Hookworm

The new england journal of medicine
review article
current concepts
Hookworm Infection
Peter J. Hotez, M.D., Ph.D., Simon Brooker, D.Phil., Jeffrey M. Bethony, Ph.D.,
Maria Elena Bottazzi, Ph.D., Alex Loukas, Ph.D., and Shuhua Xiao, M.D.
h ookworm infection in humans is caused by an infection with

the helminth nematode parasites Necator americanus and Ancylostoma duodenale
and is transmitted through contact with contaminated soil. It is one of the
most common chronic infections, with an estimated 740 million cases in areas of rural
poverty in the tropics and subtropics.1 Because hookworm infection occurs predomi-
From the Department of Microbiology and
Tropical Medicine, George Washington Uni-
versity, Washington, D.C. (P.J.H., J.M.B.,
M.E.B.); the Department of Infectious and
Tropical Diseases, London School of Hy-
giene and Tropical Medicine, London (S.B.);
the Division of Infectious Diseases and
nantly among the world’s most impoverished people,1 it holds a unique place in mod- Immunology, Queensland Institute of Med-
ern history. For example, the reputation of pre-1949 China as the “sick man of Asia” ical Research, Brisbane, Australia (A.L.);
was partly a result of the high prevalence and intensity of infection with hookworm.2 and the Institute of Parasitic Diseases, Chi-
nese Center for Disease Control and Pre-
Mohandas Gandhi had hookworm infection in the last years of his life.3 Hookworm vention, Shanghai, China (S.X.). Address
was also a contributing factor in the slowing of economic development during the early reprint requests to Dr. Hotez at the De-
part of the 20th century in the southern United States.4 Today, hookworm infection is partment of Microbiology and Tropical Med-
icine, George Washington University, Ross
among the most important tropical diseases in humans; the use of disability-adjusted Hall 736, 2300 Eye St., NW, Washington,
life years as a quantitative measure of the burden of disease reveals that this infection DC 20037, or at mtmpjh@gwumc.edu.
outranks African trypanosomiasis, dengue, Chagas’ disease, schistosomiasis, and
N Engl J Med 2004;351:799-807.
leprosy.5 Copyright © 2004 Massachusetts Medical Society.
The greatest number of hookworm cases occur in Asia, followed by sub-Saharan Af-
rica.1 In China alone, approximately 190 million people are infected, an estimate based
on a nationwide study involving the examination of fecal specimens obtained from al-
most 1.5 million people between 1988 and 1992.2 N. americanus is the most common
hookworm worldwide, whereas A. duodenale is more geographically restricted. In con-
trast to these major anthropophilic species, three species of zoonotic hookworm are
minor causes of disease in humans. A. ceylanicum infects dogs and cats and can also in-
fect humans but is not considered an important pathogen. The dog hookworm A. cani-
num causes human eosinophilic enteritis in northeastern Australia,6 and A. braziliense
causes cutaneous larva migrans.
pathophysiology and clinical disease

larval invasion of tissue
Some of the highest rates of hookworm transmission occur in the world’s coastal re-
gions, where infective third-stage larvae can migrate freely in sandy soils and where
temperatures and moisture are optimal for viability of larvae.7 In these areas, repeated
exposure to third-stage larvae of N. americanus or A. duodenale results in a local pruritic,
erythematous, papular rash known as “ground itch.” Although the entire body surface
is vulnerable, ground itch appears most frequently on the hands and feet, which are the
major sites of entry for third-stage larvae. In contrast to ground itch, skin invasion by
zoonotic A. braziliense third-stage larvae results in cutaneous larva migrans, or “creep-
ing eruption,” a self-limited dermatologic condition characterized by serpiginous bur-
rows, 1 to 5 cm long. Created by third-stage larvae migrating in the epidermis, the bur-
rows appear on the feet in 39 percent of cases (Fig. 1), the buttocks in 18 percent, and
n engl j med 351;8 www.nejm.org august 19, 2004 799
The New England Journal of Medicine

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Copyright © 2004 Massachusetts Medical Society. All rights reserved.
terized by nausea, vomiting, pharyngeal irritation,

cough, dyspnea, and hoarseness. Increased circu-
lating levels of IgE occur in response to migrations
of third-stage larvae in the lungs and intestines.13
clinical disease
The major hookworm-related injury in humans
occurs when the adult parasites cause intestinal
blood loss.14-16 The term “hookworm disease” re-
fers primarily to the iron-deficiency anemia that re-
sults from moderate or heavy infection. Blood loss
occurs when the worms use their cutting apparatus
to attach themselves to the intestinal mucosa and
submucosa and contract their muscular esophagi
to create negative pressure, which sucks a plug of
tissue into their buccal capsules (Fig. 3). Capillar-
ies and arterioles are ruptured not only mechani-
cally but also chemically, through the action of hy-
drolytic enzymes.14 To ensure blood flow, the adult
hookworms release anticlotting agents.17,18 (One
Figure 1. Cutaneous Larva Migrans Caused
by Ancylostoma braziliense.
of these, a novel factor VIIa/tissue factor inhibitor,
Reprinted from Despommier et al.,8 with the permission
is being developed as a therapeutic agent to block
of the publisher. the coagulopathy of fulminant infection with Ebola
virus.19) The hookworm ingests a portion of the
extravasated blood. Some red cells undergo lysis,
thereby releasing hemoglobin, which is digested by
the abdomen in 16 percent; in the remainder of cas- a cascade of hemoglobinases that line the gut of
es, the burrows appear predominantly in the lower the parasite.20
legs, arms, and face.9 In the United States, cutane- The major clinical manifestations of hookworm
ous larva migrans is seen commonly in military per- disease are the consequences of chronic intestinal
sonnel, in travelers returning from resorts that have blood loss. Iron-deficiency anemia occurs and hy-
sandy beaches, and in residents of Florida and the poalbuminemia develops when blood loss exceeds
Gulf Coast; it is treated successfully with short oral the intake and reserves of host iron and protein.15
courses of either albendazole or ivermectin.10,11 Depending on the status of host iron, a hookworm
While in the soil, third-stage larvae are in a state burden (i.e., the intensity of infection, or number
of developmental arrest; development resumes af- of worms per person) of 40 to 160 worms is asso-
ter the larvae enter the human host.12 In humans, ciated with hemoglobin levels below 11 g per deci-
entry through the skin is followed within 10 days liter.21,22 However, other studies have shown that
by larval migration to the lungs (Fig. 2), resulting anemia may occur with a lighter hookworm bur-
in cough and sore throat. Pulmonary hookworm in- den.23 Because infection with A. duodenale causes
fection resembles Löffler’s syndrome because of its greater blood loss than does infection with N. amer-
association with eosinophilia in the lung. In rare icanus, the degree of iron-deficiency anemia induced
cases, pneumonitis accompanies cutaneous larva by hookworms depends on the species.16 For in-
migrans. Hookworm pneumonitis is usually not stance, in Zanzibar, among children who were in-
severe, although it may last for more than a month, fected only with N. americanus hookworms, the prev-
until the larvae leave the lungs and enter the gastro- alence of hypoferritinemia (ferritin level, <12 µg per
intestinal tract. It is not commonly recognized that liter) was 33.1 percent, whereas in children who
A. duodenale third-stage larvae infect humans both were also infected with A. duodenale hookworms, the
by the oral route and through the skin. When infec- prevalence was 58.9 percent.24 When iron stores in
tion with A. duodenale occurs by the oral route, the the host become depleted, there is a direct correla-
early migrations of third-stage larvae cause a syn- tion between the intensity of hookworm infection
drome known as Wakana disease, which is charac- (typically measured by quantitative egg counts) and
800 n engl j med 351;8 www.nejm.org august 19 , 2004

current concepts
Figure 2. The Life Cycles of Necator americanus and Ancylostoma duodenale.

Humans acquire hookworm when third-stage infective larvae in soil either penetrate the skin (as do both N. americanus
and A. duodenale) or when they are ingested (A. duodenale only). The larvae are each approximately 600 µm long and are
developmentally arrested. After entering the host, the larvae receive a host-derived signal that causes them to resume
development.12 The larvae then migrate through the vasculature and are swept by the afferent circulation to the right
side of the heart and then to the pulmonary vasculature. From the lung capillaries, the larvae rupture and enter the pa-
renchyma, where they ascend the alveoli, bronchioles, bronchi, and trachea. After being coughed up and swallowed, the
larvae enter the gastrointestinal tract, where they molt twice and develop to the adult stage. Approximately six to eight
weeks pass from the time the larvae first infect humans until they reach sexual maturity and mate. Each female hook-
worm produces thousands of eggs daily. Intestinal blood loss in the host begins just before egg production and release
and continues for the life of the hookworm. Hookworm eggs exit the body in feces. When deposited in soil, with ade-
quate warmth, shade, and moisture, the eggs hatch within 24 to 48 hours and develop into first-stage larvae. These lar-
vae molt twice as they develop to the third stage. The larvae are nonfeeding organisms that can live for several weeks
in the soil, until they exhaust their lipid metabolic reserves. Transmission of hookworm is most prevalent in areas where
there is high moisture and appropriate soil conditions. Sandy soils containing silt (i.e., “sandy loam”) are most favored
and account for the high prevalence of hookworm infection in coastal areas.7 (Adapted from Despommier et al.8)

the reduction in hemoglobin, serum ferritin, and

A protoporphyrin levels (Fig. 4).15,24
Most of the physical signs of chronic hookworm
infection reflect the presence of iron-deficiency
anemia. In addition, anasarca from extensive plas-
ma hypoproteinemia is associated with edema of
the face and lower limbs and with potbelly. The skin
becomes waxy and acquires a sickly yellowish color
(a feature of tropical chlorosis). Hookworm can
cause hypothermia that is severe enough to reduce
fever caused by malaria.25 Other than hypochro-
mic microcytic anemia, the most prominent labo-
ratory finding is eosinophilia. Eosinophilia peaks
at five to nine weeks after the onset of infection, a
period that coincides with the appearance of adult
B hookworms in the intestine.13 Patients with a light
hookworm burden are usually asymptomatic; how-
ever, some patients report subjective clinical im-
provement after treatment.26 A moderate or heavy
hookworm burden results in recurrent epigastric
pain and tenderness, nausea, exertional dyspnea,
pain in the lower extremities, palpitations, joint and
sternal pain, headache, fatigue, and impotence.27,28
Some patients crave bulky substances and ingest
dirt (pica). In adults, the capacity for work may be
adversely affected, and many report an inability to
work.26,29
hookworm disease in mothers

and children
The overall prevalence and intensity of hookworm
infection are higher in males than in females, in
part because males have greater exposure to in-
fection. However, women and young children have
the lowest iron stores and are therefore most vul-
nerable to chronic blood loss as the result of hook-
worm infection.15,24 In children, chronic hook-
worm disease retards physical growth,30 which is
Figure 3. Pathogenesis and Clinical Sequelae of Hook- sometimes most apparent at puberty. Approximate-
worm Disease.
ly 80 years ago, an inverse correlation was observed
Panel A shows a scanning electron micrograph of Neca-
between the hookworm burden and a child’s intel-
tor americanus. The buccal capsule is characterized by
cutting plates, which allow the adult parasite to feed ligence quotient.31 More recent evidence suggests
on intestinal mucosa, submucosa, and blood. Each hook- that hookworm infection also has subtle yet pro-
worm ranges in length from 5 to 13 mm and causes up found adverse effects on memory, reasoning ability,
to 0.3 ml of blood loss per day. (Photograph by David and reading comprehension in childhood.32 Most
Scharf; reprinted from Despommier et al.8 with the per-
of these effects are probably attributable to the pres-
mission of the publisher.) Panel B shows an adult hook-
worm feeding on intestinal mucosa and submucosa ence of iron-deficiency anemia. Infants and pre-
(hematoxylin and eosin). (Photograph courtesy of school children are particularly vulnerable to the
Dr. Bernard Zook, Department of Pathology, George developmental and behavioral deficits caused by
Washington University Medical Center.) iron-deficiency anemia,33 and two analyses indi-
cate that hookworm infection remains an impor-

current concepts
pregnancy could result in vertical transmission to

N. americanus A. duodenale neonates, possibly through ingestion of A. duodenale
11.0 10.9 10.9
third-stage larvae in milk and colostrum.42
10.6
In many regions of sub-Saharan Africa, hook-
10.5 10.4
worm disease overlaps geographically with falcipa-
Hemoglobin (g/dl)
10.0 9.9
rum malaria. Since much of the morbidity associat-
9.8
ed with both diseases results from anemia,14,15,43
9.6
9.5 it is possible that hookworm disease exacerbates
9.2 malarial anemia and vice versa. A potentially prom-
9.0 ising avenue of research is the further examination
of co-endemic infections, such as hookworm infec-
0.0
0 1–1999 2000–3999 ≥4000 tion, malaria, and human immunodeficiency virus
No. of Hookworm Eggs per Gram of Feces (HIV) infection, in which morbidity is due largely
or at least in part to anemia.15,43,44
Figure 4. Relationship between the Hookworm Burden
and Anemia.
Quantitative egg counts serve as an indirect measure diagnosis in returning
of the adult-hookworm burden (i.e., the number of worms travelers and immigrants
per patient). Hemoglobin levels drop in proportion
to infection. (Data are from Albonico et al.16) The cutaneous manifestations of hookworm in-
fection must be differentiated from cercarial der-
matitis (“swimmer’s itch”) and creeping erup-
tant contributor to anemia in this age group.34,35 tion from other causes, such as gnathostomiasis,
Hookworm infection in children may reduce school strongyloidiasis, and infection with fly larvae. The
attendance, with subsequent effects on productivi- pulmonary manifestations are usually not specific
ty and wage-earning potential in adulthood.4,29 enough to link them specifically to hookworm. Per-
Hookworm infection is considered a major sistent eosinophilia in refugees, especially those
health threat to adolescent girls and women of re- from Southeast Asia, is commonly associated with
productive age, with adverse effects on the out- active hookworm infection.45 Abdominal tender-
come of pregnancy.22,36,37 The World Health Or- ness or the presence of iron-deficiency anemia in
ganization estimates that because of increased immigrants from areas where hookworm is endem-
physiological demands for iron during pregnancy ic warrants investigation for infection.27 The mi-
combined with malnutrition, more than half of croscopical examination of unconcentrated feces
the pregnant women in developing countries have is adequate to identify hookworm eggs and to di-
problems related to iron-deficiency anemia.37 Se- agnose clinically important infection. Several quan-
vere iron-deficiency anemia during pregnancy has titative techniques are available to estimate the
been linked to increased maternal mortality, im- output of hookworm eggs; these techniques are
paired lactation, and prematurity and low birth valuable for epidemiologic studies because they pro-
weight.37 An estimated 44 million pregnant wom- vide indirect measures of the worm burden. The
en are infected with hookworm worldwide, with eggs of A. duodenale and N. americanus are indistin-
7.5 million in sub-Saharan Africa alone.22,38 In guishable, although the polymerase chain reaction
1929, A.C. Chandler first pointed out that “preg- and morphologic examination of cultured third-
nancy is a powerful factor in accentuating the ef- stage larvae can differentiate the two species.46
fects of hookworm disease, or it might be more ac- Zoonotic hookworm infection does not cause egg-
curate to put it vice versa.”39 Estimates in Kenya bearing infections in humans.
and Nepal suggest that hookworm infection caus-
es 30 percent and 41 percent, respectively, of mod-
erate or severe cases of anemia among pregnant
epidemiology , treatment,
and prospects for control
women (hemoglobin level, <9 g per deciliter).15
The association between hookworm infection and overdispersion of and predisposition
anemia is greatest in multigravidas.40,41 It has been to hookworm infection
conjectured that in China and other regions where In all areas where hookworm is endemic, the varia-
A. duodenale occurs, hookworm infection during tion in the worm burden among persons who be-

come infected is large. High-intensity and low-

intensity infections have been recorded among sub-
jects living in similar conditions of exposure to the
Mean No. of Worms (arbitrary units)

parasite. The distribution of worm burdens among
different human hosts is highly overdispersed so
that often only 10 percent of the infected popula-
tion carries 70 percent of the worms.47 Because Hookworm
most helminths do not replicate in humans, the
rate of morbidity from infections with helminths is
typically highest among patients with the heaviest T. trichiura
worm burdens. There is evidence that some per-
sons are predisposed to a heavy (or light) hook- A. lumbricoides
worm burden owing to either genetic or exposure
factors.48,49
0 5 10 15 20 25 30 35 40 45 50
Age (yr)
hookworm and age
For many common helminthic infections, includ-
ing ascariasis, trichuriasis, and schistosomiasis, the Figure 5. Patterns of Hookworm Infection
According to Age.
intensity of infection usually peaks during child-
The hookworm burden increases with age, in contrast
hood and adolescence (Fig. 5).47 In contrast, there to the burden of other soil-transmitted helminths (e.g.,
appears to be considerable variation in the age– Ascaris lumbricoides and Trichuris trichiura), which is high-
intensity profile of hookworm infection. Although est in childhood. Worm burden is shown in arbitrary
the hookworm burden may be heavy in children, es- units to emphasize the relative shape of the curves.
pecially those in sub-Saharan Africa,30,34 the most
commonly recognized pattern is a steady rise in the
intensity of infection during childhood, with either the question of whether hookworm as well as other
a peak or a plateau in adulthood. In China, age ac- helminths promote susceptibility to HIV infection,
counts for 27 percent of the variation in the inten- malaria, tuberculosis, or other infections.56,57
sity of hookworm infection, with the highest in-
tensity among middle-aged persons, or even those school-based deworming
over the age of 60 years.50 Such infection patterns Although proper sanitation and footwear are of-
have implications for the world’s expanding elder- ten considered important for the control of hook-
ly populations.2 worm, their effect on transmission is frequently ei-
The observation that the intensity of hookworm ther marginal or evident only after decades.50,53,58
infection increases with age has led to the sugges- The specific treatment of choice for the removal of
tion that hookworms can either evade or suppress hookworms from the intestines is a single dose of
host immune responses.51,52 To understand how a benzimidazole anthelmintic, either albendazole
this occurs, several investigators have either de- (400 mg) or mebendazole (500 mg).59 Either agent
scribed or isolated antiinflammatory and other usually reduces the hookworm burden to a level be-
immunomodulatory molecules from adult hook- low the threshold that could result in disease, and
worms, including a T-cell apoptotic factor, an inte- both agents are now available generically at low
grin antagonist of host CD11b and CD18, a retinol- cost. Because of this, a resolution was put forward
binding protein, a C-type lectin, a tissue inhibitor at the 2001 World Health Assembly urging coun-
of metalloproteases, cysteine-rich secretory pro- tries to control schistosomiasis and the soil-trans-
teins, and an eotaxin-degrading factor.53 These bio- mitted helminthiases — ascariasis, trichuriasis, and
active polypeptides may also have systemwide ef- hookworm infection. The global target is by 2010
fects that down-regulate host immune responses to provide routine treatment for at least 75 percent
to other infections. In the process of mining the of all school-age children who are at risk for infec-
hookworm genome,54 researchers are likely to dis- tion, using a benzimidazole anthelmintic alone or
cover additional molecules.55 Further study of im- in conjunction with praziquantel.37 In time, this
munomodulating molecules derived from parasites would become the largest public health program
might shed light on the emerging controversy over ever attempted.60 The rationale for focusing on

current concepts
schools is that school-age children have the high- Moreover, in areas where hookworm is endemic,
est intensity of ascaris, trichuris, and schistosome reinfection often occurs within just a few months
infections of any age group, and schools provide a after deworming with the use of a benzimidazole
cost-effective way to deliver anthelmintics.37,61 Ei- anthelmintic.67 In some cases, treatments are re-
ther of the benzimidazole anthelmintics can be quired three times a year to improve the iron status
administered as a single tablet to all children, re- of the host.63,68 Additional data indicate that the
gardless of their size and age. In communities where efficacy of treatment with benzimidazole anthelm-
infection is common, clinicians can offer treatment intics diminishes after periodic therapy.69 These
to all children without the need to examine each problems, coupled with theoretical concern about
child for the presence of worms. With support from emerging resistance to benzimidazole anthelm-
the local health system, teachers can safely ad- intics,70 have led to efforts among researchers to
minister benzimidazole anthelmintics and prazi- identify new tools for the control of hookworm.
quantel.37,61 To date, the reduction of poverty and increased
School-based deworming offers a number of economic development have done more to elimi-
health-related and other benefits to children, in- nate hookworm infection in industrialized nations
cluding improvements in iron and hemoglobin than any other factor, including sanitation, the use
status,62,63 in physical growth,30,63 in cognition, in of anthelmintics, the use of footwear, and health
educational achievement, and in school absentee- education.2 Until such socioeconomic reforms be-
ism,63,64 as well as major advantages for the whole come widespread, the implementation of the World
community, including reduced helminth transmis- Health Assembly’s resolution to reduce infection
sion through soil and a lower disease burden, es- and the development of a vaccine may help control
pecially for ascariasis and trichuriasis.61,63,65 It is hookworm infection.
less obvious, however, what effect school-based Supported by grants (to Dr. Hotez) from the Human Hookworm
Vaccine Initiative of the Sabin Vaccine Institute, the Bill and Melinda
deworming will have on reducing the disease bur- Gates Foundation, the March of Dimes Birth Defects Foundation,
den of hookworm in a community. Because the dis- the China Medical Board of New York (98-674), the National Health
ease burden is often concentrated among adult pop- and Medical Research Council of Australia, the Ramaciotti Founda-
tion, and the National Institutes of Health (AI-32726) and by a
ulations (including women of reproductive age), Wellcome Trust Advanced Training Fellowship (73656, to Dr. Brook-
and because preschool children are particularly vul- er). Dr. Bethony is the recipient of an International Research Scien-
nerable to the effects of iron deficiency,33,34 in many tist Development Award (1K01 TW00009) from the John E. Fogarty
International Center, National Institutes of Health. Dr. Loukas is the
communities school-based programs miss impor- recipient of an R.D. Wright Career Development Award from the
tant vulnerable populations that are at risk for hook- National Health and Medical Research Council of Australia.
worm. In contrast to infections with ascaris and Dr. Hotez reports having received consulting fees from Pfizer and
GlaxoSmithKline, and Drs. Hotez, Bottazzi, and Loukas report hav-
trichuris, it is unlikely that school-based deworming submitted an international patent application for a hookworm
ing will reduce the transmission of hookworm.66 vaccine.
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The new england journal of medicine

h ookworm infection in humans is caused by an infection with

pathophysiology and clinical disease

n engl j med 351;8 www.nejm.org august 19, 2004 799

The New England Journal of Medicine

terized by nausea, vomiting, pharyngeal irritation,

800 n engl j med 351;8 www.nejm.org august 19 , 2004

The New England Journal of Medicine

Figure 2. The Life Cycles of Necator americanus and Ancylostoma duodenale.

n engl j med 351;8 www.nejm.org august 19, 2004 801

The New England Journal of Medicine

the reduction in hemoglobin, serum ferritin, and

hookworm disease in mothers

802 n engl j med 351;8 www.nejm.org august 19 , 2004

The New England Journal of Medicine

pregnancy could result in vertical transmission to

n engl j med 351;8 www.nejm.org august 19, 2004 803

The New England Journal of Medicine

come infected is large. High-intensity and low-

Mean No. of Worms (arbitrary units)

804 n engl j med 351;8 www.nejm.org august 19 , 2004

The New England Journal of Medicine

n engl j med 351;8 www.nejm.org august 19, 2004 805

The New England Journal of Medicine

806 n engl j med 351;8 www.nejm.org august 19, 2004

The New England Journal of Medicine

view current job postings at the nejm careercenter

n engl j med 351;8 www.nejm.org august 19, 2004 807

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