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Journal of Parasitic Diseases: Official Organ of the Indian Society for Parasitology logoLink to Journal of Parasitic Diseases: Official Organ of the Indian Society for Parasitology
. 2024 Jan 25;48(1):67–73. doi: 10.1007/s12639-024-01645-7

Intestinal Parasites Associated with American Cockroach (Periplaneta americana) in Akure, Ondo State, Nigeria

Adebayo Victor Akeju 1,, Titus Adeniyi Olusi 1, Regina-Tyra Ekwi Obi 1
PMCID: PMC10908730  PMID: 38440767

Abstract

American cockroach (Periplaneta americana) has been implicated as mechanical vector of parasites of humans and animals. Therefore, this study aimed to identify and determine the prevalence of human intestinal parasites associated with the body surface and gut of P. americana. A total of 221 cockroaches which include 104 males and 117 females were collected from household kitchen, toilet area and canteen after which they were brought to laboratory for study. The body surface of the cockroach was washed with 5 ml normal saline solution to remove external parasites on the body surface for examination and later rinsed with 70% alcohol and dried before dissecting. The cockroach was dissected to examine internal parasites. Eleven parasites were recovered and identified, these include Ascaris lumbricoides (51.58%), Strongyloides stercoralis (48.42%) Trichuris trichiura (52.49%), Enterobius vermicularis (37.10%), Taenia spp (14.93%), Toxocara (31.67%), Ancylostoma spp (34.84%), Necator americanus (53.39%), and Diphylidium spp (66.23%) Balantidium coli (66.52%). The parasites were recorded both on the body surface and gut of the cockroach. There is no significant difference (p > 0.05) between parasites infection rate comparing both sexes; though, female cockroach having a higher infection rate (91.45%) than male (81.5%). Cockroach collected from toilets carried more parasites (96.34%) as compared to those from restaurants/canteen (89.71%) and household kitchens (81.69%). All parasites encountered were pathogenic to human and animals. This study has revealed that P. americana can act as mechanical vector by transporting and transmitting these parasites easily to man and animal. Good sanitary practices, reinforcement of worms' eradication programs, and the fight against these insects remain a necessity to contain the menace of parasites burden and cockroach control.

Keywords: Periplaneta americana, American cockroach, Mechanical vector, Parasites, Pathogenic

Introduction

Since ancient times, cockroaches (Insecta: Blattaria) have thrived in a wide variety of settings consumed almost any organic material, including fresh and processed human foods, stored goods, and waste (Cochran 1999; Kramer et al. 2009). A lot of factors contributed to higher population of cockroaches, this includes poor sanitation and pest control practices, old and unmaintained building conditions, poorly managed food, socioeconomic status, food handler behaviour, and other environmental condition such as temperature, humidity and lighting (Abudin et al. 2023). The two most prevalent and well-known cockroach species in Nigeria and globally are the P. americana and Blattella germanica (Anikwe et al. 2014; Hamu et al. 2014). Aside the potential psychological stress that their sight and presence can cause, cockroaches are an important insect of public health concern (Adenusi et al. 2018). The amount of stress they cause is typically inversely correlated with cockroach size and population (Kramer et al. 2009). They are a significant source of strong environmental allergens that, especially in those who are susceptible to atopic dermatitis, cause allergic reactions and aggravate acute asthma (Jeong et al. 2015).

According to Kramer et al. (2009) and Donkor (2020), cockroaches contaminate foods with their faeces and foul-smelling secretions, rendering them disagreeable and unfit for human consumption. Despite the fact that cockroaches have not yet been identified as a biological vector for human pathogen, they mechanically act as intermediate hosts for a variety of helminth parasites, some of which are known to cause life-threatening illnesses in both humans and domestic animals (Kramer et al. 2009; Galęcki and Sokol 2019). They are susceptible to acquiring diseases pathogens and mechanically depositing disease-causing organisms due to their unclean habits, indiscriminate diet and feeding processes.

Cockroaches have been found to have a range of pathogenic and potentially harmful bacteria, fungus, and parasites in their guts and on their body surfaces (Salehzadeh et al. 2007; Adenusi et al. 2018). Through physical dislodgment, regurgitation, or faecal pellet deposition onto or into exposed human food, which may be ready to eat, cockroaches have the ability to mechanically spread pathogens. Majority of these infections are intestinal parasites, which are among the prevalent and widespread disease that affect people worldwide and are particularly dangerous for young children, the most vulnerable group of people (Yones et al. 2015). Thus, there is need to constantly check the vectorial capacity of cockroach in order to ascertain the disease pathogen associated with this mechanical vector. The aim of this study is to identify different human intestinal parasites associated with P. americana in household kitchen, toilet area, and canteen the study area.

Materials and methods

Source of cockroach and collection

Cockroaches were randomly collected from different locations in Akure, Nigeria. A total number of 221 specimens (147 adult and 74 nymph cockroaches) were individually collected alive into different sample bottles and well labelled with date and site of collection (Household kitchen, Toilet area and Canteen) The specimens were subsequently transported to the Department of Biology undergraduate research laboratory, Federal University of Technology Akure (FUTA) for identification and further studies.

Identification of American cockroach

All cockroaches used for this study was identified to be American cockroach (P. americana) using the morphological keys described by Brenner and Gefeller (1997). The morphological features of P. americana is characterised with reddish-brown and a yellowish pattern on the back of their heads, with brown-band pronounced across the wings. The sex was separated using the present of styli (singular stylus) between the cerci which arises from the sternum of the ninth abdominal segment.

Identification of parasites from the body surface and gut of American cockroach

Each cockroach was wash individually with 5 ml of 0.85% Normal saline to remove the parasites on the external body of the insect. The wash off from the individual body of the cockroach was centrifuge for 5 min at 2500 revolutions per minute (rpm), the precipitate was place on glass slide and stained with 1% Lugol’s iodine and examined under light microscope (10 × and 40x) for the presence of parasites. After the washing of individual specimen in physiological saline. The specimen (Cockroach) was fixing in 70% alcohol and subsequent air-drying, each cockroach sample was placed in a sterile Petri dish and dissected under a dissecting microscope using sterile entomological needles. Whole gut was removed and homogenized in 5 ml physiological saline, before centrifuged for 5 min at 2500 rpm as described by Dokmaikaw and Suntaravitun (2020) with slight modification. The sediment was place on slide, stained with 1% Lugol’s iodine and examined under microscope (10x and 40x) for the presence of parasite cyst and ova.

Identification of parasites

Cysts, oocysts, eggs and/or larvae of intestinal parasites were identified microscopically using bench aids of World Health Organization (WHO 1994) and with the aid of Georgis’ parasitology for veterinarians (Bowman 2009). A cockroach was considered a carrier if any parasite stage is detected from body surface or gut contents.

Data analysis

Data was analysed using Statistical Package for the Social Sciences (SPSS) version 26. Chi-square analysis was used to compare the prevalence of the parasites within the selected locations, stage of development and between the sex of P. americana (American cockroach).

Results

Prevalence of infected P. americana in the collection sites

The prevalence of infected American Cockroach P. americana in different locations was presented in Table 1. A total number of 221 P americana was collected from different location; this includes the household kitchen (71), toilet areas (82) and canteen (68). The highest prevalence infected P. americana (American Cockroach) were recorded from toilets with 96.34% infection prevalence, followed by the restaurant area (89.71%), then the household kitchen with 81.69%. From this result, it was discovered that 89.59% of the total collected cockroaches examined have the ability to act as mechanical vector of human and animal parasitic diseases. Chi-square analysis shows that there was significant difference (p < 0.05) in infection prevalence when comparing the collection sites (X2 = 8.76, df = 2, p = 0.013).

Table 1.

Prevalence of intestinal parasite based on site of collection on P. Americana

Collection site Total number of cockroaches examined Number infected with parasites Prevalence (%)
Household kitchen 71 58 81.69
Toilet area 82 79 96.34
Restaurant/Canteen 68 61 89.71
Total 221 198 89.59

Chi-square (χ2) = 8.76, degree of freedom (df) = 2; p value = 0.013. p < 0.05 indicates a significant difference)

The Fig. 1 shows the parasites that are associated with P. americana (American Cockroach) in relation to the areas where cockroaches were collected. The prevalence of Ascaris (76.83%), Dipylidium (76.82%), Balantidium (85.37%), and Entamoeba (86.59%) were very high in P. americana collected from toilet area. Entamoeba (83.82%) and Dipylidium (82.35%) prevalence was recorded from P. americana collected from restaurant/canteen. Taenia was not recovered from P. americana collected from household kitchen, but 28.05% and 14.71% prevalence of Taenia was recorded from P. americana collected from toilet area and restaurant/canteen respectively.

Fig. 1.

Fig. 1

Prevalence of Parasites Recovered from P. americana (American cockroach) in Relation to Collection sites

Frequency of infected P. americana in the collection sites in relation to the sex

Table 2 shows the prevalence of parasites recovered from P. americana in respect to the gender (female and male). With a total number of 221 P. americana collected from different locations, the males P. americana were 104 and female were 117. The number infected in male was 91; this represents 87.50% infection prevalence. The total number infected female was 107, this represents 91.45% infection prevalence. The infection prevalence was not significantly different (p > 0.05) when both were compared (X2 = 0.923, df = 1, p = 0.337).

Table 2.

Prevalence of intestinal parasite based on Cockroach sex

Sex No examined No infected Prevalence (%)
Male 104 91 87.50
Female 117 107 91.45
Total 221 198 89.59

Chi-square (χ2) = 0.923, degree of freedom (df) = 1, p value = 0.337. p > 0.05 indicates non-significant difference

Prevalence of infected P. americana in relation to the developmental stages

The prevalence of infected P. americana in the study areas in relation to the developmental stages was represented in Table 3. Out of 221 P. americana collected, 147 were adult while 74 were nymph. The number infected adults were 131, this represents 89.11% infection prevalence in adult P. americana, while the total number of nymph infected were 67 this represents with 90.54% infection prevalence. There was no significant difference (p > 0.05) in infection rate when both developmental stages were compared with chi-square analysis (X2 = 0.107, df = 1, p = 0.743).

Table 3.

Prevalence of intestinal parasite based on developmental stages of P. americana

Stage No examined No infected Prevalence (%)
Adult 147 131 89.11
Nymph 74 67 90.54
Total 221 198 89.59

Chi-square(χ2) = 0.107, degree of freedom (df) = 1, p value = 0.743. p > 0.05 indicates non-significant difference

Prevalence infected P. americana in relation to the internal and external parts

Table 4 gives the breakdown of infection rate in relation to the internal and external parts of P. americana (American cockroach). The external (body surface) and internal parts (guts) of P. americana harbour pathogens, with the internal parts harbouring more of the pathogens than the external parts. High prevalence of Ascaris (79.82%), Strongyloides (91.58%), Trichuris (87.93%), Diphylidium (87.76%), Balantidium (75.82%), and Enterobius (92.68%) were associated with the internal (gut) part of P. americana compared to the external (body surface) part.

Table 4.

Prevalence of parasite recovered in respect to the internal and external part of the Cockroach (P. americana)

Parasite recovered Total number examined Number infected Prevalence (%) Internal part (Gut) External part (Body surface)
Number infected Prevalence (%) Number infected Prevalence (%)
A. lumbricoides 221 114 51.58 91 79.82 23 20.18
S. stercoralis 221 107 48.42 98 91.58 9 8.41
T. trichiura 221 116 52.49 102 87.93 14 12.07
E. vermicularis 221 82 37.10 76 92.68 6 7.32
N. americanus 221 118 53.39 81 68.64 37 31.36
Taenia spp 221 33 14.93 7 21.21 26 78.78
Diphylidium spp 221 147 66.52 129 87.76 18 12.25
Balantidium coli 221 153 69.23 116 75.82 37 24.18
E. histolytica 221 173 78.28 79 45.66 94 54.33
Ancylostoma spp 221 77 34.84 60 77.92 17 22.08
Toxocara spp 221 70 31.67 13 18.57 57 81.43

Discussion

The results of this study showed that regardless of their developmental phases or sites from where cockroaches were collected, cockroaches play a fundamental role in the transportation of parasitic diseases and are capable of transmitting them to either humans and/or animals. Cockroaches found in houses, dormitories, hospitals, dumpsites, restaurants, and markets have been reported to carry a variety of human intestinal parasites, according to earlier research from Nigeria and other regions of the world (Isaac et al. 2014). The findings of this study make it abundantly evident that P. americana from restrooms, kitchens, and restaurants in the study area contain human intestinal parasites on their body surfaces and in their guts; this suggests that cockroaches may play a role as mechanical vectors. All of the parasites found in the cockroach body are medical and veterinary parasites that have been linked to numerous gastrointestinal disorders.

According to several studies (Mbanugo and Abazie 2002; Montresor et al. 2002; Sam-Wobo and Mafiana 2003; Tatfeng et al. 2005; Anosike et al. 2006), Entamoeba spp., B. coli, Ancylostoma spp., and A. lumbricoides can lead to chronic diarrhea, liver problems, and stunted growth. The human intestinal parasites recovered from cockroaches in this study includes Entamoeba spp, Ascaris lumbricoides, Trichuris trichiura, Strongyloides stercoralis, Taenia spp., Enterobius vermicularis, Toxocara spp., Diphylidium spp., hookworm, and Balantidium coli. These parasites are responsible for a number of disease conditions in man, some of which could be life-threatening (Pullan et al. 2014). In this study, three major soil-transmitted helminths were found in cockroaches: Ancylostoma spp., T. trichiura, and A. lumbricoides. These parasites are responsible for a significant disease burden worldwide and are linked to malnutrition, growth stunting, and cognitive disabilities in children (Pullan et al. 2014).

Strongyloides stercoralis is known to cause complicated infections with high case fatality rates from hyper-infection or dissemination, particularly in people with impaired immune systems (Meyer et al. 2015). Entamoeba histolytica causes Amoebiasis, a potentially serious and life-threatening condition that, if left untreated, could result to the death in an infected patient (Skappak et al. 2014). The human intestinal parasites recovered in this study are compatible with those reported in related research by Isaac et al. (2014), but with minor differences. The minor discrepancies, however, might be caused by variations in home and environmental hygiene standards, transmission dynamics between research locales, and the diagnostic technique used. The predominance of cockroaches in human housing, according to Ogbe et al. (2002), leaves people susceptible and increases their risk of coming in contact with intestinal parasites. The present study's findings on the prevalence of A. lumbricoides, Trichuris trichiura, Strongyloides stercoralis, Enterobius vermicularis, Dipylidium spp., and Balantidium coli in cockroach guts across all points of collection are consistent with the report of Ogbe et al. (2002).

The results of the current study show that the presence of parasites in cockroaches from all three points of collection (kitchen, toilet and restaurant) suggests that these parasites have an equal chance of being acquired by cockroaches, mainly because the toilet proximity to where food is stored and prepared may be one of the factors that encouraged pathogen transmission by cockroaches. According to Mbanugo and Onyebuchi (2002), cockroaches may enter any space and are commonplace. The recovery of the two main gastro-intestinal parasites (Entamoeba species and Ascaris lumbricoides) in cockroaches from residential settings is most concern of this study's results. According to Word Health Organisation (2016), Entamoeba species and Ascaris lumbricoides can be easily spread by body contacts of the cockroaches with food items, eating and drinking utensils in the homes. The high occurrence of A. lumbricoides and E. histolytica over other gastrointestinal parasites has also been well documented among human population in different parts of Nigeria (Ogbe and Ododu 1990; Mafiana 1995; Asaolu et al. 2002; Ogbe et al. 2002; Sam-Wobo and Mafiana 2003) and the risk of its transmission has been associated with poor sanitary conditions (Asaolu et al. 2002; Sam-Wobo and Mafiana 2003).

The present study recorded differences in individual parasite species loads between cockroaches collected from the study sites. The varied degrees of hygiene and sanitation in each collection area might therefore be used to explain variations in the specific parasite species loads between cockroaches from toilet, restaurants, and kitchens. According to Ajero et al. (2011), unsanitary environments may lead to a higher parasite contamination, which is consistent with the findings of the current investigation. From this study, it is discovered that the different developmental stages (nymph and adult) of P. americana play equal role in transmission of diseases, thus, both developmental stages could play significant role in transporting and transmitting human intestinal parasites. The results of this study revealed that female cockroaches were significantly more vectorial than males. This finding may be explained by observations made by Oyeyemi et al. (2015) and Atiokeng et al. (2017) who found that female cockroaches travel farther than males in search of food and places to lay their eggs. They are more susceptible to diseases because of these factors, which cause them to come into contact with contaminated objects. The toilet had the largest concentration of parasite-infected cockroaches. This makes sense given that cockroaches are more likely to be found near toilets, which are more likely to be contaminated by feces.

Conclusion

The findings of this study have demonstrated the significance of P. americana (American cockroach) for public health. The majority of the disease-causing pathogens carried by P. americana in the research area are infectious stages of human and/or animal intestinal parasites, and they can be found on their body surfaces and in their guts. In order to reduce cockroach interaction with unsanitary locations or substrates from which parasites are known to exist, hygiene and environmental sanitation must be improved due to the high incidence of parasites in cockroaches. Therefore, it is advised that preventative measures be taken, making a good sanitary, insect-free environment a top priority in households, especially the kitchen and toilet.

Acknowledgements

The authors appreciate the Laboratory Technologist of the Department of Biology, Federal University of Technology, Akure for their support.

Funding

This research work did not receive any external funding.

Data availability

All analysed data involved in this study are included in this manuscript.

Declarations

Competing interests

The authors declare no competing interests.

Footnotes

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

References

  1. Abudin S, Martini M, Nurjazuli N. Factors that trigger cockroach density: A literature review. Majalah Kesehatan Indonesia. 2023;4(2):71–76. doi: 10.47679/makein.2023155. [DOI] [Google Scholar]
  2. Adenusi AA, Akinyemi MI, Akinsanya D. Domiciliary cockroaches as carriers of human intestinal parasites in lagos metropolis, Southwest Nigeria: Implications for public health. J Arthropod Borne Dis. 2018;12(2):141–151. doi: 10.18502/jad.v12i2.40. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Ajero CMU, Ukaga CN, Ebirim C. The role of cockroaches (Blatta orientalis and Periplaneta americana) in mechanical transmission of parasites in households in Owerri. South East Nigeria Nig J Parasitol. 2011;32(2):153–156. [Google Scholar]
  4. Anikwe JC, Adetoro FA, Anogwih JA, Makanjuola WA, Kemabonta KA, Akinwande KL. Laboratory and field evaluation of an Indoxacarb Gel bait against two cockroach species (Dictyoptera: Blattellidae, Blattidae) in Lagos. Nigeria J Econ Entomol. 2014;107(4):1639–1642. doi: 10.1603/ec13457. [DOI] [PubMed] [Google Scholar]
  5. Anosike JC, Zaccheaus VO, Adeiyongo CM, Abanobi OC, Dada EO, Oku EE, Keke IR, Uwaezuoke JC, Amajuoyi OU, Obiukwu CE, Nwosu DC, Ogbusu FI. Studies on the intestinal worm (Helminthiasis) infection in a central Nigerian rural community. J Appl Sci Environ Manag. 2006;10(2):61–66. [Google Scholar]
  6. Asaolu SO, Ofoezie EI, Odumuyiwa PA, Sowemimo O, Ogunniyi TAB. Effect of water supply and sanitation on the prevalence and intensity of Ascaris lumbricoides among pre-school-age children in Ajebandele and Ifewara, Osun State, Nigeria. Trans R Soc Trop Med and Hyg. 2002;96(6):600–604. doi: 10.1016/s0035-9203(02)90323-8. [DOI] [PubMed] [Google Scholar]
  7. Atiokeng TRJ, Tsila HG, Wabo Pone J. Medically important parasites carried by cockroaches in Melong subdivision, Littoral. Cameroon J Parasito Res. 2017;2017:7967325. doi: 10.1155/2017/7967325. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bowman DD (2009) Georgis’ parasitology for veterinarians. 9th edition. Ed Elsevler, pp 479–89.
  9. Brenner H, Gefeller O. Deriving more up-to-date estimates of long-term patient survival. J Clin Epidem. 1997;50(2):211–216. doi: 10.1016/s0895-4356(97)00280-1. [DOI] [PubMed] [Google Scholar]
  10. Cochran DG (1999) Cockroaches: their biology, distribution and control. World Health Organization, Geneva. WHO/CDS/CPC/WHOPES/99.3.
  11. Dokmaikaw A, Suntaravitun P. Prevalence of parasitic contamination of cockroaches collected from fresh markets in Chachoengsao province, Thailand. Kobe J Med Sci. 2020;65(4):118–123. [PMC free article] [PubMed] [Google Scholar]
  12. Donkor ES. Cockroaches and food-borne pathogens. Environ Health Insights. 2020;14:1178630220913365. doi: 10.1177/1178630220913365. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Gałęcki R, Sokół R. A parasitological evaluation of edible insects and their role in the transmission of parasitic diseases to humans and animals. PLoS ONE. 2019;14(7):e0219303. doi: 10.1371/journal.pone.0219303. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hamu H, Debalke S, Zemene E, Birlie B, Mekonnen Z, Yewhalaw D. Isolation of intestinal parasites of public health importance from cockroaches (Blattella germanica) in Jimma Town. Southwestern Eth J Parasitol Res. 2014;2014:186240. doi: 10.1155/2014/186240. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Isaac C, Orue PO, Iyamu MI, Ehiaghe JI, Isaac O. Comparative analysis of pathogenic organisms in cockroaches from different community settings in Edo State, Nigeria. Kor J Parasitol. 2014;52:177–181. doi: 10.3347/kjp.2014.52.2.177. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Jeong KY, Son M, Lee JH, Hong CS, Park JW. Allergenic characterization of a novel allergen, homologous to chymotrypsin, from German cockroach. All Ast Immunol Res. 2015;7(3):283–289. doi: 10.4168/aair.2015.7.3.283. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kramer RD, Brenner RJ. Cockroaches (Blattaria) In: Mullen GR, Durden LA, editors. Medical and veterinary entomology. 2. New York, USA: Academic Press/Elsevier Inc; 2009. pp. 41–55. [Google Scholar]
  18. Mafiana CF. Intestinal helminthiasis (with particular reference to Ascariasis) among school children in Ilewo-Orile, Ogun State. Nigeria Nig J Parasitol. 1995;16:47–53. [Google Scholar]
  19. Mbanugo JI, Abazie OC. A comparative study of intestinal parasite infections of pregnant and nonpregnant women in Nkpor. Anambra State Nig J Parasitol. 2002;23(1):19–26. [Google Scholar]
  20. Mbanugo JI, Onyebuchi CJ. Prevalence of intestinal parasites in Ezifite community in Aguata LGA of Anambra state. Nig J Parasitol. 2002;23:27. [Google Scholar]
  21. Meyer J (2015) General entomology. University of North Carolina. Retrieved 9 November.
  22. Montresor A, Crompton DWT, Gyorkos TW, Savioli L. Helminth control in school-age children: a guide for managers of control programmes. World Health Organization; 2002. [Google Scholar]
  23. Ogbe MG, Ododu LA. Gastro intestinal helminthiasis in schools in Epe Local government area, Lagos State. Nigeria Nig J Parasitol. 1990;9(11):95–106. [Google Scholar]
  24. Ogbe MG, Edet EE, Isichei MN. Intestinal helminth in primary school children in areas of operation of shell petroleum development company of Nigeria (SPDC), Western division in delta sate. Nig J Parasitol. 2002;23:3–10. [Google Scholar]
  25. Oyeyemi OT, Agbaje MO, Okelue UB. Food-borne human parasitic pathogens associated with household cockroaches and houseflies in Nigeria. Parasite Epidemiol Control. 2015;1(1):10–13. doi: 10.1016/j.parepi.2015.10.001. [DOI] [Google Scholar]
  26. Pullan RL, Smith JL, Jasrasaria R, Brooker SJ. Global numbers of infection and disease burden of soil transmitted helminth infections in 2010. Para Vect. 2014;7:37. doi: 10.1186/1756-3305-7-37. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Salehzadeh A, Tavacol P, Majhub H. Bacteria, fungi and parasitic contaminants of cockroaches in Public Hospitals of Hamedah. Iran J Vect Borne Dis. 2007;44:105–110. [PubMed] [Google Scholar]
  28. Sam-Wobo SO, Mafiana CF. Prevalence and identification of helminth parasites of local chickens of Abeokuta, Nigeria. Inter J Agric Sci Environ Tech. 2003;2(2):141–147. [Google Scholar]
  29. Skappak C, Akierman S, Belga S, Novak K, Chadee K, Urbanski SJ, Church D, Beck PL. Invasive amoebiasis: a review of Entamoeba infections high-lighted with case reports. Canad J Gastroenterol Hepatol. 2014;28:355–359. doi: 10.1155/2014/745130. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Tatfeng YM, Usuanlele MU, Orukpe A. Mechanical transmission of pathogenic organisms: the role of cockroaches. J Vector Borne Dis. 2005;42(4):129–134. [PubMed] [Google Scholar]
  31. WHO . Bench aids for the diagnosis of intestinal parasites. Geneva: World Health Organization; 1994. [Google Scholar]
  32. WHO (2016). Preventable epilepsy: Taenia solium infection burdens economies, societies and individuals: a rationale for investment and action. World Health Organization, Geneva. WHO/HTM/NTD/NZD/2016.1.
  33. Yones DA, Galal LA, Abdallah AM, Zaghlol KS. Effect of enteric parasitic infection on serum trace elements and nutritional status in upper Egyptian children. Trop Parasitol. 2015;5(1):29–25. doi: 10.4103/2229-5070.145581. [DOI] [PMC free article] [PubMed] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

All analysed data involved in this study are included in this manuscript.


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