Introduction

Over 77 million dogs reside in homes in the US,¹ and it is estimated that between 1 in 3 and 1 in 4 dogs will be diagnosed with cancer at some point in their lives.^2,3 Cancer is most prevalent in older dogs and remains a leading cause of death in those over 10 years of age.⁴ The 2022 Gallup-sponsored Take CHARGE Canine Cancer Survey identified a 2.8% incidence of dogs newly diagnosed with cancer in the US, 4.6 times higher than the incidence of diagnosis in people.⁵ Due to the prevalence of the disease and size of the population served, demand for oncologic care is tremendous and expected to continue to grow. Over the last 25 years, veterinary cancer care has transformed with the development of a broader range of treatment capabilities and an increase in accessibility of specialty services and treatment centers.⁶ While the decision to pursue treatment is based on a complex interaction of factors including prognosis, cost, quality of life, availability of facilities, and individual preferences, early detection and intervention may be key to improving outcomes.^7–9 This latter point highlights the critical role that primary care veterinarians (pcVets) play in the overall management of cancer in a canine population.

Recent evidence demonstrates up to 90% of dog owners seeking veterinary services, with most visits occurring at the primary care level.¹⁰ The relationship built between a pet owner and pcVet is arguably the most important to a pet’s overall health and necessitates mutual trust and respect. These relationships may be tested by financial and emotional stressors, such as the realization of a cancer diagnosis. Cancer adds another layer of complexity to veterinary care, typically through referral to an oncologic specialist. The addition of a new doctor to the medical team to provide specialized care requires additional time and financial investment for the owner and introduces more complex treatment strategies. Logistically, financially, and emotionally, a cancer diagnosis can therefore lead to an overwhelming experience for a dog owner. Collaborative care in veterinary medicine is the involvement of multiple providers working together and with an owner to manage a pet’s diagnosis and ongoing treatment. Cancer care may be intensive and prolonged with no guaranteed success, and therefore the collaborative relationships developed between a pcVet and the specialist represent an important area of communication and coordination to minimize stress and maximize client compliance and satisfaction, with a goal of improving quality of life and optimizing outcomes.

The American Animal Hospital Association provides guidelines detailing situations in which referral or consultation should be considered and the manner of communication that should be upheld to best serve the client and patient.¹¹ In contrast to human oncologic care, guidelines for referral to veterinary oncologists by pcVets following a diagnosis of cancer are less clear and are influenced by a variety of objective and subjective factors.^12,13 In Canada, only 56% of pcVets report referring clients for specialty care following common cancer diagnoses¹³; among multiple factors evaluated in this study, referral was influenced by perceived patient health status, client finances, and pcVet confidence in the referral clinic. There is a small body of literature demonstrating the value of communication between a pcVet and specialists in the referral and collaborative process for both general patient care and specialty oncologic care.^14–16 Similarly, there is limited but powerful objective evidence that supports the value of communication between clients and veterinarians.^16,17 This includes some qualitative work evaluating perceptions of clients accessing specialty oncologic care, indicating that thorough and frequent availability and established relationships were deeply valued.¹⁶ Financial conversations represent another critical element of the overall process of client engagement.¹⁸ These findings all highlight ways to improve access to and functionality of collaborative care models, providing value for clients and their pets. Gaining more insight into the validity of these determinants would be helpful in creating the most effective framework for recommending collaborative cancer care.

Collaborative care has been investigated and discussed in a variety of specialties in human medicine, including oncology.^19,20 Despite the simultaneous need for, and benefits of, expanding access to collaborative cancer care, there is no current evidence defining the clients’ perspective on its use in veterinary medicine. There is also no objective evidence outlining how clients value access to referral oncologic care following a diagnosis of cancer. The objectives of this study were to (1) define dog owner perceptions of the value of collaborative veterinary care when treating a dog for cancer and (2) identify drivers of a positive dog owner experience related to collaborative care between the pcVet and a veterinary oncologic specialist.

Materials and Methods

Results

Collaboration segment

Most clients (76% [678/890]) whose dogs were diagnosed with cancer sought specialty care following diagnosis; the majority of these were the result of referral (79.5% [539/678]), with the remainder (20.5% [139/678]) pursuing specialty care without referral (Figure 1). Among the latter group, most clients (106/139) reported maintaining a collaborative relationship between the specialist and pcVet throughout their dog’s cancer treatment despite lack of initial referral. Among those who did not seek specialty care, few (15.6% [33/212]) were offered referral and declined; the remaining subset of clients were neither offered referral nor sought referral on their own (179/212). In total, 64% (572/890) of respondents received a referral to a specialist following a diagnosis of cancer.

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Flow chart representing collaboration path between primary care veterinarians (pcVets) and specialists following cancer diagnosis among survey respondents (n = 890). Data are further segmented by generation. Both percent and number (n) of each group selecting to pursue care are represented.

Citation: Journal of the American Veterinary Medical Association 261, 7; 10.2460/javma.23.01.0046

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Differences were observed by generation, gender, and income bracket affecting the likelihood for clients to pursue specialty oncologic care. Younger generations were more likely to pursue specialty treatment (P = .0001), with 88% of Millennial clients, 72% of Generation X clients, and 57% of Boomer-generation clients reporting seeking specialty care. Men were more likely to see specialists as compared with women (85% vs 65%, respectively; P = .0001). Income level was also significantly correlated with the decision to pursue care with an oncologic specialist, with increasing income brackets being associated with an increased likelihood of seeking specialty care as follows: < $50K, 66%; $50K to $99,999, 71%; $100K to $149,999, 81%; and > $150K, 84% (P = .0001). Finally, clients with dogs < 10 years of age were more likely to pursue specialty care (81% vs 59%; P = .0001).

Client satisfaction

Clients were asked separate questions about to what degree they were likely to recommend their pcVet or oncologic specialist to another dog owner; from these questions, an NPS was calculated to gauge customer satisfaction and degree of client advocacy. Client advocacy (NPS) for the pcVet was not different between those who saw a specialist and those who did not (P = .36) but was significantly higher (+40 vs +4; P = .01) among those who saw a specialist and received referrals following a diagnosis of cancer for their dogs compared with clients who received no referrals and sought specialty care on their own. NPS scores were high for specialists regardless of whether the client had been referred (+42; 517/890) or sought the specialist out on their own (+50; 50/890). When scores were evaluated on the basis of time to referral, delayed referral was associated with lower levels of advocacy (P = .0001). Specifically, NPS score for pcVets was +40 (417/890) among clients who received a referral within 1 to 3 visits and was +23 (113/890) among those who received a referral after 4 or more visits (Figure 2). There was no difference in client advocacy scores for pcVets or specialists between male and female clients (P = .44 and .84, respectively).

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Client advocacy scores as measured by net promoter score (NPS) for pcVets (n = 801) and specialists (678) based on time to referral following a diagnosis of cancer in their dog. NPS was generated on the basis of the question, “How likely would you be to recommend the pcVet/specialist to another dog owner?”

Citation: Journal of the American Veterinary Medical Association 261, 7; 10.2460/javma.23.01.0046

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Discussion

This survey provided novel insights into the perceptions and behaviors of dog owners regarding collaborative care following the diagnosis of cancer in their dog. Within our sample population, a large majority of respondents chose to pursue specialty oncologic care following cancer diagnosis, largely through referral but also through independent means. We found that early referral and collaboration between the pcVet and oncologic specialist resulted in improved client satisfaction for both groups of veterinarians, demonstrating the importance of collaborative cancer care. Overall, such collaborative efforts were perceived as a good value for the cost of service, regardless of the clients own financial situation, suggesting that stereotypes about socioeconomic status may be misleading. Finally, we identified specific factors that can improve the likelihood of client satisfaction with a pcVet or veterinary oncologic specialist during cancer care, providing valuable and specific insights for practitioners to improve the quality of clinical service.

This study utilized voluntary, anonymous survey methodology with participant screening to identify an eligible population of clientele who owned dogs that had received a diagnosis of cancer within the past 3 years to evaluate their experiences with collaborative cancer care. The demographics of respondents were broadly representative of age, race, ethnicity, geography, and economic status. It is possible, and even likely, that there was a response bias associated with those choosing to respond to a voluntary survey on dog cancer. However, given the lack of a control (or nonresponding) population, no definitive demographic comparisons or conclusions can be drawn that define this study cohort. While the level of evidence gathered from cross-sectional analyses is noted to be less powerful through observational sampling in comparison to, for example, a case-controlled or longitudinal methodology, the data generated here are useful to reflect the range of clientele that may engage with veterinary services in various practices and areas of the US but should be interpreted with this limitation in mind.

Seventy six percent of respondents made the choice to pursue care with an oncologic specialist after receiving a cancer diagnosis; most of these visits were a result of referral from the pcVet, yet a notable proportion (20.5%) sought out specialty services on their own, having not received any referral by their pcVet. Overall, 64% of clients received referral for specialty oncologic care, representing a smaller proportion of clients than ultimately pursued care and a higher proportion than has been previously reported receiving referral for treatment following a diagnosis of lymphoma or osteosarcoma.¹³ These findings present 2 critical pieces of knowledge: first, that the prevalence of collaborative oncologic care has grown in the 10 years since the previous report was published, but second, that the needs of clientele still may not be met at the current rates of referral. Many clients sought specialty care on their own, without referral, suggesting an opportunity for collaborative cancer care that remains underutilized at the level of the pcVet.

Among the large population of respondents who pursued specialty oncologic care, referral was associated with greater client satisfaction with the pcVet compared with no referral, demonstrating the relationship-building value of collaboration. Efficient, versus delayed, referral also proved beneficial for client advocacy. Various factors have been identified as influencing the decision to refer a client for oncologic care, including patient health status, client financial status, confidence in the referral center, and how worthwhile practitioners considered treatment for the condition diagnosed.¹³ As individual relationships and animal health are core to any veterinary-client relationship, it would be myopic to suggest that the decision to refer functions as the main driver for client satisfaction during oncologic care. However, efficient referral improved client satisfaction among a population who largely sought specialty care, even at the lower income brackets. A reevaluation of factors used in decision-making for referral by some pcVets may therefore be beneficial to optimize both client satisfaction and patient health, particularly if the result may increase access to specialty care options for cancer patients.

Multivariable modeling was used to determine the most impactful drivers of patient advocacy scores among pcVets and specialists. For the pcVet, factors related to communication and collaboration were found to be the most highly predictive of client satisfaction, including responsiveness to questions, continued involvement with the pet’s care, and willingness to collaborate. For specialists, key drivers included cancer knowledge, willingness to collaborate, and providing accurate cost estimates. Recent literature corroborates the value of communication between veterinarians and clients as well as between pcVets and specialists.^14,17 In another study¹⁶ of clients receiving oncologic care at a tertiary referral facility, the importance of answering questions and communicating medical knowledge in an understandable manner were highlighted. While corroborative with the results of the current study, many of these findings are also intuitive in a healthcare setting. Creating specific and targeted recommendations utilizing the knowledge generated here may be useful for veterinarians and veterinary trainees—including students, interns, and residents—to provide guidelines and even formal education for optimizing client-centric collaborative care for those receiving a cancer diagnosis. Even after referral, clients seek to maintain ongoing and consistent involvement of their pcVet in the dog’s cancer journey. This highlights the value of the original client-pcVet relationship as a critical anchor point from which a successful collaborative care initiative can be built.

Through multivariable regression, we were able to define different drivers of client advocacy among a population of respondents who did not identify as white. While some of these factors overlapped with those identified for respondents overall, the majority of which were white, the emphasis placed on communication and collaboration by the nonwhite population highlighted a critical area for consideration. Compared with the US population, a smaller proportion of veterinarians overall is racially and ethnically diverse, with 88% of veterinarians identifying as white.²² An even smaller proportion of specialists are thought to represent diverse racial and ethnic groups.^23,24 In human medicine, studies have shown that patient satisfaction and outcomes are both improved when there is concordance between providers and patience with respect to their racial, ethnic, and language backgrounds.^25,26 Cultural competency, trust, communication practices, and implicit or even explicit biases are all factors that may affect the veterinarian-client relationship when a lack of diversity exists within provider populations compared with the owners whose animals they treat. It is possible that these discrepancies are part of the causal elements driving the comparatively lower advocacy scores observed in this study, suggesting a broader and more universal need to expand the diversity of the oncologic and collaborative workforce in veterinary medicine.

Most clients in this study rated the value for money of specialty oncologic care as a high value; while scores varied by personal income, most respondents in even the lowest income brackets reported high levels of satisfaction. This finding points to a previous report¹³ that client finances can affect the likelihood of referral for specialty care by a pcVet. It is unclear to what extent veterinarians consistently have accurate or explicit knowledge of the finances of an individual client; therefore, referral decisions may be influenced by assumptions or biases adopted by the veterinarian or based on heuristics or implicitly held beliefs. It is true that, on an individual client basis, veterinarians may be inclined to make treatment recommendations tailored to previous financial behaviors exhibited by the client; however, a diagnosis of cancer may not fall in line with prior medical experiences or ailments and may therefore provide an alternative paradigm for client behavior. Identified among the key drivers of advocacy for pcVets and specialists in this study were providing accurate cost estimates and options for care. Combined with an overall high rating of value for services provided and higher advocacy scores among clients receiving referral, these data suggest that best practices for both the pcVet and specialist include offering referral as well as the full range of specialty care options, regardless of the clients perceived or actual financial situation. Finally, the mean expenditures reported by clients in this study were lower than the typical cost of specialist surgery or chemotherapy services. This finding may reflect a perception or recall error or may reflect a higher proportion of dog owners that did not pursue extensive specialty care—a decision possibly influenced by the type or severity of cancer diagnosed, which was not evaluated in this study. Therefore, in addition to collaborative care of cancer patients, pcVets and specialists may both serve their clients most effectively by having working knowledge of estimates for care in each other’s practice environment to counsel clients accurately and thoughtfully.

Despite objective findings from a varied national sample of dog owners, this study was not without limitations. Specific cancer diagnoses were not elicited by the survey data; therefore, assessment of variations in client behavior by various individual pathologies could not be assessed. The use of the Puppy Up Foundation database may have facilitated a biased response population, including mainly individuals who had a positive experience with cancer care to belong to a veterinary cancer nonprofit organization’s mailing list. An attempt to counteract this effect was made by purchasing a commercial listserv of dog owners who may or may not have had previous experience with oncologic care. In fact, most respondents (n = 614) were derived from this sample population, likely minimizing any implicit favorable response bias among those solicited from the Puppy Up Foundation list (120). Though a nationally representative sample was obtained, responses were not recorded with geographical identification; therefore, regionality to patterns in owner demographics, perceptions, or behaviors could not be assessed. Finally, it is important to note that this study was conducted in the spring of 2021, coinciding with the COVID-19 pandemic and a national trend toward increased utilization of veterinary services at all levels, including greater levels of pet ownership and spending. It is possible that shifting climates around the veterinary profession, as well as variations in the economy, could alter the behaviors and perceptions of owners, particularly regarding seeking specialty care.

In conclusion, following a cancer diagnosis in their dog, early referral and collaboration between a pcVet and specialist foster a high degree of client satisfaction and clients perceive good value for the money spent on the oncologic care of their dog. Furthermore, the necessity and influence of a pcVet was not lost for the client, even following referral for specialty care, highlighting the fundamental role pcVets play in a client’s veterinary experience and the added value of collaborative care. As the veterinary profession continues to strain under the demand for services by an increasing number of pet owners, as cancer diagnoses become more common in a larger population of dogs and the availability of oncologic specialists grows in number and location, collaborative cancer care will be increasingly utilized as an effective and valuable approach to servicing our clients and their pets.