“It is feasible to use a dog to detect Clostridium difficile in stool samples and in patients. The dog’s diagnostic accuracy with stool samples suggests that immediate . . . → Read More: Dogs identify C.Diff in hospitals]]> Using a dog’s superior olfactory sensitivity to identify Clostridium difficile in stools and patients: proof of principle study
BMJ 2012; 345 doi: http://dx.doi.org/10.1136/bmj.e7396 (Published 13 December 2012)
Cite this as: BMJ 2012;345:e7396

“It is feasible to use a dog to detect Clostridium difficile in stool samples and in patients. The dog’s diagnostic accuracy with stool samples suggests that immediate identification of C difficile is possible. Moreover, our data suggest that the same may be true for the rapid diagnosis of C difficile infection on clinical wards. For the purposes of detection the dog did not need a stool sample or physical contact with patients. It would seem dogs can detect C difficile in the air surrounding patients. In addition, dogs are quick and efficient: patients in a hospital ward can be screened for the presence of C difficile infection in less than 10 minutes.” Read entire study below to find more information on methods and results.

Marije K Bomers, consultant1,
Michiel A van Agtmael, consultant1,
Hotsche Luik, canine trainer and psychologist2,
Merk C van Veen, resident3,
Christina M J E Vandenbroucke-Grauls, professor4,
Yvo M Smulders, professor1
Author Affiliations
Correspondence to: M K Bomers m.bomers@vumc.nl

Abstract

Objective To investigate whether a dog’s superior olfactory sensitivity can be used to detect Clostridium difficile in stool samples and hospital patients.

Design Proof of principle study, using a case-control design.

Setting Two large Dutch teaching hospitals.

Participants A 2 year old beagle trained to identify the smell of C difficile and tested on 300 patients (30 with C difficile infection and 270 controls).

Intervention The dog was guided along the wards by its trainer, who was blinded to the participants’ infection status. Each detection round concerned 10 patients (one case and nine controls). The dog was trained to sit or lie down when C difficile was detected.

Main outcome measures Sensitivity and specificity for detection of C difficile in stool samples and in patients.

Results The dog’s sensitivity and specificity for identifying C difficile in stool samples were both 100% (95% confidence interval 91% to 100%). During the detection rounds, the dog correctly identified 25 of the 30 cases (sensitivity 83%, 65% to 94%) and 265 of the 270 controls (specificity 98%, 95% to 99%).

Conclusion A trained dog was able to detect C difficile with high estimated sensitivity and specificity, both in stool samples and in hospital patients infected with C difficile.
Introduction

Clostridium difficile infection is common, particularly in people in healthcare facilities who have received antimicrobials. C difficile causes toxin mediated intestinal disease, with symptoms ranging from mild diarrhoea to severe pseudomembranous colitis and toxic megacolon. The bacterium can be transmitted through either personal contact or the environment.1 Since 2000 more frequent and severe disease has emerged and large outbreaks in hospitals have necessitated ward closures and extensive infection control measures.2 3 4 Infection rates seem to be higher in North America than in Europe.3 5 In the Netherlands the incidence of nosocomial C difficile infection is comparable to that of other European countries (mean incidence 17.5-23/10 000 admissions)6 7; the mean incidence in the United Kingdom is 50/10 000 admissions.6

Cliff has been trained to sniff out the bacteria clostridium difficile
Video

Early and rapid identification of C difficile infection is important for the initiation of infection control measures and treatment to prevent transmission.8 Several combinations of tests are used to diagnose cases. The traditional standard is by cytotoxin assay, which if C difficile toxins are present shows cytotoxicity of faecal eluate on mammalian cells. This technique requires cell cultures, however, and results take at least 1-2 days.9 10 Culture on selective media is very sensitive but also time consuming and it lacks specificity because of possible carriage of non-toxigenic isolates. Cultured strains can subsequently be tested for the production of toxins, in which case this is referred to as a toxigenic culture.4 10 Easy and rapid enzyme immunoassays to detect C difficile toxins or antigens are often used, despite their limited sensitivity or specificity.10 11 More recently, several nucleic acid amplification tests have been developed that have a high diagnostic accuracy and short turnaround time, although these tests are expensive and require specialised equipment and expertise.4 10 11 12

In daily practice, several factors delay the identification of C difficile infections. These include doctor’s delay (for example, the doctor does not consider the possibility of a C difficile infection, or decides to wait and see if the symptoms pass), inefficient sampling, and time required to process samples in the laboratory.13 14 As a result the mean time from onset of symptoms to start of treatment in studies ranges from 2.8 to 7.7 days.13 14 This can result in spread of C difficile infection by delaying appropriate infection control measures such as transferring patients to a single room. Screening all hospital patients at regular intervals could theoretically prevent delays in diagnosis but this is costly and impractical.

In the 1970s C difficile was identified as the cause of pseudomembranous colitis.15 16 Since then, C difficile associated diarrhoea has often been described as having a characteristic smell.17 Sensitivity and specificity of the odiferous detection of C difficile by nursing staff are 55-82% and 77-83%, respectively.18 19 Dogs have a far superior sense of smell, however, which is thought to exceed that of humans by a factor of 100.20 We hypothesised that it may be possible for a dog to be trained to recognise the presence of C difficile in stool samples, or even in patients. If so, this could prove a valuable screening tool for C difficile infections in healthcare facilities.

Methods
The training process

The dog used in this study was a 2 year old male beagle (fig 1?). A professional detection dog instructor (HL) trained the dog to identify C difficile in stool samples and, if this proved possible, in patients. A reward based training method was used in which the correct behaviour was reinforced, for instance by providing a treat. The dog was taught to sit or lie down if a specific scent was detected. He had not received previous training in detection.

Beagle Scent Dog

Training began by introducing the dog to the specific odour of toxigenic C difficile strains on culture plates. Wooden sticks were placed over the sample to absorb the scent emanating from the culture plates (often described as resembling horse manure9). Initially we left the sticks in this position overnight, but eventually the exposure time was shortened to around five minutes to reduce the strength of the scent. Early recognition of the scent was achieved by using simple search and find games, which were gradually replaced by exercises of increasing difficulty, for instance by using sticks with a fainter smell (that had not been exposed to the scent as long). Also, the scent was presented to the dog on materials other than the sticks, such as paper, fabric, and metal, and in different environments such as a kitchen, forest, or petrol station to vary background odours.

The next step of training concerned discrimination between stool samples that were positive for toxin producing C difficile strains from those that were negative. Again, rather than the dog having direct contact with the stool sample, we presented the scent in various forms (absorbed on a wooden stick or on fabric, sample contained in a plastic vial, etc).

After two months’ training we formally tested the diagnostic accuracy of the dog on stool samples. Finally, we explored the dog’s abilities to detect C difficile infection in patients admitted to hospital.

Samples and participants

C difficile on culture plates

For training purposes we used clinical isolates of toxigenic C difficile strains, cultured on standard media under anaerobic conditions.
Stool samples

We used stool samples that were sent to the microbiology laboratory to test for C difficile and other infectious causes of diarrhoea. Samples were considered positive for C difficile if toxin was detected by enzyme immunoassay (VIDAS Clostridium difficile A & B; BioMérieux, France) and culture revealed a toxigenic strain of C difficile. Negative stool samples were those that gave negative results in both tests. We excluded samples with inconsistent results (for example, negative result for toxin by enzyme immunoassay but positive culture result, or an undetermined toxin enzyme immunoassay value).
Selection of participants

We further explored the dog’s ability to detect C difficile infection on the wards of two hospitals in Amsterdam: VU University medical centre (a tertiary clinical care centre) and St Lucas Andreas Hospital (a large community hospital).

Between September 2010 and May 2011, we screened for inclusion consecutive patients who had a positive result for toxin by enzyme immunoassay in their stool sample. We aimed to include 30 patients in total. Both hospitals use an enzyme immunoassay plus a toxigenic culture to diagnose C difficile infection; however, the community hospital uses an enzyme immunoassay by a different manufacturer (ImmunoCard Toxins A&B; Meridian Bioscience, Cincinnati, OH).

Eligible cases had symptoms of diarrhoea and both a positive result for toxin by enzyme immunoassay and a toxigenic C difficile strain detected by culture (in a sample taken less than seven days before the detection round). We defined diarrhoea as three or more loose or watery stool passages a day. We excluded children and adults on intensive care units or haematology wards. Patients with a first relapse after completing treatment for a previous C difficile infection were eligible but not those with subsequent relapses. Because the availability of the dog and trainer could not be guaranteed every weekend we excluded patients with positive test results during the weekend.

For each case we approached nine control patients. These patients were on the same ward as and in close proximity to the index patient. Control patients did not have diarrhoea, or had diarrhoea but a negative result for C difficile toxin by enzyme immunoassay and culture (in a sample taken less than seven days previously). All participants (n=300; 30 cases plus 270 controls) gave informed consent.
Canine testing experiment
Diagnostic accuracy for detecting C difficile in stool samples

We formally tested the dog’s diagnostic accuracy on 50 stool samples with known positivity for C difficile and 50 with known negativity after completion of a two month practice period. To avoid the possibility that the dog simply recognised the odour of the sample rather than the odour being associated with the presence of C difficile, we did not use the samples that had been used during training. The scent of each sample was again absorbed onto different materials, which were then repeatedly (10 times) presented to the dog in different environments and at different concentrations. We considered a result to be positive (or negative) when it consistently provoked the same positive (or negative) response. If a sample provoked a mixed response (?8/10 consistency: for example, eight positive responses and two negative ones), we classified it as an inconclusive result.
Diagnostic accuracy for detecting C difficile in patients

Next we evaluated the dog’s detection abilities in patients on the wards of the two hospitals. We prospectively included 30 consecutive patients with C difficile infection and 270 control patients. For each case and corresponding nine controls on the ward we organised a detection round as soon as possible, preferably before starting treatment or within 36 hours. During this round the dog, trainer, and a member of the research team simply walked past the beds of the 10 participants. The trainer classified the dog’s response as either positive (dog sat down), inconclusive (dog showed excitement, took extra time without actually sitting down), or negative (dog showed no particular interest). We assumed the dog would be able to identify the patient with a C difficile infection by smelling the air surrounding the patient (independent of a patient’s bowel movements or personal hygiene), so physical contact was unnecessary and avoided. If there was any doubt, the round was repeated once. The trainer was not aware of which patients had C difficile infection.
Statistical analyses

In the primary analyses, we interpreted inconclusive responses as negative ones. Secondary analysis was done with these responses interpreted as positive. We calculated 95% confidence intervals using an approximation (according to the efficient score method, corrected for continuity).21
Safety precautions

We consulted the hospital’s infection control committee to discuss the potential hazards of allowing a dog in the hospital. In accordance with recent guidelines, special attention was given to hand hygiene, making sure that staff and patients washed their hands both before and after contact with the dog.22 During detection rounds, the dog had no physical contact with patients, and contact with the environment (for example, bed, chair) was avoided as much as possible. The dog was not allowed in food preparation areas or on neonatal, haematology, or intensive care wards.

The dog receives a health evaluation by a licensed veterinarian four times a year. He is not fed raw meat. He is trained solely for the purpose of recognising C difficile. When at work, he neither barks nor shows aggression, is easily recognised by his outfit (fig 1), and is always on a leash.

Results
Diagnostic accuracy for detecting C difficile in stool samples

The dog was presented with a total of 100 stool samples: 50 were positive for C difficile and 50 were negative. The dog gave a positive response to all 50 positive samples and a negative response to 47 of the 50 negative samples, with the remaining three negative samples recorded as an inconclusive response. In the primary analysis (interpreting inconclusive responses as negative responses), sensitivity and specificity were both 100% (95% confidence interval 91% to 100%). If an inconclusive response was considered as a positive result (secondary analysis), the dog’s sensitivity and specificity were 100% (91% to 100%) and 94% (83% to 98%), respectively.

Patients’ characteristics

The supplementary video illustrates how the detection rounds were carried out. One round took place on a paediatric ward but the children became excitable by having an animal on the ward and distracted the dog. For this reason the round was not included and paediatric wards were excluded from the study.

Thirty patients with C difficile infection and 270 control patients were included in the study. Table 1? shows the characteristics of those patients. On the day of the detection round all 30 cases had diarrhoea compared with 16 (6%) of the controls. Stool samples from 35 controls (13%) were tested for C difficile on clinical grounds (presence of diarrhoea) in the week leading up to the detection round; these all gave negative results, although a non-toxigenic C difficile strain was cultured from two controls. All but three cases formally met the definition for C difficile infection. The first patient had symptoms of the infection and a positive result for toxin by enzyme immunoassay, but a culture was mistakenly not done. The second patient had symptoms and a positive result for toxin by enzyme immunoassay but an initial negative culture result, which turned out to be positive when repeated. The third patient had a relapse with recurring symptoms and a positive toxigenic culture result but negative result for toxin by enzyme immunoassay.

Characteristics of patients with Clostridium difficile infection and controls. Values are numbers (percentages) unless stated otherwise

Diagnostic accuracy for detecting C difficile in patients

Figure 2? illustrates the diagnostic accuracy of the dog. An inconclusive response was recorded in seven participants: three cases and four controls. In the primary analysis (interpreting inconclusive responses as negative results), the dog correctly identified 25/30 cases (sensitivity 83%, 95% confidence interval 65% to 94 %) and 265/270 controls (specificity 98%, 95% to 99%). If inconclusive responses were considered as positive results (secondary analysis), the dog correctly identified 28 cases (sensitivity 93%, 76% to 99%) and 261 controls (specificity 97%, 94% to 98%).

Fig 2, Diagnostic Accuracy of Dog for C. Diff

Fig2 Diagnostic accuracy of dog for detecting Clostridium difficile infection (CDI)

Table 2

provides information on the occasions that the dog and the laboratory gave discrepant results (inconclusive dog responses, false positives, and false negatives). In some instances the dog was clearly distracted by unrelated stimuli (for instance, by being offered a treat). Other cases were less clear and it cannot be ruled out that the dog responded to diarrhoea that was not caused by C difficile (for example, control 7, table 2) or asymptomatic carriage of a non-toxigenic strain (for example, control 8, table 2). Of all 16 participants with diarrhoea not related to C difficile infection, the dog gave a negative response in 13 controls and an inconclusive response in three controls.

Table 2

Discussion

It is feasible to use a dog to detect Clostridium difficile in stool samples and in patients. The dog’s diagnostic accuracy with stool samples suggests that immediate identification of C difficile is possible. Moreover, our data suggest that the same may be true for the rapid diagnosis of C difficile infection on clinical wards. For the purposes of detection the dog did not need a stool sample or physical contact with patients. It would seem dogs can detect C difficile in the air surrounding patients. In addition, dogs are quick and efficient: patients in a hospital ward can be screened for the presence of C difficile infection in less than 10 minutes.

This is the first report of animal assisted detection of C difficile. There have been several studies and anecdotal reports on olfactory detection in medicine, mostly using dogs—for example, to detect malignancies of bladder, lung, breast, skin, prostate, ovary, and colon.23 24 25 26 27 28 29 In nearly all the studies, however, the animals were exposed to biological samples obtained from patients and not to the patients themselves.
Limitations of the study

Our study has several limitations. The small number of patients with C difficile infection limits the precision with which we can establish the dog’s sensitivity and specificity. The design of the study consistently included one case per round of 10 patients. Anticipation of a single positive result could have influenced the trainer’s behaviour, thereby unintentionally influencing the dog’s response.30 Furthermore, two thirds of the cases had been moved to a single room (to control transmission) when the dog arrived, and occupancy of a single room might again have influenced the trainer and therefore the dog’s response.30

In this study, culture was not routinely carried out on controls to screen for asymptomatic carriage of toxigenic and non-toxigenic C difficile. This is a limitation as consequently we do not know the percentage of asymptomatic C difficile carriers in our population and how the dog responded to them. Asymptomatic carriage of both toxigenic and non-toxigenic strains occurs in up to 18-30% of patients in hospital.31 32 33 34 This argues against a positive response by the dog. As the clinical relevance of detecting C difficile infection rather than carriage is far greater (both for the patient and for the prevention of transmission1 31), this was the focus of our study.

Another concern is that the results are not easily generalisable because we used only one dog and one trainer. It could be that the findings would be less convincing for another dog or trainer. Although unlikely, we cannot rule out the possibility that our first and only experience was with an exceptional dog-trainer combination. Should more dogs become available in the future for detection of C difficile infection, trained animals would need an individual assessment of performance and regular practice to maintain their skills. A second limitation of using an animal as a diagnostic tool is that, as with humans, behaviour is not fully predictable. The dog’s reaction to other stimuli (for example, children’s play, being beckoned, being offered a treat) illustrates that, despite a high level of training, dogs are still prone to distraction.

Another limitation is that we trained the dog in the hospital setting. Outside the research protocol we visited a few patients with C difficile infection on long term care facility wards. These cases spent much of the day in a shared living room and not in their beds. This proved more difficult for the dog. We hypothesise that in the hospital setting the bed is a strong source of smell because the patients are often bedridden and the mattress is more likely absorb odours. Patients in the community setting are often less confined to their room and bed. This could make odours more diffuse and more difficult to pinpoint. Also, the dog may have been conditioned to respond to the bacterium when a patient was in a hospital room (usually in bed). This may mean that detection dogs are less suitable for other settings such as nursing homes, at least without additional training.

The use of dogs in hospitals might pose a risk to the dogs themselves, hospital staff, and patients. Dogs can be carriers of C difficile strains and other pathogens. Similar to hospital staff, the dog could be a source of transmission. This risk could be minimised by using strict preventive measures such as avoiding physical contact with patients and their surroundings.
Unanswered questions

Unanswered questions remain, such as what does the dog actually smell—is it a certain quantity of bacteria, toxins, or other bacterial products? How does the dog respond to stool samples that are negative for toxin by enzyme immunoassay but positive by toxigenic culture, cytotoxicity assay, or nucleic acid amplification tests? And how does the dog respond to patients early in the course of the infection, or those with asymptomatic carriage of toxigenic and non-toxigenic strains? Does a positive response by the dog to a patient without symptoms predict disease? Can a persistent positive response by the dog after symptoms have cleared predict relapse, as suggested by the response to one participant (control 12, table 2)? Will the dog perform equally well in a high incidence setting—that is, during an outbreak, when several patients in one room could be affected? We intend to deal with these situations in future studies.

How could a dog that detects C difficile infection be used in daily practice? With regular surveillance rounds (for instance to screen all wards in a hospital with a high incidence of infection several times a week, a “pet scan”) C difficile might be detected earlier. Early detection could overcome common diagnostic delays (lack of clinical suspicion, delays in sampling stool, and laboratory procedures) and lead to prompt hygienic measures and treatment. However, further studies will clearly have to examine whether surveillance can actually limit transmission and reduce the incidence of infection. For example, surveillance is principally different from the type of case directed diagnosis in this study design, because the dog cannot immediately receive a reward after a positive identification, potentially extinguishing the trained alert.

In conclusion, in this proof of principle study a trained dog was able to detect C difficile with high estimated sensitivity and specificity, both in stool samples and in infected patients in a hospital setting. This finding could have great potential for screening for C difficile infection in healthcare facilities and thus contribute to the control and prevention of outbreaks.
What is already known on this topic

Early and rapid identification of Clostridium difficile infection (CDI) is important to prevent transmission by initiating adequate isolation measures and treatment

Studies have, however, shown that the mean time between the onset of symptoms and treatment is about 3-8 days

Despite the availability of a wide range of diagnostic tests, CDI is still a widespread healthcare related infection

What this study adds

A dog can be trained to identify C difficile with high estimated sensitivity and specificity, both in stool samples and in hospital patients with CDI

The potential of using a dog for detection is the ability to screen hospital wards for infected patients

Such screening could overcome common delays in diagnosis and thus help to control and prevent CDI outbreaks

Notes

Cite this as: BMJ 2012;345:e7396
Footnotes

Contributors: MKB, MvA, CvdB-G, and YMS developed the concept and outlined the methods. HL trained the dog. MKB, HL, and MvV carried out the detection rounds and collected the data. MKB analysed the data and drafted the paper. MvA, CvdB-G, and YMS provided conceptual and technical guidance. All authors critically appraised the paper, revised where appropriate and approved the final version of the manuscript. MKB and YMS are the guarantors.

Competing interests: All authors have completed the ICMJE uniform disclosure form at www.icmje.org/coi_disclosure.pdf (available on request from the corresponding author) and declare: HL is the owner and chairman of the Animal Behaviour and Cognition, Scent Detection Research and Academy HL&HONDEN, Edam, Netherlands; otherwise no support from any organisation for the submitted work; no financial relationships with any organisations that might have an interest in the submitted work in the previous three years; no other relationships or activities that could appear to have influenced the submitted work.

Ethical approval: The research protocol was approved by the institutional review boards of both hospitals.

Data sharing: No additional data available.

This is an open-access article distributed under the terms of the Creative Commons Attribution Non-commercial License, which permits use, distribution, and reproduction in any medium, provided the original work is properly cited, the use is non commercial and is otherwise in compliance with the license. See: http://creativecommons.org/licenses/by-nc/2.0/ and http://creativecommons.org/licenses/by-nc/2.0/legalcode.
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Baits laden with oral rabies vaccines are important for the management of wildlife rabies in the United States (1). In August 2012, the Wildlife Services program of the U.S. Department of Agriculture’s Animal and Plant Health Inspection Service . . . → Read More: Human Contacts with Oral Rabies Vaccine Baits]]> Human Contacts with Oral Rabies Vaccine Baits Distributed for Wildlife Rabies Management — Ohio, 2012
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April 12, 2013 / 62(14);267-269

Baits laden with oral rabies vaccines are important for the management of wildlife rabies in the United States (1). In August 2012, the Wildlife Services program of the U.S. Department of Agriculture’s Animal and Plant Health Inspection Service began a field trial involving limited distribution of a new oral rabies vaccine bait in five states, including Ohio. The vaccine consisted of live recombinant human adenovirus type 5 vector, expressing rabies virus glycoprotein (AdRG1.3) (Onrab). A previously used oral rabies vaccine consisting of a live recombinant vaccinia vector, expressing rabies virus glycoprotein (V-RG) (Raboral V-RG) (2,3), was distributed in other areas of Ohio. To monitor human contacts and potential vaccine virus exposure, surveillance was conducted by the Ohio Department of Health, local Ohio health agencies, and CDC. During August 23–September 7, 2012, a total of 776,921 baits were distributed in Ohio over 4,379 square miles (11,341 square kilometers). During August 24–September 12, a total of 89 baits were reported found by the general public, with 55 human contacts with baits identified (some contacts involved more than one bait). In 27 of the 55 human contacts, the bait was not intact, and a barrier (e.g., gloves) had not been used to handle the bait, leaving persons at risk for vaccine exposure and vaccine virus infection. However, no adverse events were reported. Continued surveillance of human contacts with oral rabies vaccine baits and public warnings to avoid contact with baits are needed because of the potential for vaccine virus infection.

Wildlife accounts for more than 90% of the rabid animals reported in the United States, and raccoons are the species most frequently reported (4). Oral rabies vaccination is an effective strategy to prevent the spread of rabies in reservoirs such as raccoons, coyotes, and foxes. Baits laden with oral rabies vaccine are distributed in strategic areas where target species can find and consume the baits, thereby releasing vaccine into their oral cavity. Oral rabies vaccination has contributed to the elimination of the red fox rabies virus variant and the canine rabies virus variant from several European countries and the United States, respectively, and has helped to prevent any appreciable spread of the raccoon rabies virus variant in the eastern United States (1). V-RG has been used in the United States since 1990, with approximately 138 million doses released to date. Baiting strategies have attempted to minimize human contact with V-RG baits because of the risk for infection with the V-RG vaccine virus; only two human vaccinia infections have been reported from V-RG exposure (3,5,6). AdRG1.3 is an alternative to V-RG that might have a different human safety profile given the high prevalence of antibodies in humans to human adenovirus type 5 and the mild illness that typically results from infection with this virus (7). AdRG1.3 has been integrated successfully into raccoon rabies management programs in Canada and has shown promise when used at higher bait densities for eliminating residual rabies foci in skunks (8,9).

Before and during the 2012 distribution of baits, the Ohio Department of Health, Wildlife Services, and Ohio local health jurisdictions used print media, television, radio, and the Internet to raise awareness and provide guidance to the public regarding what to do if a bait was found by a person or domestic animal. Despite these efforts, 75% of persons who came in contact with a bait were unaware of the baiting operation. A human contact was recorded when a person reported either seeing or coming into physical contact with a single bait or multiple baits with or without a barrier such as gloves. Contacts were reported by calling the toll-free telephone numbers printed on all baits or by contacting local health departments directly.

Persons who came into physical contact with an intact bait (i.e., a bait that was neither punctured nor leaking) did not require further follow-up, even if they did not use a barrier such as gloves, because vaccine exposure was not likely to have occurred. However, persons who came into physical contact with a bait that was not intact and who did not use a barrier such as gloves were considered to be potentially exposed to vaccine and at risk for vaccine virus infection. Attempts were made to contact all persons potentially exposed to vaccine 21 days after the event to ensure that their symptoms, if any, were reported. Persons who were immunocompromised, pregnant, aged <12 years, or cognitively impaired and persons with dermatologic conditions or a history of vaccine exposure to a mucosal membrane were contacted sooner than 21 days after the potential exposure.

During August 23–September 7, 2012, a total of 776,921 baits (272,034 AdRG1.3 and 504,887 V-RG baits) (Figure) were distributed by automobile in urban areas and by aircraft in rural areas of Ohio over an area of 4,379 square miles (11,341 square kilometers). A total of 89 baits were reported found by the general population during August 24–September 12 (11.5 baits found per 100,000 baits distributed). Fifteen of the baits found were AdRG1.3 (5.5 per 100,000 AdRG1.3 baits distributed), and 74 were V-RG (14.7 per 100,000 V-RG baits distributed) (p<0.001).

Among the 89 baits found, 55 human contacts occurred (some human contacts involved more than one bait). Fourteen of the human contacts were with AdRG1.3 baits, and 41 were with V-RG baits. Among the 55 human contacts, 27 involved potential vaccine exposures. Among the AdRG1.3 bait contacts, 79% resulted in potential vaccine exposure, compared with 39% of V-RG bait contacts (odds ratio: 5.7; 95% confidence interval: 1.4–23.8) (Table 1). Only 5.8% of persons physically contacting a bait used a barrier such as gloves.

Fifty-four of the human contacts were reported through 47 telephone calls on the toll-free numbers (more than one human contact was reported on some calls). An additional human contact was reported directly to a local health department. The total report rate was 6.2 reports per 100,000 baits distributed, with 4.4 reports per 100,000 AdRG1.3 baits distributed and 7.1 reports per 100,000 V-RG baits distributed (Table 2).

Five of the persons who had potential vaccine exposures also had one of the conditions that required closer follow-up. Three of these incidents occurred with AdRG1.3 and involved a boy aged 11 years, a pregnant woman, and a woman with eczema. The other two incidents occurred with V-RG in women who had autoimmune conditions and were on immunosuppressive medications. No adverse events were reported among these five persons or among the other persons who contacted baits.

A total of 38 (79%) of the 48 reports of human contact involved domestic animals, and all of the animals were dogs. One animal adverse event resulted from an AdRG1.3 bait temporarily obstructing a dog’s airway, but the dog survived. Two other adverse events were reported for V-RG baits in which the dogs regurgitated the baits.
Reported by

Frank Kellogg, MPH, Nancy Niehus, MS, Lake County General Health District. Mary DiOrio, MD, Kathleen Smith, DVM, Ohio Dept of Health. Richard Chipman, MS, Jordona Kirby, MS, Wildlife Svcs, US Dept of Agriculture. Jesse Blanton, MPH, Jessie Dyer, MSPH, Richard Franka, DVM, PhD, Kim Hummel, PhD, Sergio Recuenco, MD, DrPH, Charles Rupprecht, VMD, PhD, Div of High-Consequence Pathogens and Pathology, National Center for Emerging and Zoonotic Infectious Diseases; Ryan Wallace, DVM, Neil M. Vora, MD, EIS officers, CDC. Corresponding contributor: Neil M. Vora, nvora@cdc.gov, 404-639-4851.
Editorial Note

Surveillance during rabies vaccine baiting operations in Ohio suggests that human and domestic animal contacts with baits are rare. In 2010 and 2011, totals of 774,714 and 863,215 baits were distributed in Ohio, respectively, compared with 776,921 in 2012 (10). Overall, fewer human contacts with baits were reported in 2012 than in the preceding 2 years: 55 in 2012, compared with 83 in both 2010 and 2011 (Ohio Department of Health, unpublished data, 2012).

Multistate surveillance of contacts with V-RG baits during 2001–2009 revealed 6.9 V-RG baits found per 100,000 V-RG baits distributed for the study period, compared with 14.7 V-RG baits found per 100,000 V-RG baits distributed in Ohio in 2012. This same multistate surveillance system found 3.5 reports of V-RG bait contacts per 100,000 V-RG baits distributed during 2001–2009 (3), compared with 7.1 reports per 100,000 V-RG baits distributed in Ohio in 2012. Similar report rates have been observed previously in other states (3).

In 2012, AdRG1.3 was distributed for the first time in Ohio. The rate of 4.4 reports of AdRG1.3 bait contacts per 100,000 baits distributed was higher than rates observed in Canada (8,9) and in the first AdRG1.3 field trial in the United States in rural West Virginia in 2011 (Wildlife Services, U.S. Department of Agriculture, unpublished data, 2012). However, no adverse events were reported as a result of human contacts with baits in Ohio, Canada, or West Virginia (Wildlife Services, U.S. Department of Agriculture, unpublished data, 2013) (8,9). Because the risk for infection arises from exposure to vaccine virus rather than from contact with an intact bait, the higher proportion of human contacts that resulted in potential vaccine exposure with AdRG1.3 baits compared with V-RG baits deserves further evaluation.

The low percentage of persons who were aware of the baiting operation at the time of bait contact suggests that public outreach strategies should be evaluated and modified to enhance public awareness. Similar low rates of awareness about baiting operations have been reported in the past (3). In addition, only 5.8% of persons physically contacting a bait reported using a barrier such as gloves to handle baits, underscoring the need to raise awareness about the potential risk of handling baits without protection.
Acknowledgments

Jay Becker, Geauga County Health Dept; Sandy Swann, Trumbull County Health Dept; Kelly Lewis, Ohio State Univ. Dennis Slate, Timothy Algeo, Wildlife Svcs, US Dept of Agriculture. Ermias Belay, Inger Damon, Robert Holman, Andrea McCollum, Lynda Osadebe, Brett Petersen, Mary Reynolds, Div of High-Consequence Pathogens and Pathology; Celia Quinn, EIS Officer, CDC.
References

Slate D, Algeo TP, Nelson KM, et al. Oral rabies vaccination in North America: opportunities, complexities, and challenges. PLoS Negl Trop Dis 2009;3:e549.
Animal and Plant Health Inspection Service. USDA expands field trials of new oral rabies vaccine for use in raccoons and other wildlife in 5 states.Washington, DC: US Department of Agriculture, Animal and Plant Health Inspection Service; 2012. Available at http://www.aphis.usda.gov/newsroom/2012/08/rabies_vaccine_expanded.shtmlExternal Web Site Icon.
Roess AA, Rea N, Lederman E, et al. National surveillance for human and pet contact with oral rabies vaccine baits, 2001–2009. J Am Vet Med Assoc 2012;240:163–8.
Blanton J, Dyer J, McBrayer J, Rupprecht C. Rabies surveillance in the United States during 2011. J Am Vet Med Assoc 2012;241:712–22.
Rupprecht CE, Blass L, Smith K, et al. Human infection due to recombinant vaccinia-rabies glycoprotein virus. N Engl J Med 2001;345:582–6.
CDC. Human vaccinia infection after contact with a raccoon rabies vaccine bait—Pennsylvania, 2009. MMWR 2009;58:1204–7.
Wold WSM, Horwitz MS. Adenoviruses. In: Knipe DM, Howley PM, eds. Fields virology. 5th ed. Philadelphia, PA: Lippincott Williams and Wilkins; 2007.
Rosatte RC, Donovan D, Davies JC, et al. Aerial distribution of ONRAB baits as a tactic to control rabies in raccoons and striped skunks in Ontario, Canada. J Wildl Dis 2009;45:363–74.
Rosatte RC, Donovan D, Davies JC, et al. High-density baiting with ONRAB rabies vaccine baits to control Arctic-variant rabies in striped skunks in Ontario, Canada. J Wildl Dis 2011;47:459–65.
Animal and Plant Health Inspection Service. Ohio ORV distribution data, 2012. Washington, DC: US Department of Agriculture, Animal and Plant Health Inspection Service; 2013. Available at http://www.aphis.usda.gov/wildlife_damage/oral_rabies/oral_rabies_info_by_state/ohio/index.shtmlExternal Web Site Icon.

* Two types of oral rabies vaccines were distributed in different areas of Ohio: a new oral rabies vaccine (AdRG1.3) and one that has been in use since 1990 (V-RG). Clockwise from upper left: two V-RG coated sachets, two V-RG fishmeal polymer blocks, two AdRG1.3 polyvinyl chloride blister packs. A U.S. quarter is shown to illustrate the size of the baits.

FOR IMMEDIATE RELEASE – March 7, 2013 – Steve’s Real Food of Murray, Utah is recalling its 5 lb. bags of “Turducken Canine Diet – 8oz. Patties due to potential contamination of Salmonella. Salmonella can affect animals eating the products and there is risk . . . → Read More: Steve’s Real Food Recalls Turducken Canine Recipe]]> Steve’s Real Food Recalls Turducken Canine Recipe Patties Because of Possible Health Risk

FOR IMMEDIATE RELEASE – March 7, 2013 – Steve’s Real Food of Murray, Utah is recalling its 5 lb. bags of “Turducken Canine Diet – 8oz. Patties due to potential contamination of Salmonella. Salmonella can affect animals eating the products and there is risk to humans from handling contaminated pet products, especially if they have not thoroughly washed their hands after having contact with the products or any surfaces exposed to these products.

Healthy people infected with Salmonella should monitor themselves for some or all of the following symptoms: nausea, vomiting, diarrhea or bloody diarrhea, abdominal cramping and fever. Rarely, Salmonella can result in more serious ailments, including arterial infections, endocarditis, arthritis, muscle pain, eye irritation, and urinary tract symptoms. Consumers exhibiting these signs after having contact with this product should contact their healthcare providers.

Pets with Salmonella infections may be lethargic and have diarrhea or bloody diarrhea, fever, and vomiting. Some pets will have only decreased appetite, fever and abdominal pain. Infected but otherwise healthy pets can be carriers and infect other animals or humans. If your pet has consumed the recalled product and have these symptoms, please contact your veterinarian.

The recalled Turducken Canine Diet – 8oz Patties in a 5 lb. bag were distributed from October 2012 to January 2013 in retail stores in Connecticut, Massachusetts, Maine, New Hampshire, New York , California, Minnesota and Tennessee.

No illnesses have been reported to date in connection with this problem.

The potential for contamination was noted after a routine sampling of one 5 lb. bag by the Minnesota Department of Agriculture.

Production of the product has been suspended while the company and the FDA continue their investigation as to the source of the problem.

The product comes in 5 lb. green and cream colored biodegradable film bags with lot number 209-10-27-13 with an expiration date of October 27, 2013.

Consumers who have purchased 5 lb. bags of Steve’s Real Food Turducken Canine Recipe are urged to return them to the place of purchase for a full refund. Consumers with questions should contact the company at 801-540-8481 or gary@stevesrealfood.com Monday through Friday from 8:00 am – 5:00 pm MST.

Contact:
Consumer:
Gary Bursell
801-540-8481
E-mail: gary@stevesrealfood.com

FOR IMMEDIATE RELEASE – April 3, 2013 – Bravo! is voluntarily recalling three of its raw diet frozen foods for dogs and cats: 5 lb tubes of Bravo! Chicken Balance product item code 21-405 with “best . . . → Read More: Bravo! Issues a Voluntary Recall for Three Raw Frozen Food Diet]]> Bravo! Issues a Voluntary Recall for Three Raw Frozen Food Diet for Dogs and Cats Because of Possible Salmonella Health Risk

FOR IMMEDIATE RELEASE – April 3, 2013 – Bravo! is voluntarily recalling three of its raw diet frozen foods for dogs and cats: 5 lb tubes of Bravo! Chicken Balance product item code 21-405 with “best used by” dates of 3_6_15 and 3_12_15; 2 lb Bravo! Chicken Blend product item code 21-102 with the “best used by” date of 3_21_15 and 5 lb. bags of Bravo! Beef Blend Burgers product item code 51-508 with the “best used by” dates of 3_21_15 and 3_22_15, because they have the potential to be contaminated with Salmonella.

This recall is being issued out of an abundance of caution, as while these products tested negative for pathogens by an independent third party prior to distribution, they were run on the same day or an adjacent day to a product that tested positive for pathogens. The product that tested positive has been 100 percent contained and is not subject to this recall.

The recall involves only:

5 lb. Bravo! Chicken Balance frozen raw diet chubs (tubes) with “best used by” dates of 3_6_15 and 3_12_15 imprinted on the side of the plastic casing. Only 26 cases with the 3_6_15 date were distributed nationally and 36 cases with 3_12_15 date were distributed nationally.
2 lb. Bravo! Chicken Blend frozen raw diet chubs (tubes) with the “best used by” date of 3_21_15 imprinted on the side of the plastic casing. Only 67 cases with 3_21_15 date were distributed nationally.
5 lb. Bravo! Beef Blend Burgers bags with the “best used by” dates of 3_21_15 and 3_22_15 imprinted on the back panel of the plastic bag. Only 47 cases with the 3_21_15 date were distributed nationally and 55 cases with the 3_22_15 date were distributed nationally.

No other products or sizes are affected.

The recalled product should not be sold or fed to pets. The company has received no reports of illness in either people or animals associated with this product.

While these products tested negative, Bravo! is allowing concerned pet owners to return unopened frozen tubes of food and patties to the store where purchased for a full refund. Pet owners should dispose of unopened product in a safe manner (example, a securely covered trash receptacle). Consumers who believe they have opened these products at home should just dispose of the product in a safe manner and contact the retailer where they purchased their product for a full refund.

Salmonella can affect animals eating the products and there is risk to humans from handling contaminated pet products, especially if they have not thoroughly washed their hands after having contact with the products or any surfaces exposed to these products.

Healthy people infected with Salmonella should monitor themselves for some or all of the following symptoms: nausea, vomiting, diarrhea or bloody diarrhea, abdominal cramping and fever. Rarely, Salmonella can result in more serious ailments, including arterial infections, endocarditis, arthritis, muscle pain, eye irritation, and urinary tract symptoms. Consumers exhibiting these signs after having contact with this product should contact their healthcare providers.

Pets with Salmonella infections may be lethargic and have diarrhea or bloody diarrhea, fever, and vomiting. Some pets will have only decreased appetite, fever and abdominal pain. Infected but otherwise healthy pets can be carriers and infect other animals or humans. If your pet has consumed the recalled product and has these symptoms, please contact your veterinarian.

In an effort to prevent the transmission of Salmonella from pets to family members and care givers, the FDA recommends that everyone follow appropriate pet food handling guidelines when feeding their pets. A list of safe pet food handling tips can be found at: http://www.fda.gov/ForConsumers/ConsumerUpdates/ucm048182.htm.

For more information on the Bravo recall, please visit www.bravorawdiet.com, or call toll free (866) 922-9222 Monday through Friday 9:00 am to 5:00 pm (EST).

Contact
Consumer:
David Bogner
(866)922-9222
E-mail: info@bravorawdiet.com
www.bravorawdiet.com

Salmonella can affect animals eating the products and there is risk to humans from handling . . . → Read More: Natura Pet Expands Voluntary Recall of Dry Pet Foods Due to Possible Health Risk]]>

FOR IMMEDIATE RELEASE – March 6, 2013 – Jones Natural Chews Co of Rockford, IL is recalling 245 boxes of Woofers (beef patties) because it has the potential to be contaminated with Salmonella. Salmonella can affect animals and there is risk to humans from . . . → Read More: Jones Natural chews recall]]> Jones Natural Chews Co Recalls Woofers Dog Treats Because Of
Possible Salmonella Health Risk

FOR IMMEDIATE RELEASE – March 6, 2013 – Jones Natural Chews Co of Rockford, IL is recalling 245 boxes of Woofers (beef patties) because it has the potential to be contaminated with Salmonella. Salmonella can affect animals and there is risk to humans from handling contaminated pet products. People handling dry pet food and/or treats can become infected with Salmonella, especially if they have not thoroughly washed their hands after having contact with the chews or any surfaces exposed to these products.

Healthy people infected with Salmonella should monitor themselves for some or all of the following symptoms: nausea, vomiting, diarrhea or bloody diarrhea, abdominal cramping and fever. Rarely, Salmonella can result in more serious ailments, including arterial infections, endocarditis, arthritis, muscle pain, eye irritation, and urinary tract symptoms. Consumers exhibiting these signs after having contact with this product should contact their healthcare providers.

Pets with Salmonella infections may be lethargic and have diarrhea or bloody diarrhea, fever, and vomiting. Some pets will have only decreased appetite, fever and abdominal pain. Infected but otherwise healthy pets can be carriers and infect other animals or humans. If your pet has consumed the recalled product and has these symptoms, please contact your veterinarian.

The recall was the result of a routine sampling program by Colorado Department of Agriculture Feed Program which revealed that the finished products contained the bacteria.

The Jones Natural Chews Woofers were distributed in AZ, CA, CO, PA, VA, and WI. They were shipped to distributors and retailers between November 1, 2012 and November 12, 2012 where they were available for purchase.

Jones Natural Chews Co Woofers (beef patties) bulk 50 count box, Item UPC 741956008169, Lot 2962GPS-Best By 10/22/15 and Lot 2892PAL-Best By 10/15/15

***Woofers in bulk 50 count box may be sold individually***

Jones Natural Chews Co Woofers (beef patties) 1 pack shrink-wrap, 50 count box, Item UPC 741956008657, Lot 3102, Best By 11/05/15.

Jones Natural Chews Co Woofers (beef patties) 1 pack shrink-wrap, 50 count box, Item UPC 741956008183, Lot 2892BF-Best By 10/15/15, Lot 2962PWV-Best By 10/22/15, Lot 2962ASC-Best By 10/22/15, and Lot 3032ASL-Best By 10/29/15.

Jones Natural Chews Co Woofers (beef patties) 2pack shrink-wrap, 25ct box, item UPC 741956008190, Lot 2962ASC-Best By 10/22/15 and Lot 3032ASL-Best By 10/29/15.

No illnesses have been reported to date.

Consumers who have purchased any of these woofers are urged to return it to the place of purchase for a full refund. Consumers with questions may contact the company at 1-877-481-2663, Monday through Friday, 8:00 AM – 4:00 PM, Central Standard Time.

Contact:
Consumer:
(877) 481-2663
(815) 874-9500

Salmonella can affect animals eating the products and there is risk to humans from handling contaminated pet products, especially if they have . . . → Read More: Natura Pet Issues Voluntary Recall of Specialized Dry Pet Foods Due to Possible Health Risk]]> FOR IMMEDIATE RELEASE -March 18, 2013 – Natura Pet Products is voluntarily recalling specific lots of dry pet food because it has the potential to be contaminated with Salmonella. No Salmonella-related illnesses have been reported.

Salmonella can affect animals eating the products and there is risk to humans from handling contaminated pet products, especially if they have not thoroughly washed their hands after having contact with the products or any surfaces exposed to these products.

Healthy people infected with Salmonella should monitor themselves for some or all of the following symptoms: nausea, vomiting, diarrhea or bloody diarrhea, abdominal cramping and fever. Rarely, Salmonella can result in more serious ailments, including arterial infections, endocarditis, arthritis, muscle pain, eye irritation, and urinary tract symptoms. Consumers exhibiting these signs after having contact with this product should contact their healthcare providers.

Pets with Salmonella infections may be lethargic and have diarrhea or bloody diarrhea, fever, and vomiting. Some pets will have only decreased appetite, fever and abdominal pain. Infected but otherwise healthy pets can be carriers and infect other animals or humans. If your pet has consumed the recalled product and has these symptoms, please contact your veterinarian.

These products were made in a single production facility during a two week window in December 2012. Routine testing by the Michigan Department of Agriculture collected from a single retail location tested positive for the presence of Salmonella. As a precautionary measure, Natura is voluntarily recalling all products from this production window.

The affected products are sold in bags through veterinary clinics, select pet specialty retailers, and online in the United States, Canada, Korea, Malaysia, Japan, Hong Kong, and Costa Rica. Product expiration dates range from 12/17/2013 – 1/2/2014. Product was distributed by Natura Pet Products between December 18, 2012 through March 15, 2013. No other dry food, canned food, biscuits, bars or treats are affected by this announcement.

A complete list of products in the scope of this recall are listed at the end of this release. Additional information on these products can be found at disclaimer icon www.naturapet.com.

Consumers who have purchased the specific dry pet foods listed should discard them.

For further information or a product replacement or refund call Natura toll-free at 800-224-6123. (Monday – Friday, 8:00 AM to 5:30 PM CST).

FOR IMMEDIATE RELEASE – March 7, 2013 – Diggin’ Your Dog™ announced today that they are voluntarily withdrawing one lot of its Strippin’ Chicks™ Pet Treats produced on 8-30-12 because they have the potential to be contaminated with Salmonella. . . . → Read More: Strippin’ Chicks Pet Treats – Recall Colorado & Nevada]]> Diggin’ Your Dog Recalls Strippin’ Chicks Pet Treats Distributed in Colorado and Nevada Due to Possible Salmonella Hazard

FOR IMMEDIATE RELEASE – March 7, 2013 – Diggin’ Your Dog™ announced today that they are voluntarily withdrawing one lot of its Strippin’ Chicks™ Pet Treats produced on 8-30-12 because they have the potential to be contaminated with Salmonella. The sample was obtained in Colorado and the company has accounted for its distribution in Colorado of this lot.

No other Diggin’ Your Dog™ products, lots, or production dates are affected.

The lot being voluntarily withdrawn is: Strippin’ Chicks™ Pet Treats 5 oz Bag. Lot Code 250322 Use By Date: 2-23-14.

Healthy people infected with Salmonella should monitor themselves for some or all of the following symptoms: nausea, vomiting, diarrhea or bloody diarrhea, abdominal cramping and fever. Rarely, Salmonella can result in more serious ailments, including arterial infections, endocarditis, arthritis, muscle pain, eye irritation, and urinary tract symptoms. Consumers exhibiting these signs after having contact with this product should contact their healthcare providers.

Animals with Salmonella infections may be lethargic and have diarrhea or bloody diarrhea, fever, and vomiting. Some animals will have only decreased appetite, fever and abdominal pain. Infected but otherwise healthy animals can be carriers and infect other animals or humans. If your animals have consumed the recalled product and have these symptoms, please contact your veterinarian.

Diggin’ Your Dog™ takes the matter of consumer protection and safety very seriously and strives to deliver only the safest products available.

Diggin’ Your Dog™ is committed to providing the highest-quality pet treats possible to their customers. As a precautionary measure, Diggin’ Your Dog™ will continue to produce all products in very small, handmade lot batches.

No Other Diggin’ Your Dog™ products are affected by this voluntary withdrawal. Customers who have purchased this lot code are urged to stop feeding the product to their pet, remove the lot code from the packaging, and discard the contents.

A full refund, plus $1.00 to cover postage will be received by mailing the UPC and lot code to:
Diggin Your Dog, LLC, PO Box 17306 Reno, NV 89511.
All refunds will be processed within ten business days (plus postage time).

Diggin’ Your Dog™ values the efforts of all agencies dedicated to the safety of the industry and is committed to consumer safety at all levels.

For questions or more information, contact Diggin’ Your Dog™.
By phone at 775-742-7295 Mon-Fri 8:30AM – 4:00PM Pacific Standard Time
Email us at info@dydusa.com.
Contact
Consumer:
1-775-742-7295