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Am. J. Trop. Med. Hyg., 74(5), 2006, pp. 850-855
Copyright © 2006 by The American Society of Tropical Medicine and Hygiene

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COMBINED HUMAN AND PORCINE MASS CHEMOTHERAPY FOR THE CONTROL OF T. SOLIUM

H. H. GARCIA*, A. E. GONZALEZ, R. H. GILMAN, L. H. MOULTON, M. VERASTEGUI, S. RODRIGUEZ, C. GAVIDIA, V. C. W. TSANG THE CYSTICERCOSIS WORKING GROUP IN PERU
Department of Microbiology, Universidad Peruana Cayetano Heredia, San Martin de Porras, Lima, Peru; Cysticercosis Unit, Instituto de Ciencias Neurologicas, Barrios Altos, Lima, Peru; Department of International Health, Johns Hopkins University Bloomberg School of Public Health, Baltimore, Maryland; School of Veterinary Medicine, Universidad Nacional Mayor de San Marcos, Salamanca de Monterrico, Lima, Peru; A.B.PRISMA, San Miguel, Lima, Peru; Parasitic Diseases Branch, Centers for Disease Control, Atlanta, Georgia


ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
A combined (human and porcine) mass chemotherapy program was tested in a controlled design in 12 village hamlets in the Peruvian highlands. A single dose of 5 mg of praziquantel was given to eliminate intestinal taeniasis in humans, and two rounds of oxfendazole (30 mg/kg) were administered to all pigs. The total population in the study villages was 5,658 resident individuals, and the porcine population at the beginning of the study was 716 pigs. Human treatment coverage was 75%, ranging from 69% to 80%. There were only a few refusals of owners for porcine treatment of their animals. The effect of the intervention was measured by comparing incidence rates (seroconversion in pigs who were seronegative 4 months before) in treatment versus control villages, before and up to 18 months after treatment. There was a clear effect in decreasing prevalence (odds ratio, 0.51; P < 0.001) and incidence (odds ratio, 0.39; P < 0.013) in the treatment area after the intervention, which did not leave to extinction of the parasite but stabilized in slightly decreased rates persisting along the follow-up period. Mass chemotherapy was effective in decreasing infection pressure in this hyperendemic area. However, the magnitude of the effect was small and did not attain the goal of eliminating transmission.


INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Taenia solium taeniasis/cysticercosis is endemic in most developing countries.1,2 The adult tapeworm (taeniasis) occurs only in humans and carries mild clinical manifestations or none at all. However, it is the source of infection with the larval form (cysticercosis), which affects humans and pigs. Human cysticercosis is a major cause of seizures and other neurologic symptoms in disease-endemic zones,3–6 and porcine cysticercosis carries important economical losses caused by damaged pork.1,7 The life cycle is sustained because of domestic pig raising and lack of sanitary conditions, which permit free-ranging pigs access to contaminated feces from a tapeworm carrier.

T. solium infection has been included into a short list of eradicable parasitic diseases,8,9 on the basis of several factors: 1) evidence of eradication in defined geographic areas (Europe, North America) through improvements in sanitation and living conditions; 2) a single (human) definitive host, source of cysticercosis infection; 3) domestic animals perpetuating the cycle, wild cycle not important in transmission; and 4) availability of control measures, including massive anthelminthic treatment of humans in endemic areas.10,11 Currently, control of porcine cysticercosis is based on inspection and condemnation of infected pig carcasses.12 Less than 10% of Peruvian pigs, however, are registered, and 55% are illegally slaughtered.7 In abattoirs where control and confiscation are not carried out, rates of infection among pigs may be as high as 30%.7 Thus, control measures to prevent human consumption are impractical and currently inadequate in endemic areas.

A series of specific control measures, in addition to abattoir inspection, must be instituted to prevent human and swine cysticercosis.13 Several groups have attempted to actively control T. solium in endemic areas by applying mass human chemotherapy,14–18 pig immunization,19–22 health education,23 and other interventions.24 However, elimination of taeniasis/cysticercosis has not been achieved to date, the effect of interventions has always been partial, and no conclusive data on sustainability exist. From all attempted interventions, mass chemotherapy has been consistently shown to decrease prevalence of infection in Ecuador,14 Mexico,17 and Guatemala,18 and thus seemed to be the most promising tool. By adding the use of oxfendazole, recently described to be effective for porcine cysticercosis,25 we performed, in an endemic area of Peru, the first combined human and porcine mass chemotherapy trial to control the transmission of T. solium.


MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Overall study design. Cohort study to evaluate the effect of a combined (human and porcine chemotherapy) intervention for the control of T. solium comparing the prevalence and incidence of porcine cysticercosis in treated versus comparison areas. Outcomes were evaluated every 4 months after the intervention for a total of 20 months.

Study site. The central highland area of Peru was selected because of shown endemicity7 and accessibility by road. The zone is cold and has at least two clearly defined seasons: dry from June to November and wet from December to May. Paved access highways are passable during all of the year, although connecting roads may not be used during the rainy season. A preliminary trip was performed to select an adequate study area on the basis of accessibility and their willingness to cooperate in a longitudinal project on the control of porcine cysticercosis. In this trip, several villages located less than 50 miles from Huancayo (population 300,000), the main city in the Department, were visited and inspected. The selection of communities near Huancayo was made because of the convenience of a city-based location for specimen handling, centrifugation, and storage.

Eight villages of the Quilcas district, located at 15 km west from Huancayo, were selected for the study. The selected villages were Veintisiete de Mayo, Santa Cruz, Pampas, Llacta, Colpar, Rangra, Casacancha, and Saño. Another village from a different district, Canchayllo, was also included to increase sample size. To increase the number of treatment units, the larger villages (27 de Mayo, Santa Cruz, Canchayllo, Pampas, Saño) were split in two treatment units of similar size (Figure 1Go). After the study communities were chosen, a second visit was done to meet key village leaders and to evaluate their interest in the project and willingness to participate. Censusing and mapping was initiated after the leaders had time to consult the community and confirm their consent. Before starting the project, the field personnel gave several talks to groups of villagers about the project and the disease. During these talks, the presence of intestinal parasites was identified by villagers as one of their principal health concerns; thus, treatment of geohelminthiasis was offered gratis as part of the study. Also, free of cost, human and veterinary medical attention, including animal vaccination campaigns for porcine hog cholera, was offered during each field trip. At the end of the study, all individuals diagnosed as having carried a tapeworm were re-visited and offered follow-up parasitological examinations and anti-parasitic treatment. The study was approved by the institutional review boards of the Johns Hopkins School of Hygiene and Public Health, the Centers for Disease Control and Prevention, and the Universidad Peruana Cayetano Heredia.


Figure 1
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  		    FIGURE 1. Study villages and treatment assignment.

 
Data collection. All pigs in each village (excluding pregnant sows, to avoid the risk of miscarriage, and piglets < 2 months old) were identified and ear-tagged with consecutive numbers. Other information recorded at each sampling included the age and sex of the pig, date of the sampling, owner, house, village, and trip number. At each trip, new animals were ear tagged and included in the cohort. All pigs were vaccinated against hog cholera.

Samples. The effect of the intervention was monitored by serology in pigs. At each visit, a 5-mL venous blood sample was taken from the cava vein of pigs using vacuum tubes. Samples were centrifuged in Huancayo the same day and aliquoted in two sets of 1.5-mL vials, stored at –4°C, and sent frozen to the laboratory in Lima to be assayed by enzyme-linked immunoelectrotransfer blot (EITB; Western blot).26 Blood samples were assigned consecutive numbers and linked with the pig’s identifier in a database. This process was repeated every 4 months (five times after the intervention).

Intervention. The control intervention consisted of one round of mass chemotherapy for intestinal tapeworm infection in humans with a single dose of 5 mg/kg of praziquantel27 and two rounds of mass chemotherapy for porcine cysticercosis with a single dose of 30 mg/kg of oxfendazole as originally described by our group.25 Villages or treatment units were paired based on size and distance from the main road and randomized to be treatment or comparison areas. Human population in comparison areas received pyrantel pamoate (a single dose of 11 mg/kg), a different anti-parasitic drug specific for intestinal nematodes. 27 de Mayo and Santa Cruz were originally scheduled to be half-treatment and half-control but received treatment in the whole village because of a procedural error. Llacta, Casacancha, and one half of the extension of Canchayllo, Pampas, and Saño received anti-parasitic treatment and were considered treatment units. Colpar and Rangra (purely control villages) and the other halves of Canchayllo, Pampas, and Saño were control units (Figure 1Go). The intervention was performed in July 1996 in all communities but Saño, which was treated in September 1996. It took 2–3 days to complete the intervention in each treatment area.

Processing. Sera samples were processed by EITB as originally described.26 In brief, this assay uses seven purified T. solium glycoprotein antigens (diagnostic bands GP50, GP42-39, GP24, GP21, GP18, GP14, and GP13, the number indicating the respective molecular weight in kilodaltons) in an immunoblot format to detect infection-specific antibodies. Reactions to at least one band are considered positive.

Data analysis. Prevalence calculations included only pigs that were bled in each sampling round. For incidence calculations, animals were defined as at risk (naive) if they were seronegative at the beginning of a period, or if being seropositive, seroconvert to negative during the 4-month observation period. An incident case was defined as an animal whose serology changed from negative to positive between two consecutive sampling rounds (one period). Confidence intervals were calculated using standard methods.28 The main analysis compared incidence in pigs (new seropositive animals) in treatment versus control units. Logistic regression models were fitted to examine the role of factors potentially associated to pig seropositivity prevalence and incidence. Generalized estimating equations29 were used to obtain population-averaged robust estimates accounting for the within group correlation for repetitions of the same animals. Examined factors include age group, sex of the animal, village, and period.


RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Characteristics of control and intervention areas. Baseline characteristics of the study population have been published elsewhere.30 Because of the inclusion of 27 de Mayo and Santa Cruz, there were more individuals in the treatment areas (Table 1Go).


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TABLE 1
Characteristics of treatment and comparison areas in Huancayo, Perú, 1996
 
Intervention coverage. Seventy-five percent (4,237/5,658 residents in the study area) of the human population received the intervention or the comparison drugs. There were no differences in coverage by sex (1,999/2,696 males, 74.1% versus 2,238/2,962 females, 75.6%; odds ratio [OR], 0.93; P = 0.222) or regarding the allocation area (1,531/2,049 residents in the comparison area, 74.7% versus 2,706/3,609 in the treatment area, 75.0%; OR, 0.99; P = 0.829). Compliance by age group varied from 71.0% in children younger than 10 to 80.3% in individuals 11–20 years of age. Compliance by village ranged from 69.2% in Canchayllo to 82.4% in Rangra.

Animal population and sampling. Given the rapid turnaround of pigs, it was not possible to keep an updated pig census to quantify the sampling or intervention coverage for each trip. However, a very high proportion of pigs were sampled, principally because hog cholera vaccines and veterinary attention gained the support of the population and sustained it throughout the study. There were only a few refusals from cases where an animal coincidentally died soon after a sampling campaign and the family attributed the death of the animal to the blood sampling. The small proportion of missing animals can be estimated from the fact that only 119 from 1,388 pigs who had two or more samples (8.6%) were not sampled in consecutive trips.

A total of 5,308 samples were collected along eight sampling rounds, corresponding to 3,177 pigs. From these animals, 1,789 (56.3%) were only sampled once, 871 (27.4%) were sampled twice, and 517 (16.3%) were sampled more than twice. Eleven animals had six samples and three animals had seven samples.

The total number of pigs varied by sampling round (716, 923, 603, 771, 661, 571, 589, and 481, respectively). The age distribution was very similar between all sampling rounds, with a peak number of animals between 4 and 6 months of age and a gradual decrease at older ages. There were similar numbers of male and female pigs in all age groups except for animals older than 12 months of age, in which there were three times more female pigs. Overall seroprevalence in the three pre-intervention rounds ranged from 54.8% (507/923) to 64.3% (388/603). Seroprevalence by age increased continuously after age 6, similarly in both male and female pigs.

Effect measurement. Unadjusted prevalence ratios. Comparison of prevalence ratios between treatment and control areas showed similar pre-treatment prevalence but lower prevalence in the treatment areas after the intervention (Table 2Go). The difference persisted over time (Figure 2Go).


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TABLE 2
Mean porcine seroprevalence ratios for each treatment unit before and after the intervention
 

Figure 2
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  		    FIGURE 2. Comparison of unadjusted porcine prevalences (left) and incidences (right) between treatment and comparison areas.

 
Unadjusted incidence rates. Pigs with at least two consecutive samplings after the intervention were entered in an incidence database. There were 2,342 animals sampled at least twice from round 3 onward (five defined post-intervention periods). A total of 224 seronegative pigs were exposed during period 1, 305 in period 2, 251 in period 3, 257 in period 4, and 143 in period 5. Comparison of incidences between treatment and control areas showed a lower incidence in the treatment areas after the intervention (Table 3Go), persisting for the whole follow-up period (Figure 2Go).


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TABLE 3
Mean porcine incidence rates for each treatment unit before and after the intervention
 
Multivariate analysis of prevalence. In the best logistic regression model, examining the effects of treatment, period (period was categorized as before or after the intervention), age of the pig, village, and the interaction between treatment and period, a protective effect was shown in the treatment area after the intervention (OR, 0.51; P < 0.001; Table 4Go). Older animals had higher prevalence. There was no association between prevalence and sex of the pigs, and inclusion of this variable did not improve the model.


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TABLE 4
Factors associated with prevalent cases of porcine cysticercosis, Perú, 1996
 
Multivariate analysis of incidence. Pig serological cumulative incidence for each period was also modeled by logistic regression, assuming that exposure periods were similar and that the odds of infection for a pig that did not get infected through the previous period were similar to those of newly entered animals of similar age. Incidence in the immediate pre-treatment period (data on 192 pigs) was included as a baseline stratum, Examined variables included treatment, period, age group, sex, village, and the interaction between treatment and period. Results of the best model are shown in Table 5Go. A protective effect was shown in the treatment area after the intervention (OR, 0.39; P = 0.013). Older animals had lower incidence rates. There was no association between incidence and sex of the pigs, and inclusion of this variable did not improve the model.


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TABLE 5
Factors associated with incident cases of porcine cysticercosis, Peru, 1996/1997
 

DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Improvement in sanitary conditions and commercial porcine production technology have been recognized as effective measures against cysticercosis.10 Other strategies for control emphasize the elimination of egg transmission in the environment using community health education23 and mass chemotherapy of the human population.14–16,27 These strategies are based on the assumption that if egg dispersion is stopped, the disease cycle will be broken. These measures were successfully used to control other animal cestodes such as Echinococcus granulosus and consequently proposed as a model for controlling T. solium cysticercosis.31 Unfortunately, sustainable control of T. solium has not yet been achieved.24,32

Chemotherapy of human carriers aims to clear all the adult forms of the parasite. Anderson and May33 developed a mathematical model to explain the effect of mass chemotherapy on human parasitic infections, highlighting two important issues: one, the rapidity with which certain helminths return to their pre-control level once chemotherapy ceases, and two, the differential impact of mass treatment on the intensity of infection and prevalence. It is likely that mass treatment of humans for tapeworm infection, leaving the porcine reservoir untouched, will result in a return to the original prevalence in a short time. There is no data to assume, however, that the intensity of infection will be the same.

This study showed an effect of combined human and porcine chemotherapy in both the prevalence and incidence of porcine infection in a wide endemic area in the Peruvian highlands. Part of this effect seems to have maintained transmission levels in treatment units during a time of secular increase (seen in control villages). Although the effect persisted for almost 2 years after the intervention, its magnitude was much smaller than expected. Several factors including incomplete coverage (~75% in humans and 90% in pigs), treatment failures, or reinfection, could contribute to explain the partial efficacy of this intervention. In our models, coverages of more than 90% are required to enhance the chances eliminating of T. solium transmission.34 Although tapeworms have been reported to live for decades, we designed our intervention using a conservative assumption that the life span of the tapeworm was greater than or equal to 5 years.34 Surprisingly, the life span seems to be significantly shorter than 5 years, and therefore we underestimated the efforts needed to control infection. It also has to be understood that antibody serology measures exposure (response to specific antigens) and not necessarily established infection. An assay able to quantify parasite biomass would be required for direct effect measurement. In any case, the data reported here show that the parasite can be affected but is able to achieve an state of endemic stability soon after a change on its transmission. If infection dynamics are not drawn out to an extinction scenario, the effect on T. solium as a whole will be limited, as shown by this program. It is probable that multiple rounds of intervention could have multiplied the effect.

The transmission cycle of T. solium can be initiated from either the intermediate or definitive host. Control of T. solium by intervening only in the human population will be broken because of transmission from existing infected pigs. Therefore, elimination of T. solium from a disease-endemic area using only a human treatment strategy would require consecutive interventions for at least the average life span of the porcine reproductive stock, approximately 3 years.34 Furthermore, the interval between interventions should not exceed the pre-patent period so that if a new tapeworm infection occurs, it would not have enough time to infect more pigs. This is also true if only the porcine population is targeted. Interventions in the porcine population have to be sustained for the entire life span of the tapeworm (not yet known). Likewise, the pig population has to be treated within the interval required for cyst maturation. The idea behind concurrent treatment of both human and porcine populations is that targeting both hosts will reduce the amount of time required to achieve elimination and will increase the likelihood of success.10 We selected combined human and porcine chemotherapy to preclude new taeniasis infections from reestablishing the endemicity, based on the cestocidal efficacy and practical dosage of oxfendazole.25,35,36

The main advantage of combined therapy and any strategy that cleans pig meat is that it will provide a tangible economic incentive to the owner in the short term. Only through active participation of peasants it can be expected that an intervention program be sustained and educational programs be accepted. The price of a pig is adversely affected by the presence of cysticercosis. Cysticercosis status is an important factor affecting pig prices in areas where infected pigs and pork are freely traded.7,10

It has been suggested that pigs only get infected at early ages. In this study, however, porcine seroprevalence increased linearly with the age of the animal. This may indicate either that older animals are as susceptible as younger pigs or that some pigs are protected through the initial exposure period but become susceptible later, perhaps through maternal transfer of antibodies (that has been shown to occur in T. solium cysticercosis,37 and it is protective for other larval cestode infections). Alternatively, seroconversion may occur at any time but established infection only at determined age groups.

While improvements in sanitation in poor zones are not to be expected in the near future, control programs are needed to face this endemic disease in the short and medium term. The data here provided shows that a single intervention will hardly succeed in eliminating T. solium taeniasis/cysticercosis. Either sustained interventions or additional alternative measures are required for this purpose.

Received October 13, 2005. Accepted for publication December 6, 2005.

Acknowledgments: We thank the population of Quilcas, who made it possible to realize the study. Help from E. Perez, Y. Arana, V. Mallqui, J. B.Phu, and D. Sara in sample management and data collection is also acknowledged.

Financial support: This study was funded by Grants U19-A145431, ABC, and ITREID from the National Institutes for Health and Fogarty Foundation. Research Grants P01 AI51976, U01 AI35894, and TW05562 from the National Institutes of Health, 01107 from Food and Drug Administration, 063109 from The Wellcome Trust, and 23981 from The Bill and Melinda Gates Foundation fund other cysticercosis research by the authors. The sponsors had no role in the design or writing of this work.

Other members of the Cysticercosis Working Group in Perú include H. Mayta, J. Jimenez, P. Castillo (Universidad Peruana Cayetano Heredia, Lima, Peru); Martinez SM (Instituto de Ciencias Neurologicas, Lima, Peru); C.A.W. Evans (Cambridge University, Cambridge, UK).

* Address correspondence to Hector H. Garcia, Department of Microbiology, Universidad Peruana Cayetano Heredia. Av. H. Delgado 430, SMP, Lima 31, Peru. E-mail: hgarcia{at}jhsph.edu Back

Authors’ addresses: Hector H. Garcia, Manuela Verastegui, and Silvia Rodriguez, Biology Department of Microbiology, Universidad Peruanan Cayetano Heredia. Av. H. Delgado 430, SMP, Lima 31, Peru, E-mail: hgarcia{at}jhsph.edu. Armando E. Gonzalez and Cesar M. Gavidia, School of Veterinary Medicine, Universidad Nacional Mayor de San Marcos. Av. Circunvalacion s/n, San Borja, Lima 3, Peru, E-mail: emico{at}terra.com.pe. Robert H. Gilman and Lawrence H. Moulton, Department of International Health, Johns Hopkins University Bloomberg School of Public Health, 615 N. Wolfe Street, Baltimore, MD 21205, E-mail: rgilman{at}jhsph.edu. Victor C.W. Tsang, Immunology Branch, Division of Parasitic Diseases, National Centers for Infectious Diseases, Centers for Disease Control and Prevention, 4770 Buford Highway, Mailstop F-13, Atlanta, GA 30341-3724, E-mail: vct1{at}cdc.gov.


REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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