WellBeing International WBI Studies Repository

2007

Free-Roaming Dogs in Developing Countries: The Benefits of Capture, Neuter, and Return Programs

Jennifer Jackman Humane Society University

Andrew N. Rowan The Humane Society of the United States

Follow this and additional works at: https://www.wellbeingintlstudiesrepository.org/sota_2007

Part of the Animal Studies Commons, Nature and Society Relations Commons, and the Population Biology Commons

Recommended Citation Jackman, J., & Rowan, A. (2007). Free-roaming dogs in developing countries: The benefits of capture, neuter, and return programs. In D.J. Salem & A.N. Rowan (Eds.), The state of the animals 2007 (pp. 55-78). Washington, DC: Humane Society Press.

This material is brought to you for free and open access by WellBeing International. It has been accepted for inclusion by an authorized administrator of the WBI Studies Repository. For more information, please contact [email protected]. Free-Roaming Dogs in Developing Countries: The Benefits of 3CHAPTER Capture, Neuter, and Return Programs Jennifer Jackman and Andrew Rowan

Introduction s a result of human popula- zoonotic diseases (Beck 2000; costly and more effective in rabies tion growth, poor waste Reece 2005). Additional social prevention. A meeting of WHO A disposal management, problems with free-roaming dogs Asia experts concluded, the absence of responsible dog include road accidents, fighting, Rabies control in dogs remains ownership policies, and height- noise, bitten children, fecal con- the only long-term, cost-effec- ened awareness of animal welfare tamination, spread of rubbish, and tive means of eliminating or and disease issues, increased atten- uncontrolled breeding. preventing most human cases. tion is being given to the problem Public health and animal protec- Human public health preven- of free-roaming dogs. The popula- tion advocates share an interest in tive measures should be paral- tion of dogs worldwide may be as reducing dog population growth, leled by programmes for dog high as 500 million (Hsu, Severing- improving the health of dog popu- rabies control. (WHO 2001) haus, and Serpell 2003). Dog-to- lations, and increasing responsible Still, high levels of dog popula- human population densities vary dog ownership. Approaches to free- tion turnover make it difficult to from 2.2 dogs/hundred people in roaming dog population manage- maintain vaccination coverage at urban Zambia (DeBalogh, Wan- ment have changed over the past threshold levels. A new consensus deler, and Meslin 1993), to 15.8 twenty years. Until recently, cap- is emerging that rabies vaccination dogs/hundred people in rural Tan- ture and kill policies prevailed as programs are not sustainable with- zania (Cleaveland et al. 2003), to the primary dog-control method. out sterilization, although some 21.3 dogs/hundred people in Kat- While even today removal of dogs animal groups remain concerned mandu, Nepal (Kato et al. 2003), continues to be a component of about the appropriateness of re- and to more than 30 dogs/hun- dog control in some countries, the turning sterilized animals to com- dred people in white communities World Health Organization (WHO), munity streets. in South Africa (Odendaal 1994) leading researchers, and animal Vaccination, habitat control, and and rural villages in Mexico (Ori- protection groups have condemned responsible pet ownership, includ- huela and Solano 1995) (Table 1). dog removal policies as ineffective ing sterilization, are now replacing Free-roaming dog populations and cruel. the capture-and-kill focus of dog have emerged as both animal wel- The 1990s saw a significant ex- control. In 1992 WHO and the fare and public health problems in pansion in the availability of post World Society for the Protection of developing countries. Free-roam- exposure treatment for dog bites Animals (WSPA) issued guidelines ing dogs face high mortality, mal- and in public awareness of the for dog population management nutrition, starvation, disease, and need to seek treatment. Postexpo- that recommended dog population abuse; account for 99 percent of sure treatment dramatically re- surveys; adoption of national legis- cases of rabies transmission world- duced rabies deaths; however, lation to regulate registration, vac- wide (WHO 2004); and are associ- treatment costs soared. Dog-vacci- cination, identification, sales, and ated with more than sixty other nation campaigns have proved less breeding; public education, subsi-

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

Argentina—La Pampa 18.30 18.3 Larrieu, Alvarez, and Cavagion (1990)

Bolivia—Santa Cruz 25.00 Widdowson et al. (2000)

Indonesia 6.25 WHO (1998a)

Bali 19.20 Peacock (2005a)

Kenya—Machakos District 13.00 13.0 Kitala et al. (2001)

Mexico—Miacatlan 33.60 33.6 Orihuela and Solano (1995)

Mexico 14.30– WHO (1998a) 16.70

Mexico—Hermasillo 12.50 12.5 Eng et al. (1993)

Nepal—Katmandu 21.30 21.3 Kato et al. (2003)

Peru—Pacoraos 16.70 16.7 Moro et al. (2005)

Philippines—Sorsogo Province 26.30 Childs et al. (1998)

South Africa 10.00 Odendaal (1994)

Asian/Colored 13.00 Odendaal (1994)

Black Urban 6.70 6.7 Odendaal (1994)

Black Rural 15.00 15.0 Odendaal (1994)

White 35.00 Odendaal (1994)

S. Africa—Soweto 8.10 8.1 McCrindle et al. (1999)

S. Africa—Maboloka 9.00 9.0 Rautenbach, Boomker, and DeVilliers (1991)

Sri Lanka—Mirgawa 17.50 17.5 Matter and Daniels (2000)

Tanzania—Serengeti District 15.80 15.8 Cleaveland et al. (2003)

Thailand 14.90 Mitmoonpitak, Tepsumethanon, and Wilde (1998)

Zambia 14.90 2.2 14.9 DeBalogh, Wandeler, and Meslin (1993)

Zimbabwe 15.40 Brooks (1990)

56 The State of the Animals IV: 2007 animal welfare, reduce dog popula- Dogs living with humans may be dogs, and feral dogs (Reece 2005). tion growth, and prevent the classified into three or four cate- Based on their level of reliance on spread of rabies and other canine- gories: pets, community dogs, humans for food, shelter, and care, transmitted diseases. Constraints strays, and ferals. In developed dogs are fully dependent (restricted and current debates on current countries the majority of dogs are dogs), semidependent (family dogs implementation of CNR programs pets (i.e., they are allowed in the and neighborhood/community are also examined. house, given names, regarded as dogs), or not dependent (feral/stray part of the family, and never eaten). dogs). Those dogs that are not pets are Increasingly, researchers agree Functions and either stray animals or true ferals that most dog populations depend (a very small percentage). Except at some level on referral house- Dynamics of in some traditional communities holds (Leney and Remfry 2000). Dog Populations (e.g., Native American), there are Only a small proportion of dogs in no community dogs. South America, Asia, and Africa in Developing In most developing countries, rely on markets, slaughterhouses, Countries the main function of dogs is to pro- dumps, and restaurants as their Cultural differences in views of dog tect property. Dogs in Soweto, sole sources of food (Leney and ownership and the role of dogs in South Africa, are used primarily to Remfry 2000; Reece 2005). An society influence the prevalence of guard livestock and property and estimated 10 percent of dogs are dogs, the condition of free-roaming to hunt (McCrindle et al. 1999). In not associated with particular dogs, and dog-control policies. In Machakos District, Kenya, 99 per- households (Bogel and Meslin some developing countries, dogs cent of households say that guard 1990). A Zimbabwe study con- are revered. In Bali, for example, duty is their dogs’ primary func- cluded that all dogs are at least dogs are an important part of tion (Kitala et al. 2001). In Zim- semidependent on people and that mythology, are treated with rever- babwe 60 percent view dogs as none is completely “ownerless” ence, and are given ceremonial guards, and 73.1 percent see dogs (Butler 2000). In Chad, ownerless food offerings (Peacock 2005a). In as a deterrent to wildlife that they dogs comprise only 1.1–10.6 per- Bali and many other developing perceive as pests, such as ele- cent of owned dogs (Kayali et al. countries, cultural traditions pro- phants, baboons, lions, and leop- 2003). A 1999 survey in Bangkok hibit or oppose euthanasia, and the ards (Butler 2000). In fact, in found that 20 percent of dogs are development of a network of shel- Africa increases in dog populations ownerless (WHO 2001). ters is impractical. Dogs may also may reflect heightened security Dogs without a referral house- be a status symbol for upper-in- concerns (Cleaveland 1998). In hold have the lowest reproductive come families in some countries New Providence, Bahamas, security and pup survival rates. These unas- (Reece 2005). The health and is also the main reason for keeping sociated dogs “do not play a signif- psychological benefits of canine dogs for 50.4 percent of house- icant role in the reproductivity of companionship have been amply holds (Fielding and Plumridge this population” (Bogel and Meslin documented in both developing 2005). In the Thungsong District 1990, 282). Instead, free-roaming and industrialized countries (Beck of Thailand, 83 percent of house- dog populations are maintained by 2000). In still other countries and holds keep dogs as guard animals recruitment from owned popula- cultural settings, particularly in (Kongkaew et al. 2004). In Miacat- tions (Boitsni et al. 1995; Leney some Muslim societies, dogs are lan, Mexico, 65 percent of house- and Remfry 2000; Matter and reviled and are less visible. For holds reported having a dog for Daniels 2000; Fielding, Samuels, example, it has been estimated that security reasons (Orihuela and and Mather 2002). there are fewer than a hundred Solano 1995). Association of dogs with particu- thousand dogs in all of Cairo, a Patterns of dog ownership in lar neighborhoods or individual Muslim metropolitan area of eleven many developing countries differ households determines the extent million plus (E. Hilby, personal from those in the United States to which these animals are deemed communication with A.N.R., 2006). and other industrialized nations. In to be accessible to vaccination and These numbers would give a dog developing countries most dogs are sterilization programs. Unreach- density of 0.09 dogs per hundred community dogs who are affiliated able strays had been assumed to people—by far the lowest density with neighborhoods rather than represent 30–70 percent of the ever recorded (Table 1). Finally, in with individual owners. WHO char- dog population (Cleaveland et al. some countries, dogs are consid- acterizes dogs in developing coun- 2006). However, in Katmandu Val- ered to be food (Reece 2005). tries as restricted dogs, semire- ley, Nepal, 86–97 percent percent stricted family dogs, neighborhood of dogs are accessible (Bogel and

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 than are males. Only 15 percent of Free-Roaming Dogs communal lands is 1.1 years (Butler 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

58 The State of the Animals IV: 2007 than do males (Kongkaew et al. 2004). In addition, in New Provi- Figure 1 dence more male dogs (59 percent) Rabies Deaths in Asia than female dogs (41 percent) are licensed (Fielding, Mather, and Number of human rabies deaths per country, Asia, 2004 Isaacs 2005). Female dogs also have shorter life spans. Higher female mortality is related to lower levels of care pro- vided to female dogs. Female dogs are more likely to be abandoned (Fielding, Mather, and Isaacs 2005) and are killed as puppies to avoid pregnancies (Boitsni et al. 1995; Matter and Daniels 2000). People also dispose of female dogs in estrus to disband groups of male 0 dogs (Matter and Daniels 2000). In 1–100 101–1000 the Machakos District, Kenya, the 1001–10,000 > 10,000 life expectancy of male dogs is 3.5 years; for female dogs it is 2.4 years (Kitala et al. 2001). The median Source: WHO (2007). age of dogs in New Providence is 1.5 years for females and three the physical consequences of re- utes one person dies from rabies, years for males (Fielding, Mather peated pregnancies, lactation, and and three hundred are exposed to and Isaacs 2005). competition for food, overpopula- the disease (Rupprecht, Hanlon, In most developing countries, tion of dogs results in human soci- and Hemachudha 2002). Rup- preferences for male dogs and ety devaluing them. Dogs who can precht, Hanlon, and Hemachudha higher mortality of female dogs re- be obtained for little or no cost are (2002, 327) state, “[f]rom a global sult in sex-based population imbal- at the greatest risk of abandon- health perspective...rabies is the ances (Matter and Daniels 2000). ment (Hsu, Severinghaus, and Ser- most important viral zoonosis.” In Istanbul, Turkey, there are 6.8 pell 2003). As Thorton (1992, Ninety-nine percent of rabies male dogs for every female dog 660) has stated, “Not allowing the deaths take place in developing (WHO 1998b). In Thailand the excess [in companion animals] is countries (WHO 2004). Fifty-six ratio of male to female dogs is 2:1 the only effective way to address percent of rabies deaths are in Asia (Kongkaew et al. 2004). Of dogs their welfare.” and 44 percent in Africa. Rabies kept in Bali, 85 percent were male mortality ranges from 0.001 per (Margawani and Robertson 1995). hundred thousand in the United When it responded to the post- Human Health States to eighteen per hundred tsunami disaster that hit Sri Lanka thousand in Ethiopia, with mortal- in 2004, Humane Society Inter- Risks and Free- ity levels of 0.01 in South Africa, national (HSI) veterinary relief Roaming Dogs 0.47 in Thailand and Vietnam, 0.57 teams found that male dogs out- in Sri Lanka, 1.75 in Bangalesh, and numbered females by 3:1. Rabies 2–4 in India (Haupt 1999) (Figure Preferences for male dogs are Free-roaming dogs who suffer from 1). Bangladesh, India, and Pakistan related to the belief that they make disease and overpopulation pose are among the countries with the better guard dogs (Kitala et al. risks of zoonoses, contact injuries, highest incidence of rabies (WHO 2001). Owners also want to avoid and environmental pollution to 2001), and half of all human rabies responsibility for dogs in estrus or human populations (Beck 2000). deaths occur in India (WHO 1996). for litters (Margawani and Robert- Rabies is the most lethal of canine Dogs are the main rabies vector son 1995; Hsu, Severinghaus, and transmitted diseases. Despite the in Africa and Asia (WHO 2001), and Serpell 2003). In addition, people development of a rabies vaccine younger dogs pose a greater bite choose male dogs more often as more than a hundred years ago, and rabies risk. A study in Thailand pets (Boitsni et al. 1995). WHO (2004) reports that half of found that 62 percent of rabid dogs Overpopulation itself is a welfare the world’s human population is at examined are younger than one problem for dogs. In addition to risk for rabies. Every fifteen min- year old (Mitmoonpitak, Wilde, and

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

60 The State of the Animals IV: 2007 some claim that free-roaming dogs Table 2 may prey upon livestock, Boitsni et al. (1995) concluded that feral Levels of Dog and Human dogs actually pose little threat to Echinococcosis in Selected domestic animals. A study of the Developing Countries relationship between dogs and wild carnivores in Zimbabwe found that Percentage the small body weight and group of Dogs Humans/ size of dogs make them poor pred- Place Infected 100,000 Source ators (Butler, du Toit, and Bing- Algeria 9.4–12.0 2.26 Seimenis (2003) ham 2004). However, others have China— 82.3 80.00 Jenkins, Romig, and expressed concern that stray dogs North Central Xinjiang Thompason (2005) may harm civet populations in Hong Kong (Dahmer 2002) and Egypt 3.0–10.0 4.29 Seimenis (2003) iguanas, giant tortoises, and flight- Morocco 35.0–48.4 5.20–7.10 Seimenis (2003) less cormorants in the Galapagos Islands (Matter and Daniels 2000). Peru—Pacaraos District 51.0 Not available Moro et al. (2005) The disease risk of free-roaming Tunisia 30.0–68.0 1.50–2.05 Seimenis (2003) dogs to livestock and wildlife is of greater concern. WHO (1996) esti- Uruguay—La Poloma 20.0 Not available Cohen (1998) mates that 25,000–27,000 domes- tic production animals contract liver (70 percent), lungs (20 per- pen 2000). Puppies often acquire rabies as a result of exposure to cent), or elsewhere in the body (10 the disease through their mothers. dogs or other rabies vectors. While percent) (Jenkins, Romig, and Toxocara eggs do not become infec- dogs pose little predation threat to Thompason 2005). Echinococcosis tious until three weeks to several African wildlife, leopards, lions, can cause serious illness or death. months after their introduction to and hyenas do prey on dogs. Wild The disease is most prevalent in the environment (Overgaauw and carnivore predation on dogs cre- the Middle East and North Africa van Knapen 2000); infectious eggs ates the risk of disease transmis- (Sadjadi 2006), Western and Central can survive up to a year. The disease sion for rabies, distemper, and par- Asia (Jenkins, Romig, and Thompa- is transmitted through contami- vovirus (Butler, du Toit, and son 2005), the Mediterranean nated soil and unwashed hands. Bingham 2004). Wild dog popula- (Jiminez et al. 2002; Seimenis Children ages one to three are espe- tions were reduced by one-third as 2003), and sheep-rearing areas in cially susceptible to exposure. a result of rabies outbreaks in Tan- South America and Australia (Meslin Improved hygiene, public educa- zania and Kenya (Cleaveland et al. 2000) (Table 2). The highest tion, removal of feces, enhanced 1998). Increased vaccination, espe- prevalence of echincoccosis is found health of animals, and reduction in cially along preserve boundaries, in Tibetan populations in Sichuan free-roaming dog populations can reduction of dog populations Province, China (Li et al. 2005). In significantly reduce disease trans- through birth control, and im- endemic areas, 2–20 people per hun- mission of both echinococcosis and provements in waste disposal dred thousand contract echinococ- toxocariasis from dogs to humans would reduce transmission of ca- cosis (Meslin et al. 2000). In hyper- (Rubel et al. 2003). Reduction in nine rabies to wild animals (Butler, endemic areas, up to 12 percent may the proportion of puppies in the du Toit, and Bingham 2004). be infected. population also helps to control tox- Toxocara canis is a common dog ocariasis spread (Rubel et al. 2003). roundworm that is spread indirectly Predecessors to through dog feces. Analysis of dog fecal samples revealed toxocara in- Free-Roaming Capture, Neuter, fection rates of 36 percent in Preto- and Return ria, South Africa; 19 percent in Jor- Dogs: Risks to dan; 13.5 percent in Santiago, Livestock and Capture and Kill Chile; and 10.5 percent in La Plata, The capture and killing of stray Buenos Aires (Rubel et al. 2003). Wildlife dogs has been the dominant strat- Free-roaming dogs also may pre- Dog infection rates range from 3.5 egy to reduce dog populations and sent predation and disease risks to percent in adults to 79 percent in dog zoonoses. In the late 1980s, both livestock and wildlife. While puppies (Overgaauw and van Kna- lethal dog-control programs were

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, For example, culls of dogs 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 country 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,

62 The State of the Animals IV: 2007 Based on epidemiological re- paigns and improved postexposure vaccination points were registered search, researchers estimate that treatment (Organizacion Panamer- and vaccinated for rabies, distem- 70 percent vaccination coverage icana 2005). In 1983 the Pan Amer- per, and parvovirus free of charge. will prevent rabies outbreaks ican Health Organization (PAHO) Colored plastic collars were placed (Coleman and Dye 1996; Coyne et and WHO set 2005 as the target on treated dogs. Vaccination cover- al. 2001; WHO 2002; Cleaveland et date for elimination of canine age was assessed at each of four al. 2003). In the field the level of rabies (PAHO and WHO 2005). phases through household surveys, coverage at which protection has Each year forty-four million dogs in observation of dogs, and number of been achieved has varied. For the region are vaccinated (Orga- rabies doses used in proportion to example, in Korea 30–40 percent nizacion Panamericana 2005). dog population. Researchers also coverage has eliminated rabies In many areas 80 percent coverage collected data from hospitals on (Cleaveland et al. 2003). However, has been achieved quickly (WHO rabies and dog bite incidences at even with 56–80 percent coverage, 2004). As a result of these efforts, each stage. Vaccination coverage of rabies remains endemic in Mexico. human rabies cases dropped by 91 60–70 percent of dogs in this area Average dog-vaccination coverage percent and dog rabies cases of Tanzania has provided sufficient is currently only 9.7 percent in dropped by 93 percent between protection from canine rabies Asia and 10.3 percent in Africa 1982 and 2003. Panama, Costa (Cleaveland et al. 2003). (Knobel et al. 2005). With commu- Rica, Chile, Uruguay, most of Ar- Similar mass rabies vaccination nity participation Bogel and Meslin gentina, and southern Brazil have campaigns have been held else- (1990) believe that 70–75 percent been rabies free for more than ten where in Africa and in Asia (Perry of dogs populations are accessible years (Organizacion Panamericana et al. 1995). In Nairobi central to rabies vaccination campaigns. 2005). point vaccination sites were WHO (2004) recommends that The Latin American experience opened for five days and supple- vaccination campaigns use only in- also makes clear the need to sus- mented with door-to-door coverage activated vaccine, that all staff in- tain vaccination programs. After during the last three days of the volved receive preexposure vaccina- twenty-five years without rabies in campaign. In Nepal vaccination tion, and that dogs be registered to Argentina, outbreaks occurred in campaigns achieved 75–80 percent provide permanent identification two provinces in 2004 (PAHO and coverage and involved public edu- of those who have been vaccinated. WHO 2005). Rabies outbreaks also cation, household surveys, central Rabies surveillance and dog popula- occurred that year in Bolivia and vaccination points for nineteen tion surveys are urged to measure in the state of Zulia in Venezuela. days, and teams that went door-to- population size, turnover, growth, Political commitment, financial door in areas where vaccination sources of ownerless dogs, degree of support for canine rabies-control levels were insufficient (Bogel and supervision of owned dogs, and dis- programs, surveillance and dog Joshi 1990). Mass vaccination tribution and accessibility of dogs population ecology data, and coor- campaigns have improved atti- to be vaccinated (Kitala et al. dination are necessary to sustain tudes toward animals and animal 2001). Dog density and frequency rabies prevention in Latin America welfare (Cleaveland et al. 2006). of immunization campaigns influ- (WHO 2001). With canine rabies Although dog-vaccination cam- ence vaccination coverage success under some control, bat transmis- paigns are more cost-effective than (Cleaveland et al. 2003). sion of rabies has become Latin postexposure treatment, countries WHO (2004) advocates cam- America’s new challenge (Organi- may experience a decline in rabies paigns that begin in one area and zacion Panamericana 2005). without a concomitant decrease in expand to cover larger areas, coun- Targeted mass dog-vaccination demand for postexposure treat- try-wide campaigns, or campaigns campaigns in Africa have achieved ment (Cleaveland et al. 2003). For in geographically separate hot some success as well. In rural north- example, in Tunisia and Thailand spots followed by expanded cover- western Tanzania, the first cam- rabies cases in dogs and humans age (WHO 2001). WHO also sup- paign reduced rabies incidence by declined significantly; however, ports free dog immunization. 70 percent (Cleaveland et al. 2003), postexposure treatments remained Dog-vaccination campaigns along and a second campaign reduced the at the same level or increased. Dog national borders also are recom- disease by 97 percent. In Tanzania rabies may need to be virtually mended to provide an “immunity advertisements through primary eliminated before demand for post- belt” (WHO 2001). schools and meetings with commu- exposure treatment decreases Many Latin American countries nity leaders took place before the (Cleaveland et al. 2003). have had success in controlling the vaccination campaign. A central Oral vaccine as a supplement to spread of rabies through mass vaccination point was set up in each current parenteral vaccination canine rabies vaccination cam- village, and all dogs brought to the campaigns is viewed as an addi-

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 of dogs for four years is necessary perceived inaccessibility for par- 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

64 The State of the Animals IV: 2007 the control of rabies transmission dogs to fill ecological niches left nancy can improve animal health, (Help in Suffering 2003). CNR for vacant by dog losses. Return of making the animal less vulnerable dogs in developing countries has sterilized dogs to their home terri- to predation, reductions in food been modeled on trap, neuter, and tories prevents a “vacuum effect” supply, bad weather, and other chal- return (TNR) programs for feral cat of attracting new dogs to unoccu- lenges. In addition, sterilization colonies in the United States (HSI pied territories (Leney and Remfry minimizes risks of some debilitat- 2002). For TNR programs, people 2000). Return of dogs to the terri- ing and fatal diseases. who put out food for stray and feral tories from which they were cap- TNR programs for feral cats colonies trap cats and bring them tured also diminishes the stress highlight some of these benefits. to a veterinary facility, where the and vulnerability of the returned Mean feral cat colony size de- cats are sterilized and vaccinated dogs after surgery. These programs creased from 7 to 5.1 after Florida for rabies and other diseases. The reduce the number of puppies in spay-and-neuter programs (Cen- cats are ear-tipped to identify them the population, who are at the tonze and Levy 2002). Neutering as having been sterilized and then greatest risk for transmission of of free-roaming cats improved body returned to the colony. Cats who rabies and other diseases. Similar weight, body condition, and life test positive for feline leukemia to vaccination programs, a 70 per- span (Scott et al. 2002; Levy, Gale, virus (FeLV) or other diseases that cent sterilization rate is necessary and Gale 2003). Eighty-two per- are not treatable are euthanized to stabilize dog populations. Some cent of feral cat colony caretakers humanely. Kittens more than seven argue that dog overpopulation will observe that spaying and neutering weeks old are removed from the continue to be a problem until the has improved the quality of cats’ colonies, sterilized, socialized, and proportion of breeding females is lives (Centonze and Levy 2002). placed for adoption. The cats are less than 20 percent (Fielding and Scott et al. (2002, 212) conclude, usually returned to caretakers on Plumridge 2005). Like TNR pro- “in addition to halting reproduc- the same day as surgery and then grams, CNR programs have strong tion, neutering may have other may be kept overnight before being public support where catch and kill effects that, combined, improve the returned to their colonies. In TNR programs do not (Leney 2002). welfare of feral and free-roaming treated feral cat colonies continue CNR programs also have pressed cats.” to be managed and monitored. for changes in waste disposal. As Contraceptive trials involving The TNR management of cats Help in Suffering (2003, n.p.) wild animals further document has been viewed as more effective notes, “The overall, ultimate an- improved body condition and re- than euthanasia because it allows swer to street dog population con- duced mortality as a result of tem- cats to continue to “occupy envi- trol is to control the availability of porary or permanent sterilization. ronmental niches” that otherwise edible wastes.” Waste disposal is a Pregnancy prevention with the would be filled by unvaccinated major factor in free-roaming dog immunocontraceptive porcine and unsterilized cats (Hughes, populations and bite incidences. zona pellucide (PZP) enhanced the Slater, and Haller 2002). In this In New Providence 25 percent of body condition of female deer way TNR colonies provide “a sub- garbage discarded each week was (Kirkpatrick 1996, 2005; McShea stantial barrier of vaccinated indi- edible (Fielding, Mather, and et al. 1997; Rutberg 2005). The viduals against disease” (Slater Isaacs 2005). In Nepal stray dogs health of wild horses on Assa- and Shain 2005, 46). TNR also are able to feed at garbage dumps teague Island, Virginia, also im- encourages colony feeders to par- that line the streets and frequent proved as a result of the PZP con- ticipate in feral cat management the makeshift slaughter facilities traceptive program (Turner and and, if done properly, leads to a in Katmandhu where offal is dis- Kirkpatrick 2002). Before PZP in- decline in the colony size. TNR has posed of. In Japan, where there is troduction, the mortality rate was been endorsed by the American no loose garbage, stray dog popula- greater than 10 percent for adult Veterinary Medical Association and tions are lower (Kato et al. 2003). horses and 3 percent for foals. most leading animal protection Central to the success of CNR With the contraceptive program, organizations. TNR also has won programs are improvements in the adult mortality decreased to less the support of caretakers of feral health, longevity, and behavior of than 4 percent and foal mortality cat colonies who oppose euthana- free-roaming dogs in addition to to about 1 percent (Turner and sia of healthy cats and are needed reductions in population growth. Kirkpatrick 2002). The mean age to implement TNR programs. For many years researchers have re- at death of mares that have not By controlling population growth ported the health benefits of sterili- been contracepted is 6.4 years, and reducing dog mortality, CNR zation and contraception. Repeated whereas it jumps to 19.9 years in programs discourage migration pregnancies can physically stress mares who have been contracepted and compensatory breeding of animals, while the absence of preg- for three or more years (J. Kirk-

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, in Bombay, Delhi, Calcutta, (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

66 The State of the Animals IV: 2007 Table 3 Selected Capture, Neuter, Return Program Locations, Duration, Sterilization Levels, and Components

Postprogram Place/ Type of Number of Sterilization Education Duration Clinic Vets Sterilizations Level Programs Source

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)

Bali Mobile Local 13,790 dogs 51 percent Yes Peacock (2005a); (September 1998– Fixed Visiting Listriani (2002) May 2005) Ongoing

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

Jaipur Fixed Local > 23,000 dogs 68 percent No Help in Suffering (February 1997– adult males and (2003) May 2006) < 3 months Ongoing excluded 12 dogs captured per day, 7 days a week

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 120 120 the next six years (to about 75 per- 107 cent sterilized) has been much 100 slower. As a result of the ABC pro- gram, the dog density also declined 80 by one third between 1997 and 2002. 60 However, these decreases have not 44 continued. The possible addition of 40 35 dogs to the population from the re- 24 production of dogs whose owners 20 17 16 have kept them on private property Number of Rabies Deaths 5 0 to avoid ABC capture, inadequate ABC coverage in some areas, and 1996 1997 1998 1999 2000 2001 2002 2003 migration or acquisition of dogs from Year outside of the district may have pre- vented further population declines. Higher reproductive and pup survival Figure 3 rates among dogs in protected envi- Number of Rabies Deaths in ronments also may contribute to higher than expected population lev- Jaipur, India, 1992–2002 els (E. Hiby, personal communication Jaipur-Walled City ABC/Started March ’96 with A.N.R., n.d. 2006). 12 Among the challenges the Jaipur 10 10 program has faced is difficulty in 10 9 getting commitments from munic- 8 ipal authorities to refrain from cap- 8 turing or killing dogs (Help in Suf- 7 fering 2003). Municipal officials 6 receive pressure from residents 5 who see dogs as a nuisance and fear 4 rabies. Officials also are concerned 3 that CNR success will result in re- 2 2 ductions in animal-control jobs. Number of Rabies Deaths 1 The absence of information on 00 0 street dog behavior and lack of 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 trained resources, staff, equip- ment, and medical supplies also Year have been problematic. HIS had initial difficulties in identifying 2003). Nonetheless, other cities in impact. If they are significantly re- Indian veterinary surgeons to par- India have also reported success ducing the number of young male ticipate in the program because with their ABC programs (Krishna dogs (the main rabies vectors) from few local veterinarians have experi- 2005). Chennai has recorded a the streets, it is conceivable that ence or training in small-animal substantial decline in human even a small reduction in teenage medicine (Nolan 2006). In addi- rabies cases since it launched its male dogs could break the infec- tion, problems with other non- ABC program in September 1996 tion cycle for rabies. The ABC pro- governmental organizations inflat- (Figure 2), and the Jaipur rabies gram in Jodhpur has been set up to ing their sterilization numbers data are also impressive (Figure 3). try to answer some of these ques- have undermined the reputation of It is not immediately apparent tions. A desert city, Jodhpur is ABC programs (Help in Suffering why ABC programs should have this essentially an island consisting of

68 The State of the Animals IV: 2007 about 950,000 people and 46,000 2002). This capture strategy has from clinics was viewed as more dogs (or 4.9 dogs per hundred peo- only served to facilitate migration important than the financial incen- ple) (K. Doyle, personal communi- of infected and intact dogs into tive (HSI 2001). cation with A.N.R., n.d. 2006). new territories. Targeted CNR cam- The Abaco program was consid- paigns in isolated geographic areas ered a success: the proportion of Thailand such as southern Thailand are owners with sterilized dogs in- In 1995 Thailand set the goal of viewed as more viable (Denduang- creased from 62 percent before the being rabies free by 2000 (Wasi et boripant et al. 2005). four clinics to 76 percent after the al. 1997). Under Thailand’s 1992 clinics (HSI 2001). With the popu- Rabies Prevention Act, every Island Nations larity of the program, AARF was owned dog must be vaccinated at CNR programs have operated suc- asked to run makeshift clinics in two to four months of age and cessfully in island areas, including other neighborhoods (HSI 2001). receive annual vaccinations (Wasi Abaco, Bali, the Galapagos, and Sri Obstacles to the program have et al. 1997). Vaccination and steril- Lanka. In Abaco, an island in the included the lack of owner partici- ization campaigns focused on com- Bahamas, a spay/neuter incentive pation and the numbers-driven munity dogs who live around tem- program (SNIP) was launched in program approach that on occa- ples and schools (Kamoltham, 1999 with support from HSI and sion has resulted in more captured Singhsa, and Promsaranee 2003). the Pegasus Foundation. In 2000, dogs than could be sterilized (HSI Methods of sterilization included after the success of the initial pro- 2001). injections of medroxyprogesterone gram, SNIP and Abaco Animals In Bali, an island with 3,151,000 acetate, surgery, and use of natural Require Friends (AARF) initiated people, there are an estimated plant hormones. Outreach to the “Project Potcake” as a CNR pro- 550,000–600,000 dogs (18–18.5 medical community and local res- gram (HSI 2001). Most “potcakes” dogs per hundred people). Eighty- idents encouraged bite victims to (local dogs) are unowned, but five percent of these animals are seek treatment (Kamoltham, these dogs are recognized and sup- street dogs (Listriani 2002). Since Singhsa, and Promsaranee 2003). ported by specific neighborhoods. its inception in 1998 by the Bali Mass vaccination campaigns For Project Potcake, two local Street Dog Foundation (Yayasan achieved 53 percent coverage veterinary clinics ran eight spay- Yudisthira Swarga [YYS]) the pro- (WHO 1996). Although rabies de- and-neuter programs for four to six gram has sterilized 13,790 dogs and clined from two thousand cases in days each (HSI 2001). Volunteers provided veterinary care to an addi- 1993 to fewer than twenty in 2003, canvassed neighborhoods and tional 31,718 (Peacock 2005a). YYS vaccination levels of 40–70 percent transported dogs to the clinics, started with a “catch, treat, and in parts of the country are viewed where the animals were sterilized release” program to treat skin dis- as inadequate, particularly in view for free. The program focused on eases, parasites, and wounds. YYS of the migration of infected dogs female dogs, but also included now operates both mobile and fixed from suburban and rural areas male dogs and cats. Project Pot- clinics; the former comprise two (Denduangboripant et al. 2005). cake exceeded its target goals (HSI doctors, one dogcatcher, and a Moreover, stray dog populations 2001). After the program had suc- driver/field assistant. The “M.A.S.H.- tripled between 1992 and 1999 cessfully reached both owned and style” surgery unit goes out four (Lumlertdacha et al. 2006). socialized dogs, it attempted with- days a week, and the CNR program With a population of six to ten out success to use baited traps to is directed at both female and male million dogs, Thailand imple- capture less accessible dogs (HSI dogs. Before the mobile clinics mented a new program of capture, 2001). At the clinics dogs received began to visit villages, about 24 per- neuter, vaccination, and return in additional medical treatment, cent of the dogs were sterilized. 2002. This program has been the including antibiotics, fluid replace- After seven years of operation, an target of criticism because it is ment, and diagnosis of skin condi- estimated 51 percent of dogs are limited to Bangkok and lacks ade- tions (HSI 2001). now sterilized. Of the spay-and- quate financial and staffing re- Initially, the program offered in- neuter surgeries, 74 percent are sources (Denduangboripant et al. centives of $10 for each male dog performed by the mobile clinics 2005). Programs in Thailand faced brought in and all cats and $15 for (Peacock 2005a). It is evident that difficulties in hiring veterinarians each female dog. Incentives were the increased proportion of steril- who are trained in small-animal important in overcoming initial ized dogs cannot be due solely to surgery. When they could not hire community suspicion, but could be YYS activities. However, YYS has enough veterinarians for surgery, decreased or eliminated as the pro- stimulated a change in community Thailand officials built kennels gram gained community support. and veterinary behavior such that to house captured dogs (Clifton Transportation for the dogs to and sterilization is now more common.

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

70 The State of the Animals IV: 2007 cases were reported in Jaipur (Fig- dogs are less likely to roam or also experienced initial resistance ure 2) in districts in which CNR fight (Help in Suffering 2003; Ani- from local veterinarians that disap- programs have been implemented. mal Balance 2005). peared when YYS activities led to In areas in which the program did While documentation of CNR an increased demand for veteri- not operate, the number of rabies program outcomes is preliminary, nary services. cases increased or stayed the same. CNR and vaccination campaign Involvement of local veterinari- After declines in rabies deaths experiences, epidemiology, and ans is imperative to meet legal throughout the 1990s and no dog ecology and behavior suggest requirements in some countries rabies deaths in 2002 in Thailand, several lessons for future pro- (Hargreaves 2002), to strengthen three people died of rabies in grams. Dog population surveys are support for CNR programs, and to Bangkok in 2003 (Lumlertdacha crucial to developing CNR and vac- ensure long-term availability of et al. 2006). The migration of peo- cination programs and monitoring spay-and-neuter services (HSI ple and dogs from affected areas, their success (Matter and Daniels 2002). CNR programs increase which, in turn, diminished rabies 2000; Wandeler and Bingham local veterinarians’ interest in vaccination coverage, most likely 2000; WHO 2004). Measurement small-animal medicine. Following contributed to this spike in the dis- of dog populations requires house- the same pattern in the United ease (Denduangboripant et al. hold surveys; collection of informa- States, low or no-cost spay-and- 2005; Lumlertdacha et al. 2006). tion on dog survival, fecundity, sex neuter programs not only make In Sri Lanka CNR possibly fore- ratio, age structure, keeping prac- services available and affordable, stalled rabies outbreaks in the tices and human population; use of but they also spur local veterinari- wake of the tsunami. capture-mark-recapture strategy ans to provide them (HSI 2002). At In many CNR program areas, to estimate owned and ownerless most locations CNR clinics were recapture of treated dogs and field population; and field observation the first veterinary services pro- observations have demonstrated to ascertain reproduction, survival, vided to dogs and helped build improved dog health. In Abaco habitat use, food sources, and public support for veterinary care. dogs who had been sterilized social behavior (Matter and Community involvement is showed weight gain, improved Daniels 2000). essential to the success of CNR coat luster and quality, improved CNR experiences in developing and vaccination programs. Resi- skin conditions, and fewer para- countries reveal important issues dents play an important role at all sites and venereal tumors (HSI regarding the involvement of the sites in assisting program imple- 2001). Following CNR implemen- veterinary community. Few veteri- mentation through bringing dogs tation in Bali, the proportion of narians in developing countries to sites and monitoring the ani- dogs classified as having poor wel- have training or experience in mals. In many programs commu- fare status decreased from 33 small-animal medicine and surgery nity leaders or “village mentors” percent to 13 percent (Peacock (WHO 2001). Most veterinary provide entrée into local commu- 2005a). As of 2006 ABC dogs in training is oriented toward agricul- nities and facilitate public educa- Jaipur were in better condition tural use of animals. To be success- tion and participation. Other pro- than was the rest of the dog popu- ful, CNR programs must incorpo- grams enlist the involvement of lation (Help in Suffering 2003). rate a training component for local “dog mommas,” who serve as care- HIS (2003) was in the process of veterinarians. The Bali program, in takers for neighborhood groups of developing more precise body con- which visiting veterinarians are dogs (HSI 2002). At all sites pro- dition scoring techniques to quan- provided with training capacity, grams gained strong community tify improvements. These tech- has done this most successfully. In support and saw improved atti- niques were being applied addition, the YYS veterinary teams tudes toward animal welfare. elsewhere. In addition, fewer dogs have trained veterinarians in Sri Field experiences also demon- were observed in emaciated condi- Lanka and India. strate the importance of transporta- tion after clinic-based sterilization CNR and sterilization programs tion of dogs to clinic sites and programs in Abaco (HSI 2003). also have identified some conflicts mobile clinics. Experiences in Little research on dog behavior with local veterinarians. In Taiwan, Abaco, Jaipur, and other settings has been carried out before and for example, veterinarians have suggest that people who are respon- after CNR programs, although evi- been reluctant to support spay- sible for dogs are often unwilling or dence from Bali suggests the pro- and-neuter programs because they unable to bring their animals to a portion of aggressive dogs has “believe [the] resulting reduction location that is any distance from decreased (from 8 percent to 3 in the dog population will be bad their home. Rabies vaccination percent [Peacock 2005a]), and for business” (Hsu, Severinghaus, campaign surveys have found that other sites report that treated and Serpell 2003, 15). In Bali YYS the proportion of vaccinated dogs

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

72 The State of the Animals IV: 2007 1996; Reece 2005). In most coun- welfare. The ability of rabies vacci- ———. 2006. Spring 2006 report. tries successful programs need the nation campaigns to reach up to http://www.animalbalance.org/ collaboration of veterinary, health, 90 percent of dogs, and their suc- index.shtml. and sanitation departments as well cess in achieving sterilization rates Bauhloul, C., D. Taieb, M. Diouani, as animal welfare nongovernmen- of 51–85 percent with CNR, S.B.H. Ahmed, Y. Chtourou, B.I. tal organizations (NGOs) (WHO demonstrates the viability of the B’chir, H. Kharmachi, and K. Del- 2001; Help in Suffering 2003). CNR approach. Because of differ- lagi. 2006. Field trials of a very Political commitment also must be ent dog ownership patterns in potent rabies DNA vaccine which sustained for effective and endur- developing countries, private, low- induced long lasting virus neu- ing rabies control (PAHO and WHO cost, and no-cost sterilization pro- tralizing antibodies and protec- 2005). While government support grams will never reach enough tion in dogs in experimental con- has varied across CNR programs, dogs to achieve population stabi- ditions. Vaccine 24: 1063–1072. Thailand is the only country in lization or reductions. CNR Beck, A. 2000. The human-dog re- which CNR has been a govern- addresses the reluctance of own- lationship: A tale of two species. ment-run activity. ers to take dogs for treatment and In Dogs, zoonoses, and public Puppies have the greatest risk the fact that community dogs health, ed. C. Macpherson, F. of contracting and transmitting often are not affiliated with individ- Meslin, and A. Wandeler, 1–16. rabies. The mortality of puppies uals who take responsibility for New York: CABI Publishing. also contributes to high popula- their veterinary care. Bogel, K., and D.D. Joshi. 1990. tion turnover. Most vaccination CNR also addresses the primary Accessibility of dog populations and CNR programs, however, ex- limitation of mass vaccination for rabies control in Kathmandu clude puppies under three months campaigns: high population Valley, Nepal. Bulletin of the of age. In Jaipur younger puppies turnover. The combination of vac- World Health Organization are not included in CNR because of cination, sterilization, and return 68(5): 611–617. belief that they should not be sep- of dogs to their territories appears Bogel, K., and F. Meslin. 1990. Eco- arated from adults and that the to enhance the health, longevity, nomics of human and canine capture and procedure would be and stability of dog populations, rabies elimination: Guidelines too stressful (Nolan 2006). While reducing movement and breeding for programme orientation. Bul- scientific literature suggests that of unsterilized and unvaccinated letin of the World Health Orga- prepubertal gonadectomy is a safe dogs. Lower dog population levels nization 68: 261–291. procedure with no increased inci- decrease the risk of rabies, echi- Boitsni, L., P. Francisci, P. Ciucci, dence of complications, health, or nococcosis, and toxocariasis. In and G. Andreoli. 1995. Popula- behavioral problems in developed the case of free-roaming dogs, ani- tion biology and ecology of feral countries (Howe et al. 2001), con- mal welfare and human health are dogs in central Italy. In The cern also has been expressed about closely linked. Ultimately, prob- domestic dog: Its evolution, neutering puppies under eight lems with free-roaming dogs can- behavior, and interactions with weeks of age outside a well- not be separated from human pop- people, ed. James Serpell, equipped clinic (Leney and Remfry ulation growth, urbanization, and 217–244. New York: Cambridge 2000) and before their immune increased waste. University Press. systems have matured (Cardwell Brooks, R. 1990. Survey of dog 1993). Modification of CNR pro- population of Zimbabwe and its grams to include on-site vaccina- Literature Cited level of rabies vaccination. tion of puppies could promote Adeyemi, I., V. Adetunji, V. James, Veterinary Record 127(24): rabies prevention and dog health. and D. Alonge. 2005. Ten year 592–596. Sterilization of puppies in field set- (1993–2002) retrospective eval- Butler, J. 2000. Demography and tings in which some supervision is uation of vaccination of dogs dog-human relationships of the available also might be a viable against rabies at the University dog population in Zimbabwean strategy. Because of differences in of Ibadan, Nigeria. African Jour- communal lands. Veterinary dog ownership patterns in develop- nal of Biomedical Research Record 147(16): 442–446. ing countries, adoption of street 8(2): 71–77. Butler, J., J. du Toit, and J. Bing- puppies has not been a part of CNR Animal Balance. 2005. Project ham. 2004. Free-ranging domes- (as is adoption of feral kittens in report—May 2005, Campaign on tic dogs as predators and prey in TNR programs). Galapagos Islands. http://www. rural Zimbabwe: Threats of com- CNR programs show great prom- animalbalance.org/index.shtml. petition and disease to wild car- ise as a strategy to decrease public nivores. Biological Conservation health risks and improve animal 115: 369–378.

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.

74 The State of the Animals IV: 2007 Howe, L. 1997. Short-term results about_us/humane_society_ Mass.: Tufts School of Veterinary and complications of prepuber- international_hsi/hsi_asia/ Medicine Center for Animals tal gonadectomy in cats and relief_efforts_focus_on_human_ and Public Policy. dogs. Journal of the American tragedy_after_catastrophic_ ———. 2005. The wild horse fertil- Veterinary Medical Association tsunami.html. ity control program. In Humane 221(1): 57–62. ———. 2006. A year after the wildlife solutions: The role of Howe, L., M. Slater, H. Boothe, H.P. tsunami, disaster responders dis- immunocontraception, ed. A. Hobson, J. Holcom, and A. cover a sea change in attitudes Rutberg, 63–75. Washing- Spann. 2001. Long-term out- toward animals. http://www.hsus. ton, D.C.: Humane Society come of gonadectomy per- org/about_us/humane_society_ Press. formed at an early age or tradi- international_hsi/hsi_asia/ Kitala, P., J. McDermott, M. Kyule, tional age in dogs. Journal of the a_year_after_the_tsunami.html. M., J. Gathuma, B. Perry, and A. American Veterinary Medical Jenkins, D., T. Romig, and R. Wandeler. 2001. Dog ecology and Association 218(2): 217–221. Thompason. 2005. Emergence/ demography information to sup- Hsu, Y., L. Severinghaus, and J. re-emergence of echinococcosis port the planning of rabies con- Serpell. 2003. Dog keeping in spp.—A global update. Interna- trol in Machakos District, Kenya. Taiwan: Its contribution to the tional Journal for Parasitology Acta Tropica 78: 217–230. problem of free-roaming dogs. 35: 1205–1219. Knobel, D., S. Cleaveland, P. Cole- Journal of Applied Animal Wel- Jiminez, S., A. Perez, H. Gil, P. man, E. Ferre, M. Meltzer, fare Science 6(1): 1–23. Schantz, E. Ramalle, and R. Juste. M.E.G. Miranda, A. Shaw, J. Hughes, K.L., M.R. Slater, and L. 2002. Progress in control of cystic Zinsstag, and F. Meslin. 2005. Haller. 2002. The effects of im- echinococcosis in La Rioja, Spain: Re-evaluating the burden of plementing a feral cat spay/ Decline in infection prevalences rabies in Africa and Asia. Bul- neuter program in a Florida in human and animal hosts and letin of the World Health Orga- county animal control service. economic costs and benefits. Acta nization 83(5): 360–369. Journal of Applied Animal Wel- Tropica 83: 213–221. Kongkaew, W., P. Coleman, D. Pfeif- fare Science 5(4): 285–298. Kamoltham, T., J. Singhsa, and P. fer, C. Antarasena, and A. Thip- Humane Society International Promsaranee. 2003. Elimination tara. 2004. Vaccination coverage (HSI). 2001. Case study of an in- of human rabies in a canine and epidemiological parameters centive program to encourage endemic province in Thai- of the owned-dog population in sterilization of dogs (and cats) land: Five-year programme. Bul- Thungsong District, Thailand. and greater attention to animal letin of the World Health Orga- Preventive Veterinary Medicine welfare on Abaco Island in the nization 81(5). 65: 105–115. Bahamas. Washington, D.C.: HSI. Kato, M., H. Yamamoto, Y. Inukai, Krishna, S.C. 2005. ABC responsi- ———. 2002. Proceedings of the and S. Kira. 2003. Survey of the ble for decline in human rabies conference: Challenges of ani- stray dog population and the cases. Unpublished. mal protection on island nations health education program on Kustritz, M. 2002. Early spay- with special emphasis on dogs the prevention of dog bites and neuter: Clinical considerations. and cats. Miami Beach, Fla. dog-acquired infections: A com- Clinical Techniques in Small ———. 2005a. Tsunami Memorial parative study in Nepal and Ok- Animal Practice 17(3): Trust supports animal welfare in ayama Prefecture, Japan. Acta 124–128. Sri Lanka. http://www.hsus.org/ Medica Okayama 57(5): Larrieu, E., T. Alvarez, and L. Cava- about_us/humane_society_ 261–266. gion. 1990. Aporte al studio de international_hsi/hsi_asia/ Kayali, U., R. Mindekem, N. la dinamica de las poblaciones tsunami_memorial_trust.html. Yemadji, A. Ndoutamia, and J. caninas. Veterinaria Argentina ———. 2005b. HSI team extends Zinsstag. 2003. Coverage of pilot 7(64): 242–247. stay in Sri Lanka to prevent mili- parenteral vaccination campaign Leney, J. 2002. Impact of compan- tary action against homeless dogs. against rabies in N’Djamena, ion animals on islands, issues http://www.hsus.org/about_us/ Chad. Bulletin of the World and problems in their manage- humane_society_international_ Health Organization 81(10): ment: DOGS. Presented at hsi/hsi_asia/extends_stay_in_sri 739–744. “Challenges of Animal Protec- _lanka.html. Kirkpatrick, J. 1996. Some recent tion on Island Nations with Spe- ———. 2005c. HSI veterinary disas- developments in immunocon- cial Emphasis on Dogs and ter teams work to collar the stray traception. In Living with Cats.” Miami Beach, Fla. dog problem in Sri Lanka and wildlife report, ed. A. Rowan Leney, J., and J. Remfry. 2000. Dog Thailand. http://www.hsus.org/ and J. Weer, 87–98. Grafton, population management. In Dogs,

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 213–256. New York: CABI 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-

76 The State of the Animals IV: 2007 creasing rabies vaccination cov- Salmeri, K., M. Bloomberg, S. American Veterinary Medical erage in urban dog populations Scruggs, and J. Shille. 1991. Association 224(3): 380–387. of high human population den- Gonadectomy in immature dogs: Sudarshan, M.K. 2005. Assessing sity suburbs: A case study in Effects on skeletal, physical, and burden of rabies in India: WHO- Nairobi, Kenya. Preventive Vet- behavioral development. Journal sponsored national multicentreic erinary Medicine 22: 137–142. of the American Veterinary rabies survey, 2003. Indian Jour- Rautenbach, G.H., J. Boomker, and Medical Association 198: nal of Community Medicine I.L. DeVilliers. 1991. A descrip- 1193–1203. 30(3). http://www.indmedica. tive study of the canine popula- Sampath, G., S. Parikh, P. Sagram, com/journals.php?journalid= tion in a rural town in southern and D. Briggs. 2005. Rabies pos- 7&issueid=57&articleid=712& Africa. Journal of the South texposure prophylaxis in mal- action=article. African Veterinary Association nourished children exposed to Tang, X, M. Lou, S. Zhang, AR 62(4): 158–162. suspect rabid animals. Vaccine Fooks, R. Hu, and C. Tu. 2005. Reece, J.F. 2005. Dogs and dog 23: 1102–1105. Pivotal role of dogs in rabies control in developing countries. Scott, K., J. Levy, S. Gorman, and transmission, China. Emerging In The state of the animals III: S. Newell. 2002. Body condition Infectious Diseases 11(12). 2005, ed. D.J. Salem and A.N. of feral cats and the effect of http://www.cdc.gov/ncidod/EID/ Rowan, 55–64. Washington, neutering. Journal of Applied vol11no12/05-0271.htm. D.C.: Humane Society Press. Animal Welfare Science 5(3): Thornton, G.W. 1992. The welfare Robinson, R. 2000. Zoonoses and 203–213. of excess animals: Status and immunosuppressed populations. Seimenis, A. 2003. Overview of needs. Journal of the American In Dogs, zoonoses, and public epidemiological situation on Veterinary Medical Association health, ed. C. Macpherson, F. echinococcosis in the Mediter- 200(5): 660–662. Meslin, and A. Wandeler, 273– ranean region. Acta Tropica 85: Turner, A., and J. Kirkpatrick. 298. New York: CABI Publishing. 191–195. 2002. Effects of immunocontra- Rodriquez-Vivas, R., A. Ortega- Sekhon, A.S., A. Singh, P. Kaur, and ception on population, longevity, Pacheco, J. Rosado-Aguilar, and S. Gupta. 2002. Misconceptions and body condition in wild G. Bolio. 2003. Factors affecting and myths in the management mares. Reproduction Supple- the prevalence of mange-mite in- of animal bite cases. Indian ment 60: 187–195. festations in stray dogs of Journal of Community Medicine Wandeler, A., and J. Bingham. Yucatan, Mexico. Veterinary Par- 27(1). http://www.indmedica. 2000. Dogs and rabies. In Dogs, asitology 115: 61–65. com/journals.php?journalid= zoonoses, and public health, ed. Rubel, D., G. Zunino, G. Santillan, 7&issueid=43&articleid=535& C. Macpherson, F. Meslin, and A. and C. Wisnivesky. 2003. Epi- action=article. Wandeler, 64–90. New York: demiology of Toxocara canis in Singh, U.S., and K.K. Choudary. CABI Publishing. the dog population from two 2005. Knowledge, attitude, be- Wasi, C., P. Chaiprasithikul, P. areas of different socio-eco- havior, and practice: Study on Thongcharoen, P. Choomkasien, nomic status, greater Buenos dog-bites and its [sic] manage- and S. Sirikawin. 1997. Progress Aires, Argentina. Veterinary Par- ment in the context of preven- and achievement of rabies con- asitology 115: 275–286. tion of rabies in a rural commu- trol in Thailand. Vaccine Sup- Rupprecht, C., C. Hanlon, and T. nity of Gujarat. Indian Journal plement 15: S7–11. Hemachudha. 2002. Rabies re- of Community Medicine 30(3). Waters, D., S. Shen, and L. Glick- examined. The Lancet Infectious http://www.indmedica.com/ man. 2000. Life expectancy, Diseases 2: 327–343. journals.php?journalid=7&issue antagonistic pleiotrophy, and Rutberg, A. 2005. Deer contracep- id=57&articleid=702&action testis of dogs and men. The tion: What we know and what we =article. Prostate 43: 272–277. don’t. In Humane wildlife solu- Slater, M., and S. Shain. 2005. Feral Wheir, W., B. Dunbar, and S. tions: The role of immunocon- cats: An overview. The state of the Prasad. 2005. Immuno-steriliza- traception, ed. A. Rutberg, animals III: 2005, ed. D.J. Salem tion in dogs using Zona Pellucida 23–42. Washington, D.C.: and A.N. Rowan, 43–54. Washing- (Zp)-based vaccine. In Humane Humane Society Press. ton, D.C.: Humane Society Press. wildlife solutions: The role of Sadjadi, S. 2006. Present situation Spain, C.V., J.M. Scarlett, and K.A. immunocontraception, ed. A. of echinococcosis in the Middle Houpt. 2004. Long-term risks Rutberg, 77–90. Washington, East and Arabic North Africa. and benefits of early-age gonad- D.C.: Humane Society Press. Parasitology International 55, ectomy in dogs. Journal of the Widdowson, M.-A., G. Morales, S. Supplement: 197–202. Chaves, and J. McGrane. 2000.

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.gov/ncidod/EID/ land 187(11): 1389–1393. vol11no12/04-0775.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.

78 The State of the Animals IV: 2007