Current Food Safety Issues of Home-Prepared Vegetables and Herbs Stored in Oil B

Home , Botulism

Current Food Safety Issues of Home-prepared Vegetables and Herbs Stored in Oil B. A. NUMMER,*1 D. W. SCHAFFNER,2 A. M. FRASER3 and E. L. ANDRESS4 1Nutrition and Food Sciences Dept., Utah State University, 8700 Old Main Hill, Logan, UT 84322, USA; 2Food Science Dept., Rutgers University, 65 Dudley Road, New Brunswick, NJ 08901, USA; 3Dept. of Food, Nutrition and Packaging Sciences, Clemson University, 206 Poole Agricultural Center, Clemson, SC 29634-0316, USA; 4Dept. of Foods and Nutrition, University of Georgia, 208 Hoke Smith Annex, Athens, GA 30602, USA

INTRODUCTION ABSTRACT Vegetables and herbs in oil provide Consumer interest in storing vegetables or herbs in oil or four conditions necessary for botulinum toxin production: (a) a likely natu- infusing oils with these products has grown over recent decades. ral presence of Clostridium botulinum Vegetables and herbs stored in oil provide several conditions spores, (b) an anaerobic environment, necessary for botulinum toxin production, including an anaerobic (c) a pH greater than 4.6, and (d) a water

environment. Studies of documented outbreaks of botulism have activity (aw) greater than 0.85. Studies of identified vegetables and herbs in oil as the food source, with documented outbreaks of botulism have most outbreaks traced to home-prepared versions. Implicated identified vegetables and herbs in oil as foods include peppers, garlic, mushrooms, and eggplant. Visual or the food source, with most outbreaks traced to home-prepared versions (16, other organoleptic clues do not provide adequate information to 28, 30–32). The U.S. FDA has pre- prevent botulism. Most Cooperative Extension resources have pared regulations for commercial proces- communicated the risks and hazards of storing these foods at sors who make vegetables and herbs in room temperature and suggest refrigeration, freezing, drying, and oils (21 CFR 114 – Acidified Foods), acidifying as alternatives. The safest recommendation is to freeze but there are no validated processes for home-prepared versions. vegetables or herbs stored in oil. If the product is not frozen, it In 1973, seven persons contract- should be refrigerated and then either consumed within four days ed botulism after eating improperly or discarded. Future research is required to clarify the potential canned vegetables in oil. Commercially of additional hurdles to preparing and storing these foods safely. canned peppers in oil were implicated Possible research areas include the use of boiling water canning, epidemiologically, and type B toxin acidification, and drying followed by an acid dip. was identified in leftover peppers. The processor voluntarily recalled the pep- per product, and no further cases were reported (6). In 1985, 37 people were sickened with botulism after eating a garlic-in-oil preparation made in a restaurant (30, 31). This was followed by a laboratory investigation indicating A peer-reviewed article the survival of and toxin production by C. botulinum in garlic in oil preparations *Author for correspondence: Phone:+1 435.797.2116; Fax: +1 435.797.2379 (29). After a second botulism outbreak E-mail: [email protected]

336 FOOD PROTECTION TRENDS | JUNE 2011 TABLE 1. Growth inhibition and heat resistance of C. botulinum (13, 26)

Clostridium Group Growth Inhibition1 Heat Resistance (min)

2 Temp pH Aw NaCl D 90˚C, 194˚F D 121˚C, 250˚F

Mesophilic/proteolytic ≤ 10°C (50°F) ≤ 4.6 ≤ 0.93 ≥ 10% toxin 0.15 spores 0.2

Psychrotrophic/non-proteolytic ≤ 3.3°C (38°F) ≤ 5.0 ≤ 0.97 ≥ 5% toxin 0.15 spores 1.5 1Under optimal conditions 2Water phase NaCl

from garlic-in-oil preparation in 1989, the divided into two major groups (Table to review the formulation and labeling FDA ordered the removal of commercial 1). of their products. When refrigeration garlic-in-oil preparations that had no acidi- is needed, both shipping cartons and fying agent (phosphoric or citric acid) from products sold at retail should be clearly Group I – Mesophilic strains store shelves and required that all future and prominently labeled with statements preparations be properly acidified before C. botulinum strains A, and pro- such as “Requires Refrigeration for the garlic is added to oil (22). Despite the teolytic strains of B and F, collectively Safety” or “Refrigerate Both Before and initial FDA warning, home-bottled garlic have very heat resistant spores. Tem- After Opening (20). If the manufacturer in oil was associated with botulism in 1991 peratures associated with home pres- wanted to sell a shelf-stable product, in California, 1999 in Florida (28), and sure canning would be required to kill they were required to add microbial in- 2003 in Denmark (21). hibitors or acidifying agents and disclose Other outbreaks of botulism have these spores in a reasonable period of these additives on their labels (20). The implicated home-prepared vegetables or time. Mesophilic strains are inhibited herbs covered in oil. As recently as 1999, a by acid (pH ≤ 4.6) and salt concentra- FDA issued a second bulletin in 1993 botulism outbreak in Florida was linked to tions greater than 10% (13). (10), in which it warned consumers not homemade garlic-infused oil, whose ingre- to prepare any homemade spices in oil, dients included cloves of garlic, rosemary, Group II – Psychrotrophic margarine or butter for extended stor- thyme, and olive oil (24). In 1998, a case strains age, because the protective additives used of botulism type A in the U.S. implicated in commercial mixes are not generally home-prepared mushrooms covered in oil C. botulinum strain E, and non- available for homemade products. Con- (16) and two cases in Britain implicated proteolytic strains B and F, can grow sumers were urged to refrigerate all such mushrooms covered in oil (27). In Italy, at refrigeration temperatures; however, products and to dispose immediately of where this method of home food preser- their spores are much less heat resistant any products suspected to be spoiled or vation is popular, two separate incidents than those of Group I. Pasteurization to have been stored unrefrigerated. By of foodborne botulism in 1993 were due temperatures that could be achieved 1999, non-acidified garlic-in-oil mix- to contaminated home-prepared eggplant in home boiling water canners could tures were formally recognized as poten- stored in oil (32). Between 1994 and 1998, kill these spores. These strains are in- tially hazardous in the FDA Food Code more than 100 cases of botulism reported hibited by acid (pH ≤ 5.0) and salt (13). in Italy have been traced to home-prepared concentrations greater than 5% and The USDA Complete Guide to Home vegetables stored in oil or water (4). These are commonly associated with seafood Canning, the most widely recognized outbreaks collectively demonstrate the need products (13). Non-proteolytic strains source of validated processes for home for validated procedures specifically target- do not usually produce overt signs of food canning (33), includes three pro- ing consumers who preserve vegetables and food spoilage (13). cedures for preparing canned vegetables herbs in oil. This paper reviews current food that have oil in the ingredient list. One safety issues with regard to home-prepared SUMMARY OF is for marinated peppers (34), the second vegetables and herbs in oil and discusses RECOMMENDATIONS ON for marinated whole mushrooms (35) various hurdles available to consumers. and the third for pickled three-bean salad VEGETABLE OR HERBS IN (36). Each of these procedures includes CLOSTRIDIUM BOTULINUM OIL FOR CONSUMERS acidulants as well as preparation steps to insure adequate reduction in pH of A summary of C. botulinum and In two bulletins for the commer- the vegetable tissue. Since the outbreaks botulism can be found online in the U.S. cial food processing industry, the U.S. FDA-CFSAN Bad Bug book (13) and the FDA has outlined procedures for safe- in the 1980s and ‘90s, five Cooperative ICMSF, Microorganisms in Foods, volume ly preparing vegetables and herbs in oil Extension publications outlining safe 5 (26). There are numerous strains of (10, 20). In 1989, the FDA notified handling procedures for home-prepared C. botulinum, but they are commonly producers of the commercial products vegetables and herbs in oil have been

JUNE 2011 | FOOD PROTECTION TRENDS 337 TABLE 2. Cooperative Extension recipes outlining handling procedures for vegetables and herbs in oil

Publication Product in/with oil Recommendations Acidify Storage Shelf life

USDA 2009 (34) Marinated peppers Yes Room None listed3 temperature1 USDA 2009 (35) Marinated whole mushrooms Yes Room None listed3 temperature1 USDA 2009 (36) Pickled three bean salad Yes Room None listed3 temperature1 Harris 1997 (17) Garlic No Refrigerate 3 days Raw or cooked garlic No Refrigerate 3 weeks Dried garlic and herbs No Room None listed temperature Unseasoned dried tomatoes No Room None listed temperature Raab and Woodburn 2009 (25) Dried tomatoes with raw or cooked No Refrigerate 3 weeks garlic added after drying Mushrooms or chilies No Refrigerate 3 weeks Pesto No Refrigerate 3 weeks Lamp 1998 (19) Sun dried tomatoes with dried spices Yes Room None listed temperature1 Refrigerate None listed Dried spices2 No Room None listed temperature Refrigerate None listed Andress 1998 (2) Herbs No Refrigerate 3 days Pesto No Refrigerate 3 days Kendall and Rausch 2006 (18) Garlic No Refrigerate 10 days Herbs and vegetables No Refrigerate 10 days Dried tomatoes No Refrigerate None listed 1Heat processed in a boiling water canner 2Simmered 120 min in hot oil 3No specific advice with the procedure; source states general advice in another chapter to use within one year for best quality

found (Table 2). While each publication etables or herbs in oil products, includ- them at room temperature. It is noted highlights the hazards of vegetables and ing raw and cooked garlic, dried garlic that the tomatoes, garlic, and herbs must be mixed fresh, and then dried before herbs stored in oil at room temperature, and herbs, unseasoned dried tomatoes, adding oil. The flavored oil recipes from recommendations (particularly with re- dried tomatoes with raw or cooked garlic this document are less clear. It appears to gard to shelf life), were not consistent added after drying; mushrooms and chil- suggest that if consumers remove all of between the documents, and the han- ies, and pesto. The authors recommend the flavoring solids (herbs or vegetables), refrigeration for up to three weeks for all dling instructions were on critical safety they may store the flavored oil at room fresh herb or vegetable in oil mixtures. parameters not always clear. temperature; otherwise refrigeration for The document notes that if consumers An Oregon State University Ex- up to three weeks is advised. place dried tomatoes or dried tomato- tension Service fact sheet (25) presents The University of California Co- garlic-herb mixtures in oil, they may store instructions for the widest range of veg- operative Extension provided a publica-

338 FOOD PROTECTION TRENDS | JUNE 2011 TABLE 3. Advice on refrigerated storage times for reduced oxygen foods (1, 12, 23)

Refrigeration Storage Time Treatment

< 3˚C No limit specified No additional hurdles are required 3–5˚C < 10 days No additional hurdles are required 5–10˚C < 4 days No additional hurdles are required < 10˚C > 10 days At least one additional hurdle is required

tion on methods to safely preserve garlic erated for up to three days. The recom- tures at or below 3.3°C (38°F). Out- (17) that stated that storing garlic in oil mendation for pesto is refrigeration for breaks of botulism cited in this review at room temperature was unsafe and that up to three days. Freezing is suggested for were due to Group I (heat resistant) suggests storage in the freezer. No recom- longer storage life. C. botulinum strains. These strains con- mendations are listed for refrigeration. The most recent publication, from taminated vegetables or herbs that were Although commercially prepared garlic is Colorado State University Cooperative stored in oil at room temperature. No acidified, the publication did not recom- Extension Service (18), has an original reported outbreaks have occurred be- mend this method to consumers, citing publication date of 2000 and an updated cause of products that were properly version publication date of 2006. Garlic- its complexity. refrigerated. Storage temperatures below in-oil and vegetables (herbs)-in-oil rec- A second publication by Lamp, from 10°C (50°F) will inhibit the growth of ommendations are to refrigerate for up the University of California Cooperative Group I strains of C. botulinum. How- to 10 days or freeze. As the authors of Extension Service, was placed online in ever, to prevent the growth of Group II some other publications have done, the (psychrotrophic) strains of C. botulinum, 1998 (19) and was available as recently as authors recommend room temperature refrigeration temperatures would have to 2004, although it does not appear to be storage for dried tomatoes-in-oil mix- currently available. Similar to the OSU tures, but they do not recommend stor- be at or below 3.3°C (38°F). While these publication (25), it recommends refrig- ing dried herbs-in-oil mixtures at room organisms are most commonly attributed eration for up to 3 weeks for flavored temperature. to seafood, they may still be considered a oils, pesto, and garlic in oil and storage concern in vegetable- and/or herbs-in-oil at room temperature of dried tomatoes PRESERVATION HURDLES mixtures. in oil. This document includes a recipe As already discussed, shelf-life guide- (BARRIERS) that calls for acidification of fresh toma- lines vary widely, from three days (2, 10, toes with a “sprinkle” of distilled vinegar, In summary, the five Cooperative 17, 20) to three weeks (19, 25). It is to which dried rosemary, basil or oregano Extension Service publications offer as believed that these shelf-life recommen- may be added and recommends refrig- recommendations (a) freezing, with an dations were determined from the mini- eration or heat processing (canning) in indeterminate shelf life, (b) refrigera- mum time required for the outgrowth of pint jars for 20 minutes at 76.7–87.8 °C tion for periods of 3–21 days, (c) acidi- botulism at refrigeration temperatures. (170–190°F). There are no research ci- fication, using various methods, and (d) The report by Peck and others (23) states tations, and the process does not adhere heat processing, using various methods. that with optimal circumstances, non- to the standards set by the USDA Com- None of the publications cite research, proteolytic C. botulinum can form toxin plete Guide to Canning (33). This pub- although they do cite research-based in 10 days or less at 8°C (46.4°F). Some lication also contains a recipe that calls information. Many recipes lack specific- research-based temperature-time barri- ity for processes, such as weights of in- for adding dried spices to oil and then ers for C. botulinum are listed in Table 3. gredients and times for acidification. It heating on “low” for 120 minutes, after These range from 4 to 10 days for tem- is clear, given the inconsistencies across which the oil is sieved through multilay- peratures between 3 and 10°C (37.4– these publications, that a consensus is ered cheesecloth into canning jars. The 50°F). If refrigeration alone is to be needed on the storage practices and shelf used as a barrier to toxin production by recommendation is to store this at room life of home-prepared vegetable and/or C. botulinum, the question of home temperature or under refrigeration. herbs-in-oil mixtures. Individually vali- The University of Georgia Cooper- dated processes are the gold standard but refrigerator performance must be ad- ative Extension Service (2) provided rec- might not be practical, given the wide ar- dressed. ommendations to county agents based on ray of product combinations. In an Audits International study (3) a review of other state Extension Service in which home refrigerator temperature recommendations and the previous cau- was analyzed for 939 refrigerators in the Cold storage tionary advice from FDA (10, 20). This U.S., 27.4% of the refrigerators had stor- publication provided recipes for infusing The best and current science-based age temperatures exceeding 5°C (41°F), herb flavors in oil andfor pesto. For the recommendation for consumers is to with 1.4% of refrigerators exceeding infusions, the oil is strained and refrig- store vegetable- and/or herbs-in-oil mix- 10.5°C (51°F). Additional data revealed

JUNE 2011 | FOOD PROTECTION TRENDS 339 that 41% of retail food product tem- resistant, dry container. The document that consumers add vinegar to the veg- peratures were in the range of 5–10.5°C recommends refrigeration for up to one etable component before any oil is added (41–51°F), while 6.7% of products were month. With boiling points over 121°C so that the ratio proportion of vegetable at temperatures > 10.5°C (51°C). These (250°F), most oils could be cooked to to vinegar by weight is not greater than data show that refrigeration alone would sufficient heat lethality temperatures for three to one. The resultant mixture will not be a reliable hurdle in the U.S. The all C. botulinum types, but this approach then contain approximately one percent shelf life and safety of these products has not been scientifically validated. It is acetic acid, which would ensure a final would depend on knowing the refrig- also not clear whether heating oil to tem- pH below 4.6. erator temperature. Only freezing would peratures greater than 100°C (212°F) accomplish the target temperature of would boil off any moisture present in ≤ 3°C (37.4°F) as a sole cold temperature the vegetables or herbs and thus preclude Drying (control of Aw) hurdle or barrier to C. botulinum risk in C. botulinum growth. Further research Controlling the amount of moisture these foods. The frozen mixture of veg- must be done before methods of heat- available in the product in a manner suf- etable or herb in oil would not support ing herbs or vegetables in oil are recom- ficient to prevent the growth of all types pathogen growth and would have a shelf mended. of C. botulinum that might be present in life dictated by changes in quality. It is the product could be difficult(13) . Be- of interest to note that many oils will Acidification cause water forms droplets in oil, even not solidify when stored in the freezer, very small amounts can be sufficient to making consumer access for portioning Using acid, naturally present or allow microbial growth (8) and botulism easier. added, to prevent C. botulinum growth toxin formation (29). Using dried rather is commonly done by consumers (33). than fresh vegetables and herbs in oil has The three existing procedures of canning Heat treatment been recommended as a way to allow for vegetables in oil available in the USDA room temperature storage (19, 25). A common resource available to Complete Guide to Canning (33) rely on consumers for heat-treating foods is can- adding lemon juice and vinegar to acidify ning. Pressure canning at 115–121°C the low-acid foods to a pH value below Multiple hurdles (barriers) (239–250°F) would be required for low 4.6. A boiling water canning process is Table 3 summarizes some scientific acid foods (33) to ensure destruction of used to destroy spoilage organisms and sources for reduced oxygen food shelf life all types of C. botulinum. However, pres- non-sporeforming pathogens. maximums based on refrigeration temp- sure canning garlic and similar vegetables Several of the publications from adversely affects texture and significantly Cooperative Extension sources reviewed erature. These times are based on refrig- alters palatability (17). Most herbs or in this publication (Table 2) recommend eration as the only hurdle. However, vegetables are placed fresh into oil for storing dried tomatoes in oil at room maintaining a refrigeration temperature preservation, but no research-based pro- temperature. While fresh tomatoes are below 3°C (37.4°F) or even below 10°C cesses are available for pressure canning considered a borderline acid food (33), (50°F) could be difficult for consumers, unacidified garlic or vegetables in oil. In the drying process concentrates the avail- as many do not have thermometers and fact, a 1990 outbreak of botulism was able acid, making dried tomatoes an apparently do not routinely monitor re- attributed to home-canned garlic in oil acidic food with a pH of approximately frigeration temperatures (3, 14). In 1992, that was heated to a temperature insuf- 4.0 (9). Sun-dried tomatoes stored in oil the ACMSF published a report that made ficient to inactivate C. botulinum spores are considered low risk as long as suffi- multiple hurdle recommendations on the cient moisture is removed in the drying (22). safe production of reduced oxygen foods process (9). One publication lists a recipe that (1). Refrigeration is the first barrier, fol- A few of the recipes reviewed (Table calls for simmering dried herbs for 120 lowed by one or more additional barriers: 2) mix low-acid foods with tomatoes, minutes in oil, followed by filtration (a) heat treatment to attain a temperature through cheesecloth into a clean canning either before or after drying, and are not of 90°C (194°F) for 10 min or equiva- jar (19). Unfortunately, the publication clear with regard to potential hazards of lent lethality (e.g. 80°C (176°F) for 129 does not cite research-based references or these foods when they are stored in oil. give the scientific rationale for choosing One recipe (19) assumes that mixing min, 85°C (185°F) for 36 min), (b) pH this heat-based method. An oven heat- fresh tomatoes with low-acid spices be- ≤ 5.0 throughout the food, (c) salt con- ing method for producing herb or veg- fore drying will acidify the spices, but no centration ≥ 3.5% throughout the food, or (d) a 0.97 throughout the food. It etable flavored oil found online from a evidence or peer-reviewed citations sup- w ≤ non-Extension related source (7) in 2004 port this claim. is important to emphasize that tempera- does not appear to be currently available One publication reviewed recom- tures below 10°C (50°F) inhibit group I online. This document recommends that mends adding 1 teaspoon of lemon juice C. botulinum, and the additional list- herbs and vegetables be heated in one or vinegar per 1 cup of oil to vegetable- ed hurdles inhibit growth of the psy- cup of canola oil in a 150°C (302°F) or herb-in-oil mixtures that are to be chrotrophic group II C. botulinum. Sub- oven until the temperature of the oil refrigerated (5). The Commonwealth inhibitory levels of pH, NaCl, or acid reaches 120°C (248°F). The hot oil is Scientific and Industrial Research Or- hurdles combined may provide inhibi- then strained into a suitable thermal ganisation of Australia (9) recommends tion of C. botulinum (11).

340 FOOD PROTECTION TRENDS | JUNE 2011 Labeling an ascorbic or citric acid dip. This hurdle of botulism: the current status in might reduce the risk for botulism if the Italy. Euro. Surveill. 4:7–9. If consumers fail to achieve the vegetables or herbs were incompletely 5. Bardsley, M., P. Kendall, and E. Ser- recommended hurdles or barriers em- dried and adequate moisture was present rano. 1998. Oil infusions and the ployed, herbs and vegetables stored in for botulinum growth. Likewise, dipping risk of botulism. Available at: http:// oil present a risk for foodborne illness. commercially dried herbs in an acid solu- www.ext.colostate.edu/safefood/ If temperature or storage time is critical tion might provide an additional barrier newsltr/v2n4s08.html. Accessed 21 to the safety of the product, then proper to botulism in the event that commer- February 2011. warning labels must be placed on pack- cially dried herbs absorbed moisture dur- 6. Barker, W. H., J. B. Weissmann, ages of such foods. Labels should include ing storage. At this time, the parameters V. R. Dowell, L. Gutmann, and statements similar to those required of for acid dip concentrations and submer- D. A. Kautter. 1977. Type B botulism industry: “keep frozen”, “refrigeration sion times are not known, and research outbreak caused by a commercial required” and “discard after [date]”. It is needed before a recommendation can food product. West Virginia and must be noted however, that labeling be made. Pennsylvania, 1973. J. Am. Med. should be a choice of last resort, as it may The salt and water activity hurdles Assoc. 237:456–459. not always be effective (15). (except drying) are not generally em- 7. CanolaInfo. Flavoured oils 101. ployed as consumer food safety hurdles Available at: http://www.canolainfo. CONCLUSIONS and would not be recommended. Salted org/html/flavouredoils101.html. butter inhibits the growth of C. botuli- Accessed 1 May 2004. The consumer recommendation num because it has 18% NaCl in its wa- 8. Ciafardini, G., and B. A. Zullo. 2002. that best ensures the safety of vegetables ter phase (7 CFR 58). However, there is Survival of microorganisms in or herbs stored in oil is to freeze the extra virgin olive oil during storage. no research-based information for con- product. The safety of frozen products Food. Microbiol. 19:105–109. sumers indicating that adding herbs or does not change over the shelf life of 9. Commonwealth Scientific and vegetables to butter results in a product the food, although quality changes will Industrial Research Organisation. that is safe at room temperature or under eventually occur. If consumers cannot or 2009. Preservation of vegetables in refrigeration. will not freeze the product, it should be oil and vinegar. Available at: http:// This review has attempted to draw www.csiro.au/resources/preserva- recommended that it be refrigerated for some consensus through a review of the no more than 4 days based on the rec- tion-in-oil-vinegar--vgnextfmt-print. literature on the acceptable shelf life of html. Accessed 21 February 2011. ommendations in Table 3. Consumers refrigerated vegetable- and/or herbs-in- must label their vegetable or herbs in oil 10. Corwin, E. 1993. Unrefrigerated oil mixtures with regard to reducing the garlic-, spice-in-oil mixes potentially accordingly to prevent confusion with risk of botulism poisoning. A need for other preserved products. dangerous. T93–39. U.S. Food and future research to determine the added Drug Administration, Washington, Future research is required to clarify hurdles and specific procedures that the potential of additional hurdles. Heat D.C. could make these foods safer has been 11. Elliott, P. H., and D. W. 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