Will dogs ever become a regular part of clinical practice?
That is certainly what people imagine, but there are many reasons why dogs are not yet in your local doctor’s surgery — despite their accuracy. For example, receiving a diagnosis of cancer can be unnerving and upsetting, and if a dog is in the room at the time, our reactions to the situation, to the physician and to the dog itself could influence how the dog responds. They could sniff samples in a back room away from patients, but the dogs usually only work for about ten minutes at a time. And dogs are fallible, just like people: they have good days and bad days.
Instead, we could have dogs teaching machines to detect diseases — something we are doing for ovarian and pancreatic cancer and for COVID-19. We are working with several people and groups, including Charlie Johnson, the director of the Nano/Bio Interface Center at the University of Pennsylvania, and a company we co-founded along with others, called VOC Health, to develop handheld electronic devices that recognize the odour signature of various diseases accurately and reliably, just as dogs do.
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We are at the forefront of the research into the fight against cancer and other life-threatening diseases, including Parkinson’s disease and bacterial infections. Our Bio Detection Dogs are trained to find the odour of those diseases in samples such as urine, breath and sweat and our work has the potential to benefit millions.
We already apply what we know about the science of canine olfaction to benefit people by training Medical Alert Assistance Dogs to detect minute changes in an individual’s personal odour triggered by their disease and alert them to an impending medical event, helping them manage complex, life-threatening medical conditions and improving their quality of life.
We take the welfare of our Medical Detection Dogs extremely seriously. From the moment they come to us as puppies we ensure the highest standards of care for our dogs. We have a strict no kennel policy and all our dogs live in the homes of our staff or fantastic local volunteers where they are loved and cared for as part of the family.
The spread of highly pathogenic AI in commercial poultry and backyard flocks in the spring of 2015 resulted in more than $800 million in damage and control costs, as well as the lethal removal of nearly 50 million domestic birds.
“We train the dogs using positive reinforcement with rewards of food or toys depending on each dog’s motivational preference,” states Golden. “The dogs are trained to respond to specific odors by either scratching at odor boxes containing materials from AI-infected birds or sitting at boxes containing materials from non-infected birds. The dogs cannot touch the infected feces or carcasses, but are able to smell items that are placed in specially-designed odor boxes and vials.”
Dogs are not susceptible to avian influenza, but Odin and his colleagues are vaccinated for rabies and other canine diseases they may be inadvertently exposed to while conducting surveillance in the field. Once finished with their training, the dogs will be paired with an APHIS Wildlife Services field specialist for disease surveillance activities or, if found unsuited for surveillance work, placed in an adoptive home.
NWRC is the research arm of APHIS’ Wildlife Services program. Its mission is to use scientific expertise to help reduce human-wildlife conflicts related to agriculture, natural resources, property, and human and health and safety. For more information, please visit our National Wildlife Research Center website.
“Dogs have been used for scat, carcass and pest detection in wildlife damage management for many years,” states NWRC research chemist and study collaborator Dr. Bruce Kimball. “They’ve also helped to diagnose diseases, such as lung and breast cancer, in people. Eventually, we hope to train these dogs to successfully detect AI-infected birds or their feces in natural settings and serve as biosensors for this and other costly agricultural diseases.”
The dogs being trained to smell cancer and disease
Biomedical detection dogs offer incredible advantages during disease outbreaks that are presently unmatched by current technologies, however, dogs still face hurdles of implementation due to lack of inter-governmental cooperation and acceptance by the public health community. Here, we refine the definition of a biomedical detection dog, discuss the potential applications, capabilities, and limitations of biomedical detection dogs in disease outbreak scenarios, and the safety measures that must be considered before and during deployment. Finally, we provide recommendations on how to address and overcome the barriers to acceptance of biomedical detection dogs through a dedicated research and development investment in olfactory sciences.
Detection dogs have played a role in society since the Middle Ages, depicted wearing armor alongside knights and the familiar howl of the bloodhound as it tracks down criminals or missing people. In modern society, detection dogs are most often seen in a law enforcement capacity, screening people, luggage, vehicles, and cargo for contraband. However, a trend is emerging in which dogs’ olfactory abilities are being harnessed to not only detect a growing list of contraband, but also in an increasing number of fields and applications completely outside of law enforcement. A small selection of these detection disciplines is listed in Table 1. TABLE 1
There are approximately 10,000 law enforcement working dogs in the United States amongst the military, federal, local, and state police agencies (1). These working dogs are present on our military bases, in our transportation hubs (e.g., train stations, airports, seaports), and on the streets of every major city in the United States. Another way of looking at these numbers and their geographical and situational distribution is to see the potential of having a network of highly adaptable sensors all throughout the country, able to detect any threat with a reproducible odor. The current COVID-19 pandemic has shown that globally, we were not prepared to handle an outbreak of that magnitude, especially of an unknown pathogen. Since there was no immediate understanding of the infectivity and transmissibility of the virus, there was a willingness to look outside the typical methods for pathogen detection and identification; potentially repurposing prophylactics, treatments and/or diagnostic/detection equipment. Ultimately, there was a need to investigate our most primitive (but not unsophisticated), yet reliable form of detection, canine olfaction.
Much of what is needed to address and terminate an outbreak is pathogen-dependent. Typically, the pathogen must be isolated, identified, cultured, its genetic material sequenced, and only then can the scientific community begin to develop effective vaccinations, therapeutics, and diagnostics. In the meantime, the community follows the “Swiss Cheese” model, relying on personal responsibilities such as personal protective equipment (PPE) (e.g., masks), social distancing, frequent handwashing, and cough etiquette (2) to combat the general spread of germs, but not the detection of the pathogen. But what can be effective while we wait for the scientific community to ramp up, is canine-based detection as canines only rely on the pathogen or the disease-state odor. We do not even need to necessarily have that odor’s volatile organic compound (VOC) profile characterized, we just need a way to safely capture/reproduce, store, and present the odor to the detection dogs. This odor detection scenario is obviously a gross oversimplification of the process, but it is currently the most straightforward of all of our detection capabilities. One should note that at this time Biomedical Detection Dog (BMDD) capabilities are considered detection or screening tool and not diagnostic technology. The distinction being that to be a diagnostic, BMDDs would need approval from the United States Food and Drug Administration (FDA) (3).
Beginning with the 1989 (4) and 2001 (5) case reports of patients’ pet dogs causing concern due to the excessive sniffing their dogs conducted at suspicious moles that were later determined to be cancerous, the ability of dogs to sniff out disease has grown from anecdotal to a full-fledged scientific discipline. Now BMDDs work as part of research teams in prestigious academic institutions such as the University of Pennsylvania’s PennVet Working Dog Center (established 2012), detecting ovarian cancer, sinonasal inverted papilloma, COVID-19, Spotted Lanternfly infestations, biofilms, and chronic wasting disease (6). An established body of literature exists demonstrating the effectiveness of dogs and their ability to detect the VOC signatures associated with disease including, but not limited to, toxigenic Clostridium difficile in stool (7), lung and breast cancers in breath (8), four different bacteria causing urinary tract infections in patient urine samples (9), bovine viral diarrheal virus (BVDV) infected cell-cultures (10), supernatant from Pseudomonas aeruginosa cultures (11), parasitic Plasmodium falciparum (malaria) infection using patient clothing (12), prostate cancer in urine (13), ovarian cancer in blood (14, 15), type 1 diabetes (16), and Parkinson’s disease (17) in sebum. Disease detection by canines has been systematically reviewed by Moser and McCulloch (18), Edwards et al. (19), Cambau and Poljak (20), and Salgirli Demirbaş et al. (21) and reported to be a scientifically sound method of detection.
BMDD history can be roughly categorized into three periods of time: the beginning starting with the 1989 case report of melanoma and culminating in 2010 with the Moser et al. review “Canine scent detection of human cancers: A review of methods and accuracy” wherein six published studies on canine detection of human cancers were reviewed in depth. This beginning period focused nearly exclusively on canine detection of cancer. The next period runs approximately from 2010 to 2020 in which the field of biomedical detection dogs expands beyond cancer and into the variety of subdisciplines (Table 2). This ten-year period is marked by an explosion of canine detection research resulting in a growing list of detectable human diseases by BMDDs and BMDDs able to detect virus [bovine viral diarrhea virus (10)], bacteria [C. difficile (7), Escherichia coli, Klebsiella pneumoniae, Enterococcus faecalis, and Staphylococcus aureus (9)], pests (brown tree snakes (22), palm weevils (23), gypsy moths (24), longhorn beetles (25), termites (26), bed bugs (27), and quagga and zebra mussels (28), fouling agents [catfight off-flavoring compounds (29), microbial growth in buildings (30)], animals important to conservation efforts [grizzly and black bears (31), brown bears (32), geckos and tuataras (33), tortoises (34), quolls (35), jackals (36), giant bullfrogs (37), wolves (38), rabbits (39), rock ptarmigans (40), bats (41), koalas (42), kit foxes (43), tigers (44), cougars (45), cheetahs (46), bobcats (47), and gorillas (48)], and disease odor directly on humans [Parkinson’s (49), epilepsy (50), diabetes (16, 51)]. TABLE 2
Table 2. Subdisciplines within the biomedical detection dog field and examples of the diseases/pathogens/pests they detect.
The third period of BMDD history began in early 2020, coinciding with the SARS-CoV-2 global pandemic. Research groups from around the world, already deeply knowledgeable about the abilities of canines to detect human diseases, embarked on proof-of-concept studies to determine if BMDDs would be able to detect a human disease caused by a virus, in the midst of a pandemic caused by said virus. Based upon BMDD detection of the wide variety of human diseases and BMDD detection of a virus (BVDV), all of the evidence supported this as a valid next step for canine detection. The novel aspect of what was being attempted was BMDD detection of a human disease (COVID-19) caused by a virus (SARS-CoV-2). The global success of the COVID-19 detection dogs demonstrated the efficacy of BMDD detection of virus-induced human disease, but more significantly, it demonstrated the potential for BMDDs during a disease outbreak.
(1) were trained, tested, and evaluated at research institutions or utilized in some capacity in at least twenty-five countries [Argentina (52), Austria (53), Australia (54), Belgium (55), Brazil (56), Cambodia (57), Canada (58), Columbia (59), Chile (60), Czech Republic (61), El Salvador (62), Finland (52), France (63), Germany (64–66), India (67), Iran (68), Italy (69), Lebanon (52), Russia (70), South Africa (71), Switzerland (72), Thailand (73), United Arab Emirates (74), United Kingdom (75), United States of America (76)] and, when assessed, demonstrated results in sensitivity and specificity, ranging from 65 to 100% and 76 to 99% (77), respectively, illustrating the consistency and robustness of their detection accuracy despite the differing training methodologies employed,
(2) were deployed in at least four countries (Finland, Lebanon, UAE, and United States) screening people for COVID-19 in airports (78, 79),
(3) demonstrated the ability in one study to achieve detection sensitivities greater than the gold standard real-time polymerase chain reaction (RT-PCR) and in less time (80), demonstrating their potential role in medical diagnostics,
(4) distinguished COVID positive from COVID negative samples with similar efficacy regardless of body fluid sampled (i.e., saliva, urine, and sweat) (66) demonstrating the range of non-invasive samples that BMDDs are capable of utilizing in a pandemic, and
(5) in one study, were able to differentiate SARS-CoV2 infections from infections with other novel coronaviruses, influenza viruses, parainfluenza viruses, an adenovirus, a rhinovirus, a metapneumovirus (HMPV), and respiratory syncytial virus (RSV)—all etiological agents common to respiratory tract infections (65), thus demonstrating the potential for BMDDs to aid in the triage and differential diagnosis process.
Utilizing the COVID-19 BMDDs as an example, one of the first questions to address during a disease outbreak would be if the BMDDs were able to detect the pathogen or disease and to what extent. The sensitivity and specificity of COVID-19 BMDDs has been reviewed in depth (77, 81–84) and the answer to this question is an overwhelming “yes.” Now that it has been irrefutably established that BMDD detection of a pandemic human disease caused by a virus is not only possible but that it is faster and more sensitive than our gold standard diagnostics, the question is what is the potential for BMDDs going forward for the next disease outbreak and what are some of the considerations that should be made around BMDD deployment.