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CASE NOTES

Lamb icteric carcase condemnations due to Anaplasma ovis

Iria Macian1, Karen Hammad1, Andrea Capilla1, Raquel Marín1, Ada Marcos1, Marcos Rupérez1, Joel Bueso-Ródenas2, Héctor Ruiz1

1. Ruminant Clinical Service of the Veterinary Faculty of Zaragoza (SCRUM). Animal Pathology Department, C/ Miguel Servet 177. 50013, Zaragoza, Spain
2. Department of Animal Production and Public Health, Faculty of Veterinary Medicine and Experimental Sciences, Catholic University of Valencia San Vicente Mártir, Spain

Posted Flock and Herd November 2024

Introduction

During the late spring of 2020, a farm in the north-western region of Spain reported a concerning increase in the number of lamb carcase condemnations due to severe jaundice, rendering them unfit for consumption. This situation persisted through early summer, causing significant economic losses for the livestock producer.

As a result, the case was referred by the farm veterinarians to the Ruminants Clinical Service of the Veterinary Faculty of Zaragoza to identify the cause and ways by which to mitigate the issue.

History

This case occurred on a 1,000-head sheep meat farm raising the Rasa Aragonesa breed, located in the province of Huesca in the north-western part of Spain. The farm followed a traditional extensive management system, where the sheep were only housed a few days before lambing and during the first week post-partum.

The lambs from the affected group were born in March 2020 with condemnations starting in late May 2020. These animals were intended for meat production under the Protected Geographical Indication (PGI) label "Ternasco de Aragón" (two- to three-month-old lambs with a live weight of 21-23 kg at slaughter). The lambs were housed throughout their lives, being fed straw, compound feed, and water ad libitum. In contrast, the ewes were sent out to graze in the morning and returned to the farm in the late afternoon from the first week post-partum. The lambs were weaned at around 45 days of age once they reached an adequate weight. After weaning, they were fattened on the farm until they reached the required slaughter weight according to PGI guidelines.

The problem of jaundiced lamb carcase condemnation first appeared in May 2020, despite the management practices of the farm remaining the same as in previous years. The farmer observed no abnormalities during the lamb rearing process, with mortality rates below 5%, and the lambs grew adequately without showing any obvious signs of illness. Both the farmer and the veterinarians were therefore surprised and perplexed when this problem arose at the slaughterhouse after the lambs were processed.

Clinical Findings

Following the initial report of the issue to the Ruminant Clinical Service, a five-week follow-up of the lambs on the farm was conducted from the last week of May until the first week of July 2020. The lambs were inspected both ante-mortem, the day before being sent to the slaughterhouse, and post-mortem after slaughter during carcase processing and subsequent refrigeration.

A total of 358 lambs from the farm were examined during this period, all managed under the same protocol regardless of the week they were slaughtered. Initially, prior to loading the animals for transport to the abattoir, each lamb underwent a complete clinical examination, assessing body condition, rectal temperature, mucous membrane colour, and any clinical signs of illness. However, none of the lambs showed clear signs of disease or jaundice, except for mild hyperthermia in some animals, which was attributed to handling stress, and pale mucous membranes, particularly noticeable in the ocular sclera of a few lambs. Blood and serum samples were collected from lambs with any abnormal findings on clinical examination for further analysis. It was noteworthy that several lambs were found to have ticks (Fig. 1), primarily located on the ears. These were collected and identified as Rhipicephalus sanguineus sensu lato.

Image of ticks on sheep ear
Figure 1. Rhipicephalus sanguineus sensu lato ticks on the inner side of the pinna of a lamb

Despite the absence of clinical signs, individual carcase tracking was possible after slaughter, and 127/358 lambs (35.47%) were condemned due to severe jaundice (Fig. 2). The jaundice was accompanied by significant splenomegaly in 79.64% (223/280) of the animals that could be examined (Fig. 3).

Image of sheep carcases showing jaundice
Figure 2. Carcase of one of the lambs condemned during May 2020 due to jaundice
Image of post-mortem splenomegaly in sheep
Figure 3. Spleen of one of the condemned lambs showing marked splenomegaly

Complementary Tests

Haematological analysis

As mentioned earlier, blood samples were collected from animals that with any abnormal clinical examination findings. A total of 73 blood samples were taken, and a complete blood count was performed using an IDEXX Procyte Dx analyser (IDEXX laboratories, Westbrook, ME, USA).

Among the lambs from which blood samples were obtained, there were both jaundiced lambs with splenomegaly (which were condemned) and lambs with grossly normal carcases at slaughter. The jaundiced lambs showed significantly lower red blood cell counts, haematocrit, and haemoglobin levels compared to the healthy lambs. Additionally, most jaundiced lambs exhibited notable reticulocytosis and elevated mean corpuscular volume, indicative of regenerative anaemia. Another significant haematological finding was marked monocytosis in the jaundiced lambs, while the non-jaundiced lambs also showed monocytosis, but to a lesser degree.

Confirmation of bilirubin accumulation

Although the haematological findings clearly pointed to severe haemolytic anaemia as the cause of the jaundice, adipose tissue samples were taken to confirm whether the yellowing of the carcases was due to carotenoid accumulation. A test was conducted by dissolving the yellowish adipose tissue in alcohol and ether, based on the physicochemical properties of bile compounds and carotenoids. After placing the paired samples in each liquid and waiting two hours, the alcohol turned yellow, confirming that the yellowing of the carcases was due to bile compound accumulation. Bile compounds are alcohol-soluble, staining the liquid, while carotenoids are ether-soluble. Biochemical studies were also conducted on some of the serum samples from condemned animals, which revealed bilirubinaemia in all the samples analysed.

Origin of Bilirubinaemia: Differential Diagnosis

Once it was confirmed that the yellowish discolouration of the carcases was due to jaundice, i.e., bilirubin accumulation, it was necessary to determine the cause of this condition to make a diagnosis and control the problem. Jaundice can result from either direct or conjugated bilirubin accumulation caused by hepatic conditions such as liver damage, which impairs the ability of the liver to metabolise bilirubin. Some described causes include:

Other causes of conjugated bilirubin accumulation include post-hepatic conditions, typically due to bile duct obstruction or pancreatic damage, resulting in post-hepatic jaundice. Some described causes include:

Another possibility was that the jaundice resulted from the accumulation of unconjugated bilirubin, causing pre-hepatic jaundice, generally associated with excessive red blood cell breakdown. Some described causes include:

Due to the absence of apparent hepatic damage during post-mortem inspection and the lack of clinical signs in the live animals, attention was turned to possible causes of massive red blood cell destruction. Microscopically, the spleen analysis revealed a diffuse increase in red pulp cellularity, primarily lymphocytes and macrophages, along with white pulp hyperplasia. These are consistent with chronic haemolytic diseases, primarily associated with the production of macrophages to destroy infected or altered erythrocytes. The splenic changes, in conjunction with haematological data, suggested that the cause might be related to massive red blood cell destruction.

Molecular Analysis

Chronic copper intoxication, leptospirosis, or Type A enterotoxaemia caused by Clostridium perfringens were ruled out as the cause of the jaundice as an outcome of the investigation. Copper intoxication and leptospirosis were excluded due to the absence of clinical signs, as these conditions typically lead to severe illness and death in affected animals. On the other hand, Type A enterotoxaemia is often associated with acute cases and is common in certain regions. The intestinal loops of the affected lambs displayed slight reactive macroscopic signs associated with mild dysbiosis by the presence of trichobezoars and hypertrophied mesenteric lymph nodes. Despite these findings, the digestive content samples in this case showed low bacterial loads by PCR test, and serological ELISA testing did not detect the presence of alpha, beta, or epsilon toxins in these samples, thereby excluding the disease.

Among the possible causes considered were haemoparasitic infections such as Babesia sp. or Theileria sp., as well as bacterial infections directly affecting red blood cells, such as Mycoplasma ovis or Anaplasma sp. These pathogens are typically transmitted by vectors, generally ticks, and due to the presence of R. sanguineus sensu lato ticks found on some lambs, they were considered more likely diagnoses. Molecular studies using PCR tests were conducted to detect the presence of bacteria. However, only the PCR for Anaplasma sp. was positive, and further analysis was conducted to identify the species. Of the 43 lambs sampled, 37 yielded positive PCR results for Anaplasma ovis, with high bacterial loads, which could explain the condition. To investigate potential differences, both condemned and healthy lambs were tested. Among the 21 jaundiced lambs analysed, all tested positive, while 16 of the 22 non-condemned lambs also tested positive. However, the bacterial load expressed in quantification cycles (Cq) in the condemned animals was significantly higher (p = 0.004) than in the non-condemned ones (25.00 vs 26.16).

Discussion

Ovine anaplasmosis has been described in recent years in Mediterranean Basin countries in Africa and Europe, as well as in some Asian countries (Yasini et al., 2012; Stuen et al., 2016; Jiménez et al., 2019; Noaman & Sazmand, 2022). Generally, outbreaks occurred in young adult sheep, causing weakness, chronic weight loss, and decreased production, all stemming from severe chronic haemolytic anaemia (Yasini et al., 2012; Jiménez et al., 2019). However, once the animal overcame the acute infection phase, it recovered but remained infected for life, acting as a reservoir for the pathogen (Ruiz et al., 2024a).

This report describes the first documented outbreak of anaplasmosis in lambs, resulting in jaundiced carcase condemnations at the abattoir. This issue has recurred during the late spring and summer of 2021 and 2022 on the same farm and others (SESC, 2020; Lacasta et al., 2020; Lacasta et al., 2022), causing severe economic problems and significantly compromising the viability of the affected farms due to the high number of carcase condemnations.

It is considered that ticks are the main vectors of Anaplasma species, particularly those of the genera Ixodes, Dermacentor, Rhipicephalus, and Amblyomma. Other mechanical transmission routes may involve fleas, horseflies, or even contaminated veterinary instruments. The coexistence of wild and domestic ruminants favours the transmission and spread of the disease (Kocan et al., 2004; Zhao et al., 2018). Transplacental transmission of the pathogen has not yet been described.

The typical production system in our area involves slaughtering animals intended for consumption when they are 2-3 months of age. During this period, affected animals exhibit severe jaundice because, at the time of slaughter, they are in the peak haemolytic phase of the the infection. However, this problem has only been observed in farms following traditional production systems, where the ewes graze during the lactation period, specifically during spring lambing, when tick activity is at its highest. In these cases, the ewes come into contact with ticks while grazing and bring them back to the facilities at night, where the ticks parasitise the lambs and transmit bacteria (Lacasta et al., 2020). Once the bacteria are transmitted through the tick's bite, they replicate within the erythrocytes. The immune system responds by destroying the infected erythrocytes, leading to anaemia, which typically appears 30-40 days after infection (Masake et al., 2010; Jiménez et al., 2019). Consequently, the time of maximum anaemia coincides with the slaughter of the lambs, despite the lack of clinical signs prior to slaughter.

Injectable oxytetracycline and injectable doxycycline have shown positive results in controlling jaundice in carcases during outbreaks (Lacasta et al., 2022). However, given global interest in reducing the use of antibiotics, prevention of infection becomes the key area of focus.

Preventive measures are primarily aimed at breaking the tick life cycle and preventing contact between the lambs and ticks. One option is to permanently house the animals, although the costs and difficulties associated with changing management practices on affected farms can be significant. Recent studies suggest that the use of topical antiparasitic products registered for use in sheep, such as Cypermethrin, Delthamethrin or similar synthetic piretroids compounds, can lead to improved outcomes, reducing jaundice-related condemnations in spring on affected farms (Ruiz et al., 2024b).

Conclusions

Currently, there are very few studies on clinical anaplasmosis in sheep worldwide. Infection with Anaplasma ovis has historically been overlooked, as it has traditionally been considered to cause only mild clinical signs, and therefore, has been deemed of limited economic impact. This article describes a newly recognised clinical presentation caused by Anaplasma ovis, which is leading to significant economic losses due to the condemnation of carcases from seemingly healthy lambs. The authors aim to draw attention to this emerging disease, which is starting to have a substantial economic impact on the Spanish sheep farming industry.

References

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Image of sheep ticks
Image of engorged sheep tick
Figure 4. Some of the ticks collected from the lambs during the examination on the farm. Presence of an engorged female of R. sanguineus sensu lato after feeding on blood
Image of sheep affected by anaplasmosis
Image of sheep affected by anaplasmosis
Image of sheep affected by anaplasmosis
Figure 5. Appearance of some of the adult sheep affected by Anaplasma ovis during the initial outbreaks of the disease in 2014 and 2015
Photomicrograph of sheep blood showing anaplasma
Photomicrograph of sheep blood showing anaplasma
Figure 6. Images of blood smears from diseased animals showing the presence of basophilic bodies inside the erythrocytes consistent with Anaplasma ovis
Image of sheep breech with ticks
Image of sheep with ticks near ear
Figure 7. Merino sheep heavily infested with ticks in the perineal area and around the ear

 

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