How to prevent behavior problems in puppies

Introduction

Despite advances in veterinary care and nutrition that have improved health outcomes for companion dogs over recent years, problem behavior remains a stubbornly consistent and major cause of death in this species. According to findings from a major study, undesirable behavior was the most common cause of death in dogs of under three years of age 1. Almost 34% of deaths in this age group were attributed to problem behavior, with the odds of death being 1.4 times greater for male than female dogs. That data was collected from 2009 to 2014 in primary-care UK veterinary practices, but more recent data collated in Australia between 2013 and 2018 and analyzed using the same methodology produced similar figures, with a death rate due to unwanted behavior of 29.7% for dogs under the age of three years 2. In both populations, aggression was the most common behavioral cause of death (Figure 1). 

The high prevalence of euthanasia is the visible tip of a much larger iceberg of issues around problematic dog behavior. These statistics are undeniably disturbing, but euthanasia is only one possible endpoint for dogs with behavior problems, and it usually only applies to the most seriously affected. Owners may also choose to rehome or treat affected dogs, or adapt their lifestyle to accommodate behavioral problems, but all these options represent an emotional, financial or time burden on pet-owning families.

Problem behavior is widely accepted as a major cause for relinquishment, as reported in many studies and in the annual statistics from rehoming and welfare organizations. This also has a high cost in terms of public funds and animal welfare. Treatment is an option, but uptake and success depend on people being highly motivated, well-informed and guided toward effective sources of help. Unfortunately, the Australian study 2 found that for 82.8% of the fatalities reported, no other intervention was recorded and the mean age of the dog when the first signs of the behavioral cause of death appeared was approximately 11 months of age. This indicates that significant opportunities to remedy behavior problems were commonly being missed. With the shelter system perennially overloaded, and owners not getting the support that they need, many people simply continue to live with dogs that are problematic. This puts people at risk, damages the human-animal bond and all the physical and mental health benefits that flow from it, and impairs the quality of life for both families and dogs.

Given how much we know about the effects of problem behavior on people and pets, why do we continue to fail to get a grip on this problem? The main reason is probably that we do not pay enough attention to prevention. On the breeders’ side this means correctly selecting dogs to breed from and providing a good environment that supports maternal care and early socialization and habituation. On the pet-owners’ side this means knowing what to look for when choosing a puppy, and then putting a lot of time and energy into continuing socialization and habituation; this involves understanding the emotional states and motivations of puppies, providing them with a good quality of life, and training them properly.

On our side as veterinarians, it means proactively working with breeders to achieve good selection and rearing practices and early vaccination, providing owners with the best sources of information, and understanding the interaction between disease prevention and behavioral development in puppies. Lack of space precludes coverage of all of these matters, so this article will focus on the things that I believe are good starting points, because they can make the most difference. It is firstly helpful to review the stages of puppy development, and how they relate to breeding and homing practices.

Stages of development

Figure 2 shows a timeline of the stages and timepoints that are of practical importance in puppy development. Before 3 weeks of age, puppies lack mobility, and the main sensory inputs to which they respond are touch and olfaction. Beyond this point puppies become more active as their sensory and locomotor systems develop. This is referred to as the “sensitive period” of development, although it is often informally called the “socialization period”. During this time they become increasingly independent of their attachment figures (such as their mother and the people they feel safe with), and become more inquisitive and exploratory. Although the sensitive period may extend up to 12-14 weeks of age, for practical purposes of socialization and habituation it is best to assume that the endpoint is 12 weeks.

Between birth and up to around ten weeks of age the puppy’s central nervous system (CNS) undergoes an extensive process of myelination and organization 3. This is a part of the process of experience-expectant development: the brains of young animals are pre-prepared to gather specific information that is expected to be present in the environment during development and is needed for the brain to mature properly 4. A well-known example of this is the development of vision in cats. If a kitten’s vision is occluded for periods as short as 3-4 days during the first 3 months of life, this leads to a persistent and mostly irreversible reduction in the number of visual cortex neurons that respond to the deprived eye. Periods of longer occlusion can lead to permanent functional vision loss in kittens, even though the same period of occlusion in an adult cat will have no effect 5. This same process applies to all the information and experiences a puppy or kitten is exposed to, so that if anything is lacking in the first weeks of life, permanent functional deficits can result. This is why the sensitive period is so important in terms of the development of normal behavior in puppies. By the end of this period the CNS transforms into a neuronal representation of the puppy’s experience up that point, into which new information can be integrated in the future.

After the sensitive period ends there is a progressive increase in neophobia; puppies will show fear and avoidance of specific unfamiliar stimuli, and may become anxious in environments that are more complex than they are used to or that include a lot of unfamiliar stimuli. Even puppies that have been well socialized and habituated can show these signs in some situations, but they will be more resilient and better able to cope.

Parental selection and pre-homing puppy rearing

In 2018 I was part of a team that was commissioned by the Dutch Government to produce a report on dog bite prevention, which involved a Delphi consensus-building process with a panel of international experts. The panel considered and ranked the importance of a wide range of factors that contribute to bite risk, including those relating to the owner, the dog, the situation and the behavior of the bite victim. Of the dog-related factors, the temperament and personality of dogs was ranked most important, closely followed by the socialization and habituation experience of individuals during puppyhood. Temperament and personality are the product of the interaction between genetics and early experience, so there is a high degree of overlap between these two factors.

To function well as an emotionally stable adult with appropriate behavior, the range of stimuli and experiences a puppy is exposed to during the sensitive period should closely match what it will go on to encounter as an adult. Most puppies are homed at around 8-9 weeks of age, about halfway through the sensitive period. This is an ideal age, because it is a time when puppies are already becoming more independent and engaged with their environment, and it is before the onset of neophobia. However, puppies are changing rapidly at this age, and whilst most are ready to move on to a new home at 8 weeks, some might benefit from a few more days with their mother.

The later a puppy is homed, the less of the sensitive period the puppy’s new family has to work with, and the greater the risk that they will have insufficient opportunity to make up for any deficiencies in the rearing environment provided by the breeder (Figure 3). The breeder’s focus should be on giving puppies an engaging and stimulating environment, plenty of well-managed social contact with other dogs and people (including children), and exposure to a wide range of normal domestic stimuli, so that the puppy is well prepared for homing at 8 weeks. This should include regular exposure to sound recordings of a wide range of domestic and urban noises. Giving puppies access to a safe, engaging and stimulating environment that encourages them to spend time away from their mother also fosters the detachment process, so that puppies gain independence from the dam before they are homed.

The influence of maternal behavior on puppy development is a relatively new area of interest. Not all dams provide the same level of care to their puppies, with first-time mothers showing lower levels of licking, nursing and mother-puppy contact than more experienced ones 6. When we looked at the effect of the amount of maternal care puppies received during the first 21 days of life on their behavior at 8 weeks of age, we found that the more maternal care a puppy received, the more exploratory behavior it showed when it was isolated in a novel environment, the less it was orientated to the enclosure (i.e., looking for its mother), and the longer it took to start yelping (a sign of stress) 7. The overall picture was that the more cared-for puppies were more confident, independent and inquisitive. These are desirable characteristics for a puppy that is being homed at this age, and they could protect it against the development of behavior problems, especially those involving attachment (e.g., separation anxiety). The implication is that breeders should choose to breed from females that are not only healthy and temperamentally sound, but that also show good maternal behavior – and in addition they should provide a secure and undisturbed environment that will promote positive dam-puppy interactions.

There is also some evidence that early human handling can affect a dog’s behavior later in life. For example, one study found that puppies which were given gentle daily handling before the age of three weeks went on to show a longer latency before yelping, more exploratory behavior and a shorter duration of vocalization in isolation tests at 8 weeks of age, compared with unhandled puppies 8. The similarity between these results and those from studies on maternal care suggests that both forms of contact are probably keying into the same mechanism. Breeders should be encouraged to gently handle puppies during their first three weeks of life, particularly when the mother is inexperienced and may not engage in sufficient maternal care behavior. To avoid stressing the dam, handling can be done when she is away from her puppies, such as when she is feeding.

Puppy selection and the post-homing period

Purchasing a puppy should be approached like any other major decision. For example, on average, people will keep a car for 6-7 years (Figure 4), and (based on US figures) they typically take around 16 weeks to decide which car to buy, spending around 100 hours researching their decision 9. Most are undecided at the start of the process, and 6 out of 10 people will consider multiple vehicle options, visiting on average 2-3 dealerships. Contrast this with puppy buying. According to a UK study looking at the effect of the pandemic on puppy buying, only 46.7% of puppy-buyers carried out pre-purchase research, and 91.6% of owners bought their first-choice breed 10. When new puppy owners were asked which of a range of factors were important, only 12% of respondents indicated that seeing several litters before choosing the right puppy was important, only 36% thought that it was important to get a puppy reared in a home environment, only 21% said that it was important to take a puppy home at the age of 8-9 weeks, and 40% did not think that seeing the mother was important (n=320) 11. Unfortunately, owners also do not make decisions based on behavior or temperament. In a 2012 study based in US rehoming shelters, 27.3% of respondents indicated that appearance was the single most important reason they chose their dog, compared with only 11.4% who said that behavior was of primary importance 12. Putting it crudely, people appear to put more thought into buying a car than a dog, and this is where we as veterinarians can help our clients.

We should try to encourage people to approach puppy selection in the same way as any other long-term decision, making choices based on factors that are known to be positively influential on ownership outcome. At the very least, we should give prospective puppy owners a checklist of simple rules that will help them to make a good decision (Table 1). If prospective owners can be persuaded to consider various breeds, this increases the likelihood that several litters will be viewed, and if we can get them to plan to see several litters then they will at least be able to explore options rather than pick a puppy from the first litter they are shown. By doing this we can help remove some of the constraints that typically result in a limited, and therefore most likely poor, choice of puppy.

Table 1. A checklist for prospective puppy owners.

The new puppy owner is then responsible for completing its socialization and habituation, and the puppy training process. Unfortunately, many new owners do not place much value on socialization or training. When asked which of a range of factors were important to dog ownership, only 44% of recent puppy purchasers thought that completing a course of socialization classes was important, and only 35% thought it was important for a puppy to attend a course of training classes before the age of 6 months 11. It may not be possible to persuade all puppy owners to go to socialization and training classes, especially if these services are unavailable locally, but there are some good online resources that can help. For example, the Dogs Trust provides a free set of recorded sounds and socialization instructions in its “Sounds Sociable” program *. This website also includes information about initial training and how to deal with early misbehavior and housetraining in puppies in a calm and gentle way that avoids punishment.

* https://www.dogstrust.org.uk/help-advice/dog-behaviour-health/sound-therapy-for-pets

Barriers to socialization and habituation

Regular exposure to a wide range of domestic stimuli and events is easily achieved if a puppy is reared in a home environment (see Figure 5). Positive exposure is likely to greatly outweigh any mildly negative exposure that might occur from 12 weeks onward, and indoor stimuli are, by their nature, less noisy and kinetic. In addition, the puppy experiences these stimuli in an environment that is already familiar and safe. However, the outdoor environment includes much larger, faster moving and noisier stimuli, such as vehicles, as well as busy and open spaces like shopping areas and parks. In addition, these events and stimuli are experienced by the puppy when it is away from the safety of the home and the secure base of its mother. It takes time for a puppy to establish a secure bond with its new family members, so during its first walks outdoors it may feel very apprehensive and vulnerable (Figure 6). If these first trips out happen when the puppy is still within the sensitive period, at least neophobia is not an additional factor, but this is dependent on vaccination. If primary vaccination is delayed, and only completed after the end of the sensitive period, then the puppy may have no opportunity to acquire positive experiences of the outdoor world. This creates a significant risk of fear, anxiety and aggression problems in adulthood.

Vaccination is therefore an essential aspect of socialization and habituation, because without it the risk of infectious disease is a barrier to behavioral development. Ideally, primary vaccination should be started as early as possible, using products that rapidly achieve protective efficacy. For example, giving first vaccinations when the puppy is with the breeder will enable it to start going outdoors as soon as possible after homing. Veterinarians should also give the best advice on local disease prevalence that balances health risks with the danger of failing to meet socialization and habituation targets.

Managing early experiences

Although the importance of socialization and habituation in the development of good adult behavior is well established, the best approach to achieving proper socialization and habituation is not yet clear 13. Puppy parties are beneficial if they are run well, and real-world experience is invaluable. However, these parties can be overwhelming for some individuals, particularly if they include puppies with a wide range of ages, and if the social interaction between puppies is mishandled. Likewise, puppies can easily be overwhelmed when they start meeting unfamiliar dogs and people during their first walks outdoors. The key to handling these experiences well is for owners to recognize and respond appropriately to signs of stress in their puppies. Common indicators of stress include lip-licking, yawning, panting, restlessness, avoidance, whining and crying, defensive behaviors (e.g., growling), loss of appetite, and a failure to respond to commands. This is another area of owner education that is well suited to the role of the veterinarian. If owners see these signs in their puppy, they should remove the pet from the situation and allow him or her to calm down. If the same signs are seen after more careful successive introductions of the puppy to similar situations, the owners should be advised to seek professional behavioral help.

Conclusion

Problem behavior is probably the most overlooked cause of death in young dogs. Behavioral problems are multifactorial in nature, and by the time they are presented to clinicians they can be very difficult to treat. Prevention is the best way forward, and whilst we do not want to alarm owners, veterinarians have a duty to make them aware of the mortality risks associated with problem behavior in young dogs. This tough conversation may be the key to opening a dialogue about the seriousness of selecting and raising a puppy, and making the right decisions. We are also in the best position to influence breeders by promoting good rearing practice and early vaccination so that puppies are properly prepared for their new homes. With the right action, we can improve outcomes for many young dogs and their owners.