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editorial
. 2018 Apr 2;98(5):1211–1212. doi: 10.4269/ajtmh.17-0934

Empowering Girls and Women through Hookworm Prevention

Peter J Hotez 1,*
PMCID: PMC5953389  PMID: 29611502

Human hookworm infection is one of the most ubiquitous illnesses in people who live in extreme poverty. The Global Burden of Disease (GBD) study estimates that in the year 2016, approximately 450 million people lived with hookworms in their small intestines.1 Hookworms feed on human blood and cause long-term intestinal blood loss, leading to iron deficiency.2 For individuals with low iron stores, blood-feeding hookworms can cause sufficient iron and blood loss, leading to anemia. A systematic analysis for the GBD study found that a high percentage of anemia disease burden in Oceania and Africa could be attributed to hookworm infection.3

Adolescent and adult women are vulnerable to hookworm anemia because of their low iron reserves as a result of menstruation, low iron intake, and other factors.2 Pregnant women in resource-poor settings are at added risk of hookworm anemia because of the iron demands of the fetus.4,5 Compounding this problem are coinfections from malaria, which together with hookworm infections can result in profound anemia.6,7 Indeed, the term “agricultural anemia” was once coined to describe the terrible accumulative effects of hookworms on top of malaria, in the setting of low iron intake and hemoglobinopathies, which are also pervasive in rural Africa.8

The adverse consequences of severe hookworm anemia among women in Africa include higher maternal morbidity and mortality.9 But another important effect is the impact of hookworm blood loss and anemia on worker productivity. However, this latter effect has been somewhat elusive to measure and assess, even though anecdotally it is often assumed that hookworm anemia is associated with low agricultural productivity.10,11 For example, the co-discovery of Necator americanus as the etiologic agent of hookworm disease by Bailey K. Ashford, a military physician working in Puerto Rico after the Spanish–American war, was simultaneous with the attribution of hookworms to low worker output.12,13 Similar observations were noted by scientists and physicians employed by the Rockefeller Sanitary Commission working in the American South, and in Brazil, China, and elsewhere globally through the Rockefeller International Health Board, which was later named the International Health Division of the Rockefeller Foundation.1416 Indeed, a retrospective analysis of studies conducted in the Southern United States during the early twentieth century found that chronic hookworm infection in children had the ability to stunt not only physical development but also future wage earnings,17 presumably because of the effects of chronic hookworm anemia on either on work capacity or intellect or some combination of factors. More recent efforts have looked at hookworms and low productivity among workers harvesting plantation-style crops such as bananas and tea,18,19 but the quantitative evidence is still modest and it remains challenging to directly attribute declines in productivity to worms.20

To better pin down and measure the associations between worms and work, Baird et al.21 looked at school-based deworming programs in Kenya, and combined this analysis with longitudinal data that tracked the school children as they became adults. They confirmed the beneficial effects of deworming for hookworm and other soil-transmitted helminthiases and then proceeded to show that programs of deworming enhanced the education of women and increased their secondary school attendance.21 Among men, deworming also increased the labor workforce both qualitatively and quantitatively.21 However, the Baird et al. study and related ones have also been criticized for methodological biases,22 moreover a Cochrane analysis found that randomized control deworming trials often do not translate to beneficial nutritional and cognitive effects.23 Such contradictory findings have led to a vigorous scholarly exchange that is sometimes referred to as “worm wars.”24,25

In this issue of the American Journal of Tropical Medicine and Hygiene, Salmon et al.26 report on a double-blind, prospective randomized effectiveness trial of single-dose albendazole (400 mg) on 250 smallholding women farmers recruited from safe motherhood groups in the Democratic Republic of Congo. Approximately 50% of the women were infected with hookworms, and two-thirds were anemic, including a significant number of women with hemoglobin concentrations less than 10 mg/dL.26 The women were randomized into anthelminthic treatment (N = 125) and placebo groups (N = 125). A major finding was that albendazole treatment of the women was beneficial in terms of aerobic work capacity, even though the effect was not shown to result from increases in blood hemoglobin concentration.26

The study is important given the dearth of randomized clinical trials with anthelminthic drugs, especially on adult women and their capacity to work. It also reinforces the importance of considering adult populations in mass drug administration campaigns and extending deworming programs beyond school-aged children to include the entire community.27,28 The study here supports the cost-effectiveness rationale of community-wide deworming, as proposed by Anderson and his colleagues,28 or a package of interventions that also includes essential medicines for schistosomiasis, lymphatic filariasis, onchocerciasis, trachoma,29 and even human immunodeficiency virus/acquired immunodeficiency syndrome and malaria.30

In addition, the new study reinforces the removal of hookworms from the human intestine as a potent antipoverty measure. Periodic and frequent deworming using albendazole or mebendazole has been the most widely practiced approach, but immunization against hookworms and other helminth pathogens is also being pursued through the development of so-called antipoverty vaccines.11,31 In any case, the Salmon et al. study provides an important piece of evidence base for hookworm prevention as a potent measure to improve the plight of girls and women who live in extreme poverty, and specifically as a means to improve their health and economic well-being. Because of hookworm’s unique effect on agricultural worker productivity in resource-poor economies, hookworm prevention needs to be better prioritized by the world’s finance ministers, and global leaders who wish to introduce or expand interventions that promote women’s health and empowerment.

REFERENCES

  • 1.GBD, 2016. Disease and Injury Incidence and Prevalence Collaborators , 2017. Global, regional, and national incidence, prevalence, and years lived with disability for 328 diseases and injuries for 195 countries, 1990–2016: a systematic analysis for the Global Burden of Disease Study 2016. Lancet 390: 1211–1259. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 2.Hotez PJ, Brooker S, Bethony JM, Bottazzi ME, Loukas A, Xiao S, 2004. Hookworm infection. N Engl J Med 351: 799–807. [DOI] [PubMed] [Google Scholar]
  • 3.Kassebaum NJ, et al. 2014. A systematic analysis of global anemia burden from 1990 to 2010. Blood 123: 615–624. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 4.Bundy DA, Chan MS, Savioli L, 1995. Hookworm infection in pregnancy. Trans R Soc Trop Med Hyg 89: 521–522. [DOI] [PubMed] [Google Scholar]
  • 5.Brooker S, Hotez PJ, Bundy DA, 2008. Hookworm-related anaemia among pregnant women: a systematic review. PLoS Negl Trop Dis 2: e291. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 6.Brooker S, Clements AC, Hotez PJ, Hay SI, Tatem AJ, Bundy DA, Snow RW, 2006. The co-distribution of Plasmodium falciparum and hookworm among African schoolchildren. Malar J 5: 99. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 7.Brooker S, Akhwale W, Pullan R, Estambale B, Clarke SE, Snow RW, Hotez PJ, 2007. Epidemiology of Plasmodium-helminth co-infection in Africa: populations at risk, potential impact on anemia, and prospects for combining control. Am J Trop Med Hyg 77 (Suppl): 88–98. [PMC free article] [PubMed] [Google Scholar]
  • 8.Fleming AF, 1994. Agriculture-related anaemias. Br J Biomed Sci 51: 345–357. [PubMed] [Google Scholar]
  • 9.Christian P, Khatry SK, West KP, Jr, 2004. Antenatal anthelmintic treatment, birthweight, and infant survival in rural Nepal. Lancet 364: 981–983. [DOI] [PubMed] [Google Scholar]
  • 10.Hotez P, 2008. Hookworm and poverty. Ann N Y Acad Sci 1136: 38–44. [DOI] [PubMed] [Google Scholar]
  • 11.Hotez PJ, Ferris MT, 2006. The antipoverty vaccines. Vaccine 24: 5787–5799. [DOI] [PubMed] [Google Scholar]
  • 12.Crosby WH, 1985. The hematology of hookworm disease. Contribution of Bailey K. Ashford. P R Health Sci J 4: 113–119. [PubMed] [Google Scholar]
  • 13.Crosby WH, 1987. The deadly hookworm. Why did the Puerto Ricans die? Arch Intern Med 147: 577–578. [DOI] [PubMed] [Google Scholar]
  • 14.Darling ST, Smilie WG, 1921. Studies on Hookworm Infection in Brazil, No. 14. Monogr. New York, NY: Rockefeller Institute of Medical Research, 42. [Google Scholar]
  • 15.Faust EC, 1929. Human Helminthology. Philadelphia, PA: Lea & Febiger, 375. [Google Scholar]
  • 16.Chandler AC, 1929. Hookworm Disease: Its Distribution, Biology, Epidemiology, Pathology, Diagnosis, Treatment and Control. New York, NY: Macmillan. [Google Scholar]
  • 17.Bleakley H, 2007. Disease and development: evidence from hookworm eradication in the American south. Q J Econ 122: 73–117. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 18.Weisbrod BA, Helminiak TW, 1977. Parasitic diseases and agricultural labor productivity. Econ Dev Cult Change 25: 505–522. [Google Scholar]
  • 19.Gilgen D, Mascie-Taylor CGN, Roetta L, 2001. Intestinal helminth infections, anaemia, and labour productivity of female tea pluckers in Bangladesh. Trop Med Int Health 6: 449–451. [DOI] [PubMed] [Google Scholar]
  • 20.Guyatt H, 2000. Do intestinal nematodes affect productivity in adulthood? Parasitol Today 16: 153–158. [DOI] [PubMed] [Google Scholar]
  • 21.Baird S, Hicks JH, Kremer M, Miguel E, 2016. Worms at work: long-run impacts of a child health investment. Q J Econ 131: 1637–1680. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 22.Jullien S, Sinclair D, Garner P, 2016. The impact of mass deworming programmes on schooling and economic development: an appraisal of long-term studies. Int J Epidemiol 45: 2140–2153. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 23.Taylor-Robinson DC, Maayan N, Soares-Weiser K, Donegan S, Garner P, 2015. Deworming drugs for soil-transmitted intestinal worms in children: effects on nutritional indicators, haemoglobin, and school performance. Cochrane Database Syst Rev CD000371. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 24.Croke K, Hicks JH, Hsu E, Kremer M, Miguel E, 2017. Should the WHO withdraw support for mass deworming? PLoS Negl Trop Dis 11: e0005481. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 25.Belluz J, 2015. Worm Wars: The Fight Tearing Apart The Global Health Community, Explained. https://www.vox.com/2015/7/24/9031909/worm-wars-explained. Accessed December 22, 2017.
  • 26.Salmon M, et al. 2018. Albendazole treatment improves work capacity in women smallholder farmers infected with hookworm: a double-blind randomized control trial. Am J Trop Med Hyg 98: 1419–1426. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 27.Lo NC, et al. 2017. A call to strengthen the global strategy against schistosomiasis and soil-transmitted helminthiasis: the time is now. Lancet Infect Dis 17: e64–e69. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 28.Turner HC, Truscott JE, Anderson RM, 2016. Cost-effectiveness of community-wide treatment for helminthiasis. Lancet Glob Health 4: e156. [DOI] [PubMed] [Google Scholar]
  • 29.Hotez PJ, Molyneux DH, Fenwick A, Kumaresan J, Sachs SE, Sachs JD, Savioli L, 2007. Control of neglected tropical diseases. N Engl J Med 357: 1018–1027. [DOI] [PubMed] [Google Scholar]
  • 30.Hotez PJ, Mistry N, Rubinstein J, Sachs JD, 2011. Integrating neglected tropical diseases into AIDS, tuberculosis, and malaria control. N Engl J Med 364: 2086–2089. [DOI] [PubMed] [Google Scholar]
  • 31.Hotez P, 2011. A handful of ‘antipoverty’ vaccines exist for neglected diseases, but the world’s poorest billion people need more. Health Aff (Millwood) 30: 1080–1087. [DOI] [PubMed] [Google Scholar]

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