8. Haemoparasites of Australian mammals

INTRODUCTION

KNOWN HAEMOPARASITES OF AUSTRALIAN MAMMALS

The haematozoa that may be encountered in Australian mammals include members of the Babesidae, Theileridae and Piroplasmidae (namely, Hepatocystis and Polychromophilus). These are typically intra-erythrocytic and one to several pleomorphic organisms will be evident. The recorded parasites and their hosts are listed in Table 8.1.

Table 8.1 Blood-borne haematozoan parasites recorded in the scientific literature from Australian mammalian hosts (O’Donoghue and Adlard, 2000)

The pathologic effects (or lack thereof) have not been determined for most species of haemoparasites recognised in Australian mammals. Under ‘normal’ circumstances, many of the organisms do not seem to cause any harm to the host. However, this may change if the host’s immune system becomes compromised. Generally, if there is a haematological consequence of pathogenic haemoparasites, it is anaemia. The pathogenic mechanisms are not fully documented, but may result from the physical effects of parasite reproduction on cells, or by the inciting of an immune response by the host. The latter is typically mediated by extravascular haemolysis resulting from antibody-mediated erythrocyte destruction by macrophages in the spleen and other tissues. Generally a ‘regenerative’ anaemia is expected (see Chapter 2), characterised by increased polychromatophilic erythrocytes, reticulocytosis, macrocytosis, metarubricytosis, increased numbers of Howell-Jolly bodies and basophilic stippling. The characteristics of this response may vary between species and is unknown for most Australian mammals.

In addition to the effects on erythrocytes, haematozoa with tissue stages, such as Hepatozoon spp., may cause destruction of tissues cells, such as endothelial cells or hepatocytes, and consequently result in necrosis and inflammation.

Babesia

Babesia species are relatively large, round to pyriform or irregular, non-pigmented organisms that exist within erythrocytes where they multiply by asexual division. Under natural conditions, infections are transmitted by ticks. Two species of Babesia, B. tachyglossi and B. thylacis, have been recognised in the blood from Australian mammals. In addition, B. canis, a pathogen of domestic dogs, has been infrequently reported in dingoes and unidentified species of Babesia have been observed in the agile antechinus, Proserpine rock-wallaby and short-beaked echidna.

Babesia thylacis are fusiform to pear-shaped organisms, approximately 3–5 × 1.5 µm in size (Figure 8.1), and 1–8 parasites per cell may be observed. Erythrocytes with 1–2 parasites are not altered; in contrast, cells with more than two parasites can be enlarged and paler than normal. Experimental infection of bandicoots with B. thylacis, via intraperitoneal inoculation of cit-rated blood containing parasites, resulted in patent infections 3–5 days later. No signs of illness were exhibited by the bandicoots. An infected animal that subsequently underwent splenectomy did not exhibit recrudescence of the disease (Mackerras, 1959).

Babesia tachyglossi has been identified in blood from a short-beaked echidna. Typically, there are 2–8 organisms per infected erythrocyte and these are similar in appearance to B. thylacis (Bolliger and Backhouse, 1959). Concurrent infection with Theileria tachyglossi has been reported (Bolliger and Backhouse, 1957; Mackerras, 1959) (Figure 8.6). The pathologic effects on the host have not been determined.

Babesia canis is an intra-erythrocytic haemoparasite of canids. It is a large organism, typically 4.0–5.0 µm in length, and pyriform in shape. Cells may contain multiple organisms. The clinical and pathological features of the disease have been well described for domestic dogs (Irwin and Hutchinson, 1991), but to the authors’ knowledge, there are very few reports of infection of dingoes and the consequences of such infections have not been determined.

Recrudescence of infection with an unidentified Babesia sp., reported in agile antechinus, was believed to contribute to the observed anaemia of males in the post-mating period (Barker et al., 1978) (Figure 8.2). These animals had decreased haematocrit, haemoglobinuria and haemosiderosis of the lung and spleen.

Theileria

Theileria spp. are pleomorphic intracellular organisms that may be round, ovoid, rod-shaped or irregularly shaped and are found in erythrocytes and lymphocytes. Typically, the organisms multiply by schizogony in leukocytes (commonly lymphocytes), forming structures called ‘Koch’s bodies’, which are released and subsequently invade erythrocytes. Ticks are usually responsible for transmission of the organism between hosts. Three species of Theileria have been identified from Australian mammals: Th. ornithorhynchi, Th. perameles and Th. tachyglossi. In addition, unidentified Theileria spp. have been observed in the northern brown bandicoot, long-nosed bandicoot and long-nosed potoroo.

Theileria ornithorhynchi (Figure 8.3), found in platypus, is the best-described of the members of the genus that infect native mammals (Mackerras, 1959; Whit-tington and Grant, 1984; Collins et al., 1986; Munday et al., 1998). Typically, the infection affects less than 1% of erythrocytes, which usually contain 1–4, round, pear-or comma-shaped bodies. Small piroplasms, similar to those found in erythrocytes, may also be found in leukocytes. In addition, leukocytes in the peripheral blood may exhibit large, basophilic Koch’s bodies, but these may be difficult to find. Infection is common, with a study in south-eastern Australia finding small numbers of organisms in the blood of 53 of 54 platypus (Collins et al., 1986). This parasite is usually regarded as nonpathogenic; however, haemolytic anaemia was diagnosed in a juvenile platypus with 12% of its erythrocytes infected (Munday et al., 1998).

Figure 8.1 Babesia thylacis within an erythrocyte from the blood of a bandicoot.

Figure 8.2 Babesia sp. within erythrocytes (arrows) from the blood of an agile antechinus.

Figure 8.3 Theileria ornithorhynchi within an erythrocyte from the blood of a platypus.

Figure 8.4 Theileria peramelis within erythrocytes from the blood of a bandicoot.

Natural infections of Th. peramelis have been observed in southern brown and long-nosed bandicoots (Mackerras, 1959). These organisms were described as minute, oval or pear-shaped, or occasionally rod-shaped, with typically 1–2 parasites per cell (Figure 8.4). Bandicoots that were experimentally infected became anaemic by 6–7 weeks after inoculation. The anaemia was characterised by increased anisocytosis, polychromatophilic erythrocytes and numerous nucleated erythrocytes, indicative of a regenerative response to the anaemia.

Theileria tachyglossi has been observed in blood from short-beaked echidnas and typically there is one (occasionally 2–4), bacilliform, round, ovoid, pyri-form or comma-shaped organism per cell (Backhouse and Bolliger 1957; Mackerras, 1959) (Figure 8.6). The effect of the parasite on the host has not been reported.

Figure 8.5 Unidentified piroplasm within erythrocytes (arrows) from the blood of a Gilbert’s potoroo.

In some cases, piroplasms of unknown classification will be observed in the blood (Figure 8.5).

Polychromophilus

Polychromophilus species are malarial parasites of bats. Gametocytes occur in erythrocytes and small schizonts with multiple merozoites are found in macrophages in impression smears of the liver, but may also be found in bone-marrow, lung and kidney. Transmission by nycteribiid flies was confirmed by Gardner and Molyneaux (1988) for P. murinus infecting Daubenton’s bat (Myotis daubentoni) in England. In Australia, P. melanipherus and P. murinus have been reported (Mackerras, 1959; O’Donoghue and Adlard, 2000). In the former species, mature gametocytes ‘filled’ slightly enlarged erythrocytes. Microgametocytes had mildly eosinophilic cytoplasm and a large nucleus, whereas macrogametocytes had mildly basophilic cytoplasm and a compact nucleus. Both exhibited coarse black pigment. The effect of these organisms on the host has not been reported.

Hepatocystis

Hepatocystis species are pigmented parasites found in bats. Gametocytes exist within erythrocytes and large, irregular cystic schizonts occur within the liver. Two species, H. levinei and H. pteropi, have been identified in Australia (Mackerras, 1959; O’Donoghue and Adlard, 2000). Unidentified species have also been reported.

In H. pteropi, there are ‘ring forms with a large vacuole and fine pigment and larger amoeboid forms with coarser pigment’ (Mackerras, 1959). Microgametocytes have a pale basophilic cytoplasm and a diffuse eccentric nucleus, whereas macrogametocytes have strongly basophilic cytoplasm and a dense nucleus. Both forms contain a yellow-brown pigment. The effect of these organisms on the host has not been reported.

Hepatozoon

Hepatozoon species are the only genus of coccidia that is found in the blood of mammals. Gametocytes are observed within erythrocytes or leukocytes, schizogony usually occurs in the endothelial cells of the liver and sporogony usually occurs in blood sucking arthropods. Several members of this genus, including H. perameles, H. dasyuroides, H. dasyuri, H. petauri and H. pseudo-cheiri, have been reported in Australian marsupials (Mackerras, 1959) and all of these parasites infect erythrocytes. In contrast, H. muris, which has been reported in native murids, infects leukocytes. Several unidentified species of Hepatozoon have also been reported (O’Donoghue and Adlard, 2000).

Hepatozoon spp. are typically oval to elongated, intracellular parasites. For example, H. petauri, is 7.5–8.0 µm × 3.5–4.0 µm in size, with a subterminal nucleus that occupies almost two-fifths of the total length of the parasite. In contrast, H. dasyuroides (Figure 8.7) is a long, narrow parasite, 12–13 µm × 1-2 µm, that is usually curved or flexed (resulting in some distension of the cell). Little is known about the route of transmission or the effects on the host.

Hepatozoon perameles has been identified from the blood of bandicoots (Mackerras, 1959). In a more recent study, 25% of eastern barred bandicoots had gametocytes of a Hepatozoon sp. in 0.05–0.2% of erythrocytes (Bettiol et al., 1996). The gametocytes were ovoid, 8.7 ± 0.2 µm × 2.1 ± 0.4 µm, with a prominently staining nucleus, and they caused the affected erythrocytes to be prominently enlarged and oval (Figure 8.8). Occasionally, extracellular gametocytes or two gametocytes per cell were observed. The arthropod intermediate hosts have not been identified.

Hepatozoon muris occurs in murids world-wide. Gametocytes are found within monocytes and shizogony occurs within hepatocytes. The infection is usually considered non-pathogenic, although anaemia with splenomegaly has been reported in rats with severe infections (Soulsby, 1982). The mite, Laelaps echidninus, has long been known as an intermediate host of this species (Miller, 1908).

Figure 8.6 Line drawings of piroplasms of the echidna, Babesia tachyglossi and Theileria tachyglossi, that illustrate the range of parasite forms that may be encountered. Figures 1–30. Forms of the parasites seen in red cells of blood and bone marrow of echidna. Figures 1–5. Commonly occurring forms. Particularly frequent are marginal forms as in Fig. 4. Often thicker than that shown and reminiscent of the ‘appliquée’ form of malarial plasmodia. Figures 6–10. Larger pleomorphic forms as observed mainly in echidna 2. Figures 11–15. Blood of echidna 3. Small, slender, wispy, ‘duplex’ forms as in Fig. 13 and Fig. 15 were present. Figures 16–20. Large forms seen only in bone marrow smears of echidna 3. Bigemminate Babesia-like organisms as in Fig. 16 were common. Cells containing from four to eight parasites (Figs. 17 and 18) and curved attenuated structures (Figs. 19 and 20) were also features of this animal. Figures 21–24. Minute forms in blood of echidna 6, which were numerous. In the bone marrow occasional red cells contain larger ovoid forms as in Fig. 25. Figures 26–30. Echidna 10. A heavy infection exhibiting many minute forms as well as those depicted.

Reprinted with permission from the Australian Journal of Science 19, 24–25 (Backhouse, T.C, and Bolliger, A. 1957).

Figure 8.7 Hepatozoon dasyuroides within an erythrocyte from the blood of a Kowari. The cell has been distended by the presence of the organism.

Figure 8.8 Hepatozoon sp. within an erythrocyte in blood from a southern brown bandicoot.

Figure 8.9 Trypanosoma binneyi in the blood of a platypus.

Figure 8.10 Trypanosoma sp. in the blood of a bandicoot (courtesy of S. Bettiol, University of Tasmania).

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