), 2015a]. In the rule, the term “covered produce” indicates produce that must adhere to the federal standards because it is likely to be consumed raw. Produce not intended for raw consumption is excluded from the definition of “covered produce” but, in this case, processors must be able to show that effective preventive controls have been put in place to reduce the risk of foodborne illness. Apples, including cider apples, can fall into either category. Therefore, apple growers must understand and follow food safety requirements, regardless of market destination, outlined in the FSMA Produce Safety Rule. Farms that generate $25,000 (adjusted for inflation) or less in produce sales averaged from the previous 3 years are not covered by the rule, as stated in 21 CFR Part 112(a). It is possible for growers to harvest apples for cider production from the ground, but both growers and cidermakers must understand how to best address food safety concerns and ensure that the process adopted for cider manufacture reduces or eliminates pathogen contamination.
This article aims to address the use of ground-harvested apples used for cider production in accordance with the FSMA Produce Safety Rule by examining 1) when apples are considered to be “covered produce,” 2) how processing methods may minimize the risk of foodborne illness when using ground-harvested cider apples for cider production, and 3) how cider apple growers and cider producers may approach compliance and processing exemptions with 21 CFR Part 112 and ensure that their foods are safe.
Alexander, T.R., King, J., Scheenstra, E. & Miles, C.A. 2016 Yield, fruit damage, yield loss, and juice quality characteristics of machine- and hand-harvested ‘Brown Snout’ specialty cider apples stored at ambient conditions in northwest Washington HortTechnology 26 614 619
Armstrong, G.L., Hollingsworth, J. & Morris, J.G. Jr 1996 Emerging foodborne pathogens: Escherichia coli O157: H7 as a model of entry of a new pathogen into the food supply of the developed world Epidemiol. Rev. 18 29 51
Barker, B.T.P. 1903 Classification of cider apples. Long Ashton Res. Stn., Bristol, UK
Barker, C. & Park, S.F. 2001 Sensitization of Listeria monocytogenes to low pH, organic acids, and osmotic stress by ethanol Appl. Environ. Microbiol. 67 1594 1600
Basaran-Akgul, N., Churey, J.J., Basaran, P. & Worobo, R.W. 2009 Inactivation of different strains of Escherichia coli O157:H7 in various apple ciders treated with dimethyl dicarbonate (DMDC) and sulfur dioxide (SO2) as an alternative method Food Microbiol. 26 8 15
Besser, R.E., Lett, S.M., Weber, J.T., Doyle, M.P., Barrett, T.J., Wells, J.G. & Griffin, P.M. 1993 An outbreak of diarrhea and hemolytic uremic syndrome from Escherichia coli O157: H7 in fresh-pressed apple cider J. Amer. Medical Assn. 269 2217 2220
Beuchat, L.R., Nail, B.V., Adler, B.B. & Clavero, M.R.S. 1998 Efficacy of spray application of chlorinated water in killing pathogenic bacteria on raw apples, tomatoes, and lettuce J. Food Prot. 61 1305 1311
Brager, D. & Crompton, M. 2017 U.S. cider trends: Increasing your odds of success by evaluating marketplace dynamics. 28 Aug. 2018. <https://ciderassociation.org/cider-trends-in-the-u-s/>
Burnett, S.L. & Beuchat, L.R. 2001 Human pathogens associated with raw produce and unpasteurized juices, and difficulties in decontamination J. Ind. Microbiol. Biotechnol. 27 104 110
Ceylan, E., Fung, D.Y. & Sabah, J.R. 2004 Antimicrobial activity and synergistic effect of cinnamon with sodium benzoate or potassium sorbate in controlling Escherichia coli O157: H7 in apple juice J. Food Sci. 69 FMS102 FMS106
Fisher, T.L. & Golden, D.A. 1998 Survival of Escherichia coli O157: H7 in apple cider as affected by dimethyl dicarbonate, sodium bisulfite, and sodium benzoate J. Food Sci. 63 904 906
Gabriel, A.A. & Nakano, H. 2009 Inactivation of Salmonella, E. coli and Listeria monocytogenes in phosphate-buffered saline and apple juice by ultraviolet and heat treatments Food Control 20 443 446
Goverd, K.A., Beech, F.W., Hobbs, R.P. & Shannon, R. 1979 The occurrence and survival of coliforms and salmonellas in apple juice and cider J. Appl. Bacteriol. 46 521 530
Hanes, D.E., Worobo, R.W., Orlandi, P.A., Burr, D.H., Miliotis, M.D., Robl, M.G., Bier, J.W., Arrowood, M.J., Churey, J.J. & Jackson, G.J. 2002 Inactivation of Cryptosporidium parvum oocysts in fresh apple cider by UV irradiation Appl. Environ. Microbiol. 68 4168 4172
Jackson, L.S., Beacham-Bowden, T., Keller, S.E., Adhikari, C., Taylor, K.T., Chirtel, S.J. & Merker, R.I. 2003 Apple quality, storage, and washing treatments affect patulin levels in apple cider J. Food Prot. 66 618 624
Jordan, S.L., Glover, J., Malcolm, L., Thomson-Carter, F.M., Booth, I.R. & Park, S.F. 1999 Augmentation of killing of Escherichia coli O157 by combinations of lactate, ethanol, and low-pH conditions Appl. Environ. Microbiol. 65 1308 1311
Keyser, M., Műller, I.A., Cilliers, F.P., Nel, W. & Gouws, P.A. 2008 Ultraviolet radiation as a non-thermal treatment for the inactivation of microorganisms in fruit juice Innov. Food Sci. Emerg. Technol. 9 348 354
Lea, A. 2015 Craft cider making. Springer, New York, NY
Mak, P.P., Ingham, B.H. & Ingham, S.C. 2001 Validation of apple cider pasteurization treatments against Escherichia coli O157:H7, Salmonella, and Listeria monocytogenes J. Food Prot. 64 1679 1689
Mazzotta, A.S. 2001 Thermal inactivation of stationary-phase and acid-adapted Escherichia coli O157: H7, Salmonella, and Listeria monocytogenes in fruit juices J. Food Prot. 64 315 320
Merwin, I.A., Valois, S. & Padilla-Zakour, O.I. 2008 Cider apples and cider-making techniques in Europe and North America Hort. Rev. 34 365 413
Miles, C.A. & King, J. 2014 Yield, labor, and fruit and juice quality characteristics of machine and hand-harvested ‘Brown Snout’ specialty cider apple HortTechnology 24 519 526
Millard, P.S., Gensheimer, K.F., Addiss, D.G., Sosin, D.M., Beckett, G.A., Houck-Jankoski, A. & Hudson, A. 1994 An outbreak of cryptosporidiosis from fresh-pressed apple cider J. Amer. Medical Assn. 272 1592 1596
National Advisory Committee on Microbiological Criteria for Foods 2017 Response to questions posed by the Department of Defense regarding microbiological criteria as indicators of process control or insanitary conditions J. Food Prot. 81 115 141
Sheng, L., Edwards, K., Tsai, H.-C., Hanrahan, I. & Zhu, M.-J. 2017 Fate of Listeria monocytogenes on fresh apples under different storage temperatures Front. Microbiol. 8 1396
Stinson, E.E., Osman, S.F., Huhtanen, C.N. & Bills, D.D. 1978 Disappearance of patulin during alcoholic fermentation of apple juice Appl. Environ. Microbiol. 36 620 622
U.S. Food and Drug Administration 2004 Guidance for industry: Juice HACCP hazards and controls guidance. 1st ed. 25 Oct. 2018. <https://www.fda.gov/Food/GuidanceRegulation/GuidanceDocumentsRegulatoryInformation/Juice/ucm072557.htm>
U.S. Food and Drug Administration 2012 Bad bug book: Handbook of foodborne pathogenic microorganisms and natural toxins. 2nd ed. 30 Aug. 2018. <https://www.fda.gov/downloads/food/foodsafety/foodborneillness/foodborneillnessfoodbornepathogensnaturaltoxins/badbugbook/ucm297627.pdf>
U.S. Food and Drug Administration 2015a Code of Federal Regulations, Title 21, Part 112. 26 Oct. 2018. <https://www.ecfr.gov/cgi-bin/text-idx?SID=ef4db2f3c4451c04ff09219acb9f9376&mc=true&node=pt21.2.112&rgn=div5>
U.S. Food and Drug Administration 2015b Code of Federal Regulations, Title 21, Part 117. 29 Oct. 2018. <https://www.ecfr.gov/cgi-bin/text-idx?SID=3ee286332416f26a91d9e6d786a604ab&mc=true&tpl=/ecfrbrowse/Title21/21tab_02.tpl>
U.S. Food and Drug Administration 2015c Standards for produce safety: Coverage and exemptions/exclusions for 21 Part 112. 26 Oct. 2018. <https://www.fda.gov/downloads/food/guidanceregulation/fsma/ucm472499.pdf>
Vojdani, J.D., Beuchat, L.R. & Tauxe, R.V. 2008 Juice-associated outbreaks of human illness in the United States, 1995 through 2005 J. Food Prot. 71 356 364
Vriesekoop, F., Krahl, M., Hucker, B. & Menz, G. 2012 125th anniversary review: Bacteria in brewing: The good, the bad and the ugly J. Inst. Brew. 118 335 345
Wisniewsky, M.A., Glatz, B.A., Gleason, M.L. & Reitmeier, C.A. 2000 Reduction of Escherichia coli O157: H7 counts on whole fresh apples by treatment with sanitizers J. Food Prot. 63 703 708
Wright, J.R., Sumner, S.S., Hackney, C.R., Pierson, M.D. & Zoecklein, B.W. 2000 Efficacy of ultraviolet light for reducing Escherichia coli O157: H7 in unpasteurized apple cider J. Food Prot. 63 563 567
Zhao, D., Barrientos, J.U., Wang, Q., Markland, S.M., Churey, J.J., Padilla-Zakour, O.I., Worobo, R.W., Kniel, K.E. & Moraru, C.I. 2015 Efficient reduction of pathogenic and spoilage microorganisms from apple cider by combining microfiltration with UV treatment J. Food Prot. 78 716 722
Zhao, T., Doyle, M.P. & Besser, R.E. 1993 Fate of enterohemorrhagic Escherichia coli O157: H7 in apple cider with and without preservatives Appl. Environ. Microbiol. 59 2526 2530