Parasitic causes of meat and organs in cattle at four slaughterhouses in Sistan‐Baluchestan Province, Southeastern Iran between 2008 and 2016

Abstract This 8‐year (from 2008 to 2016) retrospective study calculated the percentage of carcass and organ (lung and liver) condemnations and estimated the direct financial costs at four slaughterhouses in Sistan‐Baluchestan Province, Southeastern Iran. Each carcass and organ (lung and liver) was thoroughly examined through inspection, palpation and incision following the standard protocol. Identification of the parasites was performed macroscopically. The total direct economic loss due to meat's condemnation was estimated by adding weights of each organ or carcass part and multiplying individual organ totals by their 2016 market unit price. A total of 857,039 cattle were slaughtered during this period, 64,497 livers (7.5%), 31,401 lungs (3.6%) and the carcasses of 1,171 cattle (0.1%) were condemned due to lesions caused by parasites. The main parasitic lesions in the condemned livers were attributed to Echinococcus granulosus (4.2%), Fasciola spp. (3.1%) and Dicrocoelium dendriticum (0.1%). All the condemned lungs were due to E. granulosus (3.6%). Taenia saginata cysticerci were detected in 0.1% of inspected animals. Liver condemnation due to cystic echinococcosis was the highest in fall (4.7%, p < 0.001); while lung condemnation was the highest during spring (3.98%, p < 0.001). Liver condemnation due to Fasciola spp. was the lowest in winter (2.99%, p < 0.001). Carcass condemnation as a result of cysticercosis was the highest in summer (p < 0.001). Considering the 2016 market prices, condemnations due to the studied parasites caused direct costs estimated U.S. $ 3,191,879. To the best of our knowledge, this is the first report estimating the monetary losses due to parasitic infections in the slaughterhouses of this province. Due to the high financial impact of the studied parasites, a control programme should be implemented to decrease this impact.


| INTRODUC TI ON
Meat inspection is one of the most important procedures ensuring the delivery to markets of safe food and enable countries to guarantee the safety and quality of their foods entering international trade (Jaja et al., 2016). During the last two decades, the population of Iran increased from around 66.13 to about 83 million (Iranian Civil Registration Organization, 2019) leading to a significant increase in demand for food specially, animal proteins. Cattle, sheep, goats, camels and their products are the main source of red meat for Iran (Samkange et al., 2019). The slaughterhouse is a relevant occasion for screening infections, mainly those causing zoonotic diseases.
Zoonotic infections such as tuberculosis, cysticercosis and cystic echinococcosis, in addition to causing economic losses, are also important in public health.
Iranian Sistani and Brahman cattle breeds are an important and integral part of agricultural production in the Sistan-Baluchestan Province, Iran. Iranian Sistani and Brahman cattle are an important dual-purpose breed in eastern Iran .
The aim of the current study was to provide baseline data on the common causes of slaughterhouse condemnations of livers, lungs and carcass in a meat inspection survey at four slaughterhouses in the Sistan and Baluchestan Province, Iran. The financial losses due of these condemnations were also estimated for the whole period.

| MATERIAL S AND ME THODS
This study was conducted in Sistan and Baluchestan Province, Iran with a geographical area of 180,726 km 2 and 2.5 million inhabitants. This Province is bordered by Pakistan in the east and Afghanistan in the northeast, by the Southern Khorasan Province in the north; by Kerman province in the west and by the Gulf of Oman in the south.
Geographically, the Province consists of two land structures. In the North, Dasht-e-Sistan formed by Hirmand alluvium holds the largest fresh water lake in the country. The Southern region is mostly mountainous with a variety of climates due to the vicinity of Taftan Volcano and Oman Sea (Figure 1) Record of meat-inspection from these slaughterhouses were used to collect information lung, liver and carcass condemnations due to parasitic infections. Each carcass and organ (lung and liver) was thoroughly examined through inspection, palpation and incision following the standard protocol. Costs due to the parasite-related condemnations over the 8-year study period were estimated based on2016 market price of carcass, liver and lungs of cattle (Borji, Azizzadeh, & Kamelli, 2012;Borji & Parandeh, 2010).

| RE SULTS
During the 8-year period, 857,039 cattle were slaughtered at the slaughterhouses of Sistan-Baluchestan Province, Southeastern Iran. The livers of 64,497 (7.5%), the lungs of 31,401 (3.6%) and the carcasses of 1,171 (0.1%) cattle were condemned due to parasitic infections.
Hydatid cysts (HC)The condemnation rate of lungs due to HC was 3.6% of them were HC (Table 1). The annual rate of lung condemnations attributable to HC decreased from 6.3% to 4.4% from 2008 to 2016 (p < 0.001), respectively. The rate of condemned livers (4.2%) due to HC was significantly higher than the lungs (3.7%) (p < 0.001).

| Fasciola spp.
The condemnation rate of inspected livers for Fasciola spp. was 3.2% (

| Dicrocoelium dendriticum
The condemnation rate due to D. dendriticum of livers was 0.1% (

| Taenia saginata cysticerci
The overall rate of condemned carcasses due to T. saginata cysticercus infection was estimated to 0.1% (Table 3). Carcasses condemnation due to T. saginata cysticercus infection was statistically highest in summer (p < 0.001).
Condemnation carcass of cattle due to T. saginata cysticerci rate decreased from 0.12 to 0.06 between 2008 and 2013 and then increased during the rest of study period (p < 0.001) ( Table 3).  (Table 4).
There was a significant seasonal variation of liver and lung rate condemnation due to HC. Seasonal differences may be due to seasonal variation of animal ages since echinococcosis is a chronic infection with cattle remaining infected for the rest of life or a possible gradually degeneration of cysts.
Several studies showed that the HC is a growing concern for public health, as it is considered as an emerging/reemerging infection in several regions of the world. Previous studies (Mahmoudi et al., 2019) estimated the prevalence of HC in Iranian adult humans between 1990 and 2017 to 5%.
According to the present study, 3.3% of livers were condemned due to liver flukes. This rate was similar to a study in the north Khorasan Province, East Iran (5.33%) (Borji & Parandeh, 2010) and lower to North Iran (20.1%) . In the West of Iran, lower rate was reported (1.5%) (Shahbazi et al., 2016;Abdi et al., 2013). D. dendriticum condemnation rate showed a marked fluctuation during the study period that may be due to substandard training of inspectors, rapid slaughter rates and poor meat inspection facilities.
The rate of Fasciola spp. is lower in South Eastern Iran than has been reported elsewhere in the world. For instance, in Brazil a rate of 11.9% (Pritsch et al., 2019)  The rate of T. saginata cysticercus in the slaughtered cattle investigated in the present study (0.13%) was lower than those reported in other regions of Iran (0.25%) (Khaniki et al., 2010;Oryan et al., 2012) but higher than earlier reported from north Khorasan Province (0.004%) (Borji & Parandeh, 2010 (Jansen et al., 2018), 0.6% in Brazil (Rossi et al., 2017) and 3% in Rwanda (Nzeyimana et al., 2015). Additionally, bovine T.
saginata cysticercus in the Middle East and North Africa based on meat inspection was identified in Egypt and Israel, with occurrence ranging from 0.2% to 20% (Saratsis et al., 2019). There is a need for a more thorough investigation, including carcass dissection and immunological tests (Mushonga et al., 2018) Consequently, bovine T. saginata cysticercus may be more common in late spring (Taylor et al., 2016). to 19 March 2016). This figure is gross underestimation of the real total financial losses as it did not take in account several indirect losses such as reduced productivity, costs of veterinary care as well as deaths (Perry & Randolph, 1999). Consequently, even though the financial loss due to condemnation of carcasses and organs (lungs and livers) due to parasitic lesions was high, the total impact of parasites on the region's livestock industry is higher than what was estimated in the current study. Moreover it should be noted that the rate of parasitic infections based on retrospective studies in slaughterhouses are certainly underestimated and the economic impact of these infections, some of them were present but the veterinarians did not condemned the organs.

| CON CLUS ION
The estimate of the financial loss is, almost certainly, a gross underestimate of total financial losses as it takes no account of the premature deaths, low body weights and sub-optimal milk that can result from parasitic infections. Based on organ condemnation rates observed in this study, implementation and periodic review of routine livestock infection surveillance systems, including an effective trace-back system, are recommended. This will help to reduce the burden of infections in animals. However, further studies are needed to obtain a complete overview of the epidemiology of these parasitic infections in other definitive hosts, in order to implement control and preventive measures specifically targeting farms in the studied region.

ACK N OWLED G EM ENTS
The authors thank Sistan and Baluchestan Veterinary Organization for permission to collect the data from the source.

CO N FLI C T O F I NTE R E S T
The authors declare that there is no competing interests. Writing-review & editing.

E TH I C S A PPROVA L A N D CO N S E NT TO PA RTI CI PATE
With regard to what constitutes appropriate ethics and consent/animal welfare statements, Retrospective studies did not require ethics committee.

PEER R E V I E W
The peer review history for this article is available at https://publo ns.com/publo n/10.1002/vms3.475.

DATA AVA I L A B I L I T Y S TAT E M E N T
The datasets used and/or analysed during the current study available from the corresponding author on reasonable request.