Bacterial contamination of food by cockroaches.

Amongst all the insects public health authorities have to deal with in urban environments, cockroaches occupy an important place. Nowadays cockroach populations appear to have more or less replaced populations of domestic flies as the main domestic urban pests, but their presence in homes and particular on food, elicits similar reactions of disgust and aversion. "Equally important as disease carriers are flies and roaches" -- this quotation from a 1952 U.S. Public Health Service publication and reported by Roth and Willis (1) is still true.

Cockroaches are known to carry various microorganisms like bacteria, helminths, viruses and fungi. Many of the bacterial species identified from cockroaches are either opportunist or potential pathogens for man and vertebrates (1, 2, 3, 4, 5). However, direct evidence that indicates that cockroaches could be involved in the transmission of bacterial diseases is largely circumstantial (1). Cockroaches are merely passive vectors and only carry bacteria that are already present in the environment (6). Contamination could occur through other paths without the intervention of cockroaches.

Demonstrating that cockroaches can be implied in the transmission of pathogenic bacteria includes several steps. The first step was to prove that cockroaches could carry pathogenic bacteria by isolating these pathogenic species from wild-caught cockroaches in different types of urban environments. Such reports already exist (1, 4, 5). As the samples increase in number, the number of different bacterial species identified from cockroaches also appears to increase. This first point is particularly significant because it concerns microorganisms that cockroaches acquired naturally through their own activities.

The second step was to inoculate cockroaches experimentally with bacteria in food and to check that the bacteria were still viable in the guts and the feces (7, 8, 9). However, cockroaches can carry bacteria on their cuticle, collecting them simply by passive contact (5, 6). This fact diminishes the importance accorded to transition through the digestive tract in bacterial transmission. These first two steps indicate that cockroaches are potential vectors of infectious agents.

The third step to this investigation was to demonstrate that bacteria are actually deposited by cockroaches on non-contaminated areas and that cockroaches actually play a part in disseminating bacteria. The experiment described below aimed at testing the potential of cockroaches for contaminating a food source.

Material and methods

Subjects

Cockroaches were trapped in kitchens of low-income flats following the method described in Rivault (10). The traps were placed on the floor behind the refrigerator, the cooker and other electric appliances, inside cupboards and sideboards, near stored food and plates and dishes.

As soon as the cockroaches were captured, they were placed in 125 ml sterile glass containers. The cockroaches were divided into groups of five adults. One group of cockroaches was placed in each container with a 5 mg piece of fresh French bread. The cockroaches were left 16 hours with the bread, in the container. This period included a night period when cockroaches are active. This experiment was replicated 11 times.

Four control pieces of bread were placed in similar sterile containers and manipulated like in the other samples of bread. All containers were placed under the same light and temperature conditions (27 |degrees~ C).

Bacteriological analyses

The pieces of bread were collected the following morning and masserated in 10 ml sterile water. Serial dilutions of each bread sample were inoculated on various bacteriological nutritive media (AES Laboratory, France) and incubated for 48 hours at 37 |degrees~ C.

The identification of gram-negative bacteria was made after incubation by use of standard methods (API System, France) after incubation on Drigalski medium. Incubation on Chapman medium and identification by slide agglutination and respiratory tests using Staphyslide tests (BioMerieux, France) were used to investigate the presence of Staphylococcus aureus.

Results

No bacteria were found on the control pieces of bread.

However, the 11 samples of bread from the containers with cockroaches were all contaminated. One or two bacterial species were identified from each sample (mean = 1.27 |+ or -~ 0.47) (Table 1). In the bread samples contaminated by cockroaches, the bacteria came from 11 different species. These species included five species previously listed as pathogens by Roth and Willis (1) and by Cochran (2). However, no Staphylococcus sp. were found.

Our data show that during one night, a small group of cockroaches left one or two bacterial species on the bread. In previous studies, whether a sample of five cockroaches was washed, dissected or ground, we identified, on average, 1.7 |+ or -~ 0.97 bacterial species per sample (N = 256) (4, 5). This is taken to indicate that each piece of bread picked up potentially all the bacterial species carried by that group of cockroaches.

Discussion

Our results demonstrate that during one night a small group of cockroaches can deposit several bacterial species on bread. This is direct proof that wild cockroaches are capable of contaminating a previously uncontaminated food source. Therefore, in kitchens in flats and restaurants infested by cockroaches, the risk of food contamination is evident.

So far we have been unable to determine how many times a cockroach must pass over a piece of bread, of how long the contact between cockroach and bread must last for bread to become contaminated. Our experimental conditions were determined by what we have observed of the normal activity in flats and what we hypothesized could happen.

All bacteria are not able to survive and develop on all surfaces where cockroaches may deposit them. However, most of them are opportunist species able to develop when they are left where there is a sufficient degree of humidity, and many food items do provide adequate conditions.

Although these samples revealed an important specific diversity, these bacterial species represent only a fraction of the specific diversity revealed on other occasions (1, 2, 4, 5). It has been shown that cockroaches can carry other pathogenic species such as: Salmonella sp., tubercle bacillus, Escherichia coli, Staphylococcus aureus, Klebsiella sp., Pseudomonas aeruginosa, Streptococcus sp., Shigella sp. (1, 3, 9, 11, 12, 13).

The presence of cockroaches in catering and other public establishments, as well as in private kitchens, puts the quality of the food at risk, especially when, like bread, it is eaten without being cooked first.

The presence of cockroaches is all the more dangerous because they are active at night, when it is dark, and therefore people may not notice them very easily.

The general problems of hygiene in urban environments are closely related to social factors, and the level of nuisance acceptability and tolerance vary with social category and culture. The need to develop fundamental research concerning ecological and hygiene problems in urban environments is being felt more and more by the many authorities concerned (14) and this stresses the complexity of the problems to be solved concerning hygiene and environment.

Table 1
Distribution of bacteria left on the sterile bread samples by
cockroaches
                      Sample       Bacteria
With cockroaches       1           (*)Enterobacter cloacae
                       2           (*)Serratia marcescens
                       2           (*)Enterobacter cloacae
                       3           Pseudomonas dimunuta
                       4           Acinetobacter calcoaceticus
                       5           (*)Citrobacter freundii
                       6           (*)Klebsiella pneumoniae
                       7           Pseudomonas pickettii
                       7           Pseudomonas putida
                       8           Acinetobacter calcoaceticus
                       9           Acinetobacter calcoaceticus
                      10           Aeromonas sp.
                      10           Pseudomonas testosteroni
                      11           (*)Citrobacter diversus
Controls              12            -- 0 --
                      13            -- 0 --
                      14            -- 0 --
                      15            -- 0 --
* = potentially pathogenic species

References

1. Roth, L.M. and E.R. Willis (1957), The medical and veterinary importance of cockroaches. Smithson Misc. Collect. 134: 1-147.

2. Cochran, D.G. (1982), Cockroaches. Biology and control. WHO, Vector biology & control series, Geneva, Switzerland 856:1-53.

3. Story, K.O. (1986), Inspection, diagnosis, pest population monitoring, and consultation. In: G.W. Bennett and J.M. Owens (eds.), Urban Pest Management, Van Nostrand Reinhold, New York, NY 69-94.

4. Le Guyader A., C. Rivault and J. Chaperon (1989), Microbial organisms carried by brown-banded cockroaches in relation to their spatial distribution in a hospital, Epidem. Inf. 102:485-492.

5. Rivault, C. A. Le Guyader and A. Cloarec (1991), Transport de bacteries par les blattes en milieu urbain, Bull. Soc. Zool. Fr. 116:235-241.

6. Burgess, N.R.H. (1984), Hospital design and cockroach control, Trans. R. Soc. Trop. Med. Hyg. 78:293-294.

7. Burgess, N.R.H., S.N. MacDermott and J. Whiting (1973a), Aerobic bacteria occurring in the hind-gut of the cockroach, Blatta orientalis, J. Hyg. 71:1-7.

8. Burgess, N.R.H., S.N. MacDermott and J. Whiting (1973b), Laboratory transmission of Enterobacteriaceae by the oriental cockroach, Blatta orientalis, J. Hyg. 71:9-14.

9. Allen, B.W. (1987), Excretion of viable tubercle bacilli by Blatta orientalis (the oriental cockroach) following ingestion of heat-fixed sputum smears: a laboratory investigation, Trans. R. Soc. Trop. Med. Hyg. 81:98-99.

10. Rivault, C. (1989), Spatial distribution of the cockroach, Blattella germanica, in a swimming-bath facility, Entomol. Exp. Appl. 53:247-255.

11. Frishman, A.M. and I.E. Alcamo (1977), Domestic cockroach and human bacterial disease, Pest Control 45:20-46.

12. Ash, N. and B. Greenberg (1980), Vector potential of the German cockroach (Dictyoptera: Blattellidae) in dissemination of Salmonella enteridis serotype typhirium, J. Med. Entomol. 17:417-423.

13. Fotedar, R., U. Banerjee, Shrininvas, A. Verma (1991), Cockroaches (Blattella germanica) as carriers of microorganisms of medical importance in hospitals, Epidem. Inf. 107:181-187.

14. Faugere, J.G. (1991), Hygiene publique et environnement urbain, REED (Sretie info.) 36:13-15.

Colette Rivault, Laboratoire d'Ethologie, URA CNRS 373, Universite de Rennes I, Campus de Beaulieu, 35042 RENNES cedex, France.