High Tunnel and Organic : , Food Safety, and Quality Patricia MilIner USDA -ARS, Sustainable Agricultural Systems Laboratori', 10300 Baltimore Avenue, Building 001, Room 140, Beltsville, MD 20866; and Environmental A4icrohiologv and Food Safet y Laboratory, Beltsville, MI) 20705 Sara Reynolds USDA -ARS, Sustainable Agricultural Systems Laboratory, 10300 Baltimore A venue, Building 001, Room 140, Beltsville. MD 20866 Xiangwu Nou Environmental Microbiology and Food Satetv Laboratory, Beltsville, MD 20705 Donald Krizek USDA -ARS, Sustainable Agricultural Systems Laboratory, 10300 Baltimore Avenue, Building 001, Room 140, Beltsville, MD 20866 Additional index words, season extension, phytonutrient composition, phenolics, food safety, good agricultural practices, fresh fruits and vegetables, local produce. UV exclusion, , compost tea Abstract. High tunnels and protected horticultural structures provide organic and conventional growers with an economic means for extending the harvest season of fresh fruits and vegetables in a wide range of climate zones in North America and elsewhere. This report focuses on benefits associated with high tunnel production of fresh organic produce, including recent data on phvtonutrient quality. In addition, this report discusses concerns and knowledge gaps associated sith the use of and relative to food safety of fresh produce and survival of enteric pathogens in the moist, cool, reduced ultraviolet conditions often prevalent in high tunnels during cool-season production. The role of preplant and production elements of Good Agricultural Practices and Good Handling Practices applicable to high tunnel s y stems is provided.

The increasing use of plastic film-covered harvest and improved produce quality attrib- many conventional producers also rel y on structures such as high and low tunnels in utes. Furthermore, some conditions such as compost to maintain soil organic matter, many areas of the United States have enabled low winter temperatures coupled vilh in- particularly in intensive systems that do not growers to extend the cropping season with creased humidity, high organic matter soils, have a substantive period by earlier spring planting and later fall harvest- and low ultraviolet exposure from various which to reduce populations of crop pests ing without extensive environmental controls film types may be more conducive to survival and phytopathogens that target their primary common in traditional (Jett and of inadvertentl y introduced foodhorne illness . Quinn. 2005: Lamont ci at., 2003). In addi- pathogens, phytopathogens, or pests. Organic food as defined in the U.S. tion, selective choice of plastic film type for Organic Foods Production Act (USDA. these protected structures has been shown to COMPOST 2000) is a marketing term for items produced aid control of Bot rvtis and insects as well as under the authority of the National Organic growth (Krizek et al.. 2005a). Other Although production in protected struc- Program. The organic production approach is benefits of high tunnel production include tures occurs with soilless media such as based on minimizing off-lanii inputs and soil warming during periods of low ambient coir, peat, perlite. pine bark, rockwool, or synchronizing management practices with temperatures and reduced moisture fluctua- vermiculite and inorganic nutrient solutions natural biological cycles and processes to tions within the sheltered environment, (Cantliffe Ct al., 2003: Peet et al., 2004), maintain and improve agroecosystcm pro- weediness from reduced deposition of exter- such methods do not reflect basic organic ductivity while reducing adverse environ- nal sources of windblown seed, crop damage system principles. Most organic production mental impacts. Fresh fruits and egetables from wind and rain events, incidence of systems are based on improving and main- have led all categories of organic food and physiological ripening disorders from sun taining high soil quality. Composted organic feed sales in the United States since 1996 scorch, and chemical use from more effective matter is commonly used in organic, and when recordkeeping on organic production use of biocontrols (Jett and Quinn, 2005: some conventional high tunnel or protected began and are leading the expanding global Lamont et al.. 2003). Protected structures structure systems, in mid- to northern- demand for organic products (NBS. 2006). also appeal to direct market producers latitude growing regions in die United States California continues to have the largest num- because of low capital investment and oper- to improve and maintain soil quality. Coin- ber of acres in organic fields (60%) and ating costs and the extended season advan- post has long been used as a beneficial soil protected structures (20%) compared with tage of fresh produce sales in local markets. amendment in horticulture because it sup- other states (Green. 2008). However, many They are used by organic as well as conven- presses certain plant diseases, improves small farm (less than 5 to 50 acre) operators tional growers in a wide range of climates in moisture retention and cation exchange use are responding to the incrcased market Which efficient of in vegetable capacity, provides micronlilrients, slow- demand tbr fresh local organic produce. and small fruit cropping systems is needed release nitrogen, and organic matter (Stoffella Organic and/or local produce appeals to (Romanowski, 1981). and Kahn, 2001). Growers interested in consumers interested iii proiuce that has Despite these benefits, it is unclear what resource conservation also appreciate that minimal risk of containing and effects the different film types have on locally produced compost substitutes for agrichemical residues and is at its peak various cultivars and relative to early peat and other nonrenewable products and quality, flavor, and freshness. Also, some provides supportive enterprises for recycling consumers are interested in Supporting local horticultural industry organic residuals to preserve opet spaces within Received for publication II Nov. 2008. Accepted while avoiding landfill expenses and pro- regional communities. The reduced impacts for publication 27 Jan. 2009. vides retail product market options. Also, from avoiding fossil fuel and combustion

242 HoRTSciENcr• VOL.44(2) Ai'sn 2009 emissions that accrue from minimizing long, temperature of 55 to 76 OC ( 13 1 to 170 °F) commercial food waste would not be suitable complex food distribution chains recently for 3 d continuously, whereas windrow com- for CT production within the certified organic have added to the appeal of local fresh pro- posts mist achieve these temperatures for IS program. duce. Like with all produce types, consumer d, during which time the materials must he confidence in the safety. nutrition, and turned a minimum of five times. These FOOD SAFETY wholesomeness has a direct impact oil criteria are designed to destroy the most decisions. Perceived or actual knowl- resistant zoonotic pathogens (helminth ova), Foodborne illnesses associated with coil- edge of production inputs and a range of the exception being spore-forming bacteria sumption of fresh fruits and vegetables in the conditions such as pesticide and manure use, such as Bacillus spp. or Clostridium spp.: United States over several years have soil conservation, water quality, and post- however, plant pathogens also are destroyed increased concern by consumers as well as harvest processing as well as worker justice (Stoffella and Kahn, 2001 ). Simple stacking the producer -marketer and public health and coiflhlluility impacts can affect consumer of manure without managing it or providing a sectors about possible contamination from confidence. recommended insulated cover layer oil enteric pathogens at the primary field pro- Organic producers may rely on use of aerated piles, recording temperatures, or cluction stage. Between 1990 and 1998, 24% manure and manure-based inputs to supply turning at appropriate inter\ als will not of foodborne illness outbreaks associated part of the crop nitrogen (N) needs. Composts ensure adequate destruction of' pathogens like with consumption of contaminated produce typically have low N content, ranging from Esche,'ichia co/i 0157:1­17 in the unheated nearly equaled outbreaks associated with 0,811% to 2.0%, for mature compost that is exterior zone. Test-certified compost with meat consumption (29%) and several out- stabilized and no longer phytotoxie (Stoffella undetectable E. co/i, Salmonella. or Liste,'ia breaks involved small, organic in and Kahn, 2001). Consequentl y, additional N m000ci'togenes would provide users assur- which raw manure had been applied (C'tcslak must be supplied from other sources, which ance 01"111C product duality. et al.. I 993 Nelson. 1997). The types of fresh may include legume cover crops, blood and produce associated with illness outbreaks feather meal, and pelletiied poultry litter COMPOST TEA include many that are now being grown in with carefully timed applications. The recog- high tunnels and other protected horticultural nized presence of pathogenic microbes of Compost tea (CT) is of interest to organic structures (Table 2). public health importance in raw animal and other producers as a hiocontrol spray The protection afforded by tunnels and manure (Table 1) ( Bowman. 2009: Cooper br fbliar plant diseases or a soil drench for other structural and season-extenduig horn- et al.. 2007) requires that use of raw or root diseases and plant health (Seheucrell cultural innovations would appear to have composted manure in US DA-ccrti tied or- and Mahaffee, 2004). A variety of equip- inherent benefits against tligittve enteric ganic production systems follow specific ment, brewing methods, and additives are pathogen contamination from some impl conditions and practices. If raw manure is available for production of CT. However, cated sources such as certain wildlife. 1-low- used. then harvest ma y not occur before 90 ci additives purported to increase the benefi- ever, other suspected sources of enteric if the harvestable portion does not directly cial micro-organisms that impact the bio- pathogens such as contaminated water and contact the soil to which the raw manure was control effect have been shown to support manure-based soil amendments, proximity to added or 120 d if the harvestable portion growth of E. co/i 0157:1­17 and Sa/ouoimrlla livestock and poultry operations, equipment, directly contacts the amended soil (USDA, enterica sv. Typhimuriuns (Ingram and Millner, and overall poor sanitation remain as ele- 2000). Composted manure is defined in the 2(107). ments that must be managed through pur- National Organic Program as the product of For use in certified organic production, poseful use of Good Agricultural Practices managed process through which micro- Cl prepared from compost made with (GAPs) and Good Handling Practices organisms decompose plant or animal matter manure would at least need to meet the (GHPs) (Table 3). Both GAPs and GHPs mixtures with initial C':N ratios of 25:1 to thermophilic, time- temperature. and mail- (www.gaps.eornell.edLi) aim to reduce mi- 40:1 into more plant-available forms suitable agement standards described here. Raw crobial contamination risks to fresh fruits and for soil application. In-vessel or static aerated Manure, partially composted manure, or vegetables. pile composts are required to maintain a Table 2. Types of greens. herbs, l'i'uiis. and a cgciables gron n in hi gh tunnels. Greens table I Some pathogenic microorganisms of ,'-niarcintli .-t,na,-ui,uthics (rico/i,,' C. Dandelion Thu'cuxcuu - IM? o//uu,ialc' L. manure. public health concern ill Aru gu Ia Lin, a sc/lila L. t.ciiucc Lailncsu va/ui'ci L. multiple varieties Bacteria But Bela icc/gui/s L. NI tuna B,'a.vsica c'cipa suhsp. nupposiumica ( auij ,i'lobac'r co/i and ( '. jc'/ioci (L..t t. Bailey) t-tanelt Bacillus antli,acix Cabbage---Bi'cussica ole,'acea var. ('api/ucla L. Mustards B,'assica juncc'a multiple varieties Bruce/la ahoiiu,v Chard--Beta mu/gui/s var. c/c/a L. Radicchio—C 'iclioriuni ini,'hus [.. Esclic'm-ichis colt patho- and toxigenic strains (rcss--/.epucl/wm sulii'unm L. Shungiku--Cltri'.vanl/mc'mum co,'ona,'um,nm L. Lej ctoapii'a ilip. Chicory, endive, escarole Cic/to,'iuni Spinach—Spinaeea o/c'i'ac'eci t.. Listc'ria inonoci'togenc-"c imuli'ia I.- ,'t,4'cohac/,iu,n hoi'i.r I terhs :t-Ii'colccicic'ri'i,mi ui/urn pcu'atulv'i-cu/oai.v Peo'oselnmuni, ui/s/u/ni ( Salmons//a sp. Basil Ocinnun bus-ill/ruin C. Parsley M ill.) Yersi,,ia e,i(e'ocoli/ica ('hives ---Ill/um sclmoe,mop;'asmun L. Nyman ex A.W. I till Viruses Cilantro (,'o,-/ancl,'u,i, .calii'muni C. Rosemary Ro,ona,'i,mus officina/i.c L. Dill —A,mel/mu,,u gua i-co/sims L. Sage Sal via o//mcmna/us L. Avian--Ssrine influenza Lemon hahn —Melissa o /fuci,nu/is L. Shiso Pci/I/a fi'maescens (L.) Britton Hepatitis F Marjoram-0)'/gcununm ma/on/ca L. Sari-el Ri,,,w.v acelosuu L. Parasites M int ,t-Ic'nilia s,, Tarragon -,4uienus/a uh'ac'iu,ic'uliu.v L. Protozoa Nastum'tium—Tu'opcuc'o/uni ma/us C. Thyme— T/m,'i,mus spp. multiple vaneimcs Balaiic/ii,,n cc/i ('i'i 'j cto.cjiaiscliiini pcii'c'ci,n Vegetables and berries Giarclia spp. Broccoli B,'cussica a/macco s-ar, i/ui//ca Plenck (!)ui ioll '1/1mm,,,, cu/ic! C. fci 1ihis,,ici spp. Carrots ---flaiucus ca/or,, var. sat/mm/c HoiThi, Radish Rapliummmuus sat it-mis C. I telrninihs Cucumber - Cncmunus caucus C. Raspberry --Riu/,ius ic/anus C. ,4,ccaris suit/n Daikon--Rap/ma,iits scan-us L. Strawberry Prcmgaria xa,ua,ia.asa Ducts. Taenia app. longipinuma/mu.c Bailey Squash - Cut urbila pc-pu C. T,'iclnu'i.s o'ucliu:e,'a Melons ('cut -id/u.s niclo C. Tomato l.i'c'opei'aicomi ecci,lc'ntunm Mill.

HotcuSCIENCE Vo.. 44(2) APRIL 2009 243 Table /. kes elements rui(,00d ;\iirtc(ilttiiiil l'iaciices ((,AIs) an(I(iood Ilandlina Pinetices (illi's) lot cove was specifically associated with in- site preparation and crop production steps applicable to high tunnel and open held orga bc and conventional production systems. creased content of antioxidants (Wang and L in, 2003). Likewise, with compost soil Step Element amendments and other organic practices, Preplant I Select produce field site carebill y. avoid proxintits- to the total concentration of three major phetto- livestock and poultry operations lie acids. caffcic acid. p-coumaric acid, and 2. Store manure properly to avoid runoff and dust dispersal to crops fei'ulic acid, as measured by hi gh-perfor- 3. Treat manure properly to destroy pathogens and stabilize nutrients: test treated manure for pathogens before use in fresh produce systems mance liquid chromatogi'aphv from tomato 4. Use clean equipment: clean manure handling equipment to avoid fruit ( Licopericon e.s'culeniom Mill.) c ul- crosscontamination with crop production equipment, including tivars Oregon Spring and Red Sun was trucks and loaders 20% higher under 4-ultraviolet than 5. Time manure applications to ensure adequate time lapse to harvest date under--ultraviolet high tunnels at the Belts- 6. Plant crops at appropriate times so that harvest will not occur ville Research Center ( Luthria et al., 2006). before adequate time has lapsed since last application of manure In addition, selective ultraviolet wavelength Production I. Avoid use of raw or inadequatel y composted manure on direct contact transmission by plastic film type-enhanced flesh produce crops: consider testing the manure heibre use to assess presence of pathogens fruit yields in both cultivars were greater with -t 2. Take measures to exclude domestic animals and wildlife -ultraviolet than with --ultraviolet conditions from crops/tunnels and texture of Red Sun' was rated better 3. Train workers in hygienic job practices and provide in-held under -i-ultrttviolet than under --ultraviolet or hand-wash and toilet facilities in comparison with commercial field or 4. Test and remediatc (if necessary) irrigation water quality at hydroponically- grown li'uits (Krizek ci al.. regular intervals: avoid surfbcc water sources and open 2005b,2006). impoundments used by wildlife, unless disinfecting treatment Given the health benefits front dietary is implemented before use on crops. intake of fruits and vegetables high in vita- 5. Use a water-efficient irrigation method that avoids direct mins. minerals, and secondary phytochem i - contact with produce if water is not potable 6. Use Integrated Pest Management (IPM) and hiocontrol measures for cals (carotenoids, anthocyani ns. Ilavonoids. pest and disease control: use potable water for sprays. and other phenolic compounds), production 7. Observe National Organic Program standards for use of that enhances the dietary value of these compost tea spray and drenches on crops and soil commodities is desirable. Increasing Out- understanding of how and which production practices enhance ph ytonutrient content of various cultivars while reducing the risk of ENTERIC PATHOGEN SURVIVAL lengths below 380 nm (-ultraviolet) as pre- microbial contaminants that lead to illness viousl y reported (Krizek et al.. 2005a). Both among consumers is essential. 1--ligh tunnels Environmental conditions such as high films transmitted comparable amounts of and related protected horticultural structures humidity, low temperatures, and low ultravi- photosynthetically active radiation (400 to offer growers a range of beneficial character- olet radiation, which are frequently 700 nm). At each of five sample events, istics that make them compatible with during cooler periods in high tunnels, indi- populations of E. co/i were determined using organic as well as conventional production vidually are conducive to enhanced survival a most-probable number enrichment method of fresh fruits and vegetables. Further re- of enteric pathogens. However, no data are followed by selective media plating of all six search will he needed to address factors available to determine the extent to which replicates of each leaf locus sample set in related to the food safety , crop protection, these high tunnel conditions actually prolong each of four high tunnels. In general, E. co/i and quality of fresh produce in organic and survival in soil or on vegetables that contact on leaves declined 2 log 1() CFU/leaf in the conventionally managed high tunnels. the soil or whether GAPs or GI-IPs are first 24 It after inoculation regardless of leaf adequate to protect food safety in these age, position on the plant, high humidity, or Literature Cited situations. In a recent high tunnel survival ultraviolet exposure status. Steady decline study involving a nonpathogenic strain of E. continued over 28 d such that S. ('0/i pop- t)ss man. D.D. 2000. Manure pathogens.. McGraw co/i 11th, New York, NY. 0157:H7 TTI2B (Feng et al.. 2001), ulations were either on average undetectable leaves of old -lower-shaded, young-upper- Cantliftd. D.J J. Furies, F. Jovicich, A. Paranjpe, J. ( young-top leaves and youngest-ci'own Rodriguez. and N.L. Shaw. 2003. Media and exposed, and youngest-partially exposed leaves) to just barely detectable, remaining emerging crown leaves of spinach containers for soilless grown (Splizacea on average at II C'FU/inoculated leaf by Day o/c','acea L.) cv. Whale were inoculated with cucumbers, melons, peppers. and strawberries. 28. Persistence of very low numbers of S. co/i Acts Ilor. 614:199-203. 100 pL of manure extract [average 2.3 x 10 on contaminated plant tissue is consistent ('ieslak, P.R., Ti. Barrett. P.M. Griffin. K.F. colony-forming units (CFU)/leaf] or uninoc- with reports from fresh produce studies (jensheimer. G. Beckett, J. Rufbington, and ulated extract. The purpose ot'this test was to (Mukherjee et al., 2(04) and has important M.G. Sm i lb. 1993. Lsc/,eiii-h,a co/i 0157:1-17 determine if the E. co/i would -row or decline implications for the need to maintain a high infection from It manured . Lancet on leaves under high tunnel conditions. The 342:367. degree of hygiene relative to enleric pathogen load was rapidly reduced Cooper, J., U. Niggli, and C. Leifert. 2007. 1-land- handling. use 0)' water, and commodity stor- (unpublished data). All plants were grown 4 hook of' organic food safety and quality. age temperatures. These types of factors months in soil amended with mature compost Vvoodhead Publishing Ltd.. Cambridge, UK. apply equally to organic and conventionally Feng, P., M. Dey. A. determined to have undetectable concentra- Abe. and T. Jakeda. 2001. produced commodities. Isogenic strain of Ecc/ie,'f-hia ci!, 0157:1-17 tions Of E. co/i, .Sa/n,o,w'//o spp., and Liste,'ia that has lost both shi p toxin I and 2 genes. fli000c110 genes. Plants were irrigated with PHYTONUTRIENTS Clui. Diagn. Lab. Immunol. 8:711-714. drinking quality water as needed during the Green. C. 2008. Organic production -Data Sets. 4-week survival study period from Mar. In addition to microbial q ua lity, organic USDA. Economic Research Service 2008. 8 Sept. through Apr. 2008 without supplemental production has been reported to have a 2008. . Ingrain, D.T. and P.D. Millnei. tdi'tilizer; no irrigation water contacted inoc- Positive effect on the phytotiutrient (poly- 2007. Factors affecting compost tea ass potential source of ulated leaves. Duplicate tunnels covered with phenolic arid antioxidant) content of fruits film either transmitted ambient solar ultravi- Esche,'ichw co/i and Salnio,tcl/u on fresh pro- and vegetables (Zhao et al.. 2006). Compost duce. J. Food Prot. 70:828- 834. olet radiation from 290 to 400 nm use during growth of strawberry (F;'agai'ia Jett, L.W. and J. Quinn. (- I 2005. G'owing encumbers -ultraviolet) or blocked ultraviolet wave- X00000ssa Duch,) cultivars Allstar and Hon- within a high tunnel (lvtisscuri ). In: Maynard, 244 lij 11 i \' : 2) -\ait 20(10 El. and (C. Gunter (cds.). \lidnest seectable Luthria, DL., S. Mukhopadhvav. and I). F. Kri,ek. Romanosvski. R. 1951. Ens ironrnciital control variety trial report for 2005. Bulletin No. 2006. Content of total phcnolcs and phenolic structures. p. 119 127. lit: Plucknett, D.L. and B 178111- Purdue university. West Lafeyctie. acids in tomato ( L rcopela icon O.ci!/Cflht?I1i H.L. Beemer.Jr. (eds.). Vegetable famung sys- IN. Mill.) fruits as influenced by cultivar and solar tents in China. Westviess Press, Boulder, CO. Krizek, 1)1., I ID. (lark, and R.M. Mirecki. U V radiation. J. Food Compost. Anal. 19:771 Scheuerell, Si. and W.F. Mahaffee. 2004. (out- 2005a. Spectral properties of selected CV- 777. post tea asaconta i ncr mcdi urn drench for blocking and UV-transmitting covering materi- Mukherjee, A.. D. Speh. F. Dyck. and F. Die,- suppressing seedling dampin g-off caused by als with application for production ofhigh-value Gonzalez. 2004. Preharvest evaluation of coli- /'i't/ioini ultunu,n. Phytopathol ogy 94:1156- crops in high tunnels. Photochem. Photohiol tbrnis, E,sclierichia colt...tt/nionel/o, and 1163. 81:11)47 1(151. Ext /u.',it/i!a co/i Dl 57:1-17 in organic and con- Sto ffe I Ia. P.J. and B.A. Kahn. -001.1 Compost Krizek, l).T.. P.D. Millner, M.J. Camp. lID. Clark. veiitional produce grown by Minnesota fann- utilization in horticultural cropping systems. M.G. Davis. B. Butler, J.R. Tcasdale, D.R. ers'. 1. Food Prot. 67:894-900. CRC Press, Boca Raton, FL. Fravel, S. Reynolds, R.A. Mangum. and TV. NBS. 2006. An analysis of markets, trends, com- USDA. 2000. National Organic Program, 7 CER Currier. 2005h. Disease and management chal- petition and strategy in U.S. organic foods: Part 205. The Organic Foods Production Act of lenges encountered during the first year of 1996 2010. National Business Journal Organic 1990, as amended (7 U.S.C. 651)1-6522) 65 FR growing tomatoes in high tunnels in Beltsvi lIe. Foods Report: Penton Media, Inc.. Boulder. CO. 80637, 21 Dec. 2000. US Department of MD. FlortScience 40:107 1 Nelson. P.V. 1997. The contamination of organic Agriculture. Agricultural Marketing Service, Krizek, Dl., R.A. Saftner, F. Park, I.A. Abbott. produce by human pathogens in animal man- Washington. DC. M.J. Camp. and III). Clark. 2006. Yield data ures. 17 Aug,,. 2008.

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