Professional Documents
Culture Documents
Developing Countries:
The Benefits of
3 CHAPTER
Introduction
s a result of human popula- zoonotic diseases (Beck 2000; costly and more effective in rabies
55
dized neutering; and improve- programs seek to limit population view of animal welfare and public
ments in veterinary education to growth and improve dog welfare. health problems associated with
include early gonadectomy (Leney Widespread adoption of CNR pro- free-roaming dog populations and
2002). grams for dogs, along with changes strategies to resolve these prob-
More recently animal protection in human behavior and environ- lems. Placing CNR programs in the
organizations have launched cap- ment, offers a sustainable remedy context of earlier dog and rabies
ture, neuter, and return (CNR) pro- for both disease and animal welfare control methods, the chapter ex-
grams. Modeled on trap, neuter, problems posed by free-roaming plores CNR’s potential to over-
and release (TNR) programs for dogs in developing countries. come some of the shortcomings of
cats in the United States, these This chapter provides an over- earlier approaches and to improve
Table 1
Dog Populations in Developing Countries,
Number of Dogs per Hundred People
Country Dogs/100 People Source
All Urban Rural
Free-Roaming Dogs in Developing Countries: The Benefits of Capture, Neuter, and Return Programs 57
Joshi 1990). Researchers in stud- 23 percent suffered from Demodex their risk of predation (Matter and
ies around the world have con- canis (Rodriquez-Vivas et al. 2003). Daniels 2000). Because of high
firmed that at most 15 percent of In a rural community in South mortality rates, dog populations are
dogs may be inaccessible to vacci- Africa, 51 percent of the dogs had a skewed toward younger dogs. In the
nation (Cleaveland et al. 2006). serious clinical condition; of this Machakos District, Kenya, half of
Nonetheless, the majority of population 10 percent were acutely the dogs are less than one year old
dogs in developing countries face ill and half were chronically ill (Kitala et al. 2001).
few restrictions on their move- (Rautenbach, Boomker, and DeVil- Dogs receive little veterinary care
ments. In Machakos, Kenya, 69 liers 1991). Because of their unde- in developing countries, which con-
percent of dogs are never re- veloped immune systems, puppies tributes to the spread of disease and
stricted (Kitala et al. 2001). In the are particularly susceptible to dis- high mortality among dogs. Only
Thungsong District of Thailand, eases (Robinson 2000). Free-roam- 40.5 percent of households sur-
74 percent of dogs are allowed to ing dogs constantly face starvation, veyed in Zimbabwe said they would
roam freely (Kongkaew et al. malnutrition, and dehydration take their dogs to the veterinarian if
2004). In New Providence, Ba- (Matter and Daniels 2000; HSI they were ill; 12.8 percent would try
hamas, 73 percent of households 2001). Dogs also are poisoned, to cure their dogs with traditional
keep their dogs outside, and 43 harassed by people, and hit by vehi- medicine; and the remainder would
percent of households allow at cles (HSI 2001; Hargreaves 2002). seek no treatment (Butler 2000).
least one dog to roam (Fielding Dogs contract rabies. The length Dogs who are allowed to roam are
and Plumridge 2005). of time between a dog being even less likely to receive veterinary
While most dogs may depend on exposed to rabies and exhibiting care. Restricted adult dogs in New
a particular household or neigh- symptoms is two to eight weeks Providence are more likely to be
borhood, the resources provided at (Wandeler and Bingham 2000), at spayed than are those kept outside
“home” sites are often insufficient. which time he becomes aggressive (Fielding and Plumridge 2005). The
Most dogs roam to forage for food and seeks other animals to bite health of fenced dogs is much bet-
since they are not fed daily by own- (Wandeler and Bingham 2000). ter than that of free-roaming dogs,
ers (McCrindle et al. 1999; Kitala Dogs die from rabies within two to since the former are not exposed to
et al. 2001; Fielding, Mather, and three days from the onset of symp- fighting and communicable dis-
Isaacs 2005). Owners also allow toms. In addition to dog rabies eases (Fielding, Mather, and Isaacs
dogs loose because they believe deaths, the fear of rabies has re- 2005). In Thailand researchers
unrestricted dogs can better pro- sulted in the inhumane killing of found that dogs kept in the house
tect property (Fielding, Mather, dogs who are unfamiliar or who are are more likely to be vaccinated
and Isaacs 2005). suspected of having rabies (Cleave- than are those who are allowed to
land et al. 2006). roam freely (Kongkaew et al. 2004).
As a result free-roaming dogs Female dogs are less likely to be
The Welfare of have high rates of mortality. The life vaccinated, sterilized, or licensed
expectancy of dogs in Zimbabwe
Free-Roaming Dogs communal lands is 1.1 years (Butler
than are males. Only 15 percent of
male dogs—but no female dogs—in
Free-roaming dog populations suf-
2000); 71.7 percent of dogs died in the Machaskos District, Kenya, are
fer from extremely poor welfare.
their first year. Of households with sterilized (Kitala et al. 2001). Of
The New Providence, Bahamas, ani-
dogs in the Machakos District, male dogs 35 percent are vacci-
mal control unit’s visual inspection
Kenya, 67 percent reported that a nated, compared with only 20 per-
of dogs indicated that 70 percent
dog had died recently and a replace- cent of females. In Zimbabwe, only
are suffering from disease (Field-
ment was being sought (Kitala et al. 0.7 percent of females are spayed,
ing, Mather, and Isaacs 2005).
2001). In New Providence 35 per- compared with 16.3 percent of male
Echinococcus, toxocara, par-
cent of the dog population is lost dogs who are neutered (Butler
vovirus, heartworm, leptospirosis,
each year (Fielding and Plumridge 2000). In Bali only 11 percent of fe-
and venereal tumors are among the
2005). Of households surveyed in male dogs are neutered, compared
diseases that plague free-roaming
Bali, 31 percent had a dog die in the with 44 percent of males (Mar-
dogs (Boitsni et al. 1995; HSI
previous year. Very few dogs die of gawani and Robertson 1995). Ex-
2001; Fielding, Mather, and Isaacs
old age (Butler 2000); nutritional, ceptions to this trend are New Prov-
2005). Many dogs have infectious
parasite, and disease problems idence, where similar sterilization
skin diseases, such as mange, along
account for high mortality rates, rates are reported for female and
with secondary bacterial infections.
especially in puppies (Matter and male dogs (Fielding and Plumridge
A study in Mexico found that 34
Daniels 2000). Pups also are often 2005), and Thailand, where female
percent of stray dogs had mites and
left unattended, which increases dogs have a higher sterilization rate
Free-Roaming Dogs in Developing Countries: The Benefits of Capture, Neuter, and Return Programs 59
Tepsumetanon 1997). U.S. studies other parts of Asia, and 23,705 in they have increased in others. The
have found that younger dogs are Africa. rabies situation in Sri Lanka wors-
more likely to bite and their bites Eighty-four percent of rabies ened after the 2004 tsunami be-
are more severe (Wright 1991). deaths are in rural areas (WHO cause of increases in the number of
Male dogs are responsible for 2004). In India there are an esti- ownerless dogs (Dodet 2006). The
59–70 percent of bites (Wright mated 2.49 deaths per hundred Philippines also has seen an in-
1991). The rabies virus is more thousand people in rural areas, crease in rabies deaths (WHO
prevalent in male dogs, and the sex compared with 0.37 deaths per 2004).
of the dog is identified as a risk fac- hundred thousand people in urban Difficulties in controlling the
tor in Bolivia (Widdowson et al. areas. In Africa there are 3.60 spread of rabies have been associ-
2000). Differences in bite rates and deaths per hundred thousand in ated with the migration of people
rabies fatalities between female rural areas, compared with 2.00 and dogs from infected areas.
and male dogs likely stem from the per hundred thousand in urban WHO (2004) attributes the spread
fact that canine aggression is hor- areas (Knobel et al. 2005). of rabies to the growth of dog pop-
monally related (Lockwood 1995). Poverty is also associated with ulations in sub-Saharan Africa
Unneutered males have particularly rabies vulnerability. An Indian sur- associated with human population
high bite rates (Lockwood 1995). vey involving twenty-one medical growth and movement. Movement
A study of medical records at colleges found that 87.6 percent of of infected animals into new areas
Centro de Salud in Mexico found adults who died of rabies between produces outbreaks (Rupprecht,
that 65 percent of bite victims 1992 and 2001 were poor (Sudar- Hanlon, and Hemachudha 2002).
were bitten at their residence, 32 shan 2005). The risk of canine
percent in public locations, and 2 rabies in Mexico is greater in lower- Other Canine-
percent at their workplace (Eng et income areas (Eng et al. 1993). Transmitted Diseases
al. 1993). Nolan (2006) noted that Poor children also face great risk. Free-roaming dogs are associated
domestic dogs cause more serious Children under the age of fifteen with a variety of other bacterial,
bites than do feral dogs. These comprise 40–60 percent of rabies viral, and parasitic infections that
data confirm U.S. studies that have victims (WHO 2001). Half of the may pose a risk to humans.
found that dogs owned by neigh- world’s malnourished children live Echinococcosis and toxocariasis are
bors have the highest victim rate in rabies-endemic areas (Sampath among the most prevalent of these
and that bites by stray dogs are et al. 2005). health hazards (Chomel and Arzt
over-reported (Beck 2000). At the same time, rabies is 100 2000; Overgaauw and van Knapen
Some estimate that only 3 percent percent preventable for both hu- 2000) and often occur in low-
of rabies deaths are reported in de- mans and dogs. Deaths occur when income areas (Rubel et al. 2003).
veloping countries (Knobel et al. dog bites go unreported, unrecog- Echinococcosis (hydatid disease)
2005). Rabies is underreported be- nized, untreated, or are discovered is a common parasitic infection in
cause patients seek treatment from too late (WHO 2001). The lack of dogs in developing countries that
traditional healers, causes of death awareness about rabies among the results from improper livestock
are often not reported to central public, health practitioners, and slaughter practices (Jiminez et al.
authorities, and rabies may be unrec- authorities; the shortage of rabies 2002; Seimenis 2003; Reece 2005).
ognizable to medical staff without immunoglobulins and funding for Sheep, goats, camels, cattle, pigs,
laboratory confirmation (Cleaveland modern vaccine; and the lack of pri- and horses serve as intermediate
et al. 2002). An Indian household ority given to canine rabies control hosts (Meslin et al. 2000). Dogs con-
survey found that only 36.4 percent have undermined rabies-prevention tract echinococcosis by consuming
of residents said they would visit a efforts (Dodet 2006). the offal of infected livestock near
doctor if they were bitten by a dog As a result of improvements in slaughterhouses or areas of home
(Singh and Choudary 2005). postexposure treatment (Mitmoon- slaughter. Young dogs (ages three to
To compensate for underreport- pitak, Wilde, and Tepsumetanon twenty-five months) and female
ing of rabies, some researchers use 1997), rabies deaths did decline in dogs are more likely to be infected
dog bite statistics to predict num- the 1980s and 1990s. Ten million with echinococcosis (Moro et al.
bers of rabies deaths. Using a dog- people currently receive postexpo- 2005). In endemic areas, 1–40 per-
bite probability model, 55,270 sure treatment each year (WHO cent of cattle, 1–80 percent of
deaths per year or 1.38 deaths per 2002). Predicted deaths worldwide sheep, and 0.2–50 percent of dogs
hundred thousand people are pre- without postexposure treatment may be infected (Meslin et al. 2000).
dicted (Knobel et al. 2005). These would be 327,160 (Knobel et al. The disease spreads to humans
fatalities include 19,713 deaths in 2005). While rabies cases have de- through ingestion of dog feces. In
India, 2,336 in China, 9,489 in clined in some areas of the world, humans the disease develops in the
Free-Roaming Dogs in Developing Countries: The Benefits of Capture, Neuter, and Return Programs 61
challenged on both ethical and effi- 1990). Capture and kill programs reductions in vaccine costs, intra-
ciency grounds. Mass removal remove vaccinated dogs from the dermal regimens, and administra-
strategies have been criticized population who are then replaced tion of immunoglobulin at injec-
because they fail to discriminate by unvaccinated dogs (Cleaveland tion locations, all have resulted in
between owned and stray dogs and et al. 2006). According to Cleave- some progress in rabies prevention
use cruel methods of removal. land et al. (2006, 45), in Asia (WHO 2001; Wilde, Khaw-
Dogs frequently are captured using Dog elimination programmes, plod, and Khamoltham 2005; and
nooses and chains, kept in vehicles may, in fact, be counter-pro- Lumlertdacha et al. 2006). The
without food and water for hours ductive and reduce the propor- shift in most countries from the
or days, then electrocuted, gassed, tion of immunized individuals Semple vaccine (a vaccine, pre-
or drowned (Reece 2005). in a population, because some pared in the brains of adult sheep,
Fo r e x a m p l e , c u l l s o f d o g s vaccinated dogs are killed and that induces severe and long-term
occurred in China 2003–2006 in community response to dog side effects such as allergic en-
response to increases in rabies elimination campaigns is gen- cephalomyelitis) to cell culture
deaths. China has the second high- erally to buy new puppies or vaccine also has improved treat-
est rate of death and illness from adopt free-roaming (unvacci- ment (WHO 2004). To further re-
rabies in the world. From 2001 to nated) dogs. duce rabies risks, preexposure vac-
2004, the number of rabies deaths Capture and kill programs do lit- cination is now recommended for
more than tripled, from 854 to tle to reduce the size of dog popu- at-risk groups such as young chil-
2651 (Tang et al. 2005). lations. Lethal dog population dren and people who work with ani-
The upsurge in rabies deaths in control strategies require the elim- mals (WHO 2001; Wilde, Khaw-
China has been attributed to in- ination of 50–80 percent of dogs a plod, and Khamoltham 2005;
creases in dog populations, an year (WHO 1989), which is neither Dodet 2006).
extremely low rabies vaccination financially possible nor ethically However, progress in rabies pre-
rate of only 3 percent, and inade- acceptable in most countries (Rup- vention is at a standstill; no new
quate postexposure treatment precht, Hanlon, and Hemachudha Asian countr y has eradicated
(Tang et al. 2005; Zhang et al. 2002). Most catch and kill pro- rabies in recent decades (Wilde,
2005). With a dog-human ratio of grams remove only 3–5 percent of Khawplod, and Khamoltham 2005).
1:9, the dog population in China dogs per year (Bogel and Meslin Canine rabies remains endemic in
has grown to between 80 and 200 1990). While WHO initially sup- India, Pakistan, Vietnam, Thailand,
million (Tang et al. 2005). In the ported the culling of stray dogs, it the Philippines, and most Afri-
four southwestern provinces with now concedes that removal of dogs can countries.
most of the recent rabies cases, 70 does not significantly reduce dog
percent of households have one or populations or the spread of rabies Canine Rabies
more dogs (Zhang et al. 2005). In (WHO 2001). Vaccination Campaigns
China dogs are the vectors in The culling of dogs also gener- Most experts agree that dog-vacci-
85–95 percent of rabies cases. ates hostility toward dog-control nation campaigns are a more cost-
In 2006 in southwestern China, officials, which undermines coop- effective approach to rabies pre-
government officials killed 50,000 eration with rabies canine vaccina- vention than is postexposure
dogs in five days in one province tion efforts (Cleaveland et al. treatment alone (Cleaveland 1998;
in an effort to end a rabies out- 2006). In addition, killing of stray Kitala et al. 2001, 2003; Wilde,
break. Dogs who were not killed dogs negatively affects tourism Khawplod, and Khamoltham
by their owners as ordered by the (Leney and Remfry 2000). 2005). Canine-vaccination pro-
government were beaten to death. grams cost 25–56 percent of pos-
Both vaccinated and unvaccinated Postexposure texposure treatments (Bogel and
and owned and unowned dogs Rabies Treatment Meslin 1990). According to WHO
were killed. The number of people receiving (2001, 4),
Rather than reducing rabies postexposure treatment has in- Rabies control in dogs remains
risk, the culling of dogs in coun- creased dramatically over the past the only long-term, cost-effec-
tries increases population turnover decade. For example, the number tive means of eliminating or
and movement, which, in turn, of people who received postexpo- preventing most human cases.
facilitate disease transmission. Fol- sure treatment in Thailand Human public health preven-
lowing the elimination of dogs, climbed from 93,641 in 1991 to tive measures should be paral-
new dogs repopulate the areas 350,535 in 2001 (Lumlertdacha et leled by programmes for dog
through compensatory breeding al. 2006). Improved public aware- rabies control.
and migration (Bogel and Meslin ness of the need for treatment,
Free-Roaming Dogs in Developing Countries: The Benefits of Capture, Neuter, and Return Programs 63
tional strategy to increase vaccina- Wilde, Khawplod, and Khamoltham will improve vaccination coverage.
tion coverage (Cleaveland 1998; 2005; Bauhloul et al. 2006; Cleave- In Mexico puppies are vaccinated at
WHO 2004; Denduangboripant et land et al. 2006). Few dogs live one month as a part of rabies-con-
al. 2005). Trials of this drug, devel- long enough for booster vaccina- trol efforts (WHO 1998a).
oped initially to control rabies in tions (Mitmoonpitak 1997). Subse- While researchers identify mass
wild animal populations, were as of quent migration of unvaccinated canine rabies vaccination as the
2006 underway on bait delivery, dogs to areas from which dogs have most effective and affordable
safety for target and nontarget ani- been removed further reduces vac- rabies-control strategy, they
mals, safety for dogs under ten cination coverage. acknowledge that vaccination cam-
weeks, and possible virus excretion Other barriers to dog vaccination paigns often are not adequate to
in dog saliva (WHO 1998a,b). include lack of sustainable human maintain a 70–75 percent vaccina-
Results that far showed no adverse and financial resources, inaccessi- tion coverage because of the high
effects on target or nontarget bility of a large fraction of dogs, turnover of dogs (Kitala et al.
species (WHO 2004). Making baits low-quality and high-cost vaccine, 2001). However, many reports on
available to owners in central loca- lack of public awareness or collabo- mass rabies vaccination and dog
tions, placing baits in select loca- ration among agriculture and population issues in Africa ignore
tions, door-to-door delivery, and health departments, poor immune (Dodet 2006) or dismiss (Kitala et
giving baits to dogs in the street response, and movement of human al. 2001) sterilization, particularly
have been suggested as oral vac- and dog populations (Perry et al. of female dogs. According to Kitala
cine distribution strategies (Cleave- 1995; Cleaveland 1998; WHO et al. (2001, 228), “The spaying of
land 1998; WHO 1998; Wandeler 2001; Adeyemi et al. 2005; bitches is a specialized feature and
and Bingham 2000). WHO (2001) Bauhloul et al. 2006; Lodmell et conceivably out of reach for most
has endorsed oral immunization al. 2006; Lumlertdacha et al. 2006). rural poor.” However, with the help
for dogs. To achieve and maintain ade- of international animal protection
Despite widespread agreement quate vaccination coverage, suc- organizations, sterilization com-
about the ineffectiveness of stray cessive vaccination campaigns are bined with vaccination has been
dog removal to control rabies necessary. Mass vaccination cam- instituted in some communities
transmission and limit population paigns need an initial two-year with very interesting outcomes.
growth, some countries such as Sri phase to achieve 75 percent cover-
Lanka have continued to combine age (Bogel and Meslin 1990).
mass vaccination campaigns with Annual vaccination of 50 percent Capture, Neuter,
removal of dogs. Because of their
perceived inaccessibility for par-
of dogs for four years is necessary
to consolidate the 75 percent cov-
and Return/
enteral vaccination, stray dogs are erage, along with surveillance and Release
eliminated by capture and killing vaccination at borders and points
in mobile vehicles with gas cham- of entry for international travelers. Public Health and
bers (Matter et al. 2000). As a part Some researchers suggest that vac- Animal Welfare Benefits
of the immunization campaign in cination campaigns should be con- Mass vaccination campaigns and im-
Sri Lanka, twelve vaccination ducted every six to eight months provements in postexposure treat-
points were set up (Matter et al. because of high population turn- ment have significantly reduced dog
2000). The campaign was an- over (Cleaveland 1998). WHO and human rabies cases. Vaccination
nounced through posters and a (2004) also supports more fre- campaigns also have demonstrated
loudspeaker on a vehicle, and sta- quent vaccination campaigns community support for dog treat-
pled collars made it possible to where population turnover is par- ment programs, the accessibility of
identify vaccinated dogs by geo- ticularly high. free-roaming dogs for vaccination
graphic area. Dogs under three Excluding young puppies from and other treatments, and impor-
months were excluded from the vaccination programs is another tant techniques for reaching dogs.
campaign. In Sri Lanka 492,000 obstacle to rabies prevention. Capture, neuter, and return/release
dogs are vaccinated annually, but Despite the fact that young dogs are (CNR) programs directly confront
coverage remains below 70 percent most involved in rabies transmis- the problem of high turnover of dog
(WHO 1996; Matter et al. 2000). sion, puppies under three months populations, which mitigates against
High population turnover for are rarely vaccinated during cam- extensive rabies vaccination cover-
dogs as a result of dog removal and paigns. Perry (1995), Cleaveland age and dog population control.
mortality undermines the success (1998), WHO (2004), and Bauhloul CNR programs have as their goal
of mass vaccination programs et al. (2006) maintain that includ- the stabilization—not elimina-
(Cleaveland 1998; WHO 2001; ing puppies under three months tion—of street dog populations and
Free-Roaming Dogs in Developing Countries: The Benefits of Capture, Neuter, and Return Programs 65
patrick, personal communication dogs. Spayed female dogs in one use of local and visiting veterinari-
with A.N.R., n.d. 2005). study gained an additional year over ans, target populations, and sterili-
Dogs derive other health bene- intact female dogs (Michell 1998). zation levels. Table 3 provides an
fits from sterilization in addition to In this study, longevity differences overview of selected CNR programs.
fewer pregnancies. Spayed and between neutered and intact male
neutered dogs do not face the risk dogs were insignificant. However, India
of ovarian, mammary, and prostate another study found removal of With an estimated population of
diseases and disorders (Kustritz testis increases the life expectancy twenty-four million dogs, India has
2002). Cancer is less likely in both of male dogs (Waters, Shen, and been the site of pioneering CNR
female and male dogs after sterili- Glickman 2000). Neutered dogs in programs. ABC (Animal Birth Con-
zation (Michell 1998, 1999). The New Providence, The Bahamas, trol) programs were introduced fol-
cancer risk of female dogs who were found to live longer than did lowing WHO and WSPA’s publica-
have been spayed declines even intact dogs as a result of a reduc- tion of Guidelines for Dog Man-
more significantly than it does for tion in sexually transmitted dis- agement, which addressed the inef-
male dogs. Castration reduces the eases, exposure to disease, and fectiveness of capture and kill as a
duration of chronic bacterial pro- stress of mating and fighting (Field- dog-control strategy. According to
statitis infection in male dogs ing, Mather, and Isaacs 2005). WHO (2004, 54), the goal of ABC
(Cowan et al. 1991). In addition, CNR programs also have the programs is to “reduce dog popula-
all CNR programs provide a range capacity to produce behavioral tion turnover as well as the number
of treatments for parasites, nutri- changes in dogs that limit bite and of dogs susceptible to rabies and
tional deficiencies, and other disease risk. In TNR programs limit aspects of male dog behavior
health problems as well as vaccina- caretakers report that feral cats (such as dispersal and fighting) that
tion and sterilization. were friendlier, less aggressive, and facilitate the spread of rabies.”
Several studies have examined less likely to roam after they were ABC programs in India were
the relative benefits of early gonad- sterilized (Scott et al. 2002). Ster- launched in response to the use of
ectomy. Comparing spay and neuter ilization also reduces roaming and strychnine poisoning and electro-
for shelter dogs at twelve weeks, aggressive behavior in male dogs cution as the dominant animal-con-
twelve to twenty-three weeks, and (Lockwood 1995). Fewer escaping trol strategies (Help in Suffering
more than twenty-four weeks of age, behaviors have been reported after 2003). In 1992 New Delhi’s court
Howe (1997) found fewer minor gonadectomy (Spain, Scarlett, and required that ABC programs re-
complications for earlier proce- Houpt 2004). Fewer females in place cruel and ineffective methods
dures and no difference in major heat also reduces fighting and of dog control (Help in Suffering
complications. Another study con- pack formation (Help in Suffering 2003). A pilot program by Help in
cluded that the benefits of early 2003; Nolan 2006). For 60 percent Suffering (HIS) in 1994 and 1995
gonadectomy outweigh the risks of dogs in one study, castration demonstrated the effectiveness of
(Spain, Scarlett, and Houpt 2004). reduced urine marking, roaming, CNR in several Jaipur districts. The
While some researchers have sug- and mounting, and one-third of program then expanded to all of
gested that urinary incontinence dogs showed significant decreases Jaipur. ABC programs have begun
may result from ovariohysterectomy in aggressive behavior (Neilson, i n B o m b a y, D e l h i , C a l c u t t a ,
(Holt and Thrusfield 1993), other Eckstein, and Hart 1997). Madras, Bangalore, Hyderabad,
studies have revealed that urinary Uidapur, and Jodhpur. The Jaipur
incontinence is less frequent in program has developed new tech-
dogs who undergo the procedure CNR Programs niques for counting street dogs and
before first estrus than those who Despite CNR’s promise, it has been for the capture and return of such
do after first estrus (Kustritz 2002). introduced only in India, Thailand, dogs (Help in Suffering 2003).
Salmeri et al. (1991) saw little dif- island areas, and a handful of other For the ABC program, HIS (2003)
ference in health outcomes for spay countries. In many of these coun- selects an area of the district, subdi-
and neuter at seven weeks versus tries, CNR programs were launched vides the district, and establishes a
seven months, although they found in direct response to threatened or quota for the number of dogs to be
more growth plate closure delayed actual mass killings of dogs by gov- captured in each area. Before work-
in early-neutered dogs that they did ernment officials in attempts to re- ing in the area, HIS informs people
in intact dogs. duce populations and decrease about the ABC program, what will
As a result of improved body con- rabies transmission. Some CNR pro- be done to the dogs, and the bene-
dition and diminished susceptibility grams operate from fixed clinics, fits of the program. Staff then travel
to disease, sterilized dogs enjoy others depend on mobile clinics. through the areas capturing as
longer life spans than do intact The programs vary in their duration, many female adult dogs and older
Abaco Fixed Local 540 dogs and cats N/A No HSI (2001);
(February 2000– 432 dogs (75 percent) Hargreaves (2002)
October 2000) 108 cats (25 percent)
4–6 days per clinic Dogs (59 percent female,
8 clinics 41 percent male)
Galapagos Islands Mobile Visiting 2,601 dogs N/A Yes Animal Balance
(May 2004–May 2005) and cats (2005, 2006)
Isabela Island—6 weeks
Santa Cruz—3 weeks
San Cristobal—4 weeks
All three islands—
9 additional days
Sri Lanka Mobile Visiting 1,833 dogs 70–90 percent No Peacock (2005b)
(January–May 2005) (34 percent female,
13 sites 66 percent male)
81 days in field
puppies of both sexes as possible. withheld from them overnight. brought into the shelter are eutha-
With the exception of puppies, male Anesthetized female dogs are nized because they are terminally
dogs are excluded from the pro- spayed using the keyhole flank ill, badly injured, too aggressive, or
gram. Sterilization of female dogs is procedure, with the exception of suspected of being rabid or having
seen as more cost-effective, since heavily pregnant dogs on whom a come in contact with another
one male dog can impregnate mul- midline spaying procedure is per- rabid dog.
tiple females. In addition, there is a formed. Anesthetized male dogs HIS (2003) has sterilized and
belief that intact male dogs are are castrated. All dogs are vacci- vaccinated 68 percent of the dogs
more territorial, which will prevent nated and identified with individu- in the population and has per-
immigration of new dogs into terri- alized tattoos and an earmark. formed more than twenty-three
tories (Nolan 2006). Puppies under After surgery a veterinarian deter- thousand spay-and-neuter proce-
three months also are not captured. mines which dogs are ready for dures. While there has been some
Dogs are captured in the early release and which need to stay opposition to the capture of dogs
mornings and early evenings by longer. The average release time is and to their return, the program
hand or with sacks and hoops. Staff 3.79 days for females and 3.25 generally enjoys widespread public
receive incentives to encourage days for males. The dogs are then support (Nolan 2006). In her eval-
high catch rates and capture of sick returned to the areas where they uation of the Jaipur program, No-
dogs beyond their quotas. The dogs were captured. Two dogs are re- lan (2006, n.p.) observes, “Surgi-
are then transported to the clinic. leased at a time to minimize prob- cal spay and neutering of dogs
At the clinics the dogs rest for lems among the dogs and between appeared [to be] well accepted.
twelve to twenty-four hours (Help the dogs and the public. Approxi- Human population control and
in Suffering 2003), and food is mately 10 percent of the dogs health care campaigns may have
Free-Roaming Dogs in Developing Countries: The Benefits of Capture, Neuter, and Return Programs 67
helped raise awareness of this
concept.” Figure 2
WSPA also evaluated the Jaipur
program recently. WSPA found that,
Number of Rabies Deaths in
while there was a relatively rapid Chennai, India, 1996–2003
increase in the proportion of females
Chennai Citywide ABC/Started Sept. ’96
sterilized (10–60 percent over the 140
first three years), the increase over 120
Free-Roaming Dogs in Developing Countries: The The Benefits of Capture, Neuter, and Return Programs 69
Veterinary education and train- Cristobal Island in 2005, along Field clinics sterilized and vacci-
ing have been a major focus of with another week-long clinic on nated an estimated 70–90 percent
YYS’s work. WSPA initially trained Santa Cruz Island. In 2006 simul- of the dog population at each site.
staff in spay procedures using a taneous campaigns were held on In total 1,430 dogs were treated
spay hook (Listriani 2002). Since all three islands for nine days. between January and May 2005
then YYS’s fixed clinic has become Through these campaigns Animal (Peacock 2005b). The program
a teaching facility for local veteri- Balance has sterilized 2,601 dogs developed strong community sup-
narians and veterinary students. and cats. After 2007 municipal port, helped improve attitudes
Regular seminars are held in con- administrators were to assume re- toward animal welfare, and in-
junction with the Indonesia Veteri- sponsibility for the project. creased appreciation of the need
nary Association, and YYS offers The program has faced two for veterinary services (HSI 2006).
internships for veterinary students recent challenges. Animal Balance
and hosts visiting veterinarians (2006) is working with quarantine
from other countries. YYS also officials to contend with importa- The Success of
runs “kindness” classes for chil- tion of purebred dogs to the
dren and undertakes other public islands, which could compromise
CNR: Outcomes,
education efforts. vaccination and sterilization cover- Ingredients, and
To stop the poisoning of dogs age. The organization also forged a
and cats by the Galapagos National compromise in response to the de-
Constraints
CNR programs have been able to
Park Service (GNPS), Animal Bal- mand for puppies on San Cristobal
stabilize and, in some cases,
ance introduced CNR to the Gala- Island. Previously hunters had
reduce free-roaming dog popula-
pagos Islands (Animal Balance refused to have their dogs steril-
tions. The ABC program in Jaipur
2005, 2006). The local govern- ized. Animal Balance agreed to res-
achieved an initial population
ment provided clinic space, and cue and make available for adop-
reduction of 28 percent (Help in
municipal representatives did an tion excess puppies that otherwise
Suffering 2003). In Abaco 50–75
initial door-to-door survey to in- would be killed by hunters.
percent fewer dogs were seen
form residents about the upcom- CNR programs also have been
roaming the streets after Project
ing spay-and-neuter program. A list implemented in rapid response to
Potcake than during the year
of interested residents was given natural disasters that precipitate
before the program (Hargreaves
to Animal Balance, which then fear of rabies. After the huge
2002), and the number of dog
invited people to bring their dogs tsunami in 2004, the Sri Lankan
roadkills declined significantly.
and cats to the clinic, and GNPS military threatened to eradicate
Few litters of pups and pregnant or
provided vehicles to transport the street dogs to prevent rabies out-
nursing potcakes were observed
animals. Additional door-to-door breaks (HSI 2005a,b,c). The tsu-
(HSI 2001; Hargreaves 2002). With
canvassing covered every house on nami had displaced community
the YYS program, the overall dog
several of the islands to encourage dogs from familiar neighborhoods,
to human population ratio in Bali
participation. Radio commercials making it difficult for them to
declined from 1:5.6 to 1:5.2 (Pea-
publicized the program and pro- locate food and shelter. Sri Lankan
cock 2005a). The population of
vided public education on dog officials agreed to suspend plans
dogs in targeted villages in Bali was
care. Dog training and school- for shooting and poisoning dogs
reduced by over half when 75 per-
based humane education programs after HSI made a commitment to
cent of the village dogs were
also supplemented the treatment launch a CNR program to vacci-
spayed or neutered. The popula-
of dogs and cats. nate and sterilize free-roaming
tion of puppies in these areas has
Before the Animal Balance pro- dogs. Working with a Sri Lankan
decreased from 32 percent to 25
gram, no veterinary services were animal hospital, veterinarians and
percent. In the Galapagos Islands,
available on the islands for dogs other volunteers from HSI, YYS,
Animal Balance (2006) anticipated
and cats. Clinic equipment was and The Humane Society of the
pet populations would be stabilized
brought to the Galapagos, and vol- United States’ Rural Area Veteri-
on Isabela, San Cristobal, and
unteer veterinarians from abroad nary Services set up thirteen suc-
Santa Cruz islands by 2007.
were recruited to perform surger- cessive field clinics across the
Another measure of CNR success
ies in the clinics. Animal Balance country. In addition to capturing,
is reduction in canine rabies trans-
had run seven campaigns by 2006. vaccinating, neutering, and return-
mission. In Jaipur the ABC pro-
In 2004 initial clinics were held on ing community dogs, the field clin-
gram has been associated with a
Isabela Island for six weeks and on ics encouraged owners to bring in
significant decrease in rabies
Santa Cruz Island for two weeks. A their pets.
cases. In 2002 and 2003, no rabies
four-week clinic was held on San
Free-Roaming Dogs in Developing Countries: The Benefits of Capture, Neuter, and Return Programs 71
diminishes as the distance from vac- At these more isolated sites, risks more useful. Immunocontracep-
cination points increases (Matter et of migration or introduction of tives need to be administered annu-
al. 2000). Owner inability to handle infected or unsterilized dogs were ally or every two years, which pres-
animals is another obstacle to par- minimal. In contrast, the size of ents a major logistical problem in
ticipation in clinics that could be Thailand and India and territorial developing countries. Although
ameliorated through transportation borders make the integration of some have suggested that the PZP
of dogs (Matter et al. 2000). To new dogs more likely to occur and immunocontraceptive could lead
reach the maximum number of harder to manage. The failure of to sterilization of dogs (Fayrer-
dogs possible, dogs must be recent CNR programs in Thailand Hosken, Dookwah, and Brandon
brought to clinics for spay-and- makes clear this threat to main- 2000), the data are not strong, and
neuter procedures, or the clinics taining both vaccination and steril- no one has shown conclusively that
must be brought to the dogs. ization thresholds. As Thailand PZP is effective in any canid even as
Attitudinal surveys conducted studies of the distribution of differ- an immunocontraceptive.
around CNR and vaccination pro- ent rabies virus strains confirm, The difficulty of monitoring dogs
grams reveal some of the obstacles dog populations move with human after surgery in a field setting is yet
to convincing owners to seek care populations. CNR programs need another concern. WSPA tradition-
for their dogs. Overall, residents to address these population shifts ally only favors CNR as a short-
are supportive of spay-and-neuter of humans and dogs to maintain term strategy when dogs can be
programs because they want to stable dog populations and to monitored for health and welfare,
avoid the animals’ having litters achieve ongoing population reduc- the environment can support free-
(HSI 2001). However, in Abaco, for tions. “Immunization belts” and roaming dogs, and government
example, some owners did not have “sterilization belts” at borders of and public support guarantees ani-
their dogs neutered because of the CNR program areas, as well as mal safety (Leney 2002; WSPA
young age of the dog, they had revaccination campaigns, are im- 2006). In her research on gonadec-
missed a previous clinic, or they portant to maintain population tomy, Howe (1997) found greater
did not want to sterilize male or stabilization and vaccination cov- risks after sterilization the shorter
purebred dogs (HSI 2001; Field- erage. Another threat to CNR the postsurgical holding period in
ing, Samuels, and Mather 2002). progress in Thailand and elsewhere U.S. shelters. CNR programs
Older owners are more likely than is the continued capturing and/or vary in the amount of time they
are younger ones to have their killing of dogs, which further en- keep dogs before and after proce-
dogs spayed (Fielding, Samuels, courages movement and increased dures. In Jaipur dogs usually spend
and Mather 2002). Owners often breeding among the remaining the night at the clinic before sur-
let females have one litter before intact animals. gery and are generally not released
spaying (Fielding and Plumridge Researchers have greeted sterili- until three to five days after the
2005). In Africa the desire for zation programs in general and operation (Nolan 2006). In Abaco,
more guard dogs may outweigh CNR programs in particular with Bali, Sri Lanka, and the Galapagos,
concerns about overpopulation. some initial skepticism. While most surgery was performed immedi-
Owned dogs clearly play an experts agree that control of repro- ately, and the dogs were returned
important role in maintaining or duction may help in rabies preven- to their territories after relatively
increasing population levels of free- tion and with other problems asso- short (same-day) recovery times.
roaming dogs. Study after study has ciated with free-roaming dogs, In addition to logistical, resource,
found that ownerless dogs who do some do not believe these pro- and medical concerns, postsurgical
not depend on humans have low grams are sustainable, affordable, release time has competing animal
reproductive rates and cannot or sufficient (WHO 1989; Wilde, welfare implications (Nolan 2006).
maintain their population levels Khawplod, and Khamoltham 2005). On the one hand, keeping dogs
without new recruits. New recruit Many of the concerns over the longer can avoid postoperation
dogs come from the owned popula- cost and ability of CNR to reach suf- complications. On the other hand,
tion whose members are allowed to ficient numbers of dogs could be returning dogs sooner reduces
roam freely and are not sterilized. addressed with the availability of an stress to the animals and permits
Door-to-door canvassing and other antifertility vaccine (Leney and sterilization of more animals.
strategies to incorporate owned Remfry 2000; Wheir, Dunbar, and Another obstacle to CNR and
dogs are central to the overall suc- Prasad 2005). Immunocontracep- dog-vaccination programs has
cess of CNR. tive vaccines provide a possible fer- been the lack of a single govern-
CNR success in Abaco, Bali, Sri tility-control approach for many mental department to claim re-
Lanka, and the Galapagos has been species of animals, although an sponsibility and adequate re-
enhanced by their island locations. immunosterilant would be much sources for these programs (WHO
Free-Roaming Dogs in Developing Countries: The Benefits of Capture, Neuter, and Return Programs 73
Cardwell, D. 1993. Pros and cons www.animalpeoplenews.org/ Eng, T., H., Fishbein, H. Talamante,
associated with early-age neuter- 02/10/streetdog.feral1002.html. D. Hall, G. Chavez, J. Dobbins, F.
ing. Journal of the American Cohen, H., E. Paolillo, R. Bonifacino, Moro, J. Busto, M. de los Angeles
Veterinary Medical Association B. Botta, L. Parada, P. Cabrera, K. Ricardy, A. Munguia, J. Carrasco,
202(11): 1788–1789. Snowden, R. Gasser, R. Tessier, L. A. Robles, and G. Baer. 1993.
Centonze, L., and J. Levy. 2002. Dibarboure, H. Wen, J.C. Allan, Urban epizootic of rabies in Mex-
Characteristics of free-roaming H.S. De Alfaro, M.T. Rogan, and ico: Epidemiology and impact of
cats and their caretakers. Jour- P.S. Craig. 1998. Human cystic animal bite injuries. Bulletin of
nal of the American Veterinary echinococcosis in a Uruguayan the World Health Organization
Medical Association 220(11): community: A sonographic, sero- 71(5): 615–624.
1627–1633. logic, and epidemiologic study. Fayrer-Hosken, R.A., H. Dookwah,
Childs, J., L. Robinson, R. Sadek, American Journal of Tropical and C. Brandon. 2000. Immuno-
A. Madder, M.E. Miranda, and N. Medicine and Hygiene 59(4): control in dogs. Animal Repro-
Miranda, N. 1998. Density esti- 620–627. duction Science 60–61:
mates of rural dog populations Coleman, P., and C. Dye. 1996. 365–373.
and an assessment of marking Immunization coverage required Fielding, W., and S. Plumridge.
methods during a rabies vaccina- to prevent outbreaks of dog 2005. Characteristics of owned
tion campaign in the Philip- rabies. Vaccine 14(3): 185–186. dogs on the Island of New Provi-
pines. Preventive Veterinary Cowan, L., J. Barsanti, W. Crowell, dence, the Bahamas. Journal of
Medicine 33: 207–218. and J. Brown. 1991. Effects of Applied Animal Welfare Science
Chomel, B., and J. Arzt. 2000. Dogs castration on chronic bacterial 8(4): 245–260.
and bacterial zoonoses. In Dogs, prostatitis in dogs. Journal of Fielding, W., J. Mather, and
zoonoses, and public health, ed. the American Veterinary Med- M. Isaacs. 2005. Potcakes: Dog
C. Macpherson, F. Meslin, and A. ical Association 199: 346–350. ownership in New Providence,
Wandeler, 91–122. New York: Coyne, M., J. Burr, T. Yule, M. Hard- the Bahamas. W. Lafayette, Ind.:
CABI Publishing. ing, D. Tresnan, and D. McGavin. Purdue University Press.
Cleaveland, S. 1998. Epidemiology 2001. Duration of immunity in Fielding, W., D. Samuels, and J.
and control of rabies: The grow- dogs after vaccination or natu- Mather. 2002. Attitudes and
ing problem of rabies in Africa. rally acquired infection. Veteri- actions of West Indian dog owners
Transactions of the Royal Soci- nary Record 149: 509–515. towards neutering their animals.
ety of Tropical Medicine and Dahmer, T. 2002. Feral/stray dogs Anthrozoös 15(3): 206–226.
Hygiene 92: 131–134. and civet mortality on Kau Hargreaves, K. 2002. Spay Neuter
Cleaveland, S., E. Ferve, M. Kaare, Sai Chau, 2001–2002. Porcu- Incentive Program (SNIP).
and P. Coleman. 2002. Estimat- pine! Number 27. www.hku. Presented at “Challenges of
ing human rabies mortality in hk/ecology/porcupine/por27 Animal Protection on Island
the United Republic of Tanzania pdf/por27-p07-11.pdf. Nations With Special Emphasis
from dog bite injuries. Bulletin DeBalogh, K., A. Wandeler, and F. on Dogs and Cats.” April 2.
of the World Health Organiza- Meslin. 1993. A dog ecology Miami Beach, Florida.
tion 80: 304–310. study in urban and semi-rural Haupt, W. 1999. Rabies—Risk of
Cleaveland, S., M. Kaare, D. Kno- areas of Zambia. Oder- exposure and current trends in
bel, and M.K. Laurenson. 2006. stepoort Journal of Veterinary prevention of human cases. Vac-
Canine vaccination—Providing Research 60(4): 437–443. cine 17: 1742–1749.
broader benefits for disease con- Denduangboripant, J., S. Wachara- Help in Suffering. 2003. The Ani-
trol. Veterinary Microbiology pluesadee, B. Lumlertdacha, N. mal Birth Control Programme
117(1): 43–50. Ruankaew, W. Hoonsuwan, A. Help in Suffering, Jaipur: A
Cleaveland, S., M. Kaare, P. Tiringa, Puanghat, and T. Hemachudha. report of the background, meth-
T. Melengeya, and J. Barrat. 2005. Transmission of rabies ods, and results of the Help in
2003. A dogs’ rabies vaccination virus in Thailand: Implications Suffering Animal Birth Control
campaign in rural Africa: Impact for disease control. BMC Infec- Programme. Unpublished.
on the incidence of rabies and tious Diseases 5(52). http:// Holt, P., and M. Thrusfield. 1993.
human dog-bite injuries. Vac- www.biomedcentral.com/content/ Association between breed, size,
cine 21: 1965–1973. pdf/1471-2334-5-52.pdf. neutering, tail docking, and uri-
Clifton, M. 2002. Sterilization and Dodet, B. 2006. Preventing the nary incontinence due to incom-
vaccination: 70 percent or Flunk. incurable: Asian rabies experts petence of urethral sphincter
Animal People 12(8). http:// advocate rabies control. Vaccine mechanism. Veterinary Record
24: 3045–3049. 133: 177–180.
Free-Roaming Dogs in Developing Countries: The Benefits of Capture, Neuter, and Return Programs 75
zoonoses, and public health, ed. Margawani, K., and I. Robertson. Moro, P., L. Lopera, N. Bonifacio, A.
C. Macpherson, F. Meslin, and A. 1995. A survey of urban pet own- Gonzales, R. Gilman, and M.
Wandeler, 299–332. New York: ership in Bali. Veterinary Record Moro. 2005. Risk factors for
CABI Publishing. 137: 486–488. canine echinococcosis in an en-
Levy, J., D. Gale, and L. Gale. Matter, H.C., and T.J. Daniels. demic area of Peru. Veterinary
2003. Evaluation of the effect of 2000. Dog ecology and popula- Parasitology 130: 99–104.
a long-term trap-neuter-return tion biology. In Dogs, zoonoses, Neilson, J., R. Eckstein, and B.
and adoption program on a free- and public health, ed. C. Mac- Hart. 1997. Effects of castration
roaming cat population. Journal pherson, F. Meslin, and A. Wan- on problem behaviors in male
of the American Veterinary Med- deler, 17–62. New York: CABI dogs with reference to age and
ical Association 222(1): 42–46. Publishing. duration of behavior. Journal of
Li, T., J. Qui, W. Yong, P. Craig, X. Matter, H., A. Wandeler, B. Neuen- American Veterinary Medicine
Chen, N. Xiao, A. Ito, P. Giraudoux, schwander, L.P.A. Harischandra, 211: 180–182.
M. Wulamo, and P. Schantz. and F. Meslin. 2000. Study of the Nolan, K. 2006. Street dog popula-
2005. Echinococcosis in Tibetan dog population and rabies con- tion control case study. http://
populations, Western Sichuan Pro- trol activities of Sri Lanka. Acta www.vetwork.org.uk/abc.htm.
vince, China. Emerging Infectious Tropica 75: 95–108. Odendaal, J. 1994. Demographics
Diseases 11(12): 1866–1873. McCrindle, C., J. Gallant, S. Cor- of companion animals in South
Listriani, P. 2002. Yudisthira—Bali nelius, and H. Schoeman. 1999. Africa. Journal of the South
Street Dog Foundation. Pre- Changing roles of dogs in urban African Veterinary Association
sented at “Challenges of Animal African society: A South African 65(2): 67–72.
Protection on Island Nations perspective. Anthrozoös 12(3): Organizacion Panamericana de la
With Special Emphasis on Dogs 157–161. Salud Promoviendo la salud en
and Cats.” Miami Beach, Fla. McShea, W., S. Monfort, S. Hakim, las Americas. 2005. Epidemio-
Lockwood, R. 1995. The ethology J. Kirkpatrick, I. Liu, J.W. Turner, logic situation of human rabies
and epidemiology of canine L. Chassey, and L. Munson. 1997. in Latin America in 2004. Epi-
aggression. In The domestic The effect of immunocontracep- demiological Bulletin 26(1):
dog: Its evolution, behavior, and tion on the behavior and repro- 1–5.
interactions with people, ed. J. duction of the white-tailed deer. Orihuela, T.A., and V.J. Solano.
Serpell, 131–138. New York: Journal of Wildlife Management 1995. Demographics of the
Cambridge University Press. 61(2): 560–569. owned dog population in Miacat-
Lodmell, D., L. Ewalt, M. Parnell, Meslin, F., M. Miles, J.A. Vexenat, lan, Morelos, Mexico. Anthro-
C. Rupprecht, and C. Hanlon. and M. Gemmell. 2000. Zoonoses zoös 8(3): 171–175.
2006. One-time intradermal control in dogs. In Dogs, zoo- Overgaauw, P., and F. van Knapen.
DNA vaccination in ear pinnae noses, and public health, ed. C. 2000. Dogs and nematode zoo-
one year prior to infection pro- Macpherson, F. Meslin, and A. noses. In Dogs, zoonoses, and
tects dogs against rabies virus. Wandeler, 333–372. New York: public health, ed. C. Macpher-
Vaccine 24: 412–416. CABI Publishing. son, F. Meslin, and A. Wandeler,
Lumlertdacha, B., S. Warchara- Michell, A. 1998. Neutering and 2 1 3 – 2 5 6 . N e w Yo r k : C A B I
pluesadee, J. Denduangboripant, longevity in dogs. Veterinary Publishing.
N. Ruankaew, P. Sakarasaeranee, Record 142: 288. Pan American Health Organization
D. Briggs, and T. Hemachudha. Michell, A. 1999. Longevity of (PAHO) and World Health Orga-
2006. Complex genetic struc- British breeds of dog and its rela- nization (WHO). 2005. Report of
ture of the rabies virus in tionships with sex, size, cardiovas- the Tenth Meeting of Directors
Bangkok and its surrounding cular variables and disease. of the National Programs for
provinces, Thailand: Implica- Veterinary Record 145(22): Control of Rabies in Latin Amer-
tions for canine rabies control. 625–629. ica. Mexico City, Mexico.
Transactions of the Royal Soci- Mitmoonpitak, C., V. Tepsume- Peacock, D. 2005a. Dog population
ety of Tropical Medicine and thanon, and H. Wilde. 1998. survey—Bali, Indonesia, Yayasan
Hygiene 100: 276–281. Rabies in Thailand. Epidemiolog- Yudisthira (YYS) and Humane
Maarschalkerweerd, R., N. Enden- ical Infection 120: 165–169. Society International. Washing-
burg, J. Kirpensteijn, and B. Mitmoonpitak, C., H. Wilde, and W. ton, D.C. Unpublished.
Knol. 1997. Influence of orchiec- Tepsumetanon. 1997. Current ———. 2005b. Tsunami field oper-
tomy on canine behavior. Veteri- status of animal rabies in Thai- ations report. Unpublished.
nary Record 140: 617–619. land. Journal of Veterinary Med- Perry, B., T. Kyendo, A. Mbugua, J.
ical Science 59(6): 457–460. Price, and S. Varma. 1995. In-
Free-Roaming Dogs in Developing Countries: The Benefits of Capture, Neuter, and Return Programs 77
Epidemiology of urban canine World Society for the Protection of
rabies, Santa Cruz, Bolivia, Animals (WSPA). 2006. Member
1972–1997. Emerging Infec- society manual. London: WSPA.
tious Diseases 8(5). Wright, J.C. 1991. Canine aggres-
Wilde, H., P. Khawplod, and T. sion toward people: Bite scenarios
Khamoltham. 2005. Rabies and prevention. Veterinary Clin-
control in South and Southeast ics of North America: Small Ani-
Asia. Vaccine 23: 2284–2289. mal Practice 21(2): 299–314.
Windiyahingsin, C., H. Wilde, F. Zhang, Y.Z., C.L. Xiong, D.L. Xia,
Meslin, T. Suroso, and H.S. R.J. Jiang, Z.X. Wang, and L.Z.
Widarso. 2004. The rabies epi- Zhang. 2005. Human rabies in
demic on Flores Island, Indone- China. Letter. Emerging Infec-
sia (1998–2003). Journal of tious Diseases 11(12). http://
Medical Association of Thai- www.cdc.g o v / n c i d o d / E I D /
land 187(11): 1389–1393. v o l 1 1 n o 1 2 / 04-0775.htm.
World Health Organization (WHO).
1989. WHO consultation on the
feasibility of global control and
elimination of urban rabies,
December 11–13. Geneva, Switzer-
land. VPH/93.116
———. 1996. Report of the Third
International Symposium on
Rabies in Asia. September
11–15, Wuhan, China. WHO/
EMC/ZOO/96.8.
———. 1998a. Field application of
oral rabies vaccines for dogs:
Report of WHO consultation
organized in collaboration with
Office of International des Epi-
zooties. Geneva, Switzerland,
July 20–22. WHO/EMC/ZDI/
98.15.
———. 1998b. Oral immunization
of dogs against rabies: Report of
the Sixth WHO Consultation.
Geneva, Switzerland. WHO/ EMC/
ZDI/98.13.
———. 2001. Strategies for the
control and elimination of rabies
in Asia. Report of a WHO Interre-
gional Consultation. Geneva,
Switzerland, July 17–21. WHO/
CDS/CSR/EPA/2002.8.
———. 2002. Rabies vaccines.
Weekly Epidemiological Record
77: 109–120.
———. 2004. WHO expert consul-
tation on rabies, first report.
Geneva, Switzerland.
———. 2007. Rabies deaths in Asia.
http://www.who.int/rabies/
rabies_maps/en/index.html.