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Trypanosoma evansi, an extracellular protozoan parasite, causes camel trypanosomiasis, also known as “surra”. The parasite, which can be found in camels, dromedaries, horses, and other Equidae family members, can cause 3% mortality and up to 30% morbidity. This chapter focuses on trypanosome-related infections, including their morphology, classification, clinical manifestations, immuno-suppressive effects, and herbal remedies and nanoparticles for their prevention and treatment. The disease is transmitted through biting of an infected insect, usually a tsetse fly. It causes fever, anemia, lymphadenopathy, and splenomegaly, with parasite suppressing the host’s immune system, making them more susceptible to other infections. Current therapies for trypanosomiasis face challenges such as drug resistance, toxicity, and limited availability of expensive drugs. Therefore, it is necessary to look for trypanosomiasis chemotherapeutic drugs that are cheaper, more effective, readily available, and lethal. Nanomedicine approaches have been explored for treating parasitic diseases, as they efficiently transport drug molecules and enhance the biological effects of sustained drug release from nanocarriers, nanoemulsions, and quantum dots. Nanomaterials have shown promising functions in detecting and treating protozoan diseases like trypanosomiasis. Many studies have been published on nanoparticles with different physical and chemical properties that have demonstrated promising functions in increasing the effectiveness of trypanosome drugs.
Faculty of Science, Department of Zoology and Entomology, Helwan University, Cairo, Egypt
Saeed El-Ashram
College of Life Science and Engineering, Foshan University, Foshan, Guangdong Province, China
Faculty of Science, Kafrelsheikh University, Kafr El-Sheikh, Egypt
Rewaida Abdel-Gaber
Faculty of Science, Department of Zoology, Cairo University, Cairo, Egypt
*Address all correspondence to: mohameddkhil@yahoo.com
1. Introduction
Trypanosoma evansi is an extracellular protozoan parasite of salivarian trypanosomes in the genus Trypanosoma, considered the causative agent of camel trypanosomiasis “surra” [1]. Griffith Evans first identified this disease in 1880, and its term refers to the chronic evolution of the disease in animals as being “rotten” [2]. The spleen, liver, heart, lung, brain, and kidney are just a few key human organs that experience degenerative changes because of T. evansi infection. T. evansi’s primary host is still the camel, but it is also found in various other hosts, including dromedaries, horses, and other Equidae [3]. Camel productivity is crucial in dry regions because camels provide transportation, drought power, meat, and milk [4]. Camel trypanosomiasis can cause mortality of about 3% and morbidity of up to 30% [5]. It is believed that T. evansi is a descendant of T. brucei brucei, cyclically transmitted by tsetse flies. Still, it cannot go through its cycle in Glossina because a portion of the mitochondrial DNA (the maxicircles of the kinetoplast), responsible for its capacity to perform oxidative phosphorylation, has been lost [6]. This chapter discussed the morphology, classification, clinical manifestations, immunosuppressive effects of trypanosomes, and infection control via medicinal plants and nanoparticles.
Trypanosomes can exist and move within the host’s blood plasma or tissue fluid. The cytoplasm’s outermost layer, the pellicle, is flexible enough to allow the body to move while still keeping its shape [1]. A flagellum arises near the posterior end of the basal body and runs the length of the trypanosome; it may be continued as a whip-like free flagellum beyond the anterior end of the body. Along the length of the body, the pellicle and cytoplasm are compressed into a thin sheet of tissue known as the undulating membrane, through which the flagellum passes (Figure 1). Figure 2 depicts trypanosome pleiomorphism (variation in body form) at various lifecycle stages.
Trypomastigote (posterior kinetoplast: undulating membrane along the entire length of the organism)
Epimastigote (anterior kinetoplast: undulating membrane running over part of the body)
Promastigote (anterior kinetoplast: no undulating membrane)
Amastigote (anterior kinetoplast: usually spheroid or sub spheroid, no free flagellum)
Trypanosoma evansi, a salivarian trypanosome with unicellular flagellated kinetoplastid protozoa, is the causative agent of trypanosomiasis [1]. It is monomorphic morphologically, as evidenced by the trypomastigote stage, which has predominantly long, slender forms (Figure 1).
Phylum: Euglenozoa
Class: Kinetoplastea
Order: Trypanosomatida
Family: Trypansomatidae
Genus: Trypanosoma
Binomial name Trypanosoma evansi (Steel) Chauvrat, 1896
The Trypanosoma species reproduce by longitudinal binary fission, in which the flagellum and kinetoplast divide simultaneously in the host and the vector [7]. The main method of mechanical transmission in camels is through insects that bite them, so there is no need for a biological vector for T. evansi. The most significant vectors are believed to be those of the horsefly and deerfly families, Tabanidae (including the genera Atylotus, Tabanus, Lyperosia, Chrysops, and Haematopota), and Stomoxys flies [3]. The T. evansi life cycle began with flies feeding through their mouthparts on multiple hosts within a short time because the Trypanosoma is only infectious for a short time (Figure 3). It then multiplies in the midgut for 10 days, migrates to the salivary glands in the epimastigote form, and multiplies again in the salivary glands to change into the metacyclic form (infectious stage), which is then injected by a fly during a bite to become trypomastigote in the blood and lymph of the host [8]. Trypanosomes cannot survive for extended periods outside of their host and leave the body after death. After 8 h, flies can no longer spread the parasites.
Figure 3.
Trypanosome life cycle.
4.1 Clinical manifestations
A species-specific pathology is caused by T. evansi infection in various hosts [9]. Surra can affect camels at any age, including fetuses, and can cause an abortion by manifesting in both acute and chronic forms with the clinical sign severity varying between different animal species (Figure 4). The acute form of the disease in camels may last up to three months and is characterized by irregular fever, decreased appetite, and water intake. As the condition worsens, the hump disappears, there is dependent edema under the belly, there is marked depression, the coat becomes dull and rough, there is hair loss at the tail, and there is frequently rapid death [10]. The mucosal membranes of the eyes are paler, the body temperature fluctuates with early peaks of up to 41°C, and the urine usually has a distinct flavor. High body fever accompanies parasitemia [11].
Figure 4.
Trypanosoma evansi in the blood of camels (from our collections).
The majority of patients experience repeated fever episodes and are persistent. Some camels experience petechial hemorrhages in mucous membranes, dermatitis lesions, and swelling in their dependent body parts. Death is unavoidable if neglected; however, some may retain trypanosomes for two to three years as carriers for infection in vulnerable camels and other animals. Additional well-documented field reports include camel fatalities, abortions, and neurotic symptoms such as circling and trembling, odd aggression, aimless running, and collapse in severely stressed and overworked camels [10]. The higher parasite numbers in the host’s circulation affect neurotransmitter levels, and dopamine and serotonin levels were found to be greater in the brains of rodents inoculated with T. evansi [12].
4.2 Diagnosis
Diagnosing a T. evansi infection from the general clinical symptoms is difficult, and the parasite must be detected using laboratory techniques. In moderate or subclinical cases, the organism may be challenging to locate, and in animals. With chronic infection, parasitemia is frequently intermittent. In early infection or severe cases with elevated parasitemia, dyed blood slides, wet blood films, or lymph node samples may be studied to determine the trypanosomes. When parasitemia is low or in chronic cases, thick blood smear analysis, parasite concentration techniques, and laboratory rodent immunization are required. Trypanosome DNA detection methods can be employed on hosts and vectors. The most sensitive primers for surra are trypanosome-specific ones that target satellite DNA or ribosomal DNA [13]. Amplifications of the ITS1 of ribosomal DNA may identify all African Trypanosoma spp. in single or mixed infections based on the specific size of the PCR products [14]. False-negative results may occur when parasitemia is extremely low and not all isolates of a certain Trypanosoma species are detected; in these circumstances, a serological investigation may only substantiate suspicion of prospective carriers. For instance, PCRs specific for the type A RoTat 1.2 gene and specific for type B minicircles may differentiate T. evansi types A and B [15]. Real-time PCR (RT-PCR) approaches have been established for T. evansi [16], T. congolense [17], and T. brucei [18]. They were very sensitive and specific when applied to hosts and vectors, but their usage has been extremely restricted until now, most likely because of the high level of technical skill, necessary equipment, and associated costs. The effectiveness of these methods for standard diagnostic procedures has yet to be established. Beside parasitological or molecular diagnosis, serological testing may provide indirect evidence of T. evansi in a susceptible population or individual. In the most reliable testing for T. evansi type A antibodies, the variant surface glycoprotein (VSG) RoTat 1.2 is utilized as an antigen [19]. These tests include the immune trypanolysis [20], the complement fixation test (CFT) [21], the indirect fluorescent antibody test (IFAT) [22], the direct agglutination test CATT/T. evansi [23], and the ELISA/VSG RoTat 1.2 [24]. Only the latter test, which involves exposing the subject to live T. evansi RoTat 1.2, is used to detect antibodies since the OIE recommends it [25]. IFAT and CFT detect immunoglobulin G (IgG), whose levels remain relatively consistent during the infection, to aid in diagnosing trypanosomiasis.
Algeria, Chad, Egypt, Ethiopia, Kenya, Mali, Mauritania, Morocco, Nigeria, Somalia, Somaliland, Sudan, India, Iran, Jordan, Kuwait, Saudi Arabia, Palestine, Mule, United Arab, Emirates, France, Pakistan, Spain, Oman
Worldwide distribution of T. evansi among host species.
4.4 Trypanosome and vector control
Pathogen control and vector control are the two traditional components of managing a vector-borne disease. There are some additional alternative methods for preventing transmission that can be used in combination to prevent infection [5]. With surra, disease prevention primarily focuses on using trypanocide and preventive management techniques to protect animals from infection because trypanosomes lack a vaccine against them (because of a broad repertoire of variable surface antigens) [128].
4.5 Trypanosome control
T. evansi can be eliminated by injecting various trypanocidal drugs, including diminazene aceturate (Berenil), suramin, quinapyramine melarsomine, and (cymelarsan) [51]. Nevertheless, extravascular invasion or chemoresistance may cause the treatment to fail. Trypanocides can be separated into the following two groups:
Therapeutic drugs are utilized therapeutically and have a short-term effect. You cannot always eliminate parasites, but you can kill them. For example, melarsomine dihydrochloride was the newest trypanicide commercially available in 1992. A deep intramuscular injection at 0.25 mg/kg is used to control camel trypanosomosis, and this dose can be increased to 0.5 mg/kg if full therapeutic (sterile) therapy is required.
Therapeutic and prophylactic drugs are used for chemoprevention. Chemoprophylaxis helps animals eliminate parasites and prevent new infections by maintaining a curative dose in their serum. Quinapyramine methyl-sulfate at 5 mg/kg could be given subcutaneously. A stronger mixture of quinapyramine sulfate and chloride can treat/prevent T. evansi in camels when injected subcutaneously at 8 mg/kg.
4.6 Vector control
Some animals in endemic locations may be protected against T. evansi-carrying biting files by traps, insecticides/repellents, insect screens/netting in stables, and other interventions [51, 128]. In the first 30 min after feeding on an infected host, flies are most infectious and likely to spread to surrounding hosts. Tabanids are persistent feeders and seldom attack animals beyond 50 m away.
4.7 Immunosuppressive effects of trypanosomes
The host’s immune system, including innate and adaptive immunological defenses, constantly confronts trypanosomes [283]. Therefore, selective pressure has allowed them to develop sophisticated escape mechanisms. T. evansi could evade the host immune response by inhibiting the inflammatory cytokine production using T. evansi extracellular vesicles (TeEVs) to activate the TLR2-AKT pathway. KMP-11 in TeEVs was shown to be involved in the T. evansi infection. TLR2-AKT signaling is activated by extracellular vesicles (EVs) released by T. evansi to decrease the production of inflammatory cytokines, allowing the parasite to evade the host’s immunological response [284].
Antigenic variation, wherein trypanosomes repeatedly exhibit distinct surface glycoproteins (VSG), is the most prominent escape mechanism. The trypanosomes force their host to produce successive directories of antibodies to deal with emerging VSG variants, even though a new variant is intended to appear before the humoral response is effective. This is regarded as the first intentional immunosuppression, but it results from immunological exhaustion [285]. The complement system is one of the first molecular defenses in innate immunity, and antibody-dependent complement-mediated lysis is likely one of the most efficient early control methods established by the host. Despite a slight initial increase, experimental camel infections showed that classical complement pathway hemolytic activity decreased as the infection progressed and negatively correlated with parasitemia but recovered after trypanosomes were eliminated, strongly indicating immunosuppression of the molecular immune system components [286]. Macrophages play a crucial role in the innate cell-mediated immune response to trypanosomes, both as antigen-presenting cells (APCs) and as microbicidal effector cells. Infection susceptibility or resistance may be further influenced by trypanosomes, which polarize macrophages into distinct activation states (M1, M2) through parasite factors and host cytokines [287, 288]. Trypanosomes are believed to be killed by the induction of classically activated macrophages (M1-type macrophages), which produce significant amounts of inflammatory compounds such as tumor necrosis factor-alpha (TNF-α), reactive oxygen intermediates, nitric oxide synthase two-dependent reactive nitrogen intermediates such as NO, and associated molecules [288]. Dendritic cells (DCs), which are APCs, are known for being potent immune system elicitors and regulators. Splenocytes exhibit elevated levels of Ccl8 and IL-10 expression revealing a rise in regulatory DC activity and number as the underlying factor in T. evansi infections that causes the inflammatory cytokine and chemokine storm, which was mostly caused by macrophages. The inflammatory responses may be used to immunosuppress the host, but management may be necessary to prevent irreversible pathophysiological effects. As the infection progressed, the regulatory DCs became more prevalent, decreasing inflammatory DCs [289]. Trypanosome infections result in polyclonal B cell activation, primarily an IgM response with little IgG synthesis [290]. T. evansi, unlike T. brucei and T. congolense, has distinct molecular and cellular dialogues and conflicts when interacting with a mammalian host. Despite infection-associated induction of trypanocidal inflammatory molecules, only IgM antibodies have been shown to significantly contribute to trypanosome control [288]. Recent research has shown that T. evansi lymphotoxin can cause CD45-dependent lymphocyte mortality [291], consistent with the pioneering observation that T. evansi membrane fractions induce suppressor cells [292].
4.8 T. evansi infection may cause serious diseases including cancer
T. evansi can evade the host immune response by some mechanisms, including the production of immunosuppressive factors. T. evansi has been shown to down-regulate the expression of some key immune response genes, including interleukin-12 (IL-12). IL-12 is a critical cytokine for the development of Th1 responses, and its down-regulation by T. evansi results in the suppression of cell-mediated immunity [293]. This suppression of the immune response makes the host more susceptible to a variety of pathogens, including cancer-causing viruses [294]. T. evansi infection has also been linked to the development of autoimmunity. T. evansi can induce the production of autoantibodies by some mechanisms, including the cross-reactivity of its surface antigens with host proteins. This cross-reactivity results in the formation of immune complexes, which can trigger the development of autoimmune disease. T. evansi has also been shown to induce the production of proinflammatory cytokines, which can lead to the development of chronic inflammation. Chronic inflammation is a risk factor for the development of some diseases, including cancer [295, 296].
4.9 Medicinal plants against T. evansi
Drug resistance, toxicity, and the availability of expensive/limited drugs pose challenges to the current trypanosomiasis treatments [297]. Consequently, it is necessary to search for trypanosomiasis chemotherapeutic drugs that are less expensive, more potent, accessible, and lethal. Given that some ethnomedicinal plants have been shown to have effective trypanocides, and the use of herbal treatment for the disease still has a promising future [298, 299, 300, 301, 302, 303, 304]. Plants’ active metabolites are often in various plant parts, including the roots, leaves, shoots, and bark. According to Ngure et al. [305], 20,000 species of higher plants are used medicinally worldwide, with some of them being used to treat trypanosomes (Table 2). We used PubMed search to find the most important medicinal plants used in the treatment of trypanosomiasis [306, 307, 308, 309, 310, 311, 312, 313, 314, 315, 316, 317, 318, 319, 320, 321, 322, 323, 324, 325, 326, 327, 328, 329, 330, 331, 332, 333, 334, 335, 336, 337, 338, 339, 340, 341, 342, 343, 344, 345, 346, 347, 348].
Identified medicinal plants with activity against trypanosomes.
4.10 Green nanotechnology against T. evansi
The nanomedicine approach has been studied for treating parasitic diseases because it can effectively transport drug molecules to the target location and boost the biological impact of prolonged drug release from nanocarriers, nanoemulsions, and quantum dots (QDs) [349, 350, 351]. Targeting these intracellular parasites can be accomplished by carefully examining the structural and physical characteristics of nanocarriers, which largely dictate their function. Particle size, surface charge, shape, processes, and bio-distribution patterns are all important factors in how effectively nanomaterials work [352].
Many nanomaterials (NMs) have indicated usefulness in the detection and management of protozoan diseases, such as trypanosomiasis, including polymers [353], lipids [354], and metallic/inorganic systems [355]. Metal oxides, such as iron oxide, zinc oxide, copper oxide, titanium dioxide, and magnesium oxide, are examples of metallic NMs, along with gold, silver, selenium, and platinum [356]. Because internalized nanomaterials are constrained in size to less than 130 nm in the trypanosome flagellar pocket, NMs are better suited for endocytosis there [357]. Much research has been published using nanoparticles (NPs) with varying physical and chemical properties, and they have demonstrated promising functions in boosting the antitrypanosomal drug effectiveness [352, 358]. Gold (Au) and silver (Ag) nanoparticles (NPs) introduced new therapies and enhanced molecular diagnostics [359]. The two NMs are effective wound healers with excellent properties such as anticancer, antimicrobial, antidiarrheal, and antifungal activities. Against T. brucei gambience, T. evansi, T. cruzi, and T. congolense, AuNPs, and AgNPs were employed [360, 361]. These NPs inhibited growth by 50% in studies focusing on T. evansi and T. congolense, and they also showed excellent efficacy against T. brucei gambience and T. cruzi. Similarly, AuNPs and AgNPs were used to treat arginine kinase in another investigation. The enzyme arginine kinase (phosphotransferase) is required for Trypanosoma energy metabolism [362]. Piperine-loaded NCs enhance the production of ROS, which has an inhibitory effect on T. evansi’s growth according to Rani et al. [351]. Nanoemulsions, which vary in size from 10 to 600 nm and are made up of a combination of insoluble liquids in two separate phases, with vesicles in a dispersed phase bound by vesicles in a continuous phase, have shown remarkable promise as effective drug delivery agents [363]. This makes them highly effective nanocarriers for enhancing the solubility of hydrophobic medications. In a study, ursolic acid, an antitrypanosomal chemical present in nanoemulsions with a size of 57.3 nm, was found to have great stability [354]. Another study presents a nanoemulsion formulation developed using clove oil in sulfonamide that was shown to have strong antitrypanocidal action and carbonic anhydrase inhibitor activity, which inhibits the T. cruzi a-class enzyme [364]. Nanoscale crystal formations known as QDs can move electrons. These semiconducting nanoparticles can emit light of various colors when exposed to UV light, making them suitable nanomaterials for various biomedical applications, including drug administration and detection [352]. However, these NPs have negative side effects in in vitro and in vivo studies, which may harm human health [365]. When the impact of QDs of cadmium tellurium (CdTe) on epimastigotes of T. cruzi was examined [366], T. cruzi growth patterns decreased substantially after being exposed to high doses of this nanomaterial, which prompted more research in this field. When T. cruzi was incubated with 200 mM CdTeQD, significant morphological changes, DNA damage, blister formation in the plasma membrane, and mitochondrial swelling were noted.
Camel trypanosomiasis, often known as “surra,” is thought to be caused by T. evansi, an extracellular protozoan parasite of salivary trypanosomes. Therefore, it is important to seek out chemotherapeutic treatments for trypanosomiasis that are both affordable and efficacious. Current trypanosomiasis therapy faces obstacles, including medication resistance, toxicity, and expensive/limited drug supply. Trypanosomiasis is a protozoan disease that has been demonstrated to respond to various nanomaterials, including polymers, lipids, and metallic/inorganic systems.
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Written By
Mohamed Dkhil, Saeed El-Ashram and Rewaida Abdel-Gaber
Submitted: 09 April 2023Reviewed: 04 September 2023Published: 30 November 2023
Open access peer-reviewed chapter - ONLINE FIRST
