Domestic dogs (Canis lupus familiaris) are responsible for over 99% of human deaths due to rabies (1). The key objective of a successful canine rabies elimination program is to maintain a high enough level of rabies vaccination coverage to interrupt rabies transmission within a defined dog population. This in turn reduces the incidence of rabies among human populations (1).

Stable dog populations with relatively low turnover rates make continuous vaccination coverage highly feasible. However, in many countries in which canine rabies persists, economic barriers and cultural attitudes toward dogs enable the maintenance of large free-roaming dog populations (2). Where the size of the free-roaming dog population is large and turnover is high, regularly vaccinating a large enough proportion of the population to achieve rabies elimination is a huge challenge. The stabilization of dog populations, and, in some cases, the humane reduction of the population over time to a manageable size, would be valuable adjuncts to long-term canine rabies control strategies.

Dog population management (DPM) is a multifaceted concept which aims to improve the health and well-being of free-roaming dogs, reduce problems they may cause, and may also set goals to reduce the size or turnover of the population (3). DPM may be enacted for numerous animal welfare, public health and safety, and economic reasons. These reasons include reducing the incidence of human bite injuries, secondary infections, and death; reducing or eliminating the transmission of rabies and other zoonotic diseases; reducing the level of noise and the amount of fecal contamination of the environment; reducing the incidence of traffic accidents; limiting the amount of negative publicity directed at governments; and minimizing the impact of reductions in tourism associated with free-roaming dog populations (2–5). Therefore, DPM programs can have one or more goals, depending upon specific situations, and these may or may not include permanently reducing the size of a dog population. Tools to achieve DPM objectives are humane and intended to produce a long-term positive impact on free-roaming dog populations, in contrast to dog culling (6).

Whether and how to manage dog populations effectively within rabies control programs has become the subject of debate (7, 8). However, because of the potential implications of DPM measures for the sustainability of rabies control programs, the World Organisation for Animal Health (OIE) recommends DPM as an integral part of such programs (9). Incorporating a DPM program with potential to improve animal, human, and environmental health into a rabies control program may increase motivation to tackle the issues and bring on board more stakeholders to support efforts.

Assuming that a rabies vaccination program is in place or being planned, this review aims to assess how different DPM tools might benefit rabies control programs and how to choose the most appropriate tools. We also consider available evidence for the impact of DPM measures on the health, stability, and size of dog populations. Finally, we review the feasibility and costs of implementing these interventions. This review does not aim to give prescriptive advice, but presents the available evidence, and allows program designers to assess, for their particular situations, whether it may be beneficial to integrate DPM into their rabies control planning.

Domestic dog populations are dependent on people for food, either directly or indirectly (e.g., through open garbage dumps), and their presence and movements are linked tightly to human actions (10–12). Thus, dog population size is heavily dependent on human behavior, and dog-related problems are consequences of human behavior.

In most settings where this has been studied, the majority of dogs (even if free-roaming) have identifiable owners, which may be either individuals or community groups (12, 13 and see Section “Which DPM Approaches Might Be Suitable in a Particular Setting?”). RDO involves owners accepting their duties to provide the resources (e.g., food, water, shelter, health care, social interaction, exercise, and opportunity for natural behaviors) necessary for dogs to maintain an acceptable level of health and well-being in their environments; to act in accordance with the legislation in place (including vaccination); and to minimize any risks (aggression, disease transmission or injuries) that dogs may pose to communities, other animals, or the environment (3, 4). Dogs may have a single owner or be cared for collectively by a family or a group of individuals (3).

Widespread practice of RDO at a community level will be the most effective way to achieve DPM objectives, as long as veterinary services (such as vaccination and sterilization) are accessible and affordable to owners. Empowerment of communities with the knowledge to actively participate in DPM programs that are suited to the setting will be critical to ensuring DPM programs’ success and sustainability. However, the intended impacts of RDO may be severely compromised where access to veterinary services is poor and in settings where a large proportion of dogs do not have responsible owners. For unowned dogs and those without responsible owners, the responsibility for providing veterinary care often falls upon government entities and non-govermental organizations (NGOs).

The primary focus of a rabies control program in dogs is vaccination (1). Mass dog vaccination programs generally aim for a 70% vaccination coverage so that between campaigns, levels of protection stay above the threshold necessary to prevent ongoing transmission (14, 15). High enough levels of canine vaccination will break the enzootic cycle of transmission between dogs, protecting them and their communities from rabies and leading to elimination of the disease. There is now much evidence that achieving 70% vaccination coverage, even where dog population turnover is high, is feasible (16–18), but it can be challenging.

Rapid population turnover (due to high death rates) of both owned and unowned dogs can present a significant challenge for the maintenance of high vaccination coverage (6, 17). Puppies comprise large proportions of dog populations in many rabies-endemic areas, even where almost all dogs are owned (12, 19, 20). A longitudinal study in West Bengal, India, found that 67% of new puppies died within 4 months and 82% within their first year (21). A survey in Nepal estimated 60% puppy mortality (13), and studies in Latin America and Africa have reported population-wide death rates as high as 30% per year (17, 20, 22, 23). All dogs, including puppies, can transmit rabies and should be vaccinated during mass vaccination campaigns. High population turnover means that vaccinated dogs often die and annual campaigns are generally required to vaccinate their replacements (24, 25).

There are several ways in which effective DPM programs could theoretically benefit rabies control activities.

Mass dog culling is still used as a misguided emergency response to rabies outbreaks, based on the mistaken belief that reducing the size of dog populations will reduce rabies transmission (38). In fact, mass dog culling has been shown to have no long-term impact on the control of rabies within cities (36, 39, 40) or across countries such as Ecuador, Indonesia and Bangladesh (19, 41–43). When modeled in realistic scenarios, culling is not as effective as sterilization programs at reducing population size in the long term (44). This is because culling does not address the source of new or replacement animals, and has only a temporary effect on population size. Furthermore, rapid dog replacement rates have been documented in some areas following culling, leading to a younger population of generally rabies-susceptible dogs (45, 46).

Indiscriminate culling of dogs in communities where rabies vaccination programs are operating is likely to remove vaccinated dogs from communities, resulting in lower vaccination coverage and a counter-productive increase in rabies transmission as populations recover (7). Culling often meets with public resistance both within the local area and outside, especially as the methods employed are often inhumane (47). The result can be withholding of dogs from rabies vaccination efforts during current and future campaigns. People may even move dogs away from culling zones, a measure which has been documented to spread rabies (15). Some methods of culling, such as poisoning, may pose threats to public health. Culling operations can also be expensive (19, 42, 48) and harmful to tourism (49). For these reasons, the indiscriminate culling of dogs is now universally condemned as a means to control rabies (1).

The culling of dogs has now been replaced in some settings by a variety of humane DPM approaches that aim to exert sustainable, positive impacts on dog populations and the communities in which they live (6). DPM tools such as vaccination and other disease control methods, control of access to food (habitat control), the promotion of RDO, prevention and control of reproduction, identification and registration of individual dogs, the availability of shelters, rehoming centers and holding facilities, and the passage of legislation can interlink with each other to create effective DPM programs. Much of the motivation for DPM in rabies control efforts comes from the desire to reduce the size or the turnover of the free-roaming dog population to make effective vaccination more feasible. For this reason, reproductive control is usually a primary objective, but other efforts that increase longevity and reduce population turnover will also support rabies control efforts.

There can be many different relationships between people and domestic dogs within a community. Dogs may be owned for a variety of reasons, such as for companionship, for guarding the home or livestock, for hunting, or as a source of food. These relationships may affect the degree to which they are cared for and whether veterinary services or reproductive control may be sought by the owner [reviewed in Ref. (2, 6, 47)]. Where community ownership of dogs occurs, there may be some joint acceptance of responsibility for feeding these animals, but frequently this does not extend to full RDO (2, 13, 76). Understanding the ownership patterns and roles of dogs in a community is integral to choosing an appropriate DPM tool that will be acceptable to the community, thereby ensuring that it is as effective as possible.

Terminology around dog populations is varied and often misused. Dogs may be referred to as owned, unowned, semi-owned, free-roaming, unwanted, pet, feral, stray, community, village or neighborhood dogs. Local terminology may also apply. These terms are often not informative for the purposes of planning an effective DPM program. The often-used term, “stray” dog, is not consistently defined, sometimes being used interchangeably with free-roaming [which can include unowned, free-roaming owned, and owned lost dogs (4)] and elsewhere referring specifically to dogs with no owners.

Only two characteristics of dog guardianship are highly relevant to disease control and DPM: “confinement status” and “ownership status” [(3) and Box 1], and these are not mutually exclusive. Unowned dogs are never confined, but a free-roaming dog may be owned, community owned, unowned, or feral. In many countries, dogs are allowed to roam freely, but many of these dogs have owners [(10, 12–13, 24, 85, 86) and reviewed in Ref. (6)].

Community-owned and family-owned roaming dogs can enjoy high standards of welfare when their needs are fulfilled. However, regardless of ownership status, free-roaming dogs are at higher risk for contracting diseases, injuries such as those caused by road-traffic accidents or acts of cruelty, and culling by governments or local communities, compared to owned confined dogs. This can lead, in turn, to owners failing to invest in their care (17), creating a vicious cycle of neglect and poor health.

Dog populations can vary across countries (6, 70, 78) and at more local scales (85). Understanding the composition of the dog population (such as the numbers of owned and unowned dogs in each category of confinement) and identifying which of these categories are the causes of the dog-related problems, will help to decide which DPM approaches should be considered (Table 2). Characterizing a dog population with terms like “stray” is of little use. The source of those dogs must also be considered to enable the design of a DPM program that will address the problem in a sustainable manner. Ownerless puppies may be abandoned (by owners, breeders or pet shops) or be born on the streets, and each cause may require a different management strategy. Finally, potential strategies need to be assessed for a number of features, including their acceptability to the community, their potential impact, the accessibility of dogs, animal welfare considerations, veterinary infrastructure needs and cost implications (50).

No one DPM strategy should be expected to solve all problems or fit all situations (78). Knowledge, Attitude and Practices surveys of the community can be particularly helpful in elucidating what would be the most acceptable and therefore successful DPM components to apply in a particular setting (23, 75, 87). For example, if the unowned dog population is sustained mostly by owners dumping unwanted puppies, then legislative and educational efforts to increase RDO and central-point sterilization programs may improve the health and longevity of family-owned dogs and reduce the number of unwanted litters. If breeders are dumping unwanted animals, then better regulation of such establishments will be needed. However, if the unowned dog population is sustained by puppies born on the streets, then sterilization and release programs may be considered. Where there are plentiful food resources on the streets, tackling this issue may need to be prioritized in order for other DPM tools to have their anticipated impact.

Finally, it is important to understand that DPM strategies will not have the desired impact without community buy in. The whole community may not have a uniform attitude toward dogs, which can cause tension (2). It is important to assess exactly what the views are within a local community toward potential interventions. If members of a community want to own more dogs, more (generally unvaccinated) dogs will likely be bred or imported, even if DPM programs are being implemented. Assessing the dog population and understanding community attitudes are integral to development of a successful DPM program.

Community surveys in rabies-endemic countries often identify the need for improved DPM to help reduce the risk of rabies (6, 9, 17, 77), and small- and large-scale DPM interventions on free-roaming dogs are carried out in many places. However, before adding DPM interventions to an existing rabies control program, there is a need for solid evidence that DPM tools can have the desired impact on reducing dog population size or turnover, which will benefit rabies control objectives.

Although the impact of DPM programs is often assumed and sometimes informally reported (39, 51), it is often not critically assessed and even more rarely published following peer-review. A review of the literature on DPM recently compiled by the International Fund for Animal Welfare found very little information on the effectiveness of specific approaches to DPM, and found that the most comprehensive programs were generally not making their outcome data available (88).

The use of mixed DPM interventions, though often advisable, makes it very difficult to determine which of the individual interventions is responsible for success. For example, the successful impact of sterilization and release programs on reductions in rabies cases (39) is most likely due to the impact of dog vaccination and community engagement, not sterilization. While the establishment of a shelter in Erzurum City in Turkey has been credited with a 30% reduction in the number of bites from rabies suspect dogs (89), this shelter was primarily sterilizing, vaccinating, and then releasing free-roaming dogs, and the impact on rabies could be due to the vaccination component. A pilot program using Esterilsol^TM on male dogs in Raipura Island, Bangladesh was found to be flawed as it also involved extensive use of culling (90). Reported benefits of adequate waste removal practices on free-roaming dog populations could instead be explained by the ongoing collection of free-roaming dogs from the streets in that particular setting (70).

Available data on the effectiveness of DPM programs are summarized below, but their interpretation is still fundamentally limited by the lack of control areas.

The primary tool of rabies control remains canine vaccination. While DPM can in theory benefit vaccination efforts, it also incurs considerable additional costs and requires additional technical skills. DPM programs require long-term commitment, and implementing two project aims can be logistically difficult. When limited budgets and personnel are stretched too far there is a risk that trying to tackle more than one goal detracts from the achievement of either. If expensive and time consuming DPM approaches detract from vaccination goals, or draw funding away from vaccinating a sufficient proportion of dogs, then rabies control efforts will be hindered. However, if overlapping interests draw in additional partners (such as animal welfare NGOs) or additional budgets (perhaps from different government sectors such as public safety) to strategically integrate DPM tools into a rabies control program, then this could be a very positive outcome.

Data on programmatic field costs of many DPM tools are uncommon, but some estimates of DPM by sterilization (which may include rabies vaccination even if not specified), are shown in Table 4. Although these costs of sterilization may not seem very large for an individual dog, given the scale necessary, full program costs can be high. For the four years of an intervention in Colombo City, Sri Lanka, costs within the animal sector were over $1 million, compared to $190,875 for the four preceding years (35).

Higher throughput programs can reduce costs per dog (33) (Table 4) but overall, there are insufficient data available on costs in different settings. Sterilization and release programs are usually focused on urban areas, where dog and human population densities likely make economies of scale more feasible and travel costs more reasonable. A rabies control intervention that involved sterilization as well as vaccination in selected cities in Tamil Nadu, India was not considered economically viable at the scale of the entire state (53).

Programs targeting only female dogs for sterilization (with vaccination of both sexes) will be a much more cost-effective way to reduce population size and turnover (44, 59–61) although this is uncommon in the studies listed in Table 3. In areas where the community keeps more male than female dogs (34, 61) this strategy will be even more effective at impacting population-wide demographics.

The source of funding will also need to be considered as well as the cost of interventions, in planning DPM interventions. As some canine rabies-endemic countries are considered to be middle income countries, there may be at least a proportion of dog owners who can pay for sterilization of their dogs through private veterinary services. Increased training of private and non-profit veterinarians in high throughput sterilization coupled with community engagement on RDO could benefit the wider goals of DPM by increasing access to these services. However, in the poorest countries, even a very low cost of sterilization is likely to be beyond the means of dog owners. In these settings governments and non-governmental organizations will need to fund any services to owned as well as unowned dogs. In many settings, the provision of free sterilization services could be used as a way to establish a model for more RDO, and once their value is established, owners could perhaps be asked to pay some contribution toward costs.

The scarcity of data on the costs of different DPM strategies and of their effectiveness in canine rabies-endemic settings severely limits assessment of their cost effectiveness (78), and where different tools are combined in a program the cost effectiveness of different components becomes even harder to disentangle.

Given the current high costs of sterilizing sufficient numbers of dogs to impact population turnover and size, it is likely that for most settings, sterilization is not a cost-effective additional technique to support a rabies control program. An exploratory model for rabies control in India concluded that canine vaccination alone was more cost effective than combined vaccination and sterilization (61). However, further exploration of the additional costs and indirect benefits of sterilization, improvements in waste management, treatment for skin and parasitic conditions, educational interventions and legislative interventions to support rabies control would be very valuable.

Humane DPM tools offer the theoretical possibility of better integration of dogs into communities and a stabilization, or even reduction in size of dog populations where it is easier to maintain vaccination coverage.

Unfortunately, the main DPM methods successfully employed in most high-income countries (well-enforced breeding and RDO laws, encouragement of sterilization and removal of free-roaming dogs from the streets into shelters, supported by dog identification and registration) do not transfer easily to low-income settings (19, 38, 77). Laws may not exist, are not enforced, or have meager consequences; sterilization services are not always readily available or affordable; shelters quickly get overwhelmed where rates of adoption are low; and high turnover makes registration impractical. While the tools and lessons developed for rabies control in high-income countries may provide some insight, more cost effective and culturally appropriate methods must be considered for rabies control in low-income countries.

Where population reduction of free-roaming dogs is wanted by owners and communities, veterinary services are abundant, and political will and funding are sufficient to address the issue, there is evidence that high throughput sterilization and release programs can achieve population reduction (33, 34). However, where sterilization, vaccination and release programs do not reach 70% of dogs, additional vaccination must be encouraged to ensure that vaccination levels are sufficient to halt rabies transmission as quickly as possible (36, 94, 100). Combined sterilization and vaccination programs that are enacted as a rabies control strategy but fail to reach sufficient dogs will be very ineffective at achieving goals of reducing rabies transmission (94).

Where veterinary services and funding to pay for DPM programs are insufficient, theoretical arguments would suggest that waste management programs to reduce food resources for free-roaming dogs should be encouraged. Along with promotion of RDO to reduce free-roaming dog population sizes, waste management could be the best option to reduce dog populations and the spread of diseases in resource limited settings (3), but evidence of this method’s effectiveness is currently lacking.

It is possible that large-scale DPM success in most low-income countries will require the development of a cost-effective (non-surgical) safe and permanent sterilizing agent for female dogs. Such research is being actively pursued and progress is being made (50, 62, 103).

Currently, the most promising option for permanent sterilization of female free-roaming dogs is GonaCon, a single-dose GnRH-based vaccine, but issues over side effects require further work on its formulation (50). Small scale safety trials of GonaCon given along with rabies vaccinations have been completed in female dogs in Mexico (104) and on an American Indian reservation in the US (105), but there are as yet no data on its effects on fertility.

The availability of a safe and effective single-dose injectable sterilant for both sexes would enable provision of reproductive control as an additional service to owners during mass dog vaccination campaigns. Such a sterilant could also be delivered to ownerless dogs under a capture, sterilize, vaccinate and release model that did not require transportation to surgical centers. Such a tool could revolutionize DPM programs and, in some settings, rabies control as well. However, until such a permanent sterilizing agent becomes available, a safe and effective sterilant that lasted even 2–4 years could still be very beneficial to animal welfare and rabies control.

Integrating DPM programs into rabies elimination programs could supplement the goal of breaking the rabies transmission cycle with the goal of stabilizing dog populations. In theory this is the most sustainable way to eliminate canine rabies, but three factors critically limit its wider implementation in practice. First, the clear lack of systematic data collection and the paucity of DPM program evaluation need to be addressed. Organizations currently conducting DPM programs in rabies-endemic countries should strive to improve their methods of evaluating impact (78) using available guidelines (106) and publish their findings in peer-reviewed journals. Second, there needs to be an improved understanding of the costs of current DPM tools and their benefits to rabies control in order that full cost effectiveness analyses can be conducted. Third, a single-dose, permanent, non-surgical sterilant that is safe and effective in female dogs would dramatically increase the possibilities for DPM to cost-effectively improve rabies control and elimination efforts. Armed with this knowledge, integrating DPM into rabies control programs in low-income countries could move the world closer to freedom from canine-mediated human rabies deaths.

LT drafted the initial manuscript. All authors revised it critically for important intellectual content and approved the version to be published.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.