Dr.

Sulaiman Al Habib Medical Journal

Vol. 2(4); December (2020), pp. 144–150
DOI: https://doi.org/10.2991/dsahmj.k.200916.002; ISSN 2666-819X; eISSN 2590-3349
https://www.atlantis-press.com/journals/dsahmj

Review
Human Soil-transmitted Helminths and Lung Infections:
A Guide Review for Respiratory Therapists

Majed H.M. Wakid1,2,*,

1
Department of Medical Laboratory Technology, Faculty of Applied Medical Sciences, King Abdulaziz University, Jeddah, Saudi Arabia
2
Special Infectious Agents Unit, King Fahd Medical Research Center, Jeddah, Saudi Arabia

ARTICLE INFO ABSTRACT

Article History Soil-transmitted helminths are among the neglected tropical diseases, although some 1.5 billion individuals are affected.
Received 14 April 2020 Traveling to endemic regions, global immigration, and increase of immunocompromised cases, in addition to other factors, have
Accepted 04 September 2020 an influence on global susceptibility to these parasites. These helminth parasites can affect the human respiratory system during
their life cycles either directly or indirectly. A better understanding of all aspects related to these parasites will assist respiratory
Keywords therapists in putting together a proper diagnosis and management. This review covers the morphology, life cycles, epidemiology,
Parasites clinical aspects, glance about laboratory diagnosis, and control of soil-transmitted helminths.
soil-transmitted helminths
Ascaris lumbricoides
hookworm
Strongyloides stercoralis
lung © 2020 Dr. Sulaiman Al Habib Medical Group. Publishing services by Atlantis Press International B.V.
global health This is an open access article distributed under the CC BY-NC 4.0 license (http://creativecommons.org/licenses/by-nc/4.0/).

1. INTRODUCTION 2.  ASCARIS LUMBRICOIDES

Globally, the field of respiratory therapy is given more attention 2.1.  Introduction and Epidemiology
recently, and many universities established new bachelor pro-
grams among the Allied Medical Sciences Faculties. According Ascaris lumbricoides belongs to the Family Ascarididae of the
to the World Health Organization (WHO), many parasitic infec- Suborder Ascaridina. It is the largest intestinal nematoda round-
tions are among the neglected tropical diseases. This review will worm (male, 15–30 cm; female, 20–35 cm) and among the common
be a start of a comprehensive series addressed to respiratory ther- helminths that infect humans. According to the WHO, ascariasis
apists to provide an overview of the important parasites involved affects about 1 billion people worldwide in endemic countries,
as causative agents of lung infection. This paper discusses the mainly children and adolescents [3,4]. Infection with A. lumbri­
soil-transmitted helminths and their impact on the lungs and coides is cosmopolitan, mainly in tropical areas with poor sanitation
other aspects. and personal hygiene. Those who live in areas where wastewater is
used for irrigation, people defecate outdoors, or human feces are
The WHO estimated that globally more than 1.5 billion people are
used as fertilizer, are at high risk of infection associated with the
infected with soil-transmitted helminths. These helminths, which
consumption of raw vegetables. Ascaris infection in the commu-
are roundworms related to the Phylum Nematoda, have among the
nity is not age-dependent and can affect children, as well as young
highest infection rates in man, especially in tropical and subtropical
and elderly populations [5].
areas [1]. Contaminated soil plays a vital role in these worms’ trans-
mission and life cycles. The soil-­transmitted helminths include
Ascaris lumbricoides, hookworm (Ancylostoma duodenale and
Necator americanus), Strongyloides stercoralis, and Trichuris trichi­ 2.2.  Life Cycle and Modes of Infection
ura. The first three parasites are commonly associated with lung
infection and will be covered in this review (Figure 1). Very rare Ascarislumbricoides transmission to humans is through direct
instances of pneumonitis caused by T. trichiura may occur when fecal–oral transmission. It occurs mainly with soil contamination
larvae penetrate the intestinal tissues and by way of the lymph and of hands or ingestion of contaminated foods or drinks containing
blood vessels reach the lungs [2]. mature second-stage larvated (embryonated) eggs. After hatching
in the upper part of the small intestine, larvae penetrate the wall of
intestinal mucosa, and transport to the vascular capillaries, then
Email: mwakid@kau.edu.sa
* via the portal vein to the hepatic circulation. Some of the larvae can
Peer review under responsibility of the Dr. Sulaiman Al Habib Medical Group migrate to the liver directly through the intestinal wall. Larvae will
 M.H.M. Wakid / Dr. Sulaiman Al Habib Medical Journal 2(4) 144–150 145

identification of eggs (fertilized or/and unfertilized) using direct

smears, thick smears, sedimentation and flotation techniques.
Abdomen ultrasonography, Computed Tomography (CT), magnetic
resonance imaging, and X-ray can show the adult worms of
A. lumbricoides in the gut.
Immunoglobulin IgG4 antibodies against Ascaris hemoglobin
could be used as a supportive marker for diagnosis [18,19].
Chest CT and radiographs may illustrate bilateral pleural effusion,
consolidation, patchy alveolar infiltrates, and unilateral or bilat-
eral transient migratory fleeting nonsegmental opacities of various
sizes often peripherally situated [20–23]. Examination of sputum,
bronchoalveolar specimens or gastric secretions may detect larvae,
eosinophils, and Charcot–Leyden crystals. Elevated levels of total
serum Immunoglobulin E (IgE) are associated with several para-
sitic infections including Ascaris larval infection [24,25].

Figure 1 | Life cycles of the human soil-transmitted helminths. Reproduced 3. HOOKWORM

with modification from Gordon et al. [98].
3.1.  Introduction and Epidemiology
molt to the third stage, then proceed to the right side of the heart,
then to the pulmonary circulation [6]. They stay for several days, Human hookworm includes two species: A. duodenale and
then make a trip across the alveolar wall and tracheobronchial tree N. americanus. They get their common name from the hook-like
to the larynx and esophagus to the small intestine. Here, larvae teeth in the mouth part of adult worms. Hookworms are classified
molt into the fourth stage and then finally become adults. After under the Suborder Strongylina and Family Ancylostimatidea.
copulation, adult female worms begin to produce fertilized (fertile) Hookworms infect an estimated 450–740 million people world-
eggs. Meanwhile, unfertilized (infertile) eggs can be seen in cases wide [4,26]. The size of adult worms is about 1 cm long (male, 8–11
with absence of adult male worms. Fertilized eggs can survive and mm; female, 10–13 mm). A. duodenale is distributed more focally,
stay viable for several months or years depending on the surround- although its common name is “Old World hookworm.” The sizes
ing warm and moist condition [3,5,6]. of male and female adult worms are 7–9 and 9–11 mm, respec-
tively, being a little smaller than the preceding species. Although
the common name of N. americanus is “New World hookworm,”
2.3.  Pathology and Clinical Aspects this species widely found across developing regions of South Asia
and sub-Saharan Africa. In several studies, both species coexisted
Most intestinal ascariasis cases are asymptomatic or with limited in the same region with higher prevalence for N. americanus [27].
symptoms. Symptomatic cases depend on the worm burden espe- Infection with hookworms starts gradually from childhood and
cially in children. The common nonspecific symptoms include reaches the highest level during late teens and early adulthood.
abdominal pain, diarrhea, weight loss, weakness, and anorexia [7]. Intensity stabilization then begins during all age levels unless
Complications related to ascariasis may include anemia caused by effective control measures are involved [28–31].
upper gastrointestinal bleeding, intestinal obstruction, intestinal
In general, the severity of iron deficiency anemia and protein mal-
peritonitis, pancreatitis, acute appendicitis, acute cholecystitis, gas-
nutrition caused by hookworms depends on the amount of blood
tric ascariasis, and hematemesis [8–10].
loss [32], which is associated with the worm burden, and depends
When larvae accumulate in the lung during the second week of on the nutritional and iron status of the host prior to the infection.
infection, eosinophilic pneumonia, or Loeffler syndrome, may
occur because of hypersensitivity reactions to larval stages. Light
infection is usually asymptomatic. The main symptoms of heavy 3.2.  Life Cycle and Modes of Infection
infections include chest pain, dry cough, dyspnea with abnormal
breath sounds, bloody sputum (hemoptysis), and in rare cases, Humans are the principal final hosts of hookworms, and infected
pleuritis or pleural effusion. In addition, respiratory failure was persons pass thousands of eggs in feces daily. Eggs mature in soil
associated with ascariasis in immunodeficient patients. Some or any favorable warm moist conditions outside the host, forming
larvae can cause complications in other parts of the body. This rhabditiform larvae (L1 and L2) and finally filariform larvae (L3).
could lead to granulomatous peritonitis, atopic dermatitis, and eye Humans become infected via skin penetration (transcutaneous) with
infection [11–17]. L3 through bare feet (mainly N. americanus) or via the oral route in
the case of A. duodenale. As in the case of A. lumbricoides, the larvae
migrate through blood or lymph stream to the heart and lungs. Larvae
2.4. Diagnosis reach the small intestine after penetrating the alveolar wall to the tra-
chea, esophagus, and stomach. The larvae molt and become mature
The diagnosis of intestinal ascariasis depends on the macroscopic adult worms in the small intestine within 2 months, and are soon ready
detection of adult worms in stool sample, in addition to microscopic to start lay eggs [31].
146 M.H.M. Wakid / Dr. Sulaiman Al Habib Medical Journal 2(4) 144–150

3.3.  Pathology and Clinical Aspects 4.2.  Life Cycle and Modes of Infection
First, cutaneous dermatitis is caused during larval skin penetra- The females of parasitic generations in infected final hosts inhab-
tion. A red itchy papule is formed at the site of each penetration, iting the mucosa of the duodenum or the jejunum lay eggs by
the so-called “ground itch,” Scratching leads to secondary bacterial parthenogenesis. These eggs grow promptly and hatch to become
infection and formation of pustules. In rare cases, in heavy infections rhabditiform larvae (R-form) then pass in the stool. If the patient
with extensive lesions the patients suffer from creeping eruption [33]. suffers from constipation or immunodeficiency, unpassed out
R-form become infective filariform larvae (F-form), which invade
Filariform larvae that break through the pulmonary capillaries
the intestinal walls leading to internal autoinfection. Rarely
can cause bronchitis and bronchopneumonia. Larvae migration
in unclean persons, the larvae may penetrate the perianal skin
through pulmonary tissue may cause Loeffler syndrome, with
leading to external autoinfection. Both types of autoinfection
fever, cough, wheezing, dyspnea, and hemoptysis [34]. Ingestion of
enable persistent infection for several years without any extrin-
a high number of larvae causes Wakana syndrome, which is char-
sic exposure [48,54]. Meanwhile, under favorable conditions in
acterized by eosinophilia and symptoms such as pneumonitis [26].
soil, R-form passed in stool will continue the free living life cycle
Adult worms inhabit the small intestine, mainly the upper part forming both male and female adult worms. Female worms then
of the jejunum, biting the intestinal wall and sucking the mucosa lay eggs, which mature and give rise exclusively to female R-form,
with the cutting plates (N. americanus) or ventral teeth (A. duode­ then become infective F-form. These can infect humans both per-
nale). Symptoms are associated with continuous blood loss, intes- cutaneously (by penetration of the skin of the foot) and orally
tinal inflammation, and mucosa necrosis. The patient may suffer (by ingestion) [55,56], then enter the bloodstream and proceed to
from abdominal pain, diarrhea, fecal occult blood, and occasionally the heart and thereafter to the lung. The larvae migrate from the
melena. In continuous blood loss in heavy infected cases, the patient alveoli to the trachea, esophagus, stomach, then the mucosa of
suffers from severe iron deficiency, anemia with fatigue, short the small intestine, mainly in the duodenum, where they mature
breath, headache, koilonychia, and rarely allotriophagy [35–40]. to female adult worms.

3.4. Diagnosis 4.3.  Pathology and Clinical Aspects

Laboratory diagnosis during pulmonary infection depends on the Percutaneous invasion by F-form larvae may give rise to dermatitis
detection and identification of L3 filariform larvae in sputum or at the site of penetration. Like hookworm, itching and erythema are
bronchoalveolar lavage. Chest radiographs demonstrate transient noticed, but in some cases, larvae can move over intracutaneously
pulmonary infiltrates, bronchitis, and transient nonsegmental leading to “creeping eruption” [57–59].
consolidation [41].
Strongyloides stercoralis larvae gathering in the pulmonary
Diagnosis of intestinal infection relies mainly on the detection tissue can cause cough and appear in the sputum. In addition,
of eggs in stool using direct iodine and concentration techniques patients may present Loeffler syndrome with eosinophilia, hypo-
[42,43]. In addition, rhabditiform and, in rare cases, filariform albunemia, and elevated IgE. This can lead to dyspnea, broncho-
larvae can be observed in stool samples of constipation cases or pneumonia, and massive bleeding caused by alveolar hemorrhage
delayed samples. Specimens from duodenum using Entero-capsule [60]. Acute Respiratory Distress Syndrome (ARDS) and septi-
(duodenal string test) may detect the eggs and larvae [44]. cemia related to intestinal transmural migration of bacteria can
occur as a result of pulmonary hyperinfection or disseminated
strongyloidiasis [61–63]. In addition, acute anemia, acute renal
4.  STRONGYLOIDES STERCORALIS failure, and systemic inflammatory response syndrome are also
reported in hyperinfection [64–66].
4.1.  Introduction and Epidemiology
Symptoms of intestinal infection include diarrhea, abdominal
This “threadworm’” is the smallest intestinal nematode. S. ster­ discomfort, upper abdominal pain, and fever. In heavy chronic
coralis are classified under the Suborder Rhabditina and Family autoinfection cases, nausea, mucous with bloody stool, and
Strongyloididae. The female adult worms occur in two different anemia are seen. These symptoms are related to the destruction,
phases; the free living (1 mm × 65 µm) including the entire life damage, and mucosal inflammation caused by the adult and
cycle in the soil, and the parasitic (2 mm × 35 µm) generations larval stages of the parasite, particularly in the duodenum and
in man, whereas all male adults (0.7 mm × 40 µm) are free living jejunum, but may take place in the bile and pancreatic ducts. In
[45,46]. According to the WHO, strongyloidiasis affects up to 600 immunosuppressed patients, autoinfection progresses further to
million people globally, and the risk of infection is associated with hyperinfection (in the lung and intestine) and disseminates into
hygiene and walking barefoot, making children especially vulnera- multiple organs, mainly the liver, brain, heart, and urinary tract
ble to infection. Strongyloidiasis is among the most neglected trop- [67–71]. Hyperinfection can become severe and even fatal or
ical diseases, but was recently given more attention according to occur decades after the initial infection [72–75]. This is related
the WHO 2030 global target [1]. Infection with Strongyloides is not to a deficient T helper 2 (Th2) immune response, so it is dif-
restricted to tropical and subtropical countries; it also seems to be ficult to control the multiplication of huge number of larvae.
endemic in temperate regions [47]. The infection could be serious Additional ulcers/lesion caused by F-form larvae, with possible
in immunosuppression cases, certain malignancies, human T-cell destruction of muscular layers, which may lead to perforation,
lymphotropic virus type 1 infection, and alcoholism [48–53]. are also seen [76,77].
 M.H.M. Wakid / Dr. Sulaiman Al Habib Medical Journal 2(4) 144–150 147

4.4. Diagnosis smooth muscle cells, goblet cells, hypersecretion of mucus, and

enhance intestinal permeability to help expulsion of adult parasites
During pulmonary involvement, chest X-ray, and CT findings in the lumen. In addition, IL-4 and IL-13 activate the alternative
include patchy, migratory airspace consolidation, with areas of activated macrophages, which inactivate the production of Th1,
cavitation with irregular walls. A miliary pattern has also been Th2, and Th17. These cytokines also promote isotype class switch-
reported [78–81]. Sputum, bronchoalveolar lavage can be exam- ing in B cells to produce IgG.
ined microscopically for larvae detection [82–85].
Stool is the best sample for laboratory diagnosis of intestinal
6. CONTROL OF SOIL-TRANSMITTED
infection. The main applicable techniques for detection of R-form
larvae (the common diagnostic stage) are wet mount preparation HELMINTHS
and sedimentation techniques. Rarely, in certain cases, F-form
The main key in adapting control programs for any parasite is to
larvae, adult worms, and eggs can be detected in stool samples.
understand the life cycle and modes of infection. In simple terms,
Moreover, several fecal cultures are available, but infrequently
the goal of any control program is to cut or interrupt the life cycle
used. Duodenal specimens using Entero-Test are useful for detection
of the parasite.
of eggs, larvae, and/or parasitic female adult worms [44,86].
The first line of soil-transmitted helminthiasis control is treatment
Hyperinfection cases can be diagnosed by identifying female adult
of infected people. The WHO supports and recommends regular
worms, R-form larvae, F-form larvae, or eggs in biopsies from the
and mass treatment using drugs such as albendazole, mebendazole,
affected organs. Enzyme-linked immunosorbent assay and poly-
and ivermectin [1,6,92,93]. The WHO’s global target for morbidity
merase chain reaction of blood and cerebrospinal fluid have shown
control is to eliminate soil-transmitted helminths as a public health
reasonable results [87].
problem by the end of 2020 [94].
Second, use of educational materials to provide information about
5.  IMMUNE RESPONSE the modes of infections is very effective in reducing disease burden
and prevention of infection. Awareness about proper disposal of
Helminths antigens or helminth-derived Excretory/Secretory (ES) fecal matter/use of latrines/avoid soil contamination, use of foot-
activate dendritic cells, which act as antigen-presenting cells, pre- wear, washing hands, proper food preparation, consumption of
senting the antigen to T cells to commence an immune response washed food, and eliminating the use of untreated human feces
mediated by Th2 cells [88–91]. There are multiple mechanisms in as fertilizer, are examples related to these fecal-borne parasites
which helminths trigger a type 2 immune response through the [95,96]. Improvement in water, sanitation, and hygiene has import-
lymphatic/circulatory system. Prior to adult stages formation and ant short- and long-term impacts on infection rates. As these
establishment, the infective larvae invade the lungs or intestinal parasites can be transmitted to humans directly or indirectly, the
mucosa. This damage triggers tuft cells and other epithelial cells to community should therefore be supplied with information, partic-
secrete a group of alarmins, including thymic stromal lymphopoi- ularly on appropriate sanitation and hygiene standards and cleanli-
etin, Interleukin-33 (IL-33), and IL-25. These alarmins then pro- ness practices [95–97].
mote the activation and differentiation of type 2 innate lymphoid
cells and CD4 Th2 cells, leading to the release of many cytokines. In addition, we believe that the role of large-scale screening by
IL-5 promotes eosinophilia, and in integration with IL-4, IL-9, and accurate clinical/diagnostic techniques and involving well-trained
IL-13, in addition to IgE, which bind with high-affinity with Fc physicians/respiratory therapists/laboratory technologists have a
epsilon receptor, leading to activation of mast cells and basophils significant impact on the management and control programs.
and release of inflammatory mediators (e.g., histamine and heparin). Table 1 outlines the symptoms, signs, investigation, and treatment
Furthermore, IL-4 and IL-13 lead to an increased contractility of of human soil-transmitted helminths involved in lung diseases.

Table 1 | Overview of soil-transmitted helminths and human lung infections

Parasite Mode of infection Clinical presentation Radiological features Laboratory tests Treatment
Ascaris Ingestion of larvated Eosinophilic pneumonia, Transient nodular or diffuse Stool: adult worms Mebendazole
lumbricoides eggs in contami- cough, wheeze, dyspnea, pulmonary infiltrates, basal and eggs and
nated food or drink hemoptysis opacities, spontaneous Pulmonary: larvae albendazole
(fecal–oral) pneumothorax Blood: eosinophilia
Hookworm L3 larval skin Eosinophilic pneumonia, Bronchitis, bronchopneumonia, Stool: eggs and larvae Mebendazole
penetration (and cough, wheeze, dyspnea transient pulmonary infiltrates, Pulmonary: larvae and
oral route in case of transient nonsegmental areas Blood: eosinophilia albendazole
A. duodenale) of consolidation
Strongyloides L3 larval skin Eosinophilic pneumonia, chest Bronchopneumonia, pulmonary Stool or duodenal Ivermectin and
stercoralis penetration pain, fever, cough, wheeze, infiltrates, miliary nodules, specimens: larvae albendazole
dyspnea, hyperinfection airspace opacities ARDS in Pulmonary: larvae
syndrome, ARDS, intra- severe disease, rarely Blood: eosinophilia
alveolar hemorrhage granulomatous changes
148 M.H.M. Wakid / Dr. Sulaiman Al Habib Medical Journal 2(4) 144–150

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