Modeling the effect of surgical sterilization on owned dog population size in Villa de Tezontepec, Hidalgo, Mexico, using an individual-based computer simulation model
June
Modeling the effect of surgical sterilization on owned dog population size in Villa de Tezontepec, Hidalgo, Mexico, using an individual-based computer simulation model
Luz Maria Kisiel 1 2
Andria Jones-Bitton 1 2
Jan M. Sargeant 1 2
Jason B. Coe 1 2
D. T. Tyler Flockhart 0 2
Erick J. Canales Vargas 2
Amy L. Greer (ALG 1 2
0 Department of Integrative Biology, University of Guelph , Guelph, Ontario , Canada , 4 Rabies and Zoonoses Prevention Program, Servicios de Salud de Hidalgo , Mineral de la Reforma, Hidalgo , Mexico
1 Department of Population Medicine, Ontario Veterinary College, University of Guelph , Guelph, Ontario , Canada , 2 Centre for Public Health and Zoonoses, University of Guelph , Guelph, Ontario , Canada
2 Editor: Carlos E. AmbroÂsio, Faculty of Animal Sciences and Food Engineering, University of São Paulo , BRAZIL
-
Data Availability Statement: All relevant data are
within the paper and its Supporting Information
files.
Surgical sterilization programs for dogs have been proposed as interventions to control dog
population size. Models can be used to help identify the long-term impact of reproduction
control interventions for dogs. The objective of this study was to determine the projected
impact of surgical sterilization interventions on the owned dog population size in Villa de
Tezontepec, Hidalgo, Mexico. A stochastic, individual-based simulation model was
constructed and parameterized using a combination of empirical data collected on the
demographics of owned dogs in Villa de Tezontepec and data available from the peer-reviewed
literature. Model outcomes were assessed using a 20-year time horizon. The model was
used to examine: the effect of surgical sterilization strategies focused on: 1) dogs of any age
and sex, 2) female dogs of any age, 3) young dogs (i.e., not yet reached sexual maturity) of
any sex, and 4) young, female dogs. Model outcomes suggested that as surgical capacity
increases from 21 to 84 surgeries/month, (8.6% to 34.5% annual sterilization) for dogs of
any age, the mean dog population size after 20 years was reduced between 14% and 79%
compared to the base case scenario (i.e. in the absence of intervention). Surgical
sterilization interventions focused only on young dogs of any sex yielded greater reductions (81%
90%) in the mean population size, depending on the level of surgical capacity. More focused
sterilization targeted at female dogs of any age, resulted in reductions that were similar to
focusing on mixed sex sterilization of only young dogs (82% - 92%). The greatest mean
reduction in population size (90% - 91%) was associated with sterilization of only young,
female dogs. Our model suggests that targeting sterilization to young females could
enhance the efficacy of existing surgical dog population control interventions in this location,
without investing extra resources.
kind funding provided by Health Services of the
State of Hidalgo. The funders had no role in study
design, data collection and analysis, decision to
publish, or preparation of the manuscript.
1. Introduction
The overabundance of dogs in developing countries poses significant public health, animal
health, and animal welfare concerns [1±3]. Reproduction control is one of several methods
than can be used for controlling the growth of dog populations [
3
]. Surgical sterilization is the
most common type of dog reproduction control and remains the most frequently performed
pet contraception procedure in veterinary practice [
4
]. Surgical sterilization can not only help
to limit the increase of the dog population by preventing the birth of unwanted puppies [
3
],
but offers other benefits including the prevention of some canine diseases such as mammary
neoplasia or benign prostatic hyperplasia [4±8]. Furthermore, surgical sterilization can have
an impact in dog's unwanted sexual behaviors such as a reduction in roaming, mounting,
urine marking, and sexual aggression, when performed in young animals (6±16 weeks) [
7
].
While surgical sterilization is commonly used in developed countries, the high cost and limited
resources (including veterinary surgeons) in many developing countries makes surgical
sterilization an infeasible method of population control for large-scale application [
9
].
In Mexico, the Ministry of Health started a subsidized pet (owned dogs and cats), high
volume, surgical sterilization pilot program in 1994. This program was implemented as a result of
the growing number of pets participating in the yearly national rabies vaccination program in
the country [
10
]. In an effort to control the rising costs of the subsidized rabies vaccination
program [
10
], a focus was placed on surgical sterilization of owned dogs in order to reduce the
number of annual vaccine doses that would need to be administered over time. While this was
the primary reason for the implementation of the sterilization program, reducing the number
of owned dogs via sterilization could also create opportunities for unowned dogs to be
rehomed when homes become available, hence balancing the supply and demand of dogs.
Currently in Mexico, the pet sterilization program is offered in all of the 32 states and has become
the public policy for controlling the owned pet population in this country [
10
]. Nevertheless,
local health authorities in Mexico have limited funds and resources to address and control the
pet population, especially the large population of owned dogs that remain the most popular
pet in several parts of Mexico [11±13]. For this reason, dog population control programs in
Mexico need to be carefully designed to not only have high intervention effectiveness but also
be good value for money.
Mathematical models and computer simulation can evaluate various intervention
strategies, with varying degrees of effectiveness, without incurring the actual cost of implementation.
The use of simulation models can therefore help identify how to best target and optimize the
limited resources that are available for dog population control measures. Several mathematical
models have been developed to evaluate the effect of population control interventions such as
sterilization and euthanasia in dog populations (both stray and owned) [14±19]. Different
mathematical approaches have been used for the development of such models including, basic
demographic equations [
14
], differential equations [15±18], and agent base simulation [
19
].
Villa de Tezontepec is one of the 84 municipalities in the state of Hidalgo, in central-eastern
Mexico. The availability of detailed empirical data on the owned-dog population in this
community and data from the government subsidized sterilization program made it an ideal case
study for an evaluation of the owned dog population demographics and the projected
longterm effect of the subsidized sterilization program using a simulation model. The municipality
has an estimated human population of 11,746, [
20
]. Kisiel et al. [
13
] reported that Villa de
Tezontepec had an estimated human: owned dog ratio of 3.4:1 and that approximately
twothirds (65%) of the households in the municipality owned one or more dogs. Approximately
74% of the owned dogs were older than one year, and only 45% of the owned dogs were kept
confined when unsupervised. Fifty-five percent of the dogs were unconfined totally or partially
2 / 22
during a 24-hour period. Surgical sterilization was more common in female dogs (37%) than
male dogs (14%). Out of all reported surgically altered dogs, 80% were sterilized during
subsidized government surgical sterilization clinics. At the time of writing, the authors of the study
identified the government surgical sterilization program within this region used a ªmixedº
approach where both young dogs (sexually immature) and adult dogs (sexually mature) were
sterilized at an average frequency of 21 surgeries per month (8.6% annually), with no specific
preference for younger or adult dogs or sex. For our purposes, surgical sterilization refers to
both the sterilization of female and male dogs.
Using a stochastic, individual-based model, informed by empirical data collected in Villa de
Tezontepec, Hidalgo Mexico [
13
], the objective of this study was to compare the projected
impact of surgical sterilization interventions that focused differentially on dogs of different
ages and sexes, and also considered different levels of surgical capacity, on the number of
owned dogs. The model outcome of interest was the total owned dog population size over a
20-year time period. Only owned dogs were modeled and non-owned dogs were not included.
2. Materials and methods
2.1 Model description
A stochastic, individual-based model was constructed using Anylogic, University, 7.2.0 (XJ
Technologies). The model framework was based on the development of a hypothetical
population (in silico) of owned male and female dogs in Villa de Tezontepec, Hidalgo. ªOwnedº dogs
were defined as those dogs for which someone claims some right over or states that they are
their property [
21
]. The hypothetical population of dogs included dogs that were confined (not
permitted to roam-freely during a 24-hour period when unsupervised) and dogs that were
unconfined (allowed by their owners to roam-free and unsupervised, totally or partially during
a 24-hour period) as per Kisiel et al., 2016 [
13
]. The model was not spatially specific. The
individual components of the model (females and male dogs) did not interact spatially in the model.
2.2. Hypothetical model population structure
The individual entities in the model represented female and male dogs. The initial hypothetical
population of dogs consisted of 2924 dogs (1222 female dogs and 1702 male dogs), based on
observed dog ownership data from the region [
13
], specifically related to the number of
households owning dogs, and the mean number of dogs owned per household. This dog population
was used to establish an upper limit of community capacity for owned dogs. This community
capacity represented the maximum number of dogs that were owned by the current dog-owning
households in this community. This community capacity value was included in the model to
limit the exponential growth of the owned dog population. Once the community capacity value
was reached in the model, any newborn dogs added to the population were immediately removed
from the dog population, until the population size of dogs decreased below the community
capacity. The modeled population of dogs was assumed to be open with births and deaths, and
immigration and emigration (further described below). Individual male and female dogs were
characterized by defined life cycle states (stages) described in Fig 1 (males) and Fig 2 (females).
The model considered aging between life cycle states. The model was run for a period of 20
years, with one time-step representing one year.
2.3. Model parameterization
The model was parameterized using a combination of empirical data for Villa de Tezontepec,
Hidalgo, Mexico [
13
], wherever possible, and data available from the peer-reviewed literature
3 / 22
Fig 1. State chart for male dogs describing the individual life states and transitions, as well as immigration and emigration, in the individual-based model
evaluating owned dog population control interventions in Villa de Tezontepec, Hidalgo Mexico.
where empirical data specific to this case study were not available. A complete description of
all model parameters is provided in Table 1.
Age related mortality parameters (representing the risk of mortality due to old age) and
non-age-related mortality parameters (representing the risk of mortality due to traffic
accidents, disease, etc.), were considered in the model (Table 1). Non-age-related risk of mortality
did not differ between males and females but did differ between confined and unconfined
dogs. It was assumed that unconfined dogs were exposed to more risk when free-roaming and
as a result their risk of mortality due to non-age-related causes was higher than for confined
dogs. Age related mortality was different for males and females, based on empirical data
collected in Villa de Tezontepec, Hidalgo, Mexico (Table 1). Model parameters included both
static, fixed parameter values, and parameter distributions for model parameters for which
there was sufficient empirical data from Villa de Tezontepec, Hidalgo, Mexico (Table 1). Initial
model conditions were based on empirical data [
13
] (Table 2).
For this model, we used the reported proportion of owned dogs kept confined (45%) in
Villa de Tezontepec (Table 2). The parameter describing the time to sexual maturity
4 / 22
Fig 2. State chart for female dogs describing the individual life states and transitions, as well as immigration and emigration, in the individual-based model
evaluating owned dog population control interventions in Villa de Tezontepec, Hidalgo Mexico.
(representing the time that it takes for a female dog to reach sexual maturity and enter her first
heat cycle) was described by a uniform distribution (Table 1). A uniform distribution was
selected to represent the range of values described in the peer-reviewed literature for this
reproductive process [
22
]. We assumed that female dogs had an equal chance to become
reproductively active within the specified range used for the time to sexual maturity for female dogs. Age
related mortality was described by an exponential distribution (Table 1). An exponential
distribution was selected for these mortality parameters because it was assumed that dogs over a
year-old die continuously and independently from other dogs at a constant average rate.
2.4. Model parameter assumptions
The model assumed that the community capacity remained constant over the duration of the
simulation period (20 years). In the hypothetical population, all female dogs were assumed to
be equally fertile. Our assumption therefore provided a worst-case scenario in terms of
population size. The model also assumed that the risk of pregnancy was different for confined and
unconfined female dogs. Unconfined female dogs were assumed to have a higher risk of
pregnancy as described by the empirical data for Villa de Tezontepec, Hidalgo, Mexico (Table 1,
Tables A±E in S1 File). Unconfined dogs were also assumed to have a higher risk of mortality
[
28
]. For this model, we assumed that the risk of mortality for unconfined dogs was double the
value of the risk of mortality of confined dogs (Table 1). It has been reported that sterilization
5 / 22
PLOS ONE | https://doi.org/10.1371/journal.pone.0198209
Exponential (Min. 0.08 years, Max.
14.00 years, Skewness 2.27 and Kurtosis
10.24)
Exponential (Min. 0.50 years, Max.
12.00 years, Skewness 1.58 and Kurtosis
5.13)
Exponential (Min. 0.88 years, Max. Assumption (90.00% of Male age-related mortality)
15.40 years, Skewness 2.27 and Kurtosis (Sensitivity analysis: based on researchers' hypothesis)
10.24)
Exponential (Min. 0.55 years, Max. Assumption (90.00% Female age-related mortality)
13.20 years, Skewness 1.58 and Kurtosis (Sensitivity analysis: based on researchers' hypothesis)
5.13)
[
13
]
(Sensitivity analysis: based on researchers' hypothesis)
Assumption (2 X risk of pregnancy confined) (Sensitivity
analysis: based on researchers' hypothesis)
6 / 22
Distribution
(distribution parameters)
N/A
N/A
N/A
increases a dog's life expectancy [
29
]. Therefore, we assumed that both non-age-related
mortality and age-related mortality were different for dogs that were sterilized compared to those
that were not (Table 1). For this model, it was assumed that sterilization increased annual
survival by 10% [
29
]. This assumption was based on findings reported by Hoffman et al. (2013)
[
29
], which indicated that sterilization increases life expectancy by 13.8% in males and 26.3%
in female dogs. These reported results are based on data from North American veterinary
teaching hospitals, which might not reflect the health condition of animals in Villa de
Tezontepec. As a result, we constrained our assumption to a conservative 10% increase in annual
survival for sterilized owned dogs.
2.5 Reproduction
Reproduction is determined by the risk of pregnancy for female dogs and the availability of
intact animals in the hypothetical population. In the model, female dogs will continue to
reproduce provided that there is at least one intact male in the hypothetical population.
2.6. Immigration and emigration
Immigration and emigration events occurred four times a year (i.e. every 0.25 years) in the
model. At each immigration event, both female and male dogs were randomly added to the
population in the ªPuppyº state. Empirical data for Villa de Tezontepec, Hidalgo, Mexico
(Table C in S1 File) indicated that the majority of owned dogs that immigrate to the area do so
Values
45.00%
1222 dogs
4.00%
11.00%
21.00%
6.00%
21.00%
37.00%
1702 dogs
6.00%
16.00%
64.00%
14.00%
Reference
[
13
]
[
13
]
Tables A±E in S1 File
Tables A±E in S1 File
Tables A±E in S1 File
Tables A±E in S1 File
Tables A±E in S1 File
[
13
]
[
13
]
Tables A±E in S1 File
Tables A±E in S1 File
Tables A±E in S1 File
[
13
]
7 / 22
as puppies, and that these animals are purchased, adopted, or received as gifts from nearby
municipalities. As such, each of the dogs added to the population as part of an immigration
event were assumed to be intact and non-reproductive. At each emigration event, a proportion
of female and male dogs were randomly removed from the population across all age groups
and reproductive statuses. For our model, we assumed that during an emigration event, dogs
(of any age) were sold or given away by their owners to families or humane societies located
outside the population area, because they could no longer take care of them.
2.7 Model life cycle states
2.7.1. Male dogs. Male dogs followed the life cycle states described in Fig 1. This cycle
included age-specific states labeled Puppy (aged birth to 8 weeks), Young (aged 8 weeks to 8
months), and Adult (8 months and older). The choices for differentiation between age-specific
states relate to modeling the impacts of population control interventions, rather than biological
age. Transitions (arrows) governing the movement of male dogs from one state to another (Fig
1) are described in Table 1. In the model, when male dogs grow into adults, they transition
immediately to the Reproductive state (indicating that they have reached sexual maturity and
are able to reproduce). A separate Neutered state was included in the model to indicate male
dogs that had been surgically sterilized (Fig 1).
2.7.2. Female dogs. The life cycle of female dogs in the model is described in Fig 2. Female
dogs could be in one of three mutually exclusive age-based states that included Puppy (aged birth
to 8 weeks), Young (aged 8 weeks to 4±8 months), and Adult (4±8 months and older, depending
when the dog reached its sexual maturity in the model). The Adult state included three mutually
exclusive sub-states to describe the female reproductive cycle: In Heat (Reproductive), Pregnant,
and Not in Heat. An independent Spayed state was also included in the model to designate female
dogs that had been surgically sterilized (Fig 2). Transitions (arrows) governing the movement of
female dogs from one state to another (Fig 2) are described in Table 1.
When female dogs became adults in the model, they transitioned immediately to the In
Heat state (representing their first heat event). Dogs in the In Heat state were considered fertile
and available for possible mating and subsequent pregnancy. From the Pregnant state, after
the gestation period [
27
] (Fig 2, Table 1), a litter of four new puppies (two male and two
female, based on empirical data for the region [
13
]), were added to the dog population in the
Puppy state (Table 1). We assumed that female dogs were only eligible for surgical sterilization
if they were between heats. Although government subsidized surgical sterilization programs in
the municipality of Villa de Tezontepec might sterilize female dogs in heat or in the early stages
of pregnancy, this is a rare occurrence (Health Services in the State of Hidalgo (SSEH), 2016,
personal communication); therefore, we simplified the assumption to only consider females
between heats as eligible for the surgical intervention.
2.8. Model output
Each model simulation scenario used a 20-year time horizon. The primary outcome of interest
(final population size) was aggregated across 1000 model iterations by calculating the mean
and median population size, standard deviation, and absolute range (minimum to maximum)
for each intervention scenario. Standard box plots were used to graph the owned dog
population size results. Each set of model outcomes (1000 replicates per intervention) were compared
to the base case scenario (i.e. a simulation using the initial model parameter values but in the
absence of any interventions), and to each other for each type of intervention (Table 3).
Model outputs were visualized and analyzed using the statistical software package STATA/
SE for Mac (StataCorp LP, 2015).
8 / 22
2.9. Base case scenario
The model base case scenario used the initial conditions, and model parameter values
described, but in the absence of any interventions (Tables 1 and 2).
2.10. Surgical sterilization interventions
Surgical sterilization interventions were simulated using our base case model (Table 3). All the
surgical sterilization interventions evaluated used the current government sterilization sex
targeting ratios described below, and then were scaled up accordingly based on surgical capacity.
We examined four different surgical sterilization intervention strategies. These strategies
varied in that they targeted dogs of different sexes (both male and female dogs or female dogs
Surgical capacity Mean population
size (# of dogs)
Standard
deviation
Median population Range % relative change
size (# of dogs) (min±max) compare to base
case
Intervention
Base case
Surgical sterilization
A. Mixed age surgical sterilization A.1
Intervention
number
N/A
B. Young age surgical sterilization B.1
C. Female only mixed age
surgical sterilization
D. Female only young age
surgical sterilization (prior to
sexual maturity)
A.2
A.3
B.2
B.3
C.1
C.2
C.3
D.1
D.2
D.3
N/A
Level 1±21
surgeries per
month
Level 2±42
surgeries per
month
Level 3±84
surgeries per
month
Level 1±21
surgeries per
month
Level 2±42
surgeries per
month
Level 3±84
surgeries per
month
Level 1±21
surgeries per
month
Level 2±42
surgeries per
month
Level 3±84
surgeries per
month
Level 1±21
surgeries per
month
Level 2±42
surgeries per
month
Level 3±84
surgeries per
month
2934
2519
1564
624
558
339
303
532
345
235
307
287
276
only), dogs of different ages (both sexually mature and sexually immature dogs or sexually
immature dogs only), and at different levels of surgical capacity (number of surgeries
performed per unit time). The current regional government's ªmixedº approach (sterilization of
both female and male dogs, including young, sexually immature dogs and adult dogs) is one of
the strategies considered in our model. We modeled a mixed age surgical sterilization
intervention scenario and a female-only mixed age surgical sterilization intervention scenario both
at three different levels of surgical capacity. Capacity level 1 is based on the number of monthly
surgeries (21) currently performed by the Ministry of Health in the State of Hidalgo in Villa de
Tezontepec (8.6% annually); on average, this includes 6 adult males, 13 adult females, 1 young
male, and 1 young female dog (SSEH, personal communication, 2016). For comparison, we
also modeled increased surgical capacity at 42 surgeries per month and 84 surgeries per month
using the same sex and age distribution as the lowest surgical capacity described above. The
targeted sex and age ratios were adjusted accordingly for the interventions scenarios aimed at
female dogs only (Table 3).
There is evidence that targeting surgical sterilization to young female dogs (before they
reach sexual maturity) improves dog population control interventions [
14
]. Therefore, we also
examined the potential impact of focusing surgical sterilization interventions on young,
sexually immature dogs (female dogs aged 8 weeks to 4±8 months and male dogs aged 8 weeks to 8
months). For the sterilization interventions focused on young animals of both sexes, the sex
distribution was adjusted according to the current government surgical sterilization sex
distribution. And for the young dog, female-only sterilization interventions, all available surgeries
per surgical capacity were focused on sexually immature female dogs only. For these young
age surgical sterilization intervention scenarios, we examined the same three levels of surgical
capacity as for the mixed age surgical sterilization interventions (21, 42, and 84 surgeries per
month) (8.6%, 17.2%, and 34.5% annually)
2.11. Sensitivity analyses
We conducted sensitivity analyses to evaluate the impact of parameter uncertainty. The
parameter values describing the risk of mortality (non-age related, age related, and the death
of sterilized dogs), and the risk of pregnancy for female dogs, both for confined and
unconfined dogs, were identified as being of specific concern as they were based on assumptions
(empirical data from the region were not available for unconfined dogs). To identify
biologically realistic ranges for the sensitivity analyses around the empirical estimates, a literature
search for dog demographic studies conducted in Latin America that reported values for the
parameters of interest was conducted. The maximum values of the ranges used in the
sensitivity analyses (for the mortality parameters), were estimated by calculating the mean value from
all the parameters found in the peer-reviewed literature [23±26], for each of the parameters of
interest. These values were used as the maximum value of the ranges examined, because the
empirical values from Vila de Tezontepec were lower than the calculated mean values obtained
from the peer-reviewed literature. The minimum value of the ranges used in the sensitivity
analyses, were assumed to be half of the empirical values from Villa de Tezontepec. Since there
were no data available from the peer-reviewed literature (in Latin America) for the risk of
pregnancy values (the annual probability of becoming pregnant), the lower and upper range
values for this parameter were assumed to be plus 14% and minus 16% of the empirical risk of
pregnancy from Villa de Tezontepec. These values were selected for simplicity to round the
lower and upper range values from 10% to 40%. The range of parameter values used for
unconfined dogs in our sensitivity analysis included values between the values used for
confined dogs and the assumptions made for unconfined dogs in the model (Table 1). For
10 / 22
example, for the annual risk of non-age-related mortality for puppies for unconfined dogs, the
analysis included values between (5% and 50%). To test the sensitivity of the risk of mortality
for sterilized dogs, we first evaluated the assumption for confined dogs (90% risk of
non-agerelated mortality). During this evaluation, the risk of mortality for sterilized unconfined dogs
was kept as described in Table 1. When the risk of mortality for unconfined sterilized dogs was
evaluated, the risk of mortality for confined dogs was kept constant (90% risk of
non-agerelated mortality), then values of the risk of sterilized mortality for unconfined dogs was
varied. For the risk of age related mortality after sterilization, parameters values for male and
female dogs were varied simultaneously in the same magnitude within the specified range.
The baseline community capacity for owned dogs in the community was based on the
assumption that the current population of owned dogs was at a steady state and that only
dogowning households (as identified in an earlier study [
13
]), would continue to own dogs.
However, it is possible that non-dog-owning households could also be interested in owning dogs if
these become available from the owned dog population. Choices related to dog ownership are
influenced by human behaviour and other associated factors and these factors may play a
more important role that density dependent factors [
30
]. For owned dog populations, the
population size is entirely determined by the choices of humans. To examine the potential impact
of our baseline community capacity, we decided to also evaluate an ªupper boundº for the
community capacity parameter. In this ªupper boundº scenario, we assumed all households in
the community could potentially own dogs. The ªupper boundº community capacity value
was calculated by multiplying the total number of households in the municipality (2249
households) [
20
], by the mean number of owned dogs per household (2 dogs) that has been
previously documented in this community [
13
]. This resulted in an alternative scenario where the
community capacity was 4498 owned dogs.
In general, for the range of values determined as biologically reasonable for our sensitivity
analysis, all model intervention scenarios were varied independently (all parameters remained
unchanged except for the one being investigated) and the model was re-run (1000 iterations).
Model outputs were compared by calculating the percent change and absolute difference in
population size to identify if changing the model inputs resulted in numerically different
model outputs in terms of average projected population size after 20 years.
We present the results of our sensitivity analysis for the different sterilization interventions
at the lowest surgical capacity, in standard box plots showing 1000 iterations of each scenario
at each variation of sensitivity in the supporting information. Model outputs across the range
of parameter values examined were compared and graphed using the statistical software
package STATA/SE for Mac (StataCorp LP, 2015).
3. Results
3.1. Base case simulations
The base case model resulted in a dog population with a mean population size of 2934 dogs
(SD = 6.2; median: 2936, range: 2878 to 2945), over 1000 simulations with the maximum dog
population size constrained by the pre-defined community capacity of the population (2924
dogs) (Table 3).
3.2. Mixed age surgical sterilization intervention
Using a mixed age surgical sterilization intervention, the median dog population size
decreased over the 20-year time period (Fig 3, Table 3).
Mixed age surgical sterilization interventions at the lowest surgical capacity (21 surgeries,
8.6% annually), resulted in a 14.1% reduction in the mean dog population size compared to
11 / 22
Fig 3. Impact of mixed age (Panel A) and young age (Panel B) surgical sterilization interventions (both male and female dogs) after 20 years. Each box represents a
summary of the model outcome (population size) across 1000 stochastic model replicates. The top and bottom of each box are the 25th and 75th percentiles, and the line
inside the box is the median dog population size. The top whiskers are the minimum and maximum values of population size, excluding outliers, which are represented
in the figure by solid circles. The dashed line represents the population community capacity (2924 dogs).
the base case scenario with no sterilization interventions (Table 3). Intervention scenarios with
increased surgical capacity (42 and 84 surgeries per month) had a more pronounced reduction
(46.7% and 78.7%) in the dog population size (Fig 3, Table 3).
3.3. Young age surgical sterilization intervention
A surgical intervention that used the same surgical capacity (21±84 surgeries per month,
17.2%, and 34.5% annually) but focused the surgical capacity on young, sexually immature
dogs resulted in model outcomes where the mean dog population size was markedly reduced,
compared to the base case scenario (Table 3). For sterilization interventions that were focused
on young sexually immature dogs, as the surgical capacity increased, the median dog
population size also decreased (Fig 3). For example, the young age surgical sterilization intervention
at the lowest surgical capacity, resulted in a mean dog population size of 558 dogs after 20
years, which represented a mean population size reduction of 81.0% compared to the base case
12 / 22
scenario (Table 3). Furthermore, when young age surgical sterilization interventions were
compared to the mixed age surgical sterilization interventions with the same level of surgical
capacity, the projected percent reduction in population size across the three levels of surgical
capacity (21, 42 and 84 surgeries per month were -78.0%, -78.0% and -51.0% (Table A in S2
File). In general, across all levels of surgical capacity, mean population size reductions were
greater for surgical interventions focused on young dogs rather than dogs of mixed ages
(Fig 3).
3.4. Female-only, mixed age surgical sterilization intervention
A surgical intervention targeted at only female dogs (mixed ages) at the lowest surgical
capacity (8.6% annually) resulted in an 81.9% reduction in the mean dog population size compared
to the base case scenario (Table 3). When the surgical capacity was increased to 42 surgeries
(17.2% annually), the projected population size was reduced 88.4% compared to the base case
scenario (Table 3). At the highest surgical capacity, reductions increased to 92.0% (Table 3).
When the female, mixed age sterilization intervention was compared to the sterilization
approach targeting dogs of both sexes with mixed ages, at the lowest surgical capacity the
difference in population size was 1987 fewer dogs, corresponding to a 79% population size
reduction (Table B in S2 File). As surgical capacity increased, the population size reductions became
larger (Table B in S2 File).
3.5. Female-only young age surgical sterilization intervention
Surgical interventions focused on only sexually immature female dogs, resulted in even greater
population size reductions compared to the base case scenario (Table 3). At the lowest surgical
capacity, the model projected an 89.5% reduction in population size for this intervention
(Table 3). When surgical interventions treating exclusively young female dogs were compared
to surgical interventions open to female dogs of any age, no considerable difference in
population size reduction was observed (Fig 4).
The population size difference between these two interventions was more pronounced
when both interventions were compared at the lowest level of surgical capacity (Table C in S2
File). Surgical interventions directed towards young female dogs resulted in slightly larger
population size reduction compared to surgical interventions directed towards female dogs of any
age (Table 3). When surgical interventions aimed solely at young female dogs were compared
to surgical interventions accessible to young dogs of mixed sexes, a projected 45% population
size reduction was observed for the lowest level of surgical capacity. However, no considerable
population size reduction was observed for higher level of surgical capacity (Table D in S2
File).
3.6. Sensitivity analyses
For confined dogs, varying the annual risk of non-age-related mortality for adult dogs from
1.5±7.5% had a more pronounced effect as the risk of mortality increased (Figure A in S3 File).
Varying the annual risk of non-age-related mortality for puppies (from 5% to 30%) and young
dogs (from 10% to 30%) led to greater variability in the projected model outcomes (Figures B
and C in S3 File). For unconfined dogs, when the risk of non-age-related mortality dogs
increased for young from 10% to 60%, the mean population size decreased and the model
outcomes were more variable. (Figure D in S3 File). Varying the annual risk of non-age-related
mortality for puppies (from 5% to 50%) and adult dogs (from 1.5% to 9%) resulted in
outcomes with little variability (Figures E and F in S3 File). A decrease in the risk of pregnancy for
unconfined dogs between 66% and 10% led to a considerable population size reduction, in
13 / 22
Fig 4. Impact of female only mixed age surgical sterilization (Panel A) and female only young age surgical sterilization (Panel B) interventions after 20 years. Each
box represents a summary of the model outcome (population size) across 1000 model replicates. The top and bottom of each box are the 25th and 75th percentiles, and
the line inside the box is the median dog population size. The top whiskers are the minimum and maximum values of population size, excluding outliers, which are
represented in the figure by solid circles. The dashed line represents the population community capacity (2924 dogs).
addition, as the risk of pregnancy decreased the model projections became less variable
(Figure G in S3 File). Similarly, a reduction in the risk of pregnancy for confined dogs (from
26% to 10%) resulted in a less variable and more attractive outcome (Figure H in S3 File).
An increase in the community capacity parameter value from 2924 (baseline community
capacity) to 4498 dogs (full community capacity), on the outcomes for the mixed age and
young female only, surgical sterilization interventions at the lowest surgical capacity (21
surgeries, 8.6% annually), led to almost no population size reduction for the mixed age
intervention under the higher community capacity assumption (Figure I in S3 File). However, when
the increase in community capacity was evaluated for the young female sterilization
intervention also at the lowest surgical capacity, a considerable population size reduction was observed
(Figure I in S3 File). For both levels of the community capacity considered, the surgical
intervention focused on young female dogs demonstrated more significant reductions in the overall
population size compared to the mixed age intervention. These sensitivity analyses focused on
14 / 22
the community capacity assumption provide support for the finding that surgical sterilization
focused on young, female dogs has a greater impact then mixed aged sterilization in both
scenarios.
In general, model outcomes were more sensitive to the risk of pregnancy and
non-agerelated mortality for both confined and unconfined dogs which influenced the relative
effectiveness of the interventions evaluated. An increase in the community capacity influenced the
effectiveness of the intervention that targeted dogs of mixed age and sexes but did not change
the relative effect when the intervention focused on young female dogs only (Figures I and J in
S3 File). Variation in the mortality risk of sterilized dogs did not affect model outcomes
(Figures K±L in S3 File).
4. Discussion
The control of dog reproduction is one of several measures that can be used to control the size
of dog populations [
3
]. Surgical sterilization is the most commonly used method of pet
contraception [
4
]. Several mathematical models have been developed to evaluate the effect of
sterilization programs for both owned and free-roaming dog populations in different parts of the
world, including Italy [
14
], Brazil [15±17], and India [18±19]. No models have been developed
to evaluate the effect of ongoing surgical sterilization programs aimed at owned dogs in
Mexico. Currently, the government sterilization program in Villa de Tezontepec has a
maximum surgical capacity of 21 surgeries per month (equivalent to the sterilization of 8.6% of the
current owned dog population per year) and focuses on dogs of mixed ages and sexes. Our
model suggests that the long-term deployment of the mixed age surgical sterilization
intervention at the lowest surgical capacity examined (in line with the existing program), combined
with the current proportion of owned dogs that are confined (45%), and an initial population
of sterilized dogs (37% females and 14% males), would only reduce the mean dog population
by approximately 14.4% after 20 years. Our baseline model projections are comparable to
those reported by Baquero et al. (2016) [
15
], where an annual probability of sterilization of
12% and 8% for females and males resulted in a 17% reduction in the owned dog population
reduction after 30 years. We used our model to examine the impact of modifying the existing
surgical capacity, as well as the ages and sexes of the dogs receiving the intervention. Our
findings suggest that if the number of sterilizations were to double (42 surgeries/month: 18.7% of
the owned dog population sterilized annually), the owned dog population could decrease by
46.7% in the same 20-year time period. However, such surgical increases may be difficult to
sustain over the long term for a single region, due to the costs and required program
resources.
Our model projections suggest that surgical sterilization interventions directed exclusively
at female dogs of mixed ages could be more effective at reducing the dog population than
interventions open to dogs of any age and sex in the long term (20 years). Our results
demonstrate a mean population reduction of 81.9% and 88.4% at surgical capacities of 21 and 42
surgeries per month (8.6% and 17% of the owned population sterilized annually). Amaku et al.
(2010) reported that for a stray dog population, a population size reduction of 50% could be
achieved in less than 10 years if the probability of sterilization for female dogs was higher than
20% of the total dog population being sterilized per year [
17
]. It is important to note that the
model proposed by Amaku et al. (2010) [
17
] described the effect of sterilization in a stray dog
population. The population dynamics (i.e. birth and mortality rates, immigration and
emigration) of stray dogs can be very different from owned dogs. This is primarily due to human
behaviour which can influence the population dynamics of dogs (stray or owned) and act to
increase or decrease their abundance [31±32].
15 / 22
Our model suggests that surgical sterilization interventions focused only on female dogs
could improve the current government dog population control efforts in this location, without
investing extra resources. Previous studies suggest that dog population control programs
should focus on surgical sterilization of young female dogs (i.e. before they have a first litter)
in order to be most effective [
14
]. Our results provide further support for this assertion. In our
model, the most significant population size reduction (90%) was observed when surgical
sterilization at the current government surgical capacity (21 dogs per month, 8.6% of the owned
dog population per year), was applied to only female, sexually immature dogs. Qualitatively,
our findings are in line with those described by Di Nardo et al. (2007). Using a model to
describe the population dynamics of the owned dog population in an Italian province, the
authors have demonstrated that within the Italian context, surgical sterilization interventions
focused on young, female dogs have a more significant impact on long term population
dynamics than interventions focused on female dogs from all age groups [
14
]. However, in the
Mexican context, we find that adding increased surgical capacity (84 surgeries per month) to
the young female sterilization intervention did not yield further population size reductions but
rather, at the highest level of surgical intervention, focusing on female dogs of all ages resulted
in greater reductions in the final population size. We hypothesize that this outcome is likely
the result of having a very limited number of young female dogs left to sterilize as time passes.
Therefore, sterilizing only young female dogs at high surgical capacities does not improve the
effect of the surgical sterilization intervention because at a certain point, there are very few
young female dogs remaining in the population. For this reason, as the dog reproduction
control program continues, there will be a need to change the focus to other age-sex intact classes
for the program to remain effective. Di Nardo et al. have also suggested that their model is
highly sensitive to the mortality rate of the dogs in the model. Since we had access to survey
data that described the proportion of owned dogs that were allowed to roam free in this
community (55%) [
13
], we assumed that these animals had a higher risk of mortality than confined
dogs. This elevated mortality rate for a large number of the owned dogs in the model, could
have led to a larger population size reduction overtime. Baquero et al. (2016) suggest that the
effect of sterilization interventions should be evaluated on the variation of the infertile
population fraction rather than on the population [
15
]. In general, it appears that surgical sterilization
efforts focused at young female dogs could enhance the efficacy of the current surgical
intervention for the owned dog population in this community, without the need to increase the
number of sterilization surgeries performed per month.
Model sensitivity analyses were performed to evaluate the possible impact of changing
assumptions regarding the model parameters for pregnancy, mortality for both confined and
unconfined dogs, and community carrying capacity. Changes to the risk of non-age-related
mortality (within reasonable limits, based on a review of the literature) increased the variability
of the model results, and the attractiveness of surgical interventions in terms of relative benefit.
Our sensitivity analysis also indicated that for confined dogs, an increase in the risk of non-age
related mortality in young and adult dogs had a greater effect on the model outcomes than an
increase in the risk of mortality in puppies. However, for unconfined dogs, only the increase in
the risk of non-age-related mortality for young dogs had a considerable effect on the model
outcomes. Our sensitivity analysis also examined model outcomes across a range of pregnancy
values for confined and unconfined dogs and draw attention to the finding that surgical
sterilization interventions become more attractive as the baseline risk of pregnancy is reduced. This
result suggests that by reducing the interest and/or willingness of owners to breed their pets,
the interventions examined here are expected to have an even greater impact. Carrying
capacity is one of the most influential parameters in dog population model simulations [
15
]. Model
sensitivity analyses for the community capacity parameter suggest that as the population size
16 / 22
increases, the effectiveness of interventions decreases for interventions focused on dogs of any
age and sex. However, when we examined the community capacity on interventions targeting
exclusively sexually immature female dogs, our model projections were robust to the changes
in community capacity assumptions. This finding suggests that surgical sterilization
interventions aimed at young female dogs could continue to be effective over time even if the size of
the owned dog population were to increase (e.g. due to human behaviour or dog immigration).
In general, uncertainty around the baseline risk of pregnancy and non-age-related mortality
parameters, make the model relatively sensitive to these assumptions. As a result, the projected
impact of the modeled interventions demonstrates increased variability as these parameters
increase across a range of biologically realistic values. This highlights the need for robust
estimates of dog population numbers and attributes, including risk of mortality and pregnancy
estimates, especially when models are used to evaluate population control interventions [
14
].
Improved data availability for these specific parameter values would allow for the refinement
of the model projections.
5. Limitations
All models are simplifications of reality and therefore, as with any model-based analysis, ours
has limitations. This model only considered the owned dog population in this region and did
not consider stray (non-owned, free-roaming dogs) or feral (dogs living in a ªwild and free
stateº without intentional or direct food or shelter provided by people) dog populations [
33
].
Therefore, this model only describes population dynamics for a subset of all dogs within this
community. Consequently, the results of these model simulations do not reflect the total
impact of the interventions on the overall dog population size for this community. Current
surgical sterilization interventions in this region are exclusively targeted at owned dogs and
the outcome of this model can help inform current programs for the owned dog population in
this region. For this reason, we believe it was appropriate to model only the owned dog
population to evaluate the effect of surgical sterilization interventions in this subset of the dog
population. For this model, we assumed that all dogs that were unconfined (completely or partially
allowed to roam), within their age group, had equal risk of non-age-related mortality, and that
all unconfined female dogs had the same pregnancy risk; however, in reality, dogs allowed to
roam all day might have higher risk of mortality and pregnancy than those that are allowed to
roam only part of the day. In addition, it was assumed that all dogs that immigrated to the
hypothetical population did so as puppies (less than 8 weeks old). Even though empirical data
from this region suggests that this was a reasonable assumption, this may have influenced the
effectiveness of interventions being studied. This model did not consider the growth of the
human population in the 20-year period, which could influence the community capacity used
for this model. One of the implications of capping the owned dog population size in the model
(i.e. establishing a community capacity) was not being able to detect the growth of the owned
dog population over time beyond the community capacity, both in the absence and presence
of dog population control interventions (i.e. surgical sterilization control). Another limitation
of this model is that it was not spatially specific; therefore, we do not know if the effect of the
interventions varies by neighbourhood. We also assumed that participation in the sterilization
intervention was equally distributed across region. In reality, heterogeneous socioeconomic
levels could impact the participation of dogs in the subsidized sterilization program and the
enrolment might not be evenly distributed in Villa de Tezontepec. Lastly, another considerable
limitation of our model is that it did not take in account the owners' decision making, such as
the willingness to breed their dogs or to participate in dog population control initiatives.
Owned dog populations and their management are highly influenced by owner decision
17 / 22
making. For example, dog owners that breed their dogs for profit would be less likely to
participate dog reproduction control interventions; this was not considered in the model. This
model could be expanded to incorporate the free-roaming, non-owned dog population to
evaluate population control methods for the total dog population in this location, if appropriate
data resources were to become available.
6. Conclusion
Controlling the growth of the owned dog population is very important for the sustainability of
the federally subsidized rabies vaccination program in Mexico [
10
]. Our model findings
suggest that the sterilization of young, sexually immature dogs, especially females, could be more
successful at reducing the owned dog population size over a 20-year time horizon compared to
the current strategy of sterilization focused on dogs of any age and sex. Reducing the
proportion of owned female dogs becoming pregnant also had a significant effect on the overall
owned dog population size, suggesting that if owners were discouraged from breeding their
female dogs, this alone could reduce the owned dog population size. Computer simulation
models can help governments and other decision-makers explore options for optimizing the
limited resources allocated for dog population management programs.
Supporting information
S1 File. Empirical data from Villa de Tezontepec, Hidalgo, Mexico, 2015, used to
determine parameter values for the individual-base model.
(DOCX)
S2 File. Table A. Difference in mean population size between mixed age surgical
sterilization and young age surgical sterilization interventions within the same level of surgical
capacity. Level 1 represents a surgical capacity of 21 surgeries per month, Level 2
represents 42 surgeries per month, and Level 3 represents 84 surgeries per month. Percentages
in brackets are the % reduction in mean population size between the two interventions.
Table B. Difference in mean population size between mixed age surgical sterilization and
female only mixed age surgical sterilization interventions within the same level of surgical
capacity. Level 1 represents a surgical capacity of 21 surgeries per month, Level 2
represents 42 surgeries per month, and Level 3 represents 84 surgeries per month. Percentages
in brackets are the % reduction in mean population size between the two interventions.
Table C. Difference in mean population size between female only mixed age surgical
sterilization and female only young age surgical sterilization interventions within the same level
of surgical capacity. Level 1 represents a surgical capacity of 21 surgeries per month, level
2 represents 42 surgeries per month, and level 3 represents 84 surgeries per month.
Percentages in brackets are the % reduction in mean population size between the two
interventions. Table D. Difference in mean population size between young age surgical
sterilization and female only young age surgical sterilization interventions within the
same level of surgical capacity. Level 1 represents a surgical capacity of 21 surgeries per
month, level 2 represents 42 surgeries per month, and level 3 represents 84 surgeries per
month. Percentages in brackets are the % reduction in mean population size between the
two interventions.
(DOCX)
S3 File. Figure A. Comparison of the impact of increasing the annual risk of non-age
related mortality for adult confined dogs from 1.5% to 7.5% for the mixed age sterilization
interventions at the lowest level of surgical capacity. Model outcomes demonstrated
18 / 22
increased variability as the adult mortality rate increased. Figure B. Comparison of the
impact of increasing the annual risk of non-age related mortality for puppies confined
from 5% to 30% for the mixed age sterilization intervention at surgical capacity of 21
surgeries per month. Model outcomes demonstrated subtle changes in the relative impact of
the interventions under a wide range (5% - 30%) of values for this parameter value;
however, these changes introduced the greatest variability in outcome for the highest level of
puppy mortality. Figure C. Projected impact of increasing the annual risk of
non-agerelated mortality for young confined dogs from 10% to 30% for the mixed age sterilization
intervention (surgical capacity = 21 surgeries per month). Model outcomes appear highly
sensitive to this parameter value with higher mortality rates associated with significant
variability in model outcomes. Figure D. Comparison of the impact of increasing the
annual risk of non-age-related mortality for young unconfined dogs from 10% to 60% on
the outcomes for the mixed age sterilization intervention at the lowest surgical capacity.
Increasing the mortality rate for this age group resulted in more variability in the model
outcomes. Figure E. Comparison of the impact of increasing the annual risk of non-age
related mortality for unconfined puppies from 5% to 50% for the mixed age sterilization at
the lowest surgical capacity. Model outcomes appear relatively stable across a wide range
of this parameter value. Figure F. Comparison of the impact of increasing the annual risk
of non-age related mortality for adult unconfined dogs from 1.5% to 9% on the outcomes
for the mixed age sterilization intervention at the lowest surgical capacity. In general, the
model outcome appears relatively robust to variability in this parameter value. Figure G.
Comparison of the impact of increasing the annual risk of pregnancy of female unconfined
dogs from 10% to 66% on the outcomes for the mixed age sterilization intervention at the
lowest surgical capacity. Model outcomes were sensitive to this parameter value with
increases in the pregnancy rate resulting in a less favourable intervention outcome.
Figure H. Comparison of the impact of increasing the annual risk of pregnancy of female
confined dogs from 10% to 40% for the mixed age sterilization interventions at a surgical
capacity of 21 surgeries per month. Increasing the pregnancy rate to 0.4 resulted in far less
change in the population size as a result of the intervention than at lower pregnancy rates.
Figure I. Comparison of increasing the community capacity community from 2924 dogs
(Panel A±Baseline community capacity) to 4498 dogs (Panel B- Full Community
Capacity), on the outcomes of mixed age and young female only surgical sterilization
interventions at the lowest surgical capacity (21 surgeries per month). In general, model outcomes
appear relatively robust to variability in this parameter value, especially when the
intervention focuses on sexually immature female dogs exclusively. Figure J. Comparison of the
impact of increasing the risk of non-age-related mortality for sterilized confined dogs
from 1.5% to 3.6% on the outcomes for the mixed age sterilization intervention at the
lowest surgical capacity. In general, model outcomes did not demonstrate considerable
changes in the relative impact of the interventions across the range of values examined.
Figure K. Comparison of the impact of increasing the risk of non-age related mortality for
sterilized unconfined dogs from 2.7% to 6.0% on the outcomes for the mixed age
sterilization intervention at the lowest surgical capacity. In general, model outcomes did not
demonstrate substantial changes in the relative impact of the interventions across the range of
values examined. Figure L. Comparison of the percentage change in the risk of age related
mortality for sterilized dogs from -20% to +20% on the outcomes for the mixed age
sterilization intervention at the lowest surgical capacity. In general, model outcomes did not
demonstrate drastic changes in the relative impact of the interventions across the range of
values examined.
(DOCX)
19 / 22
Acknowledgments
The authors thank the Health Services of the State of Hidalgo for providing information
regarding their subsidized surgical sterilization program in Villa de Tezontepec, Hidalgo,
Mexico.
Author Contributions
Conceptualization: Luz Maria Kisiel, Andria Jones-Bitton, Amy L. Greer.
Data curation: Luz Maria Kisiel, Andria Jones-Bitton.
Formal analysis: Luz Maria Kisiel.
Funding acquisition: Amy L. Greer.
Investigation: Luz Maria Kisiel, Andria Jones-Bitton, Erick J. Canales Vargas, Amy L. Greer.
Methodology: Luz Maria Kisiel, Andria Jones-Bitton, Jan M. Sargeant, Jason B. Coe, D. T.
Tyler Flockhart, Amy L. Greer.
Project administration: Andria Jones-Bitton, Amy L. Greer.
Resources: Andria Jones-Bitton, Jan M. Sargeant, D. T. Tyler Flockhart, Erick J. Canales
Vargas, Amy L. Greer.
Supervision: Andria Jones-Bitton, Jason B. Coe, Erick J. Canales Vargas, Amy L. Greer.
Validation: Luz Maria Kisiel.
Visualization: Luz Maria Kisiel.
Writing ± original draft: Luz Maria Kisiel, Andria Jones-Bitton, Jan M. Sargeant, Jason B.
Coe, D. T. Tyler Flockhart, Amy L. Greer.
Writing ± review & editing: Luz Maria Kisiel, Andria Jones-Bitton, Jan M. Sargeant, Jason B.
Coe, D. T. Tyler Flockhart, Amy L. Greer.
20 / 22
similarities to human breast cancer. Preventive Veterinary Medicine. 2016 Apr 1; 126:183±9. https://doi.
org/10.1016/j.prevetmed.2016.02.008 PMID: 26948297
21 / 22
1. Downes M , Canty MJ , More SJ . Demography of the pet dog and cat population on the island of Ireland and human factors influencing pet ownership . Preventive Veterinary Medicine . 2009 Nov 1 ; 92 ( 1 ): 140 ± 9. https://doi.org/10.1016/j.prevetmed. 2009 . 07 .005 PMID: 19700212
2. Salamanca CA , Polo LJ , Vargas J. SobrepoblacioÂn canina y felina: tendencias y nuevas perspectivas . Revista de la Facultad de Medicina Veterinaria y de Zootecnia. 2011 Apr; 58 ( 1 ): 45 ± 53 .
3. World Organization for Animal Health (OIE) Stray dog population control . Terrestrial Animal Health Code . 2016 . Available from: http://www.oie.int/en/international-standard-setting/terrestrial-code/ access-online/)
4. Howe LM . Surgical methods of contraception and sterilization . Theriogenology. 2006 Aug 31 ; 66 ( 3 ): 500 ±9. https://doi.org/10.1016/j.theriogenology. 2006 . 04 .005 PMID: 16716381
5. Schneider R , Dorn CR , Taylor DO . Factors influencing canine mammary cancer development and postsurgical survival . Journal of the National Cancer Institute . 1969 Dec 1 ; 43 ( 6 ): 1249 ± 61 . PMID: 4319248
6. Brendler CB , Berry SJ , Ewing LL , McCullough AR , Cochran RC , Strandberg JD , et al. Spontaneous benign prostatic hyperplasia in the beagle . Age-associated changes in serum hormone levels, and the morphology and secretory function of the canine prostate . The Journal of Clinical Investigation . 1983 May 1 ; 71 ( 5 ): 1114 ± 23 . https://doi.org/10.1172/JCI110861 PMID: 6189857
7. Kustritz MV . Pros, cons, and techniques of pediatric neutering . Veterinary Clinics of North America: Small Animal Practice. 2014 Mar 1 ; 44 ( 2 ): 221 ± 33 . https://doi.org/10.1016/j.cvsm. 2013 . 10 .002 PMID: 24580988
8. Vascellari M , Capello K , Carminato A , Zanardello C , Baioni E , Mutinelli F . Incidence of mammary tumors in the canine population living in the Veneto region (Northeastern Italy): Risk factors and
9. Jana K , Samanta PK . Sterilization of male stray dogs with a single intratesticular injection of calcium chloride: a dose-dependent study . Contraception. 2007 May 31 ; 75 ( 5 ): 390 ± 400 . https://doi.org/10. 1016/j.contraception. 2007 . 01 .022 PMID: 17434022
10. Secretaria de Salud. Lineamientos generales operativos intensivos para la esterilizacion quirurgica de perros y gatos mediante cirugias de abordaje simplificado poco invasivo , 2015 . Mexico; 2015 .
11. Fishbein DB , Frontini MG , Dobbins JG , Flores-Collins E , Quiroz-Huerta G , Gamez-Rodriguez JJ , et al. Prevention of canine rabies in rural Mexico: an epidemiologic study of vaccination campaigns . The American Journal of Tropical Medicine and Hygiene . 1992 Sep 1 ; 47 ( 3 ): 317 ± 27 . PMID: 1524145
12. Ortega-Pacheco A , Rodriguez-Buenfil JC , Bolio-Gonzalez ME , Sauri-Arceo CH , JimeÂnez-Coello M , Forsberg CL . A survey of dog populations in urban and rural areas of Yucatan, Mexico . AnthrozooÈs. 2007 Sep 1 ; 20 ( 3 ): 261 ± 74 .
13. Kisiel LM , Jones-Bitton A , Sargeant JM , Coe JB , Flockhart DT , Palomar AR , et al. Owned dog ecology and demography in Villa de Tezontepec, Hidalgo, Mexico. Preventive Veterinary Medicine. 2016 Dec 1 ; 135 : 37 ± 46 . https://doi.org/10.1016/j.prevetmed. 2016 . 10 .021 PMID: 27931927
14. Di Nardo A , Candeloro L , Budke CM , Slater MR . Modeling the effect of sterilization rate on owned dog population size in central Italy . Preventive Veterinary Medicine . 2007 Dec 14 ; 82 ( 3 ): 308 ± 13 . https://doi. org/10.1016/j.prevetmed. 2007 . 06 .007 PMID: 17692414
15. Baquero OS , Akamine LA , Amaku M , Ferreira F. Defining priorities for dog population management through mathematical modeling . Preventive Veterinary Medicine . 2016 Jan 1 ; 123 : 121 ±7. https://doi. org/10.1016/j.prevetmed. 2015 . 11 .009 PMID: 26652574
16. Amaku M , Dias RA , Ferreira F. DinaÃmica populacional canina : potenciais efeitos de campanhas de esterilizacËão. Revista Panamericana de Salud Publica-pan American Journal of Public Health . 2009 ; 25 ( 4 ): 300 ± 4 . PMID: 19531317
17. Amaku M , Dias RA , Ferreira F . Dynamics and control of stray dog populations . Mathematical Population Studies. 2010 Apr 26 ; 17 ( 2 ): 69 ± 78 . https://doi.org/10.1080/08898481003689452
18. Totton SC , Wandeler AI , Zinsstag J , Bauch CT , Ribble CS , Rosatte RC , et al. Stray dog population demographics in Jodhpur, India following a population control/rabies vaccination program . Preventive Veterinary Medicine . 2010 Oct 1 ; 97 ( 1 ): 51 ±7. https://doi.org/10.1016/j.prevetmed. 2010 . 07 .009 PMID: 20696487
19. Yoak AJ , Reece JF , Gehrt SD , Hamilton IM . Optimizing free-roaming dog control programs using agent-based models . Ecological Modelling . 2016 Dec 10 ; 341 : 53 ± 61 .
20. Instituto Nacional de Estadistica, Geografia e Informatica. Censo general de poblacion y vivienda, 2010 . Mexico. 2010 .
21. International Companion Animal Management Coalition. Humane dog population management guidance . 2008 . Available from: http://www.icam-coalition.org/
22. Kustritz MR. Clinical canine and feline reproduction . Hoboken, NJ, USA: Wiley-Blackwell; 2010 .
23. Morales MA , Ibarra L. Fertilidad y mortalidad en la poblacion canina . Archivo de Medicina Veterinaria. 1979 ; 10 : 161 ± 64 .
24. Ibarra L , NuÂñez F , Cisternas P , MeÂndez P. DemografÂõa canina y felina en la Comuna de la Granja, Santiago, Chile . Avances en Ciencias Veterinarias . 1991 ; 6 ( 2 ).
25. Morales MA , Urcelay S , NuÂñez F , Cabello C. CaracterÂõsticas demograÂficas de una poblacioÂn canina rural en el aÂrea nororiente de la regioÂn metropolitana . Chile. Avances en Ciencias Veterinarias . 1992 ; 7 ( 1 ).
26. Ibarra L , Cisternas P , Valencia J , Morales MA . Indicadores poblacionales en caninos y felinos y existencias de otras especies domeÂsticas en la comuna de El Bosque , RegioÂn Metropolitana, Chile. Avances en Ciencias Veterinarias . 1997 ; 12 ( 2 ).
27. Kutzler MA , Yeager AE , Mohammed HO , Meyers-Wallen VN . Accuracy of canine parturition date prediction using fetal measurements obtained by ultrasonography . Theriogenology. 2003 Oct 15 ; 60 ( 7 ): 1309 ± 17 . https://doi.org/10.1016/ S0093 -691X( 03 ) 00146 - 8 PMID: 14511784
28. Fielding WJ . Determinants of the level of care provided for various types and sizes of dogs in New Providence, The Bahamas . The International Journal of Bahamian Studies. 2010 Oct 19 ; 16 : 63 ± 77 . https:// doi.org/10.15362/ijbs.v16i0. 119
29. Hoffman JM , Creevy KE , Promislow DE . Reproductive capability is associated with lifespan and cause of death in companion dogs . PloS One . 2013 Apr 17 ; 8 ( 4 ):e61082. https://doi.org/10.1371/journal.pone. 0061082 PMID: 23613790
30. Belo VS , Struchiner CJ , Werneck GL , Neto RG , Tonelli GB , de Carvalho JuÂnior CG , et al. Abundance, survival, recruitment and effectiveness of sterilization of free-roaming dogs: A capture and recapture study in Brazil . PLoS One . 2017 Nov 1 ; 12 ( 11 ):e0187233. https://doi.org/10.1371/journal.pone. 0187233 PMID: 29091961
31. Beck AM . The public health implications of urban dogs . American Journal of Public Health . 1975 Dec; 65 ( 12 ): 1315 ± 8 . PMID: 1200193
32. Salamanca CA , Polo LJ , Vargas J. SobrepoblacioÂn canina y felina: tendencias y nuevas perspectivas . Revista de la Facultad de Medicina Veterinaria y de Zootecnia. 2011 Apr; 58 ( 1 ): 45 ± 53 .
33. Boitani L , Ciucci P , Ortolani A . Behaviour and social ecology of free-ranging dogs . In: The Behavioural Biology of Dogs . CAB International, Wallingford, UK; 2007 . pp. 147 ± 165 .