Chapter 54 Heartwater (Ehrlichia ruminantium)
Heartwater is a noncontagious tick-borne disease of domestic ruminants and wildlife. Thought to be a wildlife-adapted disease, heartwater was first recorded in livestock after it spilled over into a domestic sheep in South Africa in 1838.28 Heartwater is one of the most devastating livestock (cattle, sheep, goat) diseases in sub-Saharan Africa, with mortality rates up to 80% in naive domestic livestock. In addition to sub-Saharan Africa, heartwater is now present in Madagascar, various small islands in the Indian Ocean and Atlantic Ocean, and islands in the eastegrn Caribbean Sea.
The causative agent, Ehrlichia ruminantium (formerly Cowdria ruminantium), is an obligate intracellular rickettsial agent, classified as a member of the Ehrlichiae tribe in the family Rickettsiaceae, order Rickettsiales.14 Three morphologic forms of the organism are recognized; elementary (electron dense), intermediate, and reticulate bodies.29 Cells are initially infected by elementary bodies, through a process resembling phagocytosis. Thereafter, the organisms divide by binary fission inside intracytoplasmic vacuoles to form large colonies of reticulate bodies. The reticulate bodies then develop into smaller intermediate bodies with an electron-dense core, before condensing further to form elementary bodies. Infected cells rupture and release elementary bodies into the bloodstream to infect other cells and, presumably, ticks feeding on the host.29 Protective immunity to heartwater in the vertebrate host is considered to be primarily cell mediated, although E. ruminantium antibodies are detected in serum and colostrum and most likely play a role in immunity.
Until the mid-1980s, when the in vitro cultivation of E. ruminantium was achieved, little was known about the epidemiology of heartwater because of the lack of antemortem diagnostic capabilities. Even today, diagnosis of heartwater remains difficult in both domestic and wildlife species. Additionally, the lack of a safe and effective vaccine has limited our ability to control this disease.
There is growing concern that Amblyomma spp. tick vectors and the disease-causing rickettsial agent may be introduced into livestock and wildlife currently living in heartwater-free regions.12 Recent epidemiologic discoveries (e.g., wildlife and domestic carriers and vertical transmission), as well as anthropogenic factors (e.g., animal trade), support the likely introduction of E. ruminantium to regions presently free of the disease. Ehrlichia ruminantium is an Office International des Epizooties (OIE) list B reportable disease.
The only known vectors capable of transmitting E. ruminantium are several species of ticks in the Amblyomma genus. The African ticks A. variegatum and A. hebraeum are the two most important vectors on a global scale.34 Three of the 13 Amblyomma spp. known to transmit E. ruminantium naturally or experimentally, A. maculatum, A. cajennense, and A. dissimile, are American ticks.5,16 Of more concern for the American mainland is A. variegatum, the most efficient vector of E. ruminantium, which was introduced into Guadeloupe Island in the early 1800s and subsequently became established on a number of islands in the Caribbean4 and has, on occasion, been imported into the United States.
Amblyomma spp. ticks have been documented to infest more than 100 species within the Aves, Mammalia, and Reptilia vertebrate classes.10 The large host range of Amblyomma spp. ticks, the ability of both trans-stadial and intrastadial transmission of E. ruminantium within the tick, and the three-host life cycle of Amblyomma spp. ticks allow an individual tick to spread the disease to more than one host. Amblyomma spp. ticks also have qualities, such as aggregation-attachment pheromone (AAP) used in host location and selection,21 continual long-term feeding of males on hosts,1 and the ability to maintain their infectivity after infecting a host,1 that contribute to the attainment of endemic stability in many parts of sub-Saharan Africa.
Five species of domestic animals-cattle (Bos taurus), sheep (Ovis aries), goat (Capra hircus), water buffalo (Bubalus bubalis), and domestic ferret (Mustela putorius furo)-are known to be susceptible to infection with E. ruminantium. Cattle, sheep, and goat are the most significant domestic species associated with the epidemiology of the disease. Wildlife ruminants have often been considered carriers, although clinical cases of heartwater do occur in wildlife species. The literature contains many reports of wildlife species that have experienced subclinical and clinical infections. These reports, reviewed in Deem12 and Peter et al.,27 include African buffalo (Syncerus caffer), African elephant (Loxodonta africana), Barbary sheep (Ammotragus lervia), black rhinoceros (Diceros bicornis), black wildebeest (Connochaetes gnou), blesbok (Damaliscus pygargus), blue wildebeest (Connochaetes taurinus), chital (Axis axis), crowned guinea-fowl (Numida meleagridis), eland (Taurotragus oryx), fallow deer (Dama dama), four-striped grass mouse (Rhabdomys pumilio), giraffe (Giraffa camelopardalis), greater kudu (Tragelaphus strepsiceros), Himalayan tahr (Hemitragus jemlahicus), impala (Aepyceros melampus), Indian spotted deer (Axis axis), lechwe (Kobus leche kafuensis), leopard tortoise (Geochelone pardalis), rusa deer (Cervus timorensis), sable antelope (Hippotragus niger), scrub hare (Lepus saxatilis), sitatunga (Tragelapus spekii), southern multimmate mouse (Mastomys coucha), steenbok (Raphicercus campestris), timor deer (Cervus timorensis), tsessebe (Damaliscus lunatus), waterbuck (Kobus ellipsiprymnus), white rhinoceros (Ceratotherium simum), and white-tailed deer (Odocoileus virginianus). However, because of poor diagnostic capabilities and problems with cross-reactions, some of these infections have been questioned as to their authenticity. For example, recent experimental data suggest that both leopard tortoises and crowned guinea-fowl cannot be infected with E. ruminantium.26 Peter et al.27 summarize those wildlife hosts in which natural and experimental heartwater infections have been confirmed. These animals include 12 African ruminants, three non-African ruminants, and two African rodents (Table 54-1). However, it is probable that other wildlife species can be infected with E. ruminantium, and surveillance must be maintained to diagnose both carrier and clinically infected animals.
|Experimentally Infected||Naturally Infected|
|African buffalo (Syncerus caffer)||Lechwe (Kobus leche kafuensis)|
|Black wildebeest (Connochaetes gnou)||Sitatunga (Tragelapus spekii)|
|Blesbok (Damaliscus pygargus)||Springbok (Antidorcas marsupialis)|
|Blue wildebeest (Connochaetes taurinus)||Steenbok (Raphicercus campestris)|
|Eland (Taurotragus oryx)|
|Giraffe (Giraffa camelopardalis)|
|Greater kudu (Tragelaphus strepsiceros)|
|Sable antelope (Hippotragus niger)|
|White-tailed deer (Odocoileus virginianus)||Chital (Axis axis)|
|Timor deer (Cervus timorensis)|
|Four-striped grass mouse (Rhabdomys pumilio)|
|Southern multimmate mouse (Mastomys coucha)|
Reviewed in Peter TF, Burridge MJ, Mahan SM: Trends Parasitol 18(5):214-218, 2002, with references available of original citation for each species.
A long-term carrier state, first demonstrated in domestic cattle, sheep, and African buffalo, can be maintained for 246, 223, and 161 days, respectively.2 Subsequently, seven other experimentally infected African ruminant species (black wildebeest, blesbok, blue wildebeest, eland, giraffe, greater kudu, and sable antelope) have demonstrated subclinical carrier status.23,24
In addition to the discoveries of new Amblyomma spp. vectors, high E. ruminantium infection rates in Amblyomma spp. ticks,20 and domestic and wildlife hosts capable of being long-term carriers of E. ruminantium, vertical transmission in cattle and the influence of colostrum in calfhood immunity have been demonstrated.13 All these discoveries—high tick infection rates, long-term carrier status of vertebrate hosts, vertical transmission of the agent, and influence of maternal immunity on neonatal immunity-explain the finding of endemic stability, now considered the epidemiologic state of heartwater in much of sub-Saharan Africa, where the Amblyomma spp. vectors exist and indigenous livestock and wildlife are present.13,21,22