Monday, February 27, 2012

Whipworm


This week at Infection Landscapes, I will cover the nematode that causes trichuriasis: whipworm. This worm is one of the three major soil-transmitted helminths, and as such causes one of the most important neglected tropical diseases in the world today.

The Worm. Trichuriasis is caused by Trichuris trichiura, and is frequently known by its common name, whipworm. The common name comes from the worm's morphology, which displays a fine, whip-like anterior section, and a more robust posterior section:


The life cycle of T. trichiura is significantly less complex than that of the giant intestinal roundworm (A. lumbricoides) or that of the hookworms. Whipworm eggs are deposited with human feces into the environment. These eggs are not embryonated at the time of passage from the human host and are not infectious at this time. Instead, they embryonate in the soil after approximately 2-3 weeks (but may require up to one month). These eggs do not hatch in the soil, but do become infectious following embryonation. Once these eggs are ingested by a new host, they will hatch in the small intestine and the larvae emerge and develop into immature adults in the epithelium over the following couple days. Subsequently these immature adults begin their descent to the colon. Once the adults gain the large intestine, the thin anterior portion of their body, which constitutes the esophagus (see photo above), penetrates the mucous membrane and embeds in the columnar epithelium of the gut wall. The worm then fashions its own essential environment in the human host by inducing a proliferation of host cells within the gut wall in which its anterior portion is embedded. The posterior section now extends out into the lumen of the colon, whereby it releases its eggs. An adult female whipworm does not begin depositing new eggs until approximately 2 to 3 months after the worm's life cycle began in the small intestine. Once the females reach sexual maturity they will produce about 5000 eggs per day for the remainder of their lives, which can last a year or more inside the human host. Below is a nice graph by the Centers for Disease Control and Prevention that depicts the life cycle of Trichuris trichiura:


The Disease. As with the other major soil-transmitted helminths of significance, whipworm infection is usually asymptomatic, although this also contributes to its insidious nature during chronic infections. The whipworm's mucosal attachment and embedding in the epithelium of the large intestine described above leads to pathogenesis. Diarrhea and abdominal discomfort are the most common presentations for symptomatic infections and frank dysentery is not uncommon with high volume infections. In addition, rectal prolapse can also present with high volume infections because of the frequent physical straining during defecation. This straining results from the massive rectal inflammatory response in heavy infections, which gives the infected person the sensation to defecate even when feces are absent. The most significant presentation at the population level is iron-deficiency anemia associated with chronic and/or high volume infections. The anemia is brought on by the large quantity of blood loss in the colon due to the infestation of worms embedded in the epithelium and the subsequent damage to the gut wall and underlying vasculature. As is the case with hookworm, chronic whipworm-associated anemia frequently leads to arrested growth with associated physical and cognitive developmental delay and impairment.

The Epidemiology and the Landscape. Trichuriasis is one of the most important neglected tropical diseases in the world today and is probably the third most common roundworm infection in humans with approximately just under 1 billion prevalent infections worldwide. However, the prevalence of both hookworm and whipworm is very close in magnitude so it is difficult to say which of the two is currently more abundant, though both of these infections are less prevalent than infection with Ascaris lumbricoides. Nevertheless, whipworm and hookworm are, together, probably the largest contributor after malnutrition to poor physical and cognitive development in children worldwide. The current global distribution is pictured in the map below:


As mentioned above, the morbidity associated with a high burden of trichuriasis is predominantly manifested as impaired physical and cognitive development in children. When this morbidity is translated into disability-adjusted life years we can see below that sub-Saharan Africa and especially Southeast Asia are saddled with a disproportionate burden of disease, and we can also see that this burden is quite substantive:

English: Age-standardised disability-adjusted life year (DALY) rates from Trichuriasis by country (per 100,000 inhabitants).
   no data
   less than 5
   5-10
   10-15
   15-20
   20-25
   25-30
   30-35
   35-40
   40-45
   45-50
   50-60
   more than 60

While the life cycles are different between whipworm and hookworm, particularly given that hookworm undergoes two larval stages in the soil, these two groups of worms nevertheless have similar soil requirements, which delineate their global distributions and define their landscape epidemiology in similar ways.

The range of T. trichiura is determined by important aspects of the physical landscape and because of this, as well as critical overlapping characteristics of the human social landscape, the occurrence of trichuriasis in humans is distinctly delineated by geographic features. Soil and climate are two critical landscape features that determine the distribution of T. trichiura. Following the passage of nonembryonated eggs with feces into the soil, these eggs require several weeks in this specific environment before they embryonate and become infectious. Sandy loamy soils, rather than hard clay soils provide a more suitable habitat for these eggs. In addition, the soils must be moist and the temperature must be warm. As such, the specific climatic conditions limit the range of the worms to the tropical and subtropical regions of the world that receive significant amounts of precipitation on an annual basis, while the pedological and edaphological constraints further define the microgeography of these worms. Notice below the global distribution of soil morphology in the map produced by the Natural Resources Conservation Service (NRCS) of the United States Department of Agriculture:


And this NRCS map below depicting the global distribution of soil moisture:



And, finally, the map below by the United Nations Food and Agriculture Organization depicts the global distribution of the annual mean temperature:


These elements described above define the critical features of the physical landscape, but there are also important features of the social landscape that must operate in order for trichuriasis to become endemic.

Lack of sanitation infrastructure, and especially a means by which human waste can be removed from sites of human occupation, results in feces being distributed directly in the human environment or in proximal spaces. When a high degree of local fecal contamination occurs, especially in combination with a lack of rigorous hand and food preparation hygiene, this leads to an abundance of points of contact between embryonated, infectious T. trichiura eggs acquired from the soil and their human hosts. The intersecting landscapes of warm, moist, structurally rich soils and conditions of poverty currently define the geography of trichuriasis, as it does hookworm. It is a geography that encompasses, almost exclusively, the developing world. 

In many poor subsistence agricultural communities, farmers use human feces as a fertilizer to enhance the growth of their crops. This readily available fertilizer provides a cheap, yet very rich, source of critical nutrients to the soil, which can mean the difference between a crop yield that provides the farmer with a livelihood and a yield that does not. Unfortunately, in areas where trichuriasis is endemic, the use of human feces as fertilizer means a constant and widespread distribution of whipworm eggs throughout the farming community, and thus a steady source of new infections.


Control and Prevention. Control and prevention of trichuriasis begins by following the usual guidelines: improving sanitation in resource poor areas. In most settings in the world where trichuriasis is a significant contributor to morbidity, improved infrastructure that can adequately remove human feces from the spaces of human occupation is a first priority in its prevention.

Where large-scale municipally-resourced sanitation infrastructure is not available, individual pit privies can be constructed for single homes, or clusters of homes. Here is a graphic that depicts the dimensions and structural components of such a privy:


Finally, changing agricultural practices that rely on human feces for fertilization of crops could dramatically help reduce the widespread distribution of whipworm in soils in many agricultural subsistence communities.


Unfortunately this, too, can be a difficult practice to disengage since human feces serves as a very rich fertilizer and, thus, can form a critical component to subsistence farming in many parts of the world where other fertilizers or farming technologies are cost prohibitive. And, of course, without an affordable substitute, refraining from human feces fertilization could very well lead to starvation. The massive scope of the problem presented by soil-transmitted helminths in general, and whipworm in particular, should now be coming into focus.

De-worming campaigns do offer some hope, since there are safe, effective, and fairly cheap anti-helminthic drugs available. However, as one might expect, there are obstacles to overcome in de-worming. First, these drugs are not free and, while cheap they may be, without adequate funding poor communities will not be able to prioritize the cost, especially since most infections are generally asymptomatic. Second, effective ways to deliver the de-worming medications to communities need to be implemented, which can be logistically challenging particularly in remote communities or during times of the year when travel may be restricted (i.e. during the rainy season). Third, the extensive use, or misuse, of these drugs will likely lead to antihelminthic-resistance in the worms, thus making the drugs ineffective. Nevertheless, if adequate resources can be put behind de-worming campaigns, and if delivery systems can be adapted to actively engage community members in the delivery and monitoring of these de-worming medications to simultaneously circumvent logistical obstacles and reduce the development of resistance, then substantial reductions in whipworm infections may still be possible.

10 comments:

  1. Education is very important to control this problem. But I wonder how much that will help. Human feces is the perfect option to increase the yield in crops. And given the high cost of artificial fertilizers, I doubt farmers would be willing to start using them unless, there are organizations handing out free/ cheap fertilizer in these communities. And artificial fertilizers come with their own set of problems..

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  2. This article discusses how stopping the use of human feces as fertilizer would drastically reduce spread of disease. However, as Yousra also mentioned, I think that this is unrealistic. When someone in a resource-poor country is faced with the choice of providing food to their family now, and the possibility of a disease, especially a potentially asymptomatic one, I think that their choice will be to risk disease. Therefore, I wondered if there is any cheap/easy way to treat human feces-based fertilizer to kill T. trichiura, but not reduce the effectiveness of the fertilizer. Since this treatment would not have to be safe for humans (it would simply have to not contaminate the crops or soil in a dangerous way), perhaps it could be cheaper than developing human pharmaceutical treatments.

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  3. That's an interesting point which Diana puts forth - treatment of human feces so that it can be used as a potent and cheap fertilizer. I guess Caleb in an earlier post also talks about 'boiling' the human feces so as to be able to use feces as a safe agricultural option. I think that would be a really great thing!!

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    1. I certainly do agree with the idea of treating the human feces, but as great an idea as that is, it also poses new issues that the farmers will have to deal with the first is the fact that treating it might not yield the same result i.e. boiling it might cause it to lose it's effectiveness and second it might create a new cost to the farmers which will take away from their profit margin which places them in the same situation as buying the expensive fertilizers, and third it might solve the problem but opens the door to new issues depending on what is use to treat the feces.

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    2. -First, what is the boiling point of human feces?
      -It is common to use human feces as fertilizer; some farms in the United States use biosolids. Establishing a low-cost biosolid utilization system in poorly resourced countries is a possible solution. Thus, people can continue to use treated human waste as fertilizer.
      Currently, chemotherapy has been used as a rapid-impact intervention method. Mass chemotherapy was performed twice a year from 1969-1995 in all South Korean school children. It took more than 25 years to lower the soil-transmitted helminths incidence rate from 84% to 3%. However, these results can also be attributed to their economic development. Another challenge for chemotherapy is drug resistance.

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  4. I think the question would be how we would treat human feces and what method would be use. A lot of time when we target one problem and try to resolve it we create a whole new set of problem that are not accounted for. For instance, flu vaccination can help protect many people from getting the flu each year, but this also cause many people to become sick because it is not suitable for them as well as causing viral mutations. Maybe one day viral mutations would be so advance that will surpass our ability to treat it.

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  5. Thu, You are correct in stating that interventions for one disease may have unanticipated and harmful effects. Care should be taken when developing any intervention to minimize harm and maximize health benefits. However, I must speak up here to clarify that currently licensed influenza vaccines are perfectly safe and do not cause illness. Neither do these vaccines cause viral mutations. Influenza virus undergoes antigenic drift primarily because of the nature and structure of its genome.

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  6. It is mentioned that the larvae are ingested to infect the host and do not penetrate through the skin which I thought was a possible mechanism. Assuming that subsistence farmers are ingesting the larvae through the produce that they make, can an intervention be made at the level of consumption? Is it possible to wash or treat the crops (in a relatively affordable or cheap way to a farmer) as an alternative to stop using human fertilizer since it is not feasible in endemic areas? Assuming that ingesting the food is the only source of infection, are certain foods more likely to get one sick with whipworm (such as vegetables that do not necessarily require cooking)?

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    1. I agree that a possible intervention for whipworm should be one that focuses on treating the human feces in an affordable and culturally acceptable way to decrease the infection; since that is sometimes the only fertilizer many populations have available. According to the CDC, the main foods that are more likely to increase risk of whipworm are any fruit and vegetable that are grown in soil using human feces. As far as washing and consuming vegetables, the CDC states that washing, peeling, and cooking raw vegetables are proper ways to prevent whipworm, however populations may not always be aware of the food handling precautions (http://www.cdc.gov/parasites/whipworm/gen_info/faqs.html). So a cheaper alternative for an intervention could be raising awareness of proper ways for washing, peeling, and cooking foods grown in human feces fertilizer.

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  7. Overall, it is safe to say that basic hygiene such as hand-washing and rinsing fruits/vegetables before consumption can go a long way in mitigating the spread of this disease. Interventions should also be tailored towards at-risk populations (young children, agricultural workers and pregnant/women of child-rearing age). This might seem far fetched but I wonder whether one can re-engineer the soil composition in environments of high-endemicity. Would such actions be even more detrimental to the landscape ecology of Trichuriasis?

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