Theileria annulata theileriosis

Previous Authors: E PIPANO AND V SHKAP

Current Authors:
J A LAWRENCE - Extraordinary Professor, DPhil, BSc, MRCVS (ret.), DTVM, Department of Paraclinical Veterinary Science, University of Zimbabwe, Harare, Zimbabwe  
B J MANS - Principal Researcher, BSc, BSc (Hons) Biochemistry, MSc (Biochemistry), PhD (Biochemistry), Agricultural Research Council, Onderstepoort Veterinary Research, 100 Old Soutpan Road, Pretoria, Gauteng, 0110, South Africa

GENERAL INTRODUCTION: THEILERIOSES OF CATTLE

Introduction

Tropical theileriosis is an infectious disease of cattle caused by the protozoan Theileria annulata, which is transmitted by ticks of the genus Hyalomma. Invasion by the parasite of cells of the macrophage and lymphoid series results in their replication or destruction, and invasion of erythrocytes results in anaemia. Peracute, acute, subacute, mild and chronic forms of the diseases are recognized. Animals that recover remain latently infected.¹⁰³

Theileria annulata was first described by Dschunkowsky and Luhs in Transcaucasian cattle in 1904;²⁵ they named it Piroplasma annulatum. During the following two decades fatal theileriosis caused by T. annulata in the Mediterranean area and India was often mistakenly attributed to Theileria mutans infections.¹²¹

Tropical theileriosis occurs in northern Africa, including the sub-Saharan territories,⁴⁶ Sudan and Eritrea, southern Europe, the Near and Middle East, Central Asia, India and northern China. The extent of its distribution in the Far East, where it overlaps with Theileria buffeli/orientalis infection,⁴⁸ is not yet clearly delimited.²⁴

Aetiology and life cycle

The life cycle of T. annulata is similar to that of T. parva⁶⁵ (see East Coast fever: Figure 29.2) and only some characteristics specific to T. annulata are discussed here.

Three of the developmental stages of T. annulata are infective for cattle: the sporozoites, which develop in the salivary glands of ticks and, in the bovine host, the schizonts in macrophages (monocytes) and the merozoites in erythrocytes. However, in nature, the disease is transmitted only by sporozoites.

Mature sporozoites are oval-shaped, measuring about 1 μm in length. Schizonts are multinucleated, round, varying in diameter from 1 to 15 μm (in some cases up to 27 μm), with an average of about 8 μm. Each nucleus measures about 1,5μm in diameter ^{65, 68}.  In cultures, schizonts contain an average of 12 nuclei, but some with 80 or more may be found.⁷³ Schizonts develop and grow in size as a result of binary fission of their nuclei. Schizonts are associated with the host cell microtubules, enabling the schizont to divide in synchrony with the host cell during mitosis and maintain the infection rate (Figure 37.1)⁷³. The schizont is able to regulate host cell function by secretion of biologically active proteins direct into the cytoplasm that modify nuclear function and transform the cell. Transformation enables proliferation, immortalization and dissemination of the host cell by means of immune evasion and resistance to apoptosis, using mechanisms similar to those of neoplastic cells ^{15,  67, 116}. Unlike neoplastic cells, there is no genomic mutation, and the cells return to normal if the parasite is killed. Host cell proliferation is reduced once merogony commences. Some of the schizonts develop merozoites, which penetrate erythrocytes.⁶⁵ Schizonts containing micromerozoites (microschizonts) are not as common in T. annulata infections as they are in those of Theileria parva. This is true both in infected cattle and in cultures.

Intra-erythrocytic merozoites (also referred to as ‘piroplasms’) are generally spherical, oval- or comma-shaped, but anaplasma-like forms measuring 0,5 μm may also be encountered; each is bounded by a single-layered cell membrane and possesses an oval nucleus.⁶⁵ Spherical forms vary in diameter from 0,5 to 1,5 μm, oval forms are 0,6 × 2,0 μm and comma-shaped forms 0,5 × 1,6 μm in size.⁶⁸ During multiplication of merozoites, nuclear division precedes cytoplasmic division, in a process characteristic of schizogony.¹⁶

Theileria annulata is transmitted transstadially by two and three-host ticks of the genus Hyalomma. After the pre-imaginal stages ingest blood containing intra-erythrocytic merozoites, spindle-shaped bodies (considered to be microgamonts, which give rise by fission to microgametes), and spherical forms (which are macrogametes) develop in the lumen of the gut.⁶⁵ The zygote-like stages which later develop in the gut wall transform into club-shaped kinetes that migrate to the salivary glands of the adult ticks after the moult. After the moulted ticks have begun to feed, the kinetes become polymorphic and undergo repeated nuclear divisions until sporozoites are formed. Generally, infective sporozoites appear in the salivary glands after the tick has been feeding for 48 to 72 hours.¹⁰⁹ However, ‘activation’ of ticks by close proximity to cattle or by being warmed to mammalian body temperatures ^{64, 96} may also trigger the transformation, so that some ticks may be infective before feeding on their host. Ticks can only become infected by ingesting intra-erythrocytic merozoites.⁹⁷

After inoculation into cattle, sporozoites penetrate mononuclear cells and develop into schizonts. These are detectable in smears made from superficial lymph nodes and the liver 7 to 28 days after infection.¹⁰³ Merozoites are detected in...