Parasitology. Alan Gunn

3.6 Life cycle of Giardia duodenalis. The trophozoite stage (T) normally infects the duodenum and upper section of the small intestine where it attaches to the gut lining. The cyst stage (C) is produced in huge, but intermittent, numbers and passed in the faeces. Transmission is via faecal‐oral contamination of the cysts. Drawings not to scale.

Giardia duodenalis normally resides in our duodenum and upper small intestine although sometimes our stomach, ileum, and colon become infected. The parasites attach to the surface epithelium and overlying mucus layer and although they may completely cover the surface of the gut, they do not invade the underlying tissues. Many people become non‐symptomatic carriers of the parasite, but some develop an acute form of enteritis, referred to as giardiasis, that manifests as profuse watery diarrhoea. The diarrhoea has a characteristic foul smell because the parasite interferes with the absorption of fats. If undiagnosed and untreated, the infection can become chronic. This is characterised by episodes of abdominal pain and defaecating loose, clay‐coloured stools that have a smell reminiscent of bad eggs. The consequence of a long‐term infection can be malnourishment due to malabsorption. It can also result in a deficiency in fat‐soluble vitamins, such as vitamin K, and hence associated metabolic disorders. Interestingly, some people who suffer giardiasis develop lactose intolerance, and this may persist even after the infection is cured. Parasite strain differences and our own immune status probably contribute to the reason G. duodenalis afflicts some of us more severely. In addition, Giardia spp. have complex interactions with the resident host gut microbiome that may lead to protection or exacerbation of an infection. For example, in mice, Giardia infection results in a dramatic shift in the balance of aerobic and anaerobic commensal bacteria (Barash et al. 2017). Whether the shift is a direct consequence of the waste products of Giardia metabolism or an indirect one resulting from the host’s immune response to the parasite is uncertain. Of course, it could also be a consequence of both factors. This interaction with the microbiome has led workers to investigate the possibility of using probiotics or prebiotics to either prevent infections or treat established infections. For example, supplementing the diet of mice with the prebiotic inulin reduces the severity of giardiasis (Shukla et al. 2016).

      Giardia duodenalis is classed as a re‐emerging infection. This is mainly due to increased incidences in the developed regions of Australasia, North America, and Western Europe. Several factors contribute to these increases. The most obvious is that global travel is now cheap and accessible to many people in high‐income countries. Consequently, increasing numbers of them travel to countries with a high prevalence where they become infected. Furthermore, they often transfer the parasite to others on their return home. However, blaming other countries is sometimes unfair. For example, a study of giardiasis in Northwest England found that 75% were acquired within the United Kingdom (Minetti et al. 2015). In addition, apparent rises in the numbers of cases of giardiasis are sometimes a consequence of hospital laboratories introducing new, more sensitive diagnostic techniques (Minetti et al. 2016). Nevertheless, giardiasis is a frequent cause of diarrhoea outbreaks among young children in day care facilities, following contamination of domestic water supplies, and among people living in buildings with inadequate sanitation. Giardia duodenalis is also a sexually transmitted infection. It is reportedly common among men who have sex with men and those indulging in risky sexual practices such as oral–anal sex (Escobedo et al. 2014).

3.3.2 Order Trichomonadida

      Most species within this group are parasites or endosymbionts within vertebrates and invertebrates. Several species are important parasites of domestic animals (e.g., Histomonas meleagridis, Tritrichomonas foetus) and humans (e.g., Trichomonas vaginalis). The trophozoites are often ovoid or pear‐like in shape: the anterior is usually rounded and the posterior pointed, although amoeboid forms occur in some species. The number of flagellae varies between species, but there are often 4–6 emerging at their anterior apex. In addition, one flagellum usually curves backwards so that it runs along the cell wall to form an undulating membrane – this flagellum is therefore described as ‘recurrent’. Most species do not form cysts. They have a single nucleus and internally there is a prominent median tube‐like organelle called the axostyle.

      Trichomonads have genomes ranging from 86 to 177 Mb. This is unusually large for protozoa: by comparison, the genome of Plasmodium falciparum is ~23 Mb, whilst that of Trypanosoma cruzi is ~34 Mb. The large size is largely a consequence of extensive gene duplication, and this may contribute to their success as parasites and facilitated their ability to infect a variety of host species (Barratt et al. 2016). Gene duplication also occurs in other parasitic protozoa although not usually to the same extent as in the trichomonads. Gene duplication is not, however, an invariable feature of a parasitic lifestyle and some parasitic protozoa have unusually small genomes. For example, in the apicomplexan Babesia bovis, it is 8.2 Mb, whilst the microsporidian Encephalitozoon intestinalis has a genome of only 2.3 Mb.

      3.3.2.1 Histomonas meleagradis

      This parasite infects a wide range of birds but for some reason it is particularly pathogenic in young turkeys, in which untreated infections are usually fatal. It lives within the lumen of the caecum and the liver parenchyma and causes the disease histomoniasis. Infected birds lose condition, become listless and suffer from anorexia, poor growth and sulphur‐yellow diarrhoea. The neck and head often become black – and hence the infection is commonly known as ‘blackhead disease’. The pathogenicity often links to concurrent infections with other parasitic protozoa, such as Coccidia spp., and pathogenic bacteria such as Escherichia coli and Salmonella typhimurium.

      The morphology of H. meleagradis is variable (i.e., it is pleomorphic) and depends upon the organ that it infects and the stage of the disease. For example, the form found free within the lumen of the caecum (and in culture) is amoeboid, 5–30 μm in diameter, with a clear outer ectoplasm a more granular endoplasm and with one or two flagella emerging from close to the nucleus. The invasive form that lives within tissues is also amoeboid, but it is smaller (8–15 μm) and the flagellum is absent.

      Histomonas meleagradis has an unusual means of transmission that involves becoming incorporated within the eggs of Heterakis gallinarum. Heterakis gallinarum is a common nematode parasite that lives in the caecum of many wild and domestic birds. The nematode has a direct life cycle in which its eggs pass out in the faeces of its host and, after embryonation, are ingested by another bird in which they hatch and initiate an infection. Earthworms can act as paratenic hosts for the nematode. Interestingly, both H. meleagradis and H. gallinarum both require interactions with bacteria to establish themselves in their bird host. The infection and subsequent pathology associated with H. meleagradis therefore depends upon a complex interplay between the protozoan, a nematode, and microbial flora (Bilic and Hess 2020).

      3.3.2.2 Trichomonas vaginalis

      Millions of people are infected with Trichomonas vaginalis and some estimates suggest that it is the most common non‐viral sexually transmitted infection in the world (Kissinger 2015). However, prevalences vary considerably between countries, and it is not especially common in the United Kingdom with around 6,000 cases per year (Field et al. 2018). By contrast, a study of trichomoniasis in four African cities found prevalences ranging from 6.5 to 40% (Buvé et al. 2001). Despite its name, T. vaginalis, frequently infects men, but it causes them little harm and they usually clear the infection rapidly. Infected men can transmit the infection to women during sexual intercourse and rectal T. vaginalis infections can occur in men‐who‐have‐sex‐with‐men (Hoffman et al. 2018).

The parasite is ‘tear‐drop’ shaped with five flagellae emerging at the anterior end: four of these flagella are free whilst the fifth curves back to form a short undulating membrane that extends just over half the length of the cell (Figure 3.7). Trichomonas vaginalis expresses only one body shape, but its size varies considerably: