Prevalence of Taenia saginata Larvae ( Cysticercus bovis ) in Feedlot Cattle Slaughtered in a Federal Inspection Type Abattoir in Northwest México

Introduction

Bovine cysticercosis is caused by Cysticercus bovis (C. bovis), the larval stage of Taenia saginata. Cattle become infected by consuming food or water contaminated with eggs from adult parasites infecting the small intestine of humans. Humans become infected by ingesting raw or undercooked meat from cattle infected with viable cysticerci (Abuseir et al., 2007; Ogunremi and Benjamin, 2010). Bovine cysticercosis is also a cause of major economic losses to the livestock industry due to the condemnation of infected carcasses (Regassa et al., 2009; Wanzala et al., 2003).

Worldwide, diagnosis of bovine cysticercosis is made through postmortem inspection of carcasses. In México, inspection of meat is regulated by federal code NOM-009-ZOO-1994, which consists of a series of partial cuts in the heart, masseters, tongue, liver, and diaphragm, sites where cysticerci are more often localized (Wanzala et al., 2003). Official reporting of bovine cysticercosis is not common practice in México. In the early 1970s, an epidemiological study for bovine cysticercosis was conducted involving 14 states of México, reporting a prevalence of bovine cysticercosis ranging from 0.001 to 0.92%. In 1973, the state of Durango reported a prevalence of 1.1%, while in a similar study conducted in the state of México in 1976 and 1977, the prevalence reported was 0.15% and 0.27%, respectively. The last report available for prevalence of bovine cysticercosis for the state of Baja California was made in 1980 in a survey in Tijuana, showing a prevalence of 0.29% (Quiróz-Romero, 2005).

The northwest economic region of México includes the states of Baja California, Baja California Sur, Sonora, and Chihuahua. During 2009, these 4 states sent to slaughter a total of 997,800 heads of cattle, from which Baja California contributes with 337,560 animals (34%). Approximately 320,000 heads of cattle, >95% males, are purchased each year and transported by trucking companies to Baja California from yearling/stocker operations in the states of Baja California Sur, Chiapas, Chihuahua, Durango, Guerrero, Jalisco, Michoacán, Nayarit, Nuevo León, Oaxaca, San Luis Potosí, Sinaloa, Sonora, Tabasco, Tamaulipas, Veracruz, and Zacatecas (FIRA, 2010). The cattle are housed in the Mexicali Valley among 32 intensive animal feeding operation feedlots, were they spend an average of 120 days feeding on high-energy rations. After feedlot, finished cattle are sent to slaughter, cut, and pack at any of four certified Mexican Federal Inspection Type (TIF) and United States Department of Agriculture approved slaughterhouses named TIF 54, TIF 120, TIF 301, and TIF 511. In 2009, meat production in the Mexicali Valley was 98,000 tons, accounting 95% of the total production for the state of Baja California. The same year, slaughterhouse TIF 301 sent to slaughter 82,800 animals, contributing with 28% of Baja California's total meat production in that period. The objective of this study was to establish the prevalence of C. bovis through postmortem inspection of carcasses in feedlot cattle slaughtered at TIF 301, a Federal Inspection Type abattoir located in the Mexicali Valley in the state of Baja California, northwest México.

Materials and Methods

The study was conducted in the Mexicali Valley, state of Baja California in northwest México, between October 2008 and July 2009, in a Federal Inspection Type (TIF 301) slaughterhouse. The postmortem inspection of carcasses was performed in all animals sent to slaughter during the study period by federal certified veterinarians (FCV). A total of 52,322 carcasses were subject to postmortem inspection seeking to identify any cyst lesion found in the heart, tongue, masseters, liver, lungs, or muscular mass. Those lesions are considered as suggestive of cysticercosis according to federal code NOM-009-ZOO-1994. Tissue sections of 3–6 cm³ (1–2 in³) containing lesions suggestive of cysticercosis were identified and sent to the laboratory for diagnostic confirmation. The identification of C. bovis was performed using stereoscopic microscopy by qualified personnel from the Laboratory of Parasitology at the Instituto de Investigaciones en Ciencias Veterinarias at Universidad Autónoma de Baja California. Viable (live) cysticerci were classified as immature when cysts lacked an evident protoscolex and as mature when the cyst presented an evident protoscolex. Cysticerci were also classified as calcified when cysts appear as a colloid, caseous, or as a solid mass, depending on the degree of mineralization (Minozzo et al., 2002; Abuseir et al., 2006). The prevalence of cysticercosis was calculated by dividing the total number of carcasses with a positive diagnosis of cysticercosis by the total number of carcasses inspected. Odds ratio (OR) was calculated with a confidence interval (CI) of 95%. Also, Chi-square (Xi ²) was calculated to establish statistical association between positive cases of carcasses of cattle introduced from other states of México and cattle native to Baja California.

Results

A total of 52,322 cattle were slaughtered and inspected at slaughterhouse TIF 301 located in the municipality of Mexicali, Baja California, México, including 31,393 (60%) animals purchased from 17 states of México and 20,929 (40%) cattle native to Baja California. FCV detected 208 carcasses with lesions suggestive of cysticercosis, from which 109 were found to be positive for cysticercosis after morphological identification of the parasite using stereoscopic microscopy. The overall prevalence of bovine cysticercosis was established in 0.21% (109/52,322), equivalent to 2.1 carcasses positive per 1000 animals; for cattle purchased from other states of México, the prevalence was 0.28% (88/31,384), equivalent to 2.8 carcasses positive per 1000 animals; and for cattle native to Baja California, the prevalence was 0.10 (21/20,929), equivalent to 1.0 carcass positive per 1000 animals. The results show 2.8 times more cases positive for bovine cysticercosis in cattle purchased from other states of México compared to positive cases of cattle native to Baja California (OR=2.8, 95%; CI 1.71–4.66; p<0.0001) (Table 1). Tracking the specific state of origin of cattle was not possible because all ear tags were removed from the animals at arrival to feedlot in order to sort into similar types and sizes. Based on the lesion detected during the postmortem inspection performed at TIF 301, the sensitivity of the postmortem inspection, when compared to a gold standard of stereoscopic microscopy, was 52.4% (95% CI 45.38%–59.35%). The prevalence obtained in this study was 28% lower than the last available survey of bovine cysticercosis for Baja California, conducted in Tijuana in 1980, with a reported prevalence of 0.29% (Quiróz-Romero, 2005). Our results are also comparable to those reported for bovine cysticercosis in European countries such as Spain, with a prevalence range of 0.007%–0.1%; Belgium, 0.03%–0.2%; Italy, 0.02%–2.4%; Denmark, 0.1%–0.7%; and Germany, with 0.4%–0.8% (Eichenberger et al., 2011). The organ with the most frequent finding of C. bovis was the heart with 93 cases, of which 14 were viable and 74 were calcified cysticerci, followed by the liver with 8 cases, with 2 viable and 6 calcified cysticerci, and masseter muscles with 8 cases, with 2 viable and 6 calcified cysticerci (Table 2). No cysticerci, viable or calcified, were detected in the tongue.

Discussion

Our findings suggest T. saginata egg contamination of forage and water in the states of origin of cattle, where the sociocultural and economic situation is low, with poor sanitation, poor animal husbandry practices, and high prevalence of parasitic infections among the general population, which increases the risk infection of Taenia and other parasitic infections in cattle. Our results also suggest T. saginata infection in the human population working in the feedlot cattle production systems of the Mexicali Valley, which implies a public health problem that needs to be addressed by health and sanitary authorities.

Open-air fecalism is a common practice in rural areas where stocker operations and feedlot facilities are located. We have knowledge of the occurrence of T. saginata infection in feedlot workers from the Mexicali Valley detected by state health authorities. Bovine cysticercosis results by consuming food or water contaminated with eggs from adult parasites infecting humans. Mature tapeworm proglottids containing thousands of eggs are commonly passed in the feces of infected individuals and can contaminate water, forage, grain, and other ingredients used to prepare feeding rations, favoring infection of cattle (Lees et al., 2002; Ogunremi et al., 2004).

Given the low sensitivity of postmortem examination ranging from 10% to 50% (Scandrett et al., 2009; Eichenberger et al., 2011), the actual prevalence of bovine cysticercosis can be up to 10 times higher than that reported in this study (Dorny and Praet, 2007), resulting in an underestimation of the magnitude of the problem of T. saginata infection in the human population, especially in regions characterized by intensive cattle production, like the Mexicali Valley. The findings of cysticerci by anatomical location show that the heart was the site where the presence of the parasite was more frequently found and confirmed, followed by the liver and masseter muscles; this is consistent with the reports of cattle naturally and experimentally infected with T. saginata eggs, demonstrating an anatomical distribution of parasites similar to that reported in this study (Minozzo et al., 2002; Wanzala et al., 2003). In our study, the highest proportions of cysts were observed in the heart. A simple technique consisting of performing additional cuts to the heart could increase the sensitivity of the routine postmortem meat inspection, minimizing additional damages to valuable muscular masses of the carcass (Eichenberger et al., 2011).

It is important to emphasize that the majority of cysticerci (71.4%) found in cattle native to the state of Baja California were detected in the vesicular state, which is fully viable and capable of producing tapeworm infection if consumed. This suggests that cattle from other states of México acquire T. saginata infection through contaminated forage or water in their place of origin, while animals native in the state of Baja California were infected at the feedlot premises (Table 3). This can be explained considering that the time the animals spend at the feedlot systems in Mexicali does not exceed 4 months and according to the pathophysiology of cysticercosis, it takes 4–6 months to begin the process of inflammation, infiltration, necrosis, and mineralization of the parasite (Cayo-Rojas et al., 2011). The prevalence of bovine cysticercosis established in 0.21% for this study at slaughterhouse TIF 301 is lower than the only previous report available for Baja California in a survey made in the municipality of Tijuana in 1980, where prevalence was established in 0.29% (Quiróz-Romero, 2005). The prevalence obtained here is also comparable to that of countries reporting light infections with low numbers of cysticerci found during postmortem inspection. However, given that the sensitivity of the postmortem inspection has been calculated to be as low as 16.5% (Eichenberger et al., 2013), it is possible that an undetermined number of carcasses pass as being free of cysticerci and that the meat reached both domestic and international wholesale markets, increasing the possibility of human infection and causing substantial economic loss through condemnation of infected meat and trade restrictions for endemic regions.