High Tunnel and Organic : , Food Safety, and Quality Patricia Millner USDA-ARS, Sustainable Agricultural Systems Laboratory, 10300 Baltimore Avenue, Building 001, Room 140, Beltsville, MD 20866; and Environmental Microbiology and Food Safety Laboratory, Beltsville, MD 20705 Sara Reynolds USDA-ARS, Sustainable Agricultural Systems Laboratory, 10300 Baltimore Avenue, Building 001, Room 140, Beltsville, MD 20866 Xiangwu Nou Environmental Microbiology and Food Safety 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 phytonutrient quality. In addition, this report discusses concerns and knowledge gaps associated with 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 systems is provided.

The increasing use of plastic film-covered harvest and improved produce quality attrib- many conventional producers also rely 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 with 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 inadvertently introduced foodborne illness . Quinn, 2005; Lamont et al., 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 Botrytis 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-farm 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 et al., 2003; Peet et al., 2004), maintain and improve 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 vegetables 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 the United States California continues to have the largest num- because of low capital investment and oper- to improve and maintain soil quality. Com- 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 are responding to the increased market which efficient use of in vegetable capacity, provides micronutrients, slow- demand for 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 in produce 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 open spaces within Received for publication 11 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 HORTSCIENCE VOL. 44(2) APRIL 2009 emissions that accrue from minimizing long, temperature of 55 to 76 C (131 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 must achieve these temperatures for 15 program. duce. Like with all produce types, consumer d, during which time the materials must be confidence in the safety, nutrition, and turned a minimum of five times. These FOOD SAFETY wholesomeness has a direct impact on pur- criteria are designed to destroy the most chase decisions. Perceived or actual knowl- resistant zoonotic pathogens (helminth ova), Foodborne illnesses associated with con- 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 community impacts can affect consumer of manure without managing it or providing a sectors about possible contamination from confidence. recommended insulated cover layer on static enteric pathogens at the primary field pro- Organic producers may rely on use of aerated piles, recording temperatures, or duction stage. Between 1990 and 1998, 24% manure and manure-based inputs to supply turning at appropriate intervals 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 Escherichia coli O157:H7 in the unheated nearly equaled outbreaks associated with 0.8% to 2.0%, for mature compost that is exterior zone. Test-certified compost with meat consumption (29%) and several out- stabilized and no longer phytotoxic (Stoffella undetectable E. coli, Salmonella,orListeria breaks involved small, organic in and Kahn, 2001). Consequently, additional N monocytogenes would provide users assur- which raw manure had been applied (Cieslak must be supplied from other sources, which ance of the product quality. et al., 1993; Nelson, 1997). The types of fresh may include legume cover crops, blood and produce associated with illness outbreaks feather meal, and pelletized 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 biocontrol spray The protection afforded by tunnels and manure (Table 1) (Bowman, 2009; Cooper for foliar plant diseases or a soil drench for other structural and season-extending horti- et al., 2007) requires that use of raw or root diseases and plant health (Scheuerell cultural innovations would appear to have composted manure in USDA-certified or- and Mahaffee, 2004). A variety of equip- inherent benefits against fugitive enteric ganic production systems follow specific ment, brewing methods, and additives are pathogen contamination from some impli- conditions and practices. If raw manure is available for production of CT. However, cated sources such as certain wildlife. How- used, then harvest may not occur before 90 d 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. coli O157:H7 and Salmonella livestock and poultry operations, equipment, directly contacts the amended soil (USDA, enterica sv. Typhimurium (Ingram and Millner, and overall poor sanitation remain as ele- 2000). Composted manure is defined in the 2007). ments that must be managed through pur- National Organic Program as the product of a For use in certified organic production, poseful use of Good Agricultural Practices managed process through which micro- CT 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 man- (www.gaps.cornell.edu) 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, fruits, and vegetables grown in high tunnels. Greens Table 1. Some pathogenic microorganisms of Amaranth—Amaranthus tricolor L. Dandelion—Taraxacum officinale L. public health concern in manure. Arugula—Eruca sativa L. Lettuce—Lactuca sativa L. multiple varieties Bacteria Beet—Beta vulgaris L. Mizuna—Brassica rapa subsp. nipposinica Campylobacter coli and C. jejuni (L.H. Bailey) Hanelt Bacillus anthracis Cabbage—Brassica oleracea var. capitata L. Mustards—Brassica juncea multiple varieties Brucella abortus Chard—Beta vulgaris var. cicla L. Radicchio—Cichorium intybus L. Escherichia coli patho- and toxigenic strains Cress—Lepidium sativum L. Shungiku—Chrysanthemum coronarium L. Leptospira spp. Chicory, endive, escarole—Cichorium Spinach—Spinacea oleracea L. Listeria monocytogenes endivia L. Mycobacterium bovis Mycobacterium avium paratuberculosis Herbs Salmonella spp. Basil—Ocimum basillicum L. Parsley—Petroselinum crispum (Mill.) Yersinia enterocolitica Chives—Allium schoenoprasum L. Nyman ex A.W. Hill Viruses Cilantro—Coriandrum sativum L. Rosemary—Rosmarinus officinalis L. Dill—Anethum graveolens L. Sage—Salvia officinalis L. Avian–Swine influenza Lemon balm—Melissa officinialis L. Shiso—Perilla frutescens (L.) Britton Hepatitis E Marjoram—Origanum majoraca L. Sorrel—Rumex acetosa L. Parasites Mint—Mentha spp. Tarragon—Artemisia dracunculus L. Protozoa Nasturtium—Tropaeolum majus L. Thyme—Thymus spp., multiple varieties Balatidium coli Cryptosporidium parvum Vegetables and berries Giardia spp. Broccoli—Brassica oleracea var. italica Plenck Onion—Allium cepa L. Toxoplasma spp. Carrots—Daucus carota var. sativus Hoffm. Radish—Raphanus sativus L. Helminths Cucumber—Cucumis sativus L. Raspberry—Rubus idaeus L. Ascaris suum Daikon—Raphanus sativus L. Strawberry—Fragaria ·ananassa Duch. Taenia spp. longipinnatus Bailey Squash—Cucurbita pepo L. Trichuris trichiura Melons—Cucumis melo L. Tomato—Lycopersicon esculentum Mill.

HORTSCIENCE VOL. 44(2) APRIL 2009 243 Table 3. Key elements of Good Agricultural Practices (GAPs) and Good Handling Practices (GHPs) for eoye was specifically associated with in- site preparation and crop production steps applicable to high tunnel and open field organic and creased content of antioxidants (Wang and conventional production systems. Lin, 2003). Likewise, with compost soil Step Element amendments and other organic practices, Preplant 1. Select produce field sites carefully, avoid proximity to the total concentration of three major pheno- livestock and poultry operations lic acids, caffeic acid, p-coumaric acid, and 2. Store manure properly to avoid runoff and dust dispersal to crops ferulic acid, as measured by high-perfor- 3. Treat manure properly to destroy pathogens and stabilize nutrients; mance liquid chromatography from tomato test treated manure for pathogens before use in fresh produce systems fruit (Lycopericon esculentum Mill.) cul- 4. Use clean equipment; clean manure handling equipment to avoid crosscontamination with crop production equipment, including tivars Oregon Spring and Red Sun was trucks and loaders 20% higher under +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 1. Avoid use of raw or inadequately composted manure on direct contact transmission by plastic film type-enhanced fresh produce crops; consider testing the manure before use to fruit yields in both cultivars were greater with assess presence of pathogens +ultraviolet than with –ultraviolet conditions 2. Take measures to exclude domestic animals and wildlife and texture of ‘Red Sun’ was rated better from crops/tunnels 3. Train workers in hygienic job practices and provide in-field under +ultraviolet than under –ultraviolet or hand-wash and toilet facilities in comparison with commercial field or 4. Test and remediate (if necessary) irrigation water quality at hydroponically grown fruits (Krizek et al., regular intervals; avoid surface water sources and open 2005b, 2006). impoundments used by wildlife, unless disinfecting treatment Given the health benefits from 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 phytochemi- contact with produce if water is not potable cals (carotenoids, anthocyanins, flavonoids, 6. Use Integrated Pest Management (IPM) and biocontrol measures for and other phenolic compounds), production pest and disease control; use potable water for sprays. 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 our understanding of how and which production practices enhance phytonutrient 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 viously reported (Krizek et al., 2005a). Both among consumers is essential. High 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 present 700 nm). At each of five sample events, istics that make them compatible with during cooler periods in high tunnels, indi- populations of E. coli 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 be 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. coli and quality of fresh produce in organic and survival in soil or on vegetables that contact on leaves declined 2 log10 CFU/leaf in the conventionally managed high tunnels. the soil or whether GAPs or GHPs are first 24 h 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 Bowman, D.D. 2009. Manure pathogens.. McGraw study involving a nonpathogenic strain of E. continued over 28 d such that E. coli pop- coli O157:H7 TT12B (Feng et al., 2001), Hill, New York, NY. ulations were either on average undetectable Cantliffe, D.J., J. Funes, E. Jovicich, A. Paranjpe, J. leaves of old–lower-shaded, young–upper- (young–top leaves and youngest–crown Rodriguez, and N.L. Shaw. 2003. Media and exposed, and youngest–partially exposed leaves) to just barely detectable, remaining containers for soilless grown emerging crown leaves of spinach (Spinacea on average at 11 CFU/inoculated leaf by Day cucumbers, melons, peppers, and strawberries. oleracea L.) cv. Whale were inoculated with 28. Persistence of very low numbers of E. coli Acta Hort. 614:199–203. 100 mL of manure extract [average 2.3 · 105 on contaminated plant tissue is consistent Cieslak, P.R., T.J. Barrett, P.M. Griffin, K.F. colony-forming units (CFU)/leaf] or uninoc- with reports from fresh produce studies Gensheimer, G. Beckett, J. Buffington, and ulated extract. The purpose of this test was to (Mukherjee et al., 2004) and has important M.G. Smith. 1993. Escherichia coli O157:H7 infection from a manured . Lancet determine if the E. coli would grow or decline implications for the need to maintain a high on leaves under high tunnel conditions. The 342:367. degree of hygiene relative to Cooper, J., U. Niggli, and C. Leifert. 2007. Hand- enteric pathogen load was rapidly reduced handling, use of water, and commodity stor- book of organic food safety and quality. (unpublished data). All plants were grown 4 age temperatures. These types of factors Woodhead Publishing Ltd., Cambridge, UK. months in soil amended with mature compost apply equally to organic and conventionally Feng, P., M. Dey, A. Abe, and T. Takeda. 2001. determined to have undetectable concentra- produced commodities. Isogenic strain of Escherichia coli O157:H7 tions of E. coli, Salmonella spp., and Listeria that has lost both shiga toxin 1 and 2 genes. monocytogenes. Plants were irrigated with PHYTONUTRIENTS Clin. 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 quality, organic USDA, Economic Research Service 2008. 8 Sept. through Apr. 2008 without supplemental production has been reported to have a 2008. . Ingram, D.T. and P.D. Millner. 2007. Factors ; no irrigation water contacted inoc- positive effect on the phytonutrient (poly- affecting compost tea as a potential source of ulated leaves. Duplicate tunnels covered with phenolic and antioxidant) content of fruits Escherichia coli and Salmonella on fresh pro- film either transmitted ambient solar ultravi- 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 (Fragaria Jett, L.W. and J. Quinn. 2005. Growing cucumbers (+ultraviolet) or blocked ultraviolet wave- ·ananassa Duch.) cultivars Allstar and Hon- within a high tunnel (Missouri). In: Maynard,

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