Microbial flora on restaurant beverage lemon slices.Introduction
The antimicrobial properties of lemons are well documented. One study (Dabbah, Edwards, & Moats, 1970) demonstrated significant inhibition of bacterial growth in nutrient broth when lemon oil was added. Other studies report similar antimicrobial activity by lemons and lemon extract against numerous microbes, including Candida albicans Candida albicans,
n a pathogenic yeast, which is the causal agent of thrush, vaginal infections, and systemic candidiasis.
Candida albicans , Escherichia coli Escherichia coli (ĕsh'ərĭk`ēə kō`lī), common bacterium that normally inhabits the intestinal tracts of humans and animals, but can cause infection in other parts of the body, especially the urinary tract. , Escherichia coli O157:H7, Helicobacter pylori Helicobacter pylori
A gramnegative rod-shaped bacterium that lives in the tissues of the stomach and causes inflammation of the stomach lining.
Mentioned in: Indigestion, Ulcers
Helicobacter pylori , Klebsiella pneumoniae Klebsiella pneu·mo·ni·ae
Friedlander's bacillus. , Listeria Listeria /Lis·te·ria/ (lis-ter´e-ah) a genus of gram-negative bacteria (family Corynebacterium); L. monocyto´genes causes listeriosis.
n. innocua, Listeria monocytogenes, Mycobacterium tuberculosis Mycobacterium tuberculosis
Mycobacterium tuberculosis , Neisseria gonorrhoeae Neisseria gon·or·rhoe·ae
The bacterium that causes gonorrhea. It cannot survive for any length of time outside the human body. , Penicillium digitatum, Penicillium italicum, Pseudomonas aeruginosa Pseudomonas aeruginosa A normal soil inhabitant and human saprophyte that may contaminate various solutions in a hospital, causing opportunistic infection in weakened Pts Clinical Infective endocarditis in IVDAs, RTIs, UTIs, bacteremia, meningitis, 'malignant' , Saccharomyces Saccharomyces: see yeast. cerevisiae, Salmonella spp., Salmonella typhi Salmonella ty·phi
Typhoid bacillus. , Shigella dysenteriae Shigella dys·en·ter·i·ae
Shigella dysenteriae Shigella group A Microbiology The least commonly isolated and most virulent Shigella serotype , Staphylococcus aureus Staphylococcus au·re·us
A bacterium that causes furunculosis, pyemia, osteomyelitis, suppuration of wounds, and food poisoning.
Staphylococcus aureus Staphylococcus pyogenes , and Streptococcus streptococcus (strĕp'təkŏk`əs), any of a group of gram-positive bacteria, genus Streptococcus, some of which cause disease. faecalis. (Adeleye & Opiah, 2003; Belletti et al., 2004; Brock & Ketchum, 1951; Caccioni, Guizzardi, Biondi, Renda, & Ruberto, 1998; Dabbah et al., 2002; Dada, Alade, Ahmad, & Yadock, 2002; Francis & O'Beime, 2002; Nogueira, Oyarzabal, & Gombas, 2003; Ohno et al., 2003; & Saleem, Afza, Anwar, Hai, & Ali, 2003). Lemon juice has even been shown to be useful as an anti-HIV agent when applied vaginally in sexually active women (Potts, Perlman, Mandara, Prata, & Campbell, 2004; Short, McCoombe, Maslin, & Crowe, 2004). Another study reported significant larvicidal activity by a fresh lemon peel extract (Salvatore, Borkosky, Willink, & Bardon, 2004). Many nonscientific Web sites proclaim the antimicrobial effects of lemons and lemon juice as a benefit in food preparation, sterilization of the rind of fruits and vegetables, sterilization of kitchen cutting boards, and as a sore-throat remedy (Boschen, n.d.; iVillage, 2002; Rall & Center for Unhindered unhindered
not prevented or obstructed: unhindered access
without being prevented or obstructed: he was able to go about his work unhindered Living, 2005; Podleski, 2006; Weiss, 2005). One site encourages restaurant patrons to squeeze lemon juice into drinking water drinking water
supply of water available to animals for drinking supplied via nipples, in troughs, dams, ponds and larger natural water sources; an insufficient supply leads to dehydration; it can be the source of infection, e.g. leptospirosis, salmonellosis, or of poisoning, e.g. , onto the hands, and all over the silverware in order to kill microbes (Tufarelli, n.d.).
Water containing lemon, however, was found to actually enhance the growth of Pseudomonas aeruginosa in one study (Ibrahim & Ogunmodede, 1991). Moreover, some lemon exporters spray the fruit with antimicrobial chemicals in order to kill Vibrio cholerae Vibrio chol·er·ae
A bacterium that causes Asiatic cholera in humans; Koch's bacillus.
Vibrio cholerae Infectious disease The Vibrio , Penicillium digitatum, Botrytis cinerea, and other microbes that may be contaminating the rind; this procedure indicates a lack of faith in the antimicrobial properties of lemon. (Cheah & Hunt, 1994; Cheah & Tran, 1995; de Castillo et al., 1998).
In restaurants, a lemon slice is commonly placed on the rim of a beverage glass, or afloat in the beverage, as a flavor enhancer or a decorative garnish. Although a patron might ask for this embellishment, frequently the lemon is added without the customer's request. Our study investigated whether these lemon slices contain microbial microbial
pertaining to or emanating from a microbe.
the breakdown of organic material, especially feedstuffs, by microbial organisms. contamination that might be ingested by restaurant patrons.
Materials and Methods
Samples were collected surreptitiously sur·rep·ti·tious
1. Obtained, done, or made by clandestine or stealthy means.
2. Acting with or marked by stealth. See Synonyms at secret. , without the knowledge of the restaurant staff. Two StarPlex[R] brand specimen-collection swabs were used for each sample. Samples were taken as soon as the beverage was served, before a sip was taken, and before the lemon slice was touched by the patron. One swab was rubbed along the rind. The second swab was rubbed along the flesh of the fruit. A total of 76 lemons from 21 restaurants were sampled during 43 visits. Water and soda were the only beverages used in the study.
Each swab was cultured onto a TSA-II 5 percent sheep's blood agar blood agar
A nutrient culture medium that is enriched with whole blood and used for the growth of certain strains of bacteria. plate and a MacConkey II agar plate. Plates were incubated at 35[degrees]C in a C[O.sub.2]-enriched aerobic atmosphere. Since samples were taken from the surfaces of the lemon slices, anaerobe anaerobe /an·aer·obe/ (an´ah-rob) an organism that lives and grows in the absence of molecular oxygen.
facultative anaerobes recovery was not attempted. Culture plates were examined for growth at 24 hours, reincubated, and examined again after 48 hours. Isolates were identified by Gram stain gram stain
Staining technique for the initial identification of bacteria, devised in 1884 by the Danish physician Hans Christian Gram (1853–1938). The stain reveals basic differences in the biochemical and structural properties of a living cell. , colony characteristics, API 20C Aux[R] for yeast, API 20E API 20E
a commerically available kit used for the identification of Enterobacteriaceae and some other gram-negative bacteria. [R] for Enterobacteriaceae, PYR PYR Pyrrolidonyl Aminopeptidase
PYR Per Your Request
PYR Prior Year Report Test Kit for Enterococcus enterococcus /en·tero·coc·cus/ (en?ter-o-kok´us) pl. enterococ´ci an organism belonging to the genus Enterococcus.
Enterococcus /En·tero·coc·cus/ ( , [H.sub.2][O.sub.2] for catalase catalase /cat·a·lase/ (kat´ah-las) a hemoprotein enzyme that catalyzes the decomposition of hydrogen peroxide to water and oxygen, protecting cells. , and rabbit plasma for coagulase coagulase /co·ag·u·lase/ (-las) an antigenic substance of bacterial origin, produced by staphylococci, which may be causally related to thrombus formation.
n. . Isolates were not quantified.
Culture results are found in Table 1, Table 2, Table 3, and Table 4. Twenty-three (30.3 percent) of the lemon slices produced no microbial growth from the rind or the flesh. A total of 25 different microorganisms were recovered, including bacteria and yeasts. Fifty-three (69.7 percent) of the lemon slices produced some microbial growth, either from the rind, the flesh, or both (Table 1). Thirteen (17.1 percent) of the lemon slices had microbes only on the rind; this number represented 24.5 percent of the lemon slices that produced microbial growth (Table 2). Eleven (14.5 percent) of the lemon slices had microbes only on the flesh; this number represented 20.8 percent of the lemon slices that produced microbial growth (Table 3). Twenty-nine (38.2 percent) of the lemon slices had microbes on both the flesh and the rind; this represented 54.7 percent of those lemon slices that produced microbial growth (Table 4). Of the 29 samples that had microbial growth on the flesh and the rind, 9 (31 percent) had exactly the same microorganism microorganism /mi·cro·or·gan·ism/ (-or´gah-nizm) a microscopic organism; those of medical interest include bacteria, fungi, and protozoa. or microorganisms on both locations, whereas 20 (69 percent) had some differences in the microorganisms that were recovered from the rind and the flesh (Table 3). In 15 instances (19.7 percent), the microorganisms recovered from the rind were completely different from those that were recovered from the flesh; this situation occurred in 51.7 percent of the 29 slices that produced microbial growth from both the flesh and the rind (Table 3). Six of the lemon slices (7.9 percent) produced three or more species; this number represented 11.3 percent of the lemon slices that produced microbial growth (Table 3).
Possible Origins of the Microbial Contaminants
It is not possible to definitively identify the origins of the microorganisms. While the Enterobacteriaceae and nonfermentative Gramnegative bacilli bacilli /ba·cil·li/ (bah-sil´i) plural of bacillus.
see bacillus. could have come from the fingertips of a restaurant employee via human fecal or raw-meat or poultry contamination, they might have contaminated the lemons before they even arrived at the restaurant. The Gram-positive cocci cocci /coc·ci/ (kok´si) plural of coccus.
[L.] plural of coccus. and Corynebacterium Corynebacterium /Co·ry·ne·bac·te·ri·um/ (-bak-ter´e-um) a genus of bacteria including C. ac´nes, a species present in acne lesions, C. diphthe´riae, the etiologic agent of diphtheria, C. isolates may have been introduced onto the lemons from the skin or oral flora of anyone who handled them, before or after they arrived in the restaurant. The Bacillus bacillus (bəsĭl`əs), any rod-shaped bacterium or, more particularly, a rod-shaped bacterium of the genus Bacillus. Some bacterium in the genus cause disease, for example B. species are ubiquitous and could have had numerous sources, including airborne spores landing on the fruit or on the knife used to cut the lemon.
There are three possible origins for the various yeasts that were isolated. Some yeasts commonly colonize col·o·nize
v. col·o·nized, col·o·niz·ing, col·o·niz·es
1. To form or establish a colony or colonies in.
2. To migrate to and settle in; occupy as a colony.
3. lemons and other foods, and are classified by the food industry as "food spoilage spoilage
decomposition; said of meat, milk, animal feeds especially ensilage. yeasts" (Adegoke, Iwahashi, Komatsu, Obuchi, & Iwahashi, 2000). Some distributors add yeasts to lemons and other fruits in order to retard the growth of other, destructive fungi (Cheah et al., 1994; Cheah et al., 1995; Droby, Chalutz, & Wilson, 1991). Finally, the yeasts could have originated from oral, fecal, or vaginal secretions contaminating the fingertips of a restaurant employee or another food handler.
Diseases Caused by the Microbes Found on the Lemon Samples
The microbes found on the lemon samples in our investigation all have the potential to cause infectious diseases at various body sites, although the likelihood was not determined in this study. An extensive search of the literature yielded no reported outbreaks or illnesses attributed to lemon slices in beverages. Establishment of an infection would depend upon the number of microbes introduced; this investigation did not include a quantitative determination of the numbers of microorganisms on the lemons. Other factors that would contribute to the establishment of an infection would include whether the organisms were resistant to multiple antibiotics, the general health and age of the individual, the status of the immune system immune system
Cells, cell products, organs, and structures of the body involved in the detection and destruction of foreign invaders, such as bacteria, viruses, and cancer cells. Immunity is based on the system's ability to launch a defense against such invaders. , and the integrity of the mucous membranes Mucous membranes
The inner tissue that covers or lines body cavities or canals open to the outside, such as nose and mouth. These membranes secrete mucus and absorb water and salts.
Mentioned in: Leprosy, Pulmonary Fibrosis, Topical Anesthesia of the lips and mouth.
Although lemons have known antimicrobial properties, the results of our study indicate that a wide variety of microorganisms may survive on the flesh and the rind of a sliced lemon. Restaurant patrons should be aware that lemon slices added to beverages may include potentially pathogenic microbes. Further investigations could determine the source of these microorganisms, establish the actual threat (if any) posed by their presence on the rim of a beverage, and develop possible means for preventing the contamination of the lemons. It could also be worthwhile to study contamination on other beverage garnishes, such as olives, limes limes
In ancient Rome, a strip of open land along which troops advanced into unfriendly territory. It came to mean a Roman military road, fortified with watchtowers and forts. , celery, and cherries, and to investigate whether alcoholic beverages have an effect not seen with water and soda.
Corresponding author: Anne LaGrange Loving, M.S., M(ASCP ASCP American Society of Clinical Pathologists. ), Assistant Professor of Science, Passaic County Community College Passaic County Community College is an accredited, co-educational, two-year, public, community college located in Passaic County, New Jersey. The school's main campus is located in Paterson. , One College Boulevard, Paterson, NJ 07505. E-mail: firstname.lastname@example.org.
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Anne LaGrange Loving, M.S., M(ASCP)
John Perz, M.S., MT(ASCP)
TABLE 1 Positive Culture Results* Sample** Site Culture Results 1 Rind A. baumanii, C. guilliermondii Flesh E. cloacae, E. sakazakii, S. epidermidis, S. viridans 2 Rind No growth Flesh C. lusitaniae 3 Rind No growth Flesh C. lusitaniae 4 Rind No growth Flesh C. lusitaniae 5 Rind A. baumanii, S. epidermidis Flesh A. baumanii 6 Rind A. baumanii Flesh A. baumanii, S. epidermidis, Corynebacterium spp. 7 Rind No growth Flesh B. subtilis 8 Rind S. epidermidis, S. viridans Flesh No growth 9 Rind B. subtilis Flesh No growth 10 Rind C. parapsilosis Flesh No growth 11 Rind C. tropicalis Flesh C. krusei 12 Rind T. glabrata Flesh C. tropicalis 13 Rind C. tropicalis, Bacillus spp. Flesh C. tropicalis 14 Rind C. tropicalis Flesh T. glabrata, C. krusei 15 Rind C. albicans, Bacillus spp. Flesh No growth 16 Rind B. subtilis Flesh B. subtilis 17 Rind C. guilliermondii Flesh C. guilliermondii 18 Rind B. subtilis Flesh C. guilliermondii 19 Rind C. krusei Flesh C. tropicalis 20 Rind C. lusitaniae Flesh C. lusitaniae 21 Rind C. guilliermondii Flesh S. epidermidis 22 Rind Bacillus spp. Flesh C. parapsilosis 23 Rind C. parapsilosis Flesh C. parapsilosis 24 Rind Enterococcus spp., S. epidermidis Flesh C. guilliermondii 25 Rind S. epidermidis, C. parapsilosis Flesh C. parapsilosis 26 Rind No growth Flesh S. marcescens 27 Rind C. guilliermondii Flesh C. guilliermondii 28 Rind A. baumanii, C. parapsilosis Flesh No growth 29 Rind C. guilliermondii Flesh E. cloacae 30 Rind K. oxytoca Flesh C. guilliermondii, T. asahii 31 Rind No growth Flesh B. subtilis 32 Rind B. cereus Flesh No growth 33 Rind P. fluorescens, P. putida Flesh No growth 34 Rind C. krusei Flesh C. guilliermondii 35 Rind C. krusei Flesh C. guilliermondii 36 Rind No growth Flesh B. subtilis 37 Rind S. viridans Flesh A. baumanii 38 Rind No growth Flesh B. subtilis 39 Rind No growth Flesh B. subtilis 40 Rind S. epidermidis Flesh No growth 41 Rind No growth Flesh Micrococcus spp. 42 Rind E. coli Flesh E. coli 43 Rind E. coli, P. mirabilis Flesh E. coli 44 Rind S. epidermidis, Bacillus spp., Enterococcus spp. Flesh S. epidermidis, Bacillus spp., Enterococcus spp. 45 Rind Bacillus spp. Flesh No growth 46 Rind Bacillus spp. Flesh No growth 47 Rind E. coli Flesh E. coli 48 Rind E. coli Flesh No growth 49 Rind Bacillus spp. Flesh No growth 50 Rind Bacillus spp. Flesh Bacillus spp. 51 Rind S. viridans Flesh C. tropicalis 52 Rind No growth Flesh Enterococcus spp. 53 Rind Enterococcus spp. Flesh No growth * 53 of the 76 lemon samples produced some microbial growth on the rind, the flesh, or both. ** Shading denotes one restaurant visit. TABLE 2 Culture Results from Samples with Growth on the Rind* Sample** Site Culture Results 1 Rind S. epidermidis, S. viridans Flesh No growth 2 Rind B. subtilis Flesh No growth 3 Rind C. parapsilosis Flesh No growth 4 Rind C. albicans, Bacillus spp. Flesh No growth 5 Rind A. baumanii, C. parapsilosis Flesh No growth 6 Rind B. cereus Flesh No growth 7 Rind P. fluorescens, P. putida Flesh No growth 8 Rind S. epidermidis Flesh No growth 9 Rind Bacillus spp. Flesh No growth 10 Rind Bacillus spp. Flesh No growth 11 Rind E. coli Flesh No growth 12 Rind Bacillus spp. Flesh No growth 13 Rind Enterococcus spp. Flesh No growth * 13 samples produced microbial growth only on the rind. ** Shading denotes one restaurant visit. TABLE 3 Culture Results from Samples with Growth Only on the Flesh* Sample** Site Culture Results 1 Rind No growth Flesh C. lusitaniae 2 Rind No growth Flesh C. lusitaniae 3 Rind No growth Flesh C. lusitaniae 4 Rind No growth Flesh B. subtilis 5 Rind No growth Flesh S. marcescens 6 Rind No growth Flesh B. subtilis 7 Rind No growth Flesh B. subtilis 8 Rind No growth Flesh B. subtilis 9 Rind No growth Flesh B. subtilis 10 Rind No growth Flesh Micrococcus spp. 11 Rind No growth Flesh Enterococcus spp. * 11 samples produced microbial growth only on the flesh. ** Shading denotes one restaurant visit. TABLE 4 Culture Results from Samples with Growth on the Flesh and the Rind* Sample** Site Culture Results 1 Rind A. baumanii, C. guilliermondii Flesh E. cloacae, E. sakazakii, S. epidermidis, S. viridans 2 Rind A. baumanii, S. epidermidis Flesh A. baumanii 3 Rind A. baumanii Flesh A. baumanii, S. epidermidis, Corynebacterium spp. 4 Rind C. tropicalis Flesh C. krusei 5 Rind T. glabrata Flesh C. tropicalis 6 Rind C. tropicalis, Bacillus spp. Flesh C. tropicalis 7 Rind C. tropicalis Flesh T. glabrata, C. krusei 8 Rind B. subtilis Flesh B. subtilis 9 Rind C. guilliermondii Flesh C. guilliermondii 10 Rind B. subtilis Flesh C. guilliermondii 11 Rind C. krusei Flesh C. tropicalis 12 Rind C. lusitaniae Flesh C. lusitaniae 13 Rind C. guilliermondii Flesh S. epidermidis 14 Rind Bacillus spp. Flesh C. parapsilosis 15 Rind C. parapsilosis Flesh C. parapsilosis 16 Rind Enterococcus spp., S. epidermidis Flesh C. guilliermondii 17 Rind S. epidermidis, C. parapsilosis Flesh C. parapsilosis 18 Rind C. guilliermondii Flesh C. guilliermondii 19 Rind C. guilliermondii Flesh E. cloacae 20 Rind K. oxytoca Flesh C. guilliermondii, T. asahii 21 Rind C. krusei Flesh C. guilliermondii 22 Rind C. krusei Flesh C. guilliermondii 23 Rind S. viridans Flesh A. baumanii 24 Rind E. coli Flesh E. coli 25 Rind E. coli, P.mirabilis Flesh E. coli 26 Rind S. epidermidis, Bacillus spp., Enterococcus spp. Flesh S. epidermidis, Bacillus spp., Enterococcus spp. 27 Rind E. coli Flesh E. coli 28 Rind Bacillus spp. Flesh Bacillus spp. 29 Rind S. viridans Flesh C. tropicalis * 29 samples produced microbial growth on both the flesh and the rind. ** Shading denotes one restaurant visit.