EXOTİC-Produce as apotential source of bacterial infectious in exotics pets

8/14/2019 EXOTC-Produce as apotential source of bacterial infectious in exotics pets

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Vol. 22, No. 7 July 2000

Refereed Peer Review

FOCAL POINT

KEY FACTS

# Exotic pets, particularly iguanas,may become infected withbacterial pathogens existingon fresh produce.

Produce as a PotentialSource of BacterialInfections in Exotic PetsUniversity of Georgia

Peter J. Taormina, MS

ABSTRACT:Exotic pets are susceptible to symptomatic or asymptomatic carriage of bacteriapathogenic to humans. Fatalities in exotic pets and transmission of illnesses to humans per-sist as serious consequences to these infections. Many types of vegetables can harbor bacteri-al pathogens and are potentially a source of infection in exotic pets. Fruits and vegetables sup-port good growth of pathogenic bacteria, especially at or above ambient temperatures.Carriage and transmission of human bacterial pathogens by iguanas, psittacines, and otherexotics, as well as the illnesses that may result in these animals, could possibly be reduced bytreating all food sources, including fresh produce, as biologically active growth media forpathogens.

H uman illnesses resulting from contact with reptiles persist despite warn-ings, educational bulletins, and intervention strategies; the frequency of human salmonellosis attributable to handling iguanas has also increased.1Studies have revealed thatSalmonella species are present in approximately 50% of lizards and other reptiles, most of which exhibit no outward signs of illness.24 Rep-tiles, particularly iguanas, are believed to carry stable mixtures of Salmonella serotypes and continuously or intermittently shed the organisms in their feces.57 Ithas been suggested that the organism is transferred to reptiles primarily via the oralroute, but other mechanisms of contamination (e.g., aerosolization of contaminat-ed materials, egg transmission) have also been suspected.8

Infectious bacteria also exist in exotic birds and often cause illness or mal-aise.9,10 Such gram-negative bacteria asEscherichia coli , Enterobacter species, andKlebsiella species are commonly isolated from psittacines; these organisms are of-ten regarded as part of the birds natural flora.11,12 However, some studies haveconcluded that gram-negative bacteria are unnaturally introduced to the gas-trointestinal tract of exotic birds.13,14 According to one study,15 psittaciform birdscan potentially become infected with enteropathogenicE. coli and transmit suchinfections to humans. Salmonella has also been implicated in diseases in captivebirds.9,10 Because iguanas and exotic birds are often symptomatic or asymp-tomatic carriers of pathogenic bacteria, information regarding how these pets areinitially exposed to bacterial pathogens could lead to better control and reducetransmission to humans.

CE

V

I For several years, food scientistshave known that bacteria onproduce can cause disease inlivestock and humans.

I Fruits and vegetables can becomecontaminated with pathogenicmicroorganisms while growing or

during harvesting, postharvesthandling, processing, anddistribution.

I The temperature of an iguanacage, typically between 21C and37C (69.8F and 98.6F) is withinthe optimal growth temperaturerange for many pathogenicbacteria.

I Lettuce samples sprayed with

200 ppm chlorine contained 1log fewerSalmonella cells thandid samples sprayed with wateralone.


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A less obvious potential sourceof bacterial pathogens in exoticpets is the food they eat. Rou-tinely culturing Salmonella fromsome reptiles may not seem re-

markable given the nature of their diets; snakes, for example,may eat baby chickens, rats, andmice. Other reptiles, however,such as iguanas, strictly adhereto vegetarian diets. The diets of companion birds may consist of a variety of fresh produce, vari-ous types of seeds, alfalfa hay,and freeze-dried vegetables16 andthus are not always representa-tive of their natural feeding habits.

Speculation about the sourcesand/or causes of occasionally fa-tal, often chronic, and certainly transmissible bacterial infectionsin iguanas, psittacines, and otherexotic animals often disregardsfood source because of the mis-conception that harmful bacteriaare absent from vegetarian diets.However, the presence and eventhe prevalence of disease-causingbacteria on fresh produce has

been recognized within the foodscience community for severalyears because of outbreaks of hu-man gastrointestinal illnesses as-sociated with the consumptionof fresh and/or minimally pro-cessed fruits and vegetables.1719

Outbreaks of human illnessprompted worldwide microbio-logic surveillance of fresh fruitsand vegetables and revealed valu-able information regarding the

microbiologic safety of fresh pro-duce. The incidence of patho-genic bacteria in exotic pets war-rants a further look at plant-basedfood as a source of infection.This article discusses the inci-dence of disease-causing mi-croorganisms on fresh produce,conditions influencing their sur-vival and growth, and interven-tion strategies to eliminate orsatisfactorily reduce bacterial

Compendium July 2000 Small Animal/Exotics

V E G E TA R I A N D I E T SI B A C T E R I A L P R E VA L E N C E

TABLE IBacterial Pathogens Isolated from Produce

Produce Item Country of Origin Pathogen Prevalence

Alfalfa sprouts United States46

Aeromonas United States47 Salmonella meleagridis United States48 Bacillus cereus

Alfalfa seeds United States49 Salmonella havana,Salmonella cubaba,Salmonella tennessee

United States, Salmonella newport Denmark 50

Artichoke Spain51 Salmonella 3/25 (12%) Asparagus United States52 Aeromonas Bean sprouts Malaysia53 Listeria monocytogenes 6/7 (85%)

Sweden54 Salmonella Thailand55 Salmonella 30/344 (8.7%)

Beet leaves Spain51 Salmonella 4/52 (7.7%)Broccoli United States56 Aeromonas

United States46 Aeromonas 5/16 (31.3%)Cabbage Canada57 L. monocytogenes 2/92 (2.2%)

Mexico58 Escherichia coli 1/4 (25.0%)O157:H7

Peru59 Vibrio cholera Spain51 Salmonella 7/41 (17.1%)Sri Lanka60 L. monocytogenes 6/18 (33%)United States61 L. monocytogenes 1/92 (1.1%)

Carrots Lebanon62 Staphylococcus (14.3%)Cauliflower The Netherlands63 Salmonella 1/13 (7.7%)

Spain51 Salmonella 1/23 (4.3%)United States56 Aeromonas

Celery Mexico58 E. coli O157:H7 6/34 (17.6%)Spain51 Salmonella 2/26 (7.7%)

Chili Surinam63 Salmonella 5/16 (31.3%)Cilantro Mexico58 E. coli O157:H7 8/41 (19.5%)Coriander Mexico58 E. coli O157:H7 2/20 (10.0%)Cress sprouts United States48 Bacillus cereus Cucumber Malaysia53 L. monocytogenes 4/5 (80%)

Pakistan64 L. monocytogenes 1/15 (6.7%)United States61 L. monocytogenes 2/92 (2.2%)

Eggplant The Netherlands63 Salmonella 2/13 (15%)Endive The Netherlands63 Salmonella 2/26 (7.7%)Fennel Italy 65 Salmonella 4/89 (4.5%)Green onion Canada66 Campylobacter 1/40 (2.5%)Leafy vegetables Malaysia53 L. monocytogenes 5/22 (22.7%)Lettuce Canada66 Campylobacter 2/67 (3.0%)

Italy 65 Salmonella 82/120 (68.3%)Kuala Lumpur67 L. monocytogenes 1/28 (3.6%)Lebanon62 Staphylococcus (14.3%)The Netherlands63 Salmonella 2/28 (7.1%)Spain51 Salmonella 5/80 (6.3%)Sri Lanka60 L. monocytogenes 10/20 (50%)United States46 Aeromonas


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pathogens on fresh fruit and veg-etables intended for consump-tion by exotic pets.

PATHOGENIC

BACTERIA ASSOCIATEDWITH FRESH PRODUCEFruits and vegetables can be-

come contaminated with patho-genic microorganisms whilegrowing or during harvesting,postharvest handling, process-ing, and distribution.18,20 Sourcesof preharvest contamination in-clude feces, soil, irrigation water,green or inadequately compost-ed manure, air (dust), wild and

domestic animals, and humanhandling. Depending on the de-gree of processing (e.g., sorting,cutting, washing, packing, trans-porting), a variety of other vec-tors can contaminate vegetablesand fruit after they are removedfrom the field.18 Although mi-crobial contamination can in-clude bacteria, viruses, and para-sites, this article focuses onbacterial pathogens on produce.

Table I summarizes surveys of various fresh vegetables andfruits for the presence of bacteriathat are pathogenic to humans.Such organisms as Salmonella species, E. coli O157:H7, andListeria monocytogenes are rou-tinely isolated from vegetables.Fruits may also harbor bacterialpathogens; although publishedisolation frequency data are lim-ited, several outbreaks of human

illness have resulted from con-sumption of tomatoes, water-melon, and cantaloupe contami-nated with gram-negativebacterial pathogens.1719 The in-formation assembled here doesnot include the many reportedcases of human illness that wereepidemiologically linked to freshfruits and vegetables but in

which the causative organism was not isolated from the pro-

Small Animal/Exotics Compendium July 2000

S O U R C E S O F C O N TA M I N AT I O NI H U M A N I L L N E S S

TABLE I(continued)

Produce Item Country of Origin Pathogen Prevalence

Mung bean sprouts United Kingdom68 Salmonella saint-paul Mushrooms United States69 Campylobacter jejuni 3/200 (1.5%)Mustard cress United Kingdom70 Salmonella gold-coast Mustard sprouts United States48 B. cereus Parsley Canada66 Campylobacter 1/42 (2.4%)

Egypt32 Shigella 1/250 (0.4%)Lebanon62 Staphylococcus (7.7%)Spain51 Salmonella 1/23 (4.3%)

Pepper Canada66 Campylobacter 1/63 (1.6%)United States46 Aeromonas Sweden71 Salmonella

Potatoes United States61 L. monocytogenes 19/70 (27.1%)United States72 L. monocytogenes 28/132 (21.2%)

Radish Lebanon62 Staphylococcus (6.3%)United States61 L. monocytogenes 25/68 (36.8%)United States72 L. monocytogenes 19/132 (14.4%)

Salad greens Egypt32 Salmonella 1/250 (0.4%)United Kingdom75 Staphylococcus aureus 13/256 (5.1%)

Salad vegetables Egypt32 Shigella 3/250 (1.2%)Egypt32 S. aureus 3/36 (8.3%)Germany 76 L. monocytogenes 6/263 (2.3%)Northern Ireland73 L. monocytogenes 4/16 (25%)United Kingdom77 Yersinia enterocolitica 4/16 (25%)United Kingdom78 L. monocytogenes 2/108 (1.9%)

Salads Canada66

Campylobacter 2/74 (2.7%)(prepackaged) Northern Ireland73 L. monocytogenes 3/21 (14.3%)United Kingdom74 L. monocytogenes 4/60 (6.7%)

Seed sprouts Canada79 Staphylococcus 13/54 (24%)Soybean sprouts United States48 B. cereus Spinach Canada66 Campylobacter 2/60 (3.3%)

Spain51 Salmonella 2/38 (5.3%)United States46 Aeromonas

Sprouting seeds United States80 B. cereus 56/98 (57%)Tomatoes Pakistan64 L. monocytogenes 2/15 (13.3%)Vegetables Egypt32 Salmonella 2/250 (0.8%)

France81

Y. enterocolitica 4/58 (7%)France82 Y. enterocolitica 15/30 (50%)Iraq83 Salmonella 3/43 (7.0 %)Italy 84 L. monocytogenes 7/102 (6.9%)Italy 84 Y. enterocolitica 1/102 (1.0%)Spain85 L. monocytogenes 8/103 (7.8%)Spain86 Salmonella 46/849 (5.4%)Taiwan87 L. monocytogenes 6/49 (12.2%)United Kingdom88 L. monocytogenes 4/64 (6.3%)United States89 Salmonella 4/50 (8.0%)

Watermelon United States90 E. coli, S. aureus


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duce item. Surveys in which pathogenic bacteria werenot detected in sampled items are likewise excluded.Variations in isolation and sampling methods must alsobe considered when drawing conclusions based on thiscollection of surveys.

The surveys discussed here reveal that bacterialpathogens occur on fresh produce worldwide and thatthe occurrence of pathogens on produce ranges fromrare to frequent. Rather than alarming exotic pet care-givers of the dangers of feeding raw vegetable matter totheir captives, this information is meant to educatethem about potential sources of contamination to helpcontrol and perhaps eliminate these pathogens from themicroflora of exotic pets. Based on the information inTable I, it is apparent that vegetables can harbor bacte-ria dangerous to exotic pets and humans and that ap-propriate measures should be taken to control or limit

bacterial growth on produce. Sanitary care of exoticpets and maintenance of their environments can reducethe risk of contact with pathogenic bacteria via pro-duce.

HUSBANDRY AS A BACTERIAL GROWTH STEPFeeding routines may contribute to the proliferation

of harmful bacteria. For example, iguana owners com-monly allow produce to remain in their pets cage untilit is eaten or becomes visibly rotted and spoiled. Thetemperature of an iguana cagetypically between21C and 37C (69.8F and 98.6F)is within the

optimal growth temperature range for many pathogenicbacteria, including Salmonella and E. coli O157:H7. 21,22Therefore, otherwise small populations of harmful bac-teria present on fruits and vegetables are given an op-portunity to proliferate before being consumed. Thesame situation is likely to exist in the care of other exot-ic animals maintained at these temperatures.

Many exotic pets prefer warm and often humid cli-mates typical of their native habitats, and fresh producetends to degrade more rapidly under these conditions.Higher temperature accelerates the senescence of planttissue, which in turn hinders innate defense mecha-

nisms that would otherwise restrain microbial attack.Pathogenic bacteria are among the many types of mi-croorganisms that grow in the less-inhibiting substrateof decaying produce.

Intact whole fresh fruits and vegetables are protectedfrom microbial invasion by peels or skins, although thisprotection does not eliminate the risk of contamina-tion. Once a fruit or vegetable is cut, the inner tissue isopen to microbial contamination.23 Moreover, nutrient-laden juices are exuded from plant tissue and become amore accessible food source for microbes.

Handling of produce can also increase the diversity

of contaminating microorganisms present. The moredamaged and abused the fruit or vegetable is, the moresusceptible it becomes to colonization and growth of microorganisms. In addition, spoiled or partially spoiled produce is more likely to support pathogen

growth. Fresh fruits and vegetables exhibiting signs of bacterial soft rot potentially have moreSalmonella con-tamination than do healthy samples.24

Conditions that favor the growth and survival of Salmonella are found in tomatoes. Several serotypes of Salmonella were found to be able to grow in the acidicsubstrate of tomatoes at 22C and 30C (71.6F and86F). 25 Other studies have shown that Salmonella montevideo can survive on tomato skin up to 3 daysand on stem scars up to 7 days when stored at 20C to25C (68F to 77F). 26,27 Tomato slices and wholetomatoes with puncture wounds permit rapid growth

of bacteria.26

An acid-tolerance response inSalmonella is believed to enable the organism to survive, grow, andoutcompete other microorganisms in such low-pHfoods as tomatoes.21 Other acidic fruits (e.g., papaya, ji-cama, watermelon) support good growth of Salmonella at 22C to 27C (71.6F to 80.6F). 28 A mixture of fiveSalmonella serotypes (S. anatum , S. chester , S. havana,S. poona , and S. senftenberg ) inoculated onto pieces of rind-free cantaloupe, watermelon, and honeydew mel-on increased 5 to nearly 7 log-units during storage at23C (73.4F) over a 24-hour period. 29

Salmonellae can survive for prolonged periods in a

variety of environments.21

Several species of Salmonella were able to survive on lettuce for 3 to 4 weeks at roomtemperature and 6 to 8 weeks at 2C to 4C (35.6F to39.2F).30 Similar results were seen in samples of cab-bage and carrots inoculated with the pathogen.

Other bacteria harmful to humans and potentially toanimals can survive and grow on produce. Populationsof Shigella sonnei can increase by more than 1000-foldon lettuce stored at 22C (71.6F), 31 and Shigella species can grow on shredded cabbage stored at 24C 2C (75.2F 3.6F). 32 E. coli O157:H7 grew well onshredded lettuce and sliced cucumber stored at 12C

and 21C (53.6F and 69.8F) but was inhibited onshredded carrots at the same temperatures.33 E. coli O157:H7 can grow rapidly in cantaloupe and water-melon cubes stored at 25C (77F).34 At the same tem-perature, L. monocytogenes grew rapidly on lettuce (in-creasing by 1 log in 8 hours35) and cabbage (increasingby 2 logs in 1 day 36). In an actual aviculture setting,numbers of gram-negative microorganisms, includingEnterobacter species, Pseudomonas species, and E. coli ,increased on sliced produce maintained at room tem-perature for 24 to 48 hours.37

In a review of husbandry practices and their role in


F E E D I N G R O U T I N E SI W H O L E V S . C U T P R O D U C EI TO M ATO E S


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mals, as well the infections that may occur in these ani-mals, could possibly be reduced by treating all foodsources, including fresh produce, as biologically activegrowth media for pathogens. Although several studiesindicate that Salmonella species are present in the nor-

mal intestinal microflora of iguanas even under ade-quate sanitary conditions,6,9,45 handlers must still takemeasures to decrease the likelihood of introducing newpathogens. Iguanas may be asymptomatic carriers of certain Salmonella serovars, but fresh produce can con-tain a diversity of Salmonella serovars as well as a rangeof other pathogens (Table I); these pathogens may beseverely objectionable to the animal or transmitted toother animals or humans. Appropriate precautionsshould be taken in the care and feeding of all exoticpets, not only for their health but also because they may be capable of transmitting bacterial infections.15

Temperature is the primary factor affecting microbialsurvival and growth on produce. Pathogenic microor-ganisms may be present on fruits and vegetables in suchlow numbers that they escape detection in representa-tive samples, but favorable growth temperatures canrapidly increase the numbers to dangerous levels. If pathogenic bacteria on produce are given an opportuni-ty to reproduce before being consumed, the enlargedpopulation may have greater opportunity to colonizethe pets intestinal tract (or other areas) or its environ-ment.

Whole, intact fruits and vegetables (e.g., apples, or-

anges, potatoes, onions) can generally be stored for sev-eral days to weeks at ambient temperatures withoutpresenting much opportunity for bacterial pathogens togrow; however, once produce has been cut or otherwisedamaged, refrigeration becomes crucial in retardingrapid microbial proliferation. Fresh, cut produce (e.g.,diced fruit, green leafy vegetables, cabbages, celery,broccoli) should not be subjected to ambient tempera-ture (approximately 20C [68F]) indefinitely butrather refrigerated. Even refrigerated produce can per-mit growth of certain psychrotrophic pathogens andthus should not be stored for prolonged periods. The

amount of time any produce is exposed to temperaturesof 25.5C (78F) or higher should be kept to a mini-mum. In aviaries or terrariums maintained at or nearthese temperatures, uneaten produce should be re-moved and discarded within a few hours after feeding.

Reducing bacterial contamination on produce is nosimple task. A common approach is to rinse or soak produce in an antimicrobial chemical solution and thenrinse with clean water. No one treatment is optimal forall types of produce or against all contaminating mi-croorganisms because many factors affect each treat-ments efficacy. At the very least, all produce should be


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rinsed for 30 seconds in clean water before use. Blanch-ing vegetables in boiling water for several seconds to aminute can greatly reduce populations of microorgan-isms but may also reduce the appeal and freshness of the produce.

Many commercially available chemical treatmentscan more thoroughly clean produce and reduce thenumber of microorganisms than can a water rinse. Asdiscussed, rinsing or soaking fruits and vegetables inchlorinated water can be very effective in reducing pop-ulations of pathogenic bacteria. Chlorine concentra-tions ranging from 100 to 200 ppm have typically shown efficacy against a variety of pathogens on severaltypes of produce. However, chlorine solutions havelimitations, and their efficacy can be reduced by elevat-ed water temperatures (above 20C [68F]), pH levelsabove 7, or contact with organic matter. Ultimately, the

people preparing produce for exotic pets must choose atreatment based on the type of produce, the goals of treating produce, available resources, and chemical safe-ty for themselves and the pets.

Washing produce with either water or a disinfectantbefore use, avoiding temperature abuse of fruits andvegetables, discarding uneaten produce, frequently changing bedding materials, and cleaning permanentcomponents of the animals environments are all neces-sary practices for reducing the risk of exposure to bacte-rial pathogens. Omitting any of these practices fromthe routine maintenance and care of these animals may

assist in creating a niche for harmful bacteria and com-promise the safety of exotic pets and their caretakers.

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About the AuthorMr. Taormina is affiliated with the Center for Food Safetyand Quality Enhancement, University of Georgia, Griffin.


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