Bacterial Contamination of Shopping Carts and Approaches to Control

Charles P. Gerba and Sherri Maxwell

Department of Soil, Water and Environmental Science University of Arizona Tucson, AZ 85721

Abstract
Placement of children in grocery shopping carts has recently been implicated as a source of infection with Salmonella and Campylobacter infections in young children. This study was conducted to assess the occurrence of total numbers of bacteria, coliform bacteria and Escherichia coli on grocery shopping cart handles and seats. A total of 85 shopping carts in parking lots of gocery stores were tested in five major methropoltian areas across the United States. The total number of heterotrophic bacteria averaged 117,000 per sampled area. Coliforms were detected on 72% of the carts, and E. coli identified on 50% of the carts tested. Shopping carts appear to be one of the most bacterially contaminated objects that the general public may come into contact on a regular basis in public facilities. The exceptionally high level of coliform bacteria suggests that fecal material may be involved in cart contamination. The results

of this study reaffirm the need for improved sanitation of shopping cards/baskets to reduce exposure and potential transmission of microbial infections among shoppers. Disposable plastic barriers with antimicrobial adhesive for shopping cart handles are an option for reducing risk of the consumer from potentially pathogen bacteria that does not rely on disinfectant use.

Introduction Contamination of raw meat products with the bacterial enteric pathogens, such as, Salmonella, Campylobacter and Escherichia coli is common (Beier et al., 2004). Recent studies have shown that children are at increased risk of both Salmonella and Camplyobacter infections if they ride in a shopping cart carrying meat products (Jones et al., 2006; Fullterton et al., 2007; Patrick et al., 2010). This suggests that exposure of children to enteric bacterial pathogens in shopping carts occurs on a regular basis. Mizumachi et al. (2010) also reported frequent exposure to pathogenic Staphylococcus aureus on shopping cart handles and suggested that this was a hidden reservoir of this organism and the need for shopping basket sanitation. Contamination of shopping carts may occur from direct handling of raw food products, contamination of the cart from previous users.

The goal of this project was to determine the general sanitation of shopping carts relative to bacteria.

Material and Methods

Cart sampling. Grocery store shopping carts were selected at random in store parking lots in Sioux City, IA, San Francisco, CA, Los Angeles, CA, Portland, OR and

Atlanta, GA. A total of 85 carts were sampled, with 50 carts tested in the greater Los Angeles area. The cart handle and seat were swabbed using the same Sponge stick containing a neutralizing buffer (3M Corporation, St. Paul, MN) and delivered overnight packed in ice to the University of Arizona where they were processed. The estimated surface area sampled was 668 sq. cm. Three ml of fluid was extracted from the sponge-stick by squeezing it from the sponge in a plastic bag. One ml of this extract was used to test for coliforms/E. coli. Bacterial assays and identifications. Total heterotrophic plate count bacteria were determined by dilution of samples in buffered peptone water and spread plating on R2A media (Difco, Sparks, MD). This media is designed to enhance the recovery of stressed bacteria. The plates were incubated for five days at room temperature and colonies counted. Coliform and Escherichia coli bacteria were identified by placing one ml of the sponge sickle extract into 99 ml of Colilert media (IDDEX, Westbrook, ME) and placement in a quantitray system and inoculation overnight at 37 oC. Coliform and E. coli numbers were then determined using a most probable number (MPN) table provided by the manufacture. Identification was conducted by diluting positive quantitray samples on MacConkleys agar (Difco) to confirm the presence of coliform bacteria, since the Colilert media is not specially designed for isolation of coliform bacteria from fomites. Colonies of different morphology were selected and subcultured on Trypticase Soy Agar (Difco). The bacteria were then identified using APIE20 strips (Biomerieux, Durham, NC).

Results Table 1 shows the total number of bacteria isolated per cart collected from store parking lots. The numbers of bacteria are reported as colony forming units (CFU)/cart. The number of bacteria detected on the shopping carts ranged from 110 to 11,000,000, and

coliform bacteria from <3 to greater than >7,259. The geometric mean of HPC bacteria was 23,291 per cart or 34.8 per sq. cm. The concentrations of coliforms >7,259 were detected on 72% of the carts sampled.

Table.1. Bacterial concentrations detected on shopping carts Bacteria Average Minimum Maximum Average per sq. cm 513

Total

3.43 X 105

110

1.1 X 107

Coliforms

767

<3

>7,259

1.1

E. coli was the most common coliform identified being detected on 50% of the cart samples tested (35 carts positive for coliforms where tested) (Table 2).

Table 2. Types of enteric bacteria detected on shopping carts (36 tested)

Bacteria isolated

Number of Carts

Escherichia coli Klebsiella pneumoniae Enterobacter sakazkii Enterobacteria cloascae Klebsiella oxytoca Yersina pseudotuberculosis

18 5 6 2 1 1

Discussion

The common occurrence of coliform and E. coli bacteria on shopping carts indicate that the consumer is exposed to fecal bacteria on a regular basis when using grocery shopping carts. Total bacterial levels are far greater than found in public restrooms and other public places and objects that are commonly touched in these environments (i.e. airports, bus stations, public bathroom, shopping malls, etc. Reynolds et al. (2005) found the geometric mean of HPC bacteria on these objects ranged from 5 to 41.5 sq. cm. with the higher average found in public restrooms. Coliforms and E. coli also appear to be in greater numbers on shopping cart handles than other common surfaces consumers may come into contact. In testing of diaper changing tables, chair arm rests, playground equipment, ATM button, restaurant tabletops, escalators, restaurant condiments coliforms were only detected on 7% (16/200 samples) (Reynolds et al., 2005) vs. 72% on shopping carts in the present study. Coliform bacteria usually originate from feces and are associated with poor sanitary conditions. Coliform bacteria and E. coli detected on the carts may originated from contact with raw foods, birds (while sitting in the parking lots between use) or other animal feces, contact with fecally contaminated hands or other body parts (hands).

The high numbers of HPC bacteria and coliform bacteria indicate extreme unsanitary conditions of the carts compared to other public places and surfaces that the general public comes into contact. This increases the risk of coming into contact with a disease causing organism. Results of several epidemiological studies have shown that a risk of infection from common enteric bacteria is related to placement of small children in shopping carts (Jones et al., 2006; Fullterton et al., 2007; Patrick et al., 2010). The

results of this study reaffirm the need for improved sanitation of shopping cards/baskets to reduce exposure and transmission of bacterial infections among shoppers. Two solutions to reduce exposure to consumers are to provide the consumer with a disinfectant as contained in a wipe and the use of disposable barriers with antimicrobial adhesive. In Arkansas legislation has passed which encourages grocers to offer complementary sanitary wipes (CBS News, 2008). Most disinfecting wipes provided today contain quaternary ammonium based compounds which require at least a10 minute contact time to be effective against many organisms (Block, 2001). Disposable plastic barriers are design to fit over the hand contact area, such as the handle of the cart, and then be discarded in a recycle bin after use or by the next user. These barriers contain antimicrobial adhesive on one side and we assessed the effect of attachment and detachment of a barrier on removal of bacteria on a shopping handle compared to a disinfecting wipe.

Conclusions

In conclusion, grocery store shopping carts appear to be one of the most bacterially contaminated objects that the general public may come into contact on a regular basis in public facilities. The exceptionally high levels of coliform bacteria and E. coli suggest that fecal material may be involved in cart contamination. Improved sanitation or the use of antimicrobial adhesive barrier devices, which prevent cross contamination among products and shoppers, appears justified.

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