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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, Escherichia coli, Escherichia coli O157:H7, Helicobacter pylori, Klebsiella pneumoniae, Listeria innocua, Listeria monocytogenes, Mycobacterium tuberculosis, Neisseria gonorrhoeae, Penicillium digitatum, Penicillium italicum, Pseudomonas aeruginosa, Saccharomyces cerevisiae, Salmonella spp., Salmonella typhi, Shigella dysenteriae, Staphylococcus aureus, and Streptococcus 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 Living, 2005; Podleski, 2006; Weiss, 2005). One site encourages restaurant patrons to squeeze lemon juice into drinking water, 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, 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 contamination that might be ingested by restaurant patrons.

Materials and Methods

Samples were collected surreptitiously, 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 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 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, colony characteristics, API 20C Aux[R] for yeast, API 20E[R] for Enterobacteriaceae, PYR Test Kit for Enterococcus, [H.sub.2][O.sub.2] for catalase, and rabbit plasma for coagulase. Isolates were not quantified.

Results

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 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).

Discussion

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 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 and Corynebacterium 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 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 lemons and other foods, and are classified by the food industry as "food spoilage 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, and the integrity of the mucous membranes of the lips and mouth.

Conclusion

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, 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), Assistant Professor of Science, Passaic County Community College, One College Boulevard, Paterson, NJ 07505. E-mail: aloving@pccc.edu.

REFERENCES

Adegoke, G.O., Iwahashi H., Komatsu, Y., Obuchi, K., & Iwahashi, Y. (2000). Inhibition of food spoilage yeasts and aflatoxigenic moulds by monoterpenes of the spice Aframonum danielli. African Journal of Biotechnology, 2(9), 254-263.

Adeleye, I.A., & Opiah, L. (2003). Antimicrobial activity of extracts of local cough mixtures on upper respiratory tract bacterial pathogens. West Indian Medical Journal, 52(3), 188-190.

Belletti, N., Ndagijimana, M., Sisto, C., Guerzoni, M.E., Lanciotti, R., & Gardini, F. (2004). Evaluation of the antimicrobial activity of citrus essences on Saccharomyces cerevisiae. Journal of Agricultural and Food Chemistry, 52(23), 6932-6938.

Boschen, H. (n.d.). Organically grown foods. Retrieved June 5, 2006, from http://www.juiceguy.com/organic.shtml.

Brock, B.L., & Ketchum, H.M. (1951). The antibacterial action of citrus peel oil on the tubercule bacillus in vitro. Diseases of the Chest, 20(6), 671-674.

Caccioni, D.R, Guizzardi, M., Biondi, D.M., Renda, S., & Ruberto, G. (1998). Relationship between volatile components of citrus fruit essential oils and antimicrobial action on Penicillium digitatum and Penicillium italicum. International Journal of Food Microbiology, 43(1-2), 73-79.

Cheah, L.H., & Hunt, A.W. (1994). Screening of industrial yeasts for biocontrol of Botrytis storage rot in kiwifruit. Proceedings of the 47th New Zealand Plant Protection Conference. Retrieved January 24, 2005, from http://www.hortnet.co.nz/publications/nzpps/proceedings/94/94_362.htm.

Cheah, L.H., & Tran, T.B. (1995). Postharvest biocontrol of Penicillium rot of lemons with industrial yeasts. In Proceedings of the 48th New Zealand Plant Protection Conference. Retrieved January 18, 2005, from http://www.hortnet.co.nz/publications/nzpps/proceedings/95/95_155.htm.

Dabbah, R., Edwards, V.M., & Moats, W.A. (1970). Antimicrobial action of some citrus fruit oils on selected food-borne bacteria. Applied Microbiology, 19(1), 27-31

Dada, J.D., Alade, P.I., Ahmad, A.A., & Yadock, L.H. (2002). Antimicrobial activities of some medicinal plants from Soba-Zaria, Nigeria. Nigerian Quarterly Journal of Hospital Medicine, 12(1-4), 55-56

de Castillo, M.C., de Allori, C.G., de Gutierrez, R.C., de Saab, O.A., de Fernandez, N.P., de Ruiz, C.S., de Ruiz Holgado, A.P., & de Nader, O. (1998). Action against Vibrio cholerae O1 To[x.sup.+] of chemical products used in the lemon production. Revista Latinoamericana de Microbiologia, 40(3-4), 120-123.

Droby, S., Chalutz, E., & Wilson, C.L. (1991). Antagonistic micro-organisms as biological control agents of postharvest diseases of fruits and vegetables. Postharvest News and Information, 2(3), 169-173.

Francis, G.A., & O'Beime, D. (2002). Effects of vegetable type and antimicrobial dipping on survival and growth of Listeria innocua and E. coli. International Journal of Food Science and Technology, 37(6), 711.

Ibrahim, Y.K., & Ogunmodede, M.S. (1991). Growth and survival of Pseudomonas aeruginosa in some aromatic waters. Pharmaceutica acta Helvetiae, 66(9-10), 286-288.

iVillage Garden Web Herbalism Forum. (December 2, 2002). Tea tree for sore throats? Retrieved June 5, 2006, from http://forums2.gardenweb.com/forums/load/herbal/msg1212325510562.html.

Nogueira, M.C., Oyarzabal, O.A., & Gombas, D.E. (2003). Inactivation of Escherichia coli O157:H7, Listeria monocytogenes, and Salmonella in cranberry, lemon, and lime juice concentrates. Journal of Food Protection, 66(9), 1637-1641.

Ohno, T., Kita, M., Yamaoka, Y., Imamura, S., Yamamoto, T., Mitsufuji, S., Kodama, T., Kashima, K., & Imanishi, J. (2003). Antimicrobial activity of essential oils against Helicobacter pylori. Helicobacter, 8(3), 207-215.

Podleski, G. (May 12, 2006). Eat, shrink, & be merry: Lemony snippets. Retrieved June 4, 2006, from http://www.jyi.org/features/ft.php?id=443

Potts, M., Perlman, D., Mandara, M., Prata, N., & Campbell, M. (2004). Is lime/lemon juice an effective microbicide? Paper presented at the XV International AIDS Conference, Bangkok. Abstract (Number C11663) retrieved March 24, 2006, from http://www.iasociety.org/ejias/show.asp?abstract_id=2170959.

Rall, J.C., & Center for Unhindered Living. (2005). House beautiful ... or house deadly? Retrieved June 5, 2006, from http://forums2.gardenweb.com/forums/load/herbal/msgl212325510562.html

Saleem, M., Afza, N., Anwar, M.A., Hai, S.M., & Ali, M.S. (2003). A comparative study of essential oils of Cymbopogon citratus and some members of the genus Citrus. Natural Product Research, 17(5), 369-373.

Salvatore, A., Borkosky, S., Willink, E., & Bardon, A. (2004). Toxic effects of lemon peel constituents on Ceratitis capitata. Journal of Chemical Ecology, 30(2), 323-333.

Short, R.V., McCoombe, S.G., Maslin, C., & Crowe, S. (July 11, 2004). Lemon and lime juice as potent natural microbicides. Paper presented at the XV International AIDS Conference, Bangkok. Abstract (Number TuPeB4668) retrieved February 15, 2006, from http://www.iasocietyorg/ejias/show.asp?abstract_id=2167631.

Tufarelli, M. (n.d.). Love your lemons. Pioneer Thinking. Retrieved June 3, 2006, from http://www.pioneerthinking.com/rbtl4.html

Weiss, R. (2005). A quest to understand the spices of life: The antimicrobial powers of spices. Journal of Youth Investigation. Retrieved June 4, 2006, from http://www.jyi.org/features/ft.php?id=443.

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.
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Title Annotation:FEATURES
Author:Loving, Anne LaGrange; Perz, John
Publication:Journal of Environmental Health
Geographic Code:1USA
Date:Dec 1, 2007
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