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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 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
n.
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.

Lis·te·ri·a
n.
 innocua, Listeria monocytogenes, Mycobacterium tuberculosis Mycobacterium tuberculosis
n.
Tubercic bacillus.


Mycobacterium tuberculosis
, Neisseria gonorrhoeae Neisseria gon·or·rhoe·ae
n.
Gonococcus.


Neisseria gonorrhoeae
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
n.
Typhoid bacillus.
, Shigella dysenteriae Shigella dys·en·ter·i·ae
n.
Shiga-Kruse bacillus.


Shigella dysenteriae Shigella group A Microbiology The least commonly isolated and most virulent Shigella serotype
, Staphylococcus aureus Staphylococcus au·re·us
n.
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
Adjective

not prevented or obstructed: unhindered access

Adverb

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
n.
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.


microbial digestion
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  
adj.
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
n.
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.

co·ag·u·lase
n.
. 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 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).

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 bacilli /ba·cil·li/ (bah-sil´i) plural of bacillus.

bacilli

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.

cocci

[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

v.tr.
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.

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 limes
 plural limites
(Latin; “path”)

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: aloving@pccc.edu.

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n.
The fruit of the kiwi plant.
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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.
COPYRIGHT 2007 National Environmental Health Association
No portion of this article can be reproduced without the express written permission from the copyright holder.
Copyright 2007, Gale Group. All rights reserved.

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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
Words:3136
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