The Potential Cause of Allergy for Children: Soil Contamination with Mites, Bugs, and Geohelminths

AUTHORS

Mohammad Ali Mohaghegh 1 , 2 , Mojtaba Azimi Resketi 3 , Mehdi Azami 4 , Seyed Hossein Hejazi 3 , 4 , Hamed Kalani 3 , Mohsen Ghomashlooyan 3 , *

1 Department of Laboratory Sciences, Torbat Heydariyeh University of Medical Sciences, Torbat Heydariyeh, IR Iran

2 Health Sciences Research Center, Torbat Heydariyeh University of Medical Sciences, Torbat Heydariyeh, IR Iran

3 Department of Parasitology and Mycology, School of Medicine, Isfahan University of Medical Science, Isfahan, IR Iran

4 Skin Diseases and Leishmaniasis Research Center, Isfahan University of Medical Sciences, Isfahan, IR Iran

How to Cite: Mohaghegh M A, Azimi Resketi M, Azami M, Hejazi S H, Kalani H, et al. The Potential Cause of Allergy for Children: Soil Contamination with Mites, Bugs, and Geohelminths, Arch Pediatr Infect Dis. 2018 ; 6(1):e12604. doi: 10.5812/pedinfect.12604.

ARTICLE INFORMATION

Archives of Pediatric Infectious Diseases: 6 (1); e12604
Published Online: January 10, 2018
Article Type: Research Article
Received: March 16, 2016
Revised: September 29, 2017
Accepted: December 25, 2017
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Abstract

Background: Ectoparasitic infections are very important in poor countries. On the other hand, comprehensive information on the epidemiology of these parasites, especially in the North of Iran, remains scarce.

Objectives: The aim of this study was to assess soil contamination with mites, geohelminths, and bugs in residential areas of Sari city, north of Iran.

Methods: A total of 90 soil samples from 3 areas were collected via multistage, cluster, and random sampling in order to examine their contamination with mites, geohelminths, and bugs during summer, 2014. The results were analyzed using the SPSS 16 software.

Results: Of the 90 soil samples that were studied in different environmental areas of Sari, 30 (33.3%) were observed to be contaminated with mites, 10 (11.1%) had bugs, and 21 (23.3%) contained geohelminths. Mites were the most commonly seen parasite among the 3 studied region.

Conclusions: Based on the literature, North of Iran accounts for a high rate of allergic disorders. The current results showed high contamination rate of soil with ectoparasites in Sari. Thus, these organisms could be potential causes of allergic disorders and further studies on the subject is needed.

Keywords

Soil Contamination Mites Bugs Geohelminth Iran Allergic Disorders

Copyright © 2018, Archives of Pediatric Infectious Diseases. This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 International License (http://creativecommons.org/licenses/by-nc/4.0/) which permits copy and redistribute the material just in noncommercial usages, provided the original work is properly cited.

1. Background

Scabies, pediculosis, cutaneous larva migrans, myiasis, ticks, and fleas are common and prevalent ectoparasitic infestations, yet are rather neglected. They are a serious threat for poor communities, especially in developing countries, with significant effects, such as morbidity. Also, there is no adequate authentic information on the epidemiology of the infestation with these parasites. Control of skin complications of infestation with these parasites in endemic areas is still a challenge (1).

Scabies or mange is one of the most common skin diseases around the world, and more than 300,000,000 people from all social classes are infested each year. The disease is common worldwide in tropical and humid regions and lack of personal hygiene, poor economy, and living in densely populated areas plays an important role in the spreading of the disease (2-4). Scabies and pyoderma are 2 risk factors for renal failure and other chronic morbidities (5). It is believed that these mites could cause asthma or exacerbate complications when inhaled. In general, both body parts and proteins in the feces of mites could cause allergies (6). Mite’s reproduction is very rapid, about 3 weeks for each generation, and this explains why house dust mite could cause significant problems for allergic people.

Geohelminths infections are one of the most important diseases in communities that have no access to safe water. Soil transmitted helminth (STH) are among the most important geohelminth, which infect approximately two billion humans all over the world (7). Infection with geohelminths effects feeding, growth and fitness, and also causes chronic infections in the population of endemic areas (7, 8). Soil provides the appropriate conditions for conversion of eggs to the infective stage. Also, presence of eggs in the superficial layers of soil could be considered as a factor affecting their transition to humans in each region (9). It seems that soil is the main source for human infection (8, 10). Evidence indicates that STH infections effect children in developing and developed countries and is directly associated with growth retardation, physical activity reduction, and disorders in learning abilities (9, 11-13). Soil Transmitted Helminth infections are considered as neglected diseases, which in case of suitable conditions can cause serious problems (10, 14).

Bedbug infection is seen in crowded areas and communities that do not adhere to hygienic precautions. In the past few years, bedbug infection has been reported in travelers (15). Nowadays, a large number of infections are reported in the medical literature in different areas of the world (16). International journey, emigration, changes made in the pest control method, and resistance to insecticides may contribute to the development of this blood-sucking insect in developed countries (16-18). The prevalence of bedbugs is not known in Iran. It is not well known whether bedbug’s bites lead to severe allergic reactions (19).

2. Objectives

Sari is subjected to a high prevalence of asthma, yet its exact cause is not completely clear (20). This research hypothesized that ectoparasites may be the cause and this study aimed at determining soil contamination with mites, geohelminths, and bugs as potential causes of allergic disorders in residential areas of Sari city, North of Iran.

3. Methods

3.1. Study Area

Sari is the provincial capital of Mazandaran, which is located in the north of the Caspian Sea, south of Alborz Mountains, east of Neka and Behshahr cities, and west of Qaemshahr city. Sari is the largest and most densely populated city of the Mazandaran province. The human population of Sari is around 500,000. The city is located between the 53° 5 of the northern latitude and between 36° 4 of the eastern longitude. Sari has a Mediterranean climate with cold and rainy winters and humid and hot summers (21).

2.2. Sampling/Parasitological Procedure

A total of 90 soil samples were collected via multistage, cluster, random sampling method from 3 areas of the city from backyards during September to December, 2014 (30 samples per area). Each sample was about 200 grams of soil from a depth of 2 to 5 cm of the ground, in an area that was not exposed to direct sunlight. The soil samples were dried overnight at room temperature, and then screened through 150 μm sieves, and finally about 2 g of soil was obtained. The sieved samples were transferred to a 10-mL test tube, suspended in approximately 10 mL of Tween-80 (0.05%), and centrifuged at 1500 rpm for 5 minutes. After discarding the supernatant, the test tube containing the sediments was filled to approximately 1 cm from the top with sucrose solution (1.2 g/cm3) and the sediment was suspended, vortexed, and then centrifuged for 15 minutes at 1500 rpm. Finally, up to the upper edge of the tube was filled with sucrose solution and a cover slip was placed on the surface of the tube in contact with the sucrose solution for 30 minutes and then observed under a microscope using 10X and 40X objective.

4. Results

A total of 90 soil samples were examined, and mites (33.3%), geohelminths (23.3%) and bugs (11.1%) were observed in the studied samples (Table 1). In region 2, contamination rate with mites, bugs, and geohelminths was higher than that of region 1 and 3. Mites were the most commonly seen parasite among the 3 studied regions (Table 1).

Table 1. The Frequency of Mites, Bugs and Geohelminthes Among Different Regions of Saria
RegionsSamplesMitesBugsGeohelminthes
Region1308 (26.7)2 (6.7)5 (16.7)
Region23012 (40)4 (13.3)10 (33.3)
Region33010 (33.3)4 (13.3)6 (20)
Total9030 (33.3)10 (11.1)21 (23.3)

aValues are expressed as No. (%).

5. Discussion

There are several reports on the prevalence of allergic diseases in different countries, and environmental factors, such as soil, also play an important role in the development of clinical inflammation (22, 23).

The role of mites as an important source of house dust allergen was introduced many years ago (24-27). So far, there is no evidence for the role of mite eggs in house dust mite allergies, yet Der p I, a protease, is one of the major known allergens in mites (28-30). It seems that mites could affect the host inflammatory processes and immune responses and lead to delay (31, 32). Mites are able to produce components, which can modulate their host's immune response (33-35). The arthropods are genetically endowed with immunological substances that neutralize the host immune response during their presence on the skin. Therefore, soil could be considered as a potential source for distribution of these allergens (36-39).

Living in places contaminated with dust mite particles and allergen agents causes asthma in children (40). The analysis of ecological and epidemiological studies has not been able to support the etiologic relationship of the disease.

The results of a recent survey form 16 countries that studied the relationship between allergy, asthma, and sensitization showed a high overall prevalence for asthma with house dust mite and sensitization. The ratio of asthma to each allergen is wide (4% to 61%) and heavily dependent on the diagnostic technique (41). This indicates that the discrepancy in the use of diagnostic tools could lead to disruption of epidemiological studies (42).

In a case–control study carried out to determine the prevalence of allergic disorders, such as asthma, allergic rhinitis, and eczema in primary schools of Sari, out of the 1,818 studied cases, 35% had allergic disorder; 12% had asthma, 17% allergic rhinitis, and 6% had eczema. Also, allergic disorders were more frequently observed to occur among males (65%) than females (40%) (20).

As mentioned previously, mites and dust are factors responsible for allergy and asthma (43). Based on a meta-analysis study that was conducted in Iran, the prevalence of asthma in primary schools was 3.9% (44).

Soil transmitted helminthes are the most prevalent geohelminth infections. Also, there are several reports on the relationship between geohelminth infections and atopy and wheeze symptoms (45). These soil transmitted helminthes are among major causes of physical and mental retardation around the world. However, despite the economic, educational, and health importance of these parasites, they have been largely forgotten (10).

Evidence from epidemiological studies suggests that aeroallergens are environmental risk factors in relation to allergic disorders in industrialized countries (46). Contamination with geohelminths, infection with the pulmonary form of visceral migratory larvae, leads to anti-inflammatory responses and prevents inflammatory responses to airways. In a study in a rural area of Ecuador, results indicated an intense protective effect against atopy with higher parasite burden of ascariasis and trichuriasis (47). It seems that infection with geohelminths is associated with a lower prevalence of symptoms of allergy. In general, there is no evidence of any difference between these parasites in the effectiveness of allergen skin test reactivity (48).

Insect bites and stings are very common and could cause a variety of skin reactions. These reactions are often local, and their evolution depends on the host immune response (49).

In a study of dust particles at home involving babies aged 12 to 18 months old, the effect of mite allergen (Der p1) in dust was evaluated. At the age of 18 to 36 months, stool specimens were collected for examination of geohelminths and study of the relationship with allergy. Exposure to more 10 µg/g of dust allergen (Der p1) was 31.8%. Geohelminths were reported in 25% of children and was most related to Ascaris lumbricoides. In one case, a hookworm infection was reported due to wheezing and medical diagnosis at the hospital. Hospitalization due to wheezing was significantly observed in children in contact with 2 to 10 µg/g of dust. Helminthic infections were not associated with mite allergy as a risk factor for wheezing.

This study suggested that hookworm infection and mite allergen was an independent risk factor for wheezing, and there was no evidence of significant interaction between them (50).

Bite of bed bugs cause very itchy local reactions after repeated exposure with hemorrhagic or bullous bites, but systemic allergic reactions are rare (15). Kissing Bugs are known as a vector of Chagas’ disease. Anaphylaxis caused by this insect’s sting has been proven for more than 100 years (19). Unfortunately, there is no exact information available about the prevalence of anaphylaxis caused by kissing bug bites.

In most northern areas of Iran, because of the climate and geographical location and exposure to the edges of forests, buildings are mostly made by wood. Rainy season, wooden buildings and temperature are positively associated with populations of bugs, especially head bugs. Thus, according to the suitable ecology of this area for reproduction of these ectoparasites, their relatively high prevalence in soil, and high prevalence of allergic diseases in the North of Iran with unknown etiology, further studies on the association between allergic disorders in people with these ectoparasites seems necessary. While these outcomes indicate that the residents in this region were at high risk for allergic disorders, health education is essential for disease prevention.

Footnotes

References

  • 1.

    Heukelbach J, Walton SF, Feldmeier H. Ectoparasitic infestations. Curr Infect Dis Rep. 2005;7(5):373-80. [PubMed: 16107235].

  • 2.

    Hengge UR, Currie BJ, Jager G, Lupi O, Schwartz RA. Scabies, a ubiquitous neglected skin disease. Lancet Infect Dis. 2006;6(12):769-79. doi: 10.1016/s1473-3099(06)70654-5.

  • 3.

    Fakoorziba MR, Amin M, Moemenbellah Fard M, Najafi ME. The frequency rate of scabies and its associated demographic factors in Kazerun, Fars province, Iran. Zahedan J Res Med Sci. 2012;14(8):90-1.

  • 4.

    Shamsaddini S, Nasiri Kashani M, Sharifi I, Khajeh Karimoddini M, Pourlashkari M. Prevalence of infectious skin diseases in the central prison of Kerman. Iran J Dermatol. 2000;4(13):19-25.

  • 5.

    Hoy W, McDonald SP. Albuminuria: marker or target in indigenous populations. Kidney Int Suppl. 2004;(92):25-31. doi: 10.1111/j.1523-1755.2004.09207.x. [PubMed: 15485412].

  • 6.

    Gruchalla RS, Pongracic J, Plaut M, Evans R3, Visness CM, Walter M, et al. Inner City Asthma Study: relationships among sensitivity, allergen exposure, and asthma morbidity. J Allergy Clin Immunol. 2005;115(3):478-85. doi: 10.1016/j.jaci.2004.12.006. [PubMed: 15753892].

  • 7.

    Mohaghegh MA, Vafaei MR, Azami M, Hashemi N, Hejazi SH, Mirzaei F, et al. Soil contamination with soil transmitted helminthes in schools and play areas of Kermanshah city, west of Iran. Int J Infect. 2016;4(1):38311. doi: 10.17795/iji-38311.

  • 8.

    Savioli L, Albonico M. Soil-transmitted helminthiasis. Nat Rev Microbiol. 2004;2(8):618-9. doi: 10.1038/nrmicro962. [PubMed: 15303271].

  • 9.

    Mizgajska H. The distribution and survival eggs of Ascaris suum in six different natural soil profiles. Acta parasitologica. 1993;38(4):170-4.

  • 10.

    Bethony J, Brooker S, Albonico M, Geiger SM, Loukas A, Diemert D, et al. Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet. 2006;367(9521):1521-32. doi: 10.1016/S0140-6736(06)68653-4. [PubMed: 16679166].

  • 11.

    Brooker S, Peshu N, Warn PA, Mosobo M, Guyatt HL, Marsh K, et al. The epidemiology of hookworm infection and its contribution to anaemia among pre school children on the Kenyan coast. Trans R Soc Trop Med Hyg. 1999;93(3):240-6. doi: 10.1016/s0035-9203(99)90007-x.

  • 12.

    Hotez PJ, Brindley PJ, Bethony JM, King CH, Pearce EJ, Jacobson J. Helminth infections: the great neglected tropical diseases. J Clin Invest. 2008;118(4):1311-21. doi: 10.1172/JCI34261. [PubMed: 18382743].

  • 13.

    Petney TN. Environmental, cultural and social changes and their influence on parasite infections. Int J Parasitol. 2001;31(9):919-32. [PubMed: 11406141].

  • 14.

    Umar AA, Bassey SE. Incidence of strongyloides stercoralis infection in ungogo, nassarawa, dala and fagge local government areas of Kano state, Nigeria. Bayero J Pure Appl Sci. 2010;3(2):76-80. doi: 10.4314/bajopas.v3i2.63224.

  • 15.

    Scarupa MD, Economides A. Bedbug bites masquerading as urticaria. J Allergy Clin Immunol. 2006;117(6):1508-9. doi: 10.1016/j.jaci.2006.03.034. [PubMed: 16751024].

  • 16.

    Criado PR, Belda Junior W, Criado RF, Vasconcelos e Silva R, Vasconcellos C. Bedbugs (Cimicidae infestation): the worldwide renaissance of an old partner of human kind. Braz J Infect Dis. 2011;15(1):74-80. [PubMed: 21412594].

  • 17.

    Mumcuoglu KY. A case of imported bedbug (Cimex lectularius) infestation in Israel. Isr Med Assoc J. 2008;10(5):388-9. [PubMed: 18605368].

  • 18.

    Pritchard MJ, Hwang SW. Cases: Severe anemia from bedbugs. CMAJ. 2009;181(5):287-8. doi: 10.1503/cmaj.090482. [PubMed: 19720710].

  • 19.

    Klotz JH, Dorn PL, Logan JL, Stevens L, Pinnas JL, Schmidt JO, et al. "Kissing bugs": potential disease vectors and cause of anaphylaxis. Clin Infect Dis. 2010;50(12):1629-34. doi: 10.1086/652769. [PubMed: 20462351].

  • 20.

    Ghaffari J, Mohammadzadeh I, Khalilian A, Rafatpanah H, Mohammadjafari H, Davoudi A. Prevalence of asthma, allergic rhinitis and eczema in elementary schools in Sari (Iran). Caspian J Intern Med. 2012;3(1):372-6. [PubMed: 26557289].

  • 21.

    Sharif M, Daryani A, Nasrolahei M, Ziapour SP. Prevalence of Toxoplasma gondii antibodies in stray cats in Sari, northern Iran. Trop Anim Health Prod. 2009;41(2):183-7. doi: 10.1007/s11250-008-9173-y. [PubMed: 18473184].

  • 22.

    Ellwood P, Asher MI, Beasley R, Clayton TO, Stewart AW, Isaac Steering Committee . The international study of asthma and allergies in childhood (ISAAC): phase three rationale and methods. Int J Tuberc Lung Dis. 2005;9(1):10-6. [PubMed: 15675544].

  • 23.

    Von Mutius E. Environmental factors influencing the development and progression of pediatric asthma. J Allergy Clin Immunol. 2002;109(6 Suppl):525-32. [PubMed: 12063508].

  • 24.

    Arlian LG, Bernstein D, Bernstein IL, Friedman S, Grant A, Lieberman P, et al. Prevalence of dust mites in the homes of people with asthma living in eight different geographic areas of the United States. J Allergy Clin Immunol. 1992;90(3 Pt 1):292-300. [PubMed: 1527314].

  • 25.

    Vanbronswijk J, Drs B, Sinha R. Pyroglyphid mites (Acari) and house dust allergy, a review. J Allergy Clin Immunol. 1971;47(1):31-52. doi: 10.1016/s0091-6749(71)80315-9.

  • 26.

    Bernstein JA. Allergic and mixed rhinitis: Epidemiology and natural history. Allergy Asthma Proc. 2010;31(5):365-9. doi: 10.2500/aap.2010.31.3380. [PubMed: 20929601].

  • 27.

    Katelaris CH, Lee BW, Potter PC, Maspero JF, Cingi C, Lopatin A, et al. Prevalence and diversity of allergic rhinitis in regions of the world beyond Europe and North America. Clin Exp Allergy. 2012;42(2):186-207. doi: 10.1111/j.1365-2222.2011.03891.x. [PubMed: 22092947].

  • 28.

    Tovey ER, Chapman MD, Platts-Mills TA. Mite faeces are a major source of house dust allergens. Nature. 1981;289(5798):592-3. [PubMed: 7464922].

  • 29.

    Thomas WR, Hales BJ, Smith WA. House dust mite allergens in asthma and allergy. Trends Mol Med. 2010;16(7):321-8. doi: 10.1016/j.molmed.2010.04.008. [PubMed: 20605742].

  • 30.

    Weghofer M, Dall'Antonia Y, Grote M, Stocklinger A, Kneidinger M, Balic N, et al. Characterization of Der p 21, a new important allergen derived from the gut of house dust mites. Allergy. 2008;63(6):758-67. doi: 10.1111/j.1398-9995.2008.01647.x. [PubMed: 18445190].

  • 31.

    Elder BL, Arlian LG, Morgan MS. Sarcoptes scabiei (Acari: Sarcoptidae) mite extract modulates expression of cytokines and adhesion molecules by human dermal microvascular endothelial cells. J Med Entomol. 2006;43(5):910-5. [PubMed: 17017228].

  • 32.

    Rapp CM, Morgan MS, Arlian LG. Presence of host immunoglobulin in the gut of Sarcoptes scabiei (Acari: Sarcoptidae). J Med Entomol. 2006;43(3):539-42. [PubMed: 16739413].

  • 33.

    Arlian LG, Morgan MS, Paul CC. Evidence that scabies mites (Acari: Sarcoptidae) influence production of interleukin-10 and the function of T-regulatory cells (Tr1) in humans. J Med Entomol. 2006;43(2):283-7. [PubMed: 16619612].

  • 34.

    Elder BL, Arlian LG, Morgan MS. Modulation of human dermal microvascular endothelial cells by Sarcoptes scabiei in combination with proinflammatory cytokines, histamine, and lipid-derived biologic mediators. Cytokine. 2009;47(2):103-11. doi: 10.1016/j.cyto.2009.05.008. [PubMed: 19523846].

  • 35.

    Morgan MS, Arlian LG. Response of human skin equivalents to Sarcoptes scabiei. J Med Entomol. 2010;47(5):877-83. [PubMed: 20939384].

  • 36.

    Sato Y, Alba JM, Sabelis MW. Testing for reproductive interference in the population dynamics of two congeneric species of herbivorous mites. Heredity (Edinb). 2014;113(6):495-502. doi: 10.1038/hdy.2014.53. [PubMed: 24865602].

  • 37.

    Aydogan M, Eifan AO, Keles S, Akkoc T, Nursoy MA, Bahceciler NN, et al. Sublingual immunotherapy in children with allergic rhinoconjunctivitis mono-sensitized to house-dust-mites: a double-blind-placebo-controlled randomised trial. Respir Med. 2013;107(9):1322-9. doi: 10.1016/j.rmed.2013.06.021. [PubMed: 23886432].

  • 38.

    Zinkeviciene A, Girkontaite I, Citavicius D. Specific immunoglobulin E antibodies to saprophytic yeasts in sera of atopic patients allergic to house dust mites. J Investig Allergol Clin Immunol. 2012;22(6):412-8. [PubMed: 23101185].

  • 39.

    Jeong KY, Park JW, Hong CS. House dust mite allergy in Korea: the most important inhalant allergen in current and future. Allergy Asthma Immunol Res. 2012;4(6):313-25. doi: 10.4168/aair.2012.4.6.313. [PubMed: 23115727].

  • 40.

    Pearce N, Douwes J, Beasley R. Is allergen exposure the major primary cause of asthma?. Thorax. 2000;55(5):424-31. [PubMed: 10770825].

  • 41.

    Sunyer J, Jarvis D, Pekkanen J, Chinn S, Janson C, Leynaert B, et al. Geographic variations in the effect of atopy on asthma in the European Community Respiratory Health Study. J Allergy Clin Immunol. 2004;114(5):1033-9. doi: 10.1016/j.jaci.2004.05.072. [PubMed: 15536406].

  • 42.

    Bousquet PJ, Chinn S, Janson C, Kogevinas M, Burney P, Jarvis D, et al. Geographical variation in the prevalence of positive skin tests to environmental aeroallergens in the European Community Respiratory Health Survey I. Allergy. 2007;62(3):301-9. doi: 10.1111/j.1398-9995.2006.01293.x. [PubMed: 17298348].

  • 43.

    Habbick BF, Pizzichini MM, Taylor B, Rennie D, Senthilselvan A, Sears MR. Prevalence of asthma, rhinitis and eczema among children in 2 Canadian cities: the International Study of Asthma and Allergies in Childhood. CMAJ. 1999;160(13):1824-8. [PubMed: 10405666].

  • 44.

    Mohammadbeigi A, Hassanzadeh J, Mousavizadeh A. Prevalence of asthma in elementary school age children in Iran--a systematic review and meta analysis study. Pak J Biol Sci. 2011;14(19):887-93. [PubMed: 22518932].

  • 45.

    Hagel I, Lynch NR, Perez M, Di Prisco MC, Lopez R, Rojas E. Modulation of the allergic reactivity of slum children by helminthic infection. Parasite Immunol. 1993;15(6):311-5. [PubMed: 8361773].

  • 46.

    Burrows B, Martinez FD, Halonen M, Barbee RA, Cline MG. Association of asthma with serum IgE levels and skin-test reactivity to allergens. N Engl J Med. 1989;320(5):271-7. doi: 10.1056/NEJM198902023200502. [PubMed: 2911321].

  • 47.

    Cooper PJ, Chico ME, Rodrigues LC, Ordonez M, Strachan D, Griffin GE, et al. Reduced risk of atopy among school-age children infected with geohelminth parasites in a rural area of the tropics. J Allergy Clin Immunol. 2003;111(5):995-1000. [PubMed: 12743563].

  • 48.

    Ghadirian E, Sanati A. Preliminary studies on the treatment of hookworm with pyrantel pamoate in Iran. J Trop Med Hyg. 1972;75(10):199-201. [PubMed: 4564699].

  • 49.

    Goddard J, deShazo R. Bed bugs (Cimex lectularius) and clinical consequences of their bites. JAMA. 2009;301(13):1358-66. doi: 10.1001/jama.2009.405. [PubMed: 19336711].

  • 50.

    Sangsupawanich P, Mahakittikun V, Chongsuvivatwong V, Mo-suwan L, Choprapawon C. Effect of helminthic infections together with mite allergen exposure on the risk of wheeze in preschool children. Asian Pac J Allergy Immunol. 2010;28(1):29-34. [PubMed: 20527513].

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