Skip to main content
SpringerLink
Log in

Enterobius vermicularis infection among appendectomy specimens in Qom Province, Central Iran: a retrospective study

  • Original Article
  • Published:
Comparative Clinical Pathology Aims and scope Submit manuscript

Abstract

The role of parasites in the pathogenesis of appendicitis has long been discussed. Enterobius vermicularis (E. vermicularis) is the most common parasitic worm found in the removed appendices. The main objective of this study was to determine the prevalence of parasitic infections among appendectomy specimens in Qom Province, Central Iran. This retrospective study was conducted at Nekoii Hospital of Qom City, from 21 March 2005 to 19 March 2016 (11-year period). The histopathology reports and recorded demographic data concerning 13,744 performed appendectomies were reviewed and then extracted using a structured template form. Out of the 13,744 surgically removed appendices, E. vermicularis was observed in 31 (0.22%) specimens. A total of the patients having E. vermicularis infection, 21 (67.74%) were female and 22 (70.97%) were less than 15 years old. According to the histopathology examinations, the appendix tissue was inflamed only in 3 (9.68%) specimens infected with E. vermicularis worm. The obtained results indicate that the presence of E. vermicularis in the appendix lumen rarely causes inflammation, and in most cases can lead to clinical signs of appendiceal colic or symptoms mimicking acute appendicitis. Therefore, the parasitic infections should be considered in the differential diagnosis of appendicitis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Ahmed MU, Bilal M, Anis K, Khan AM, Fatima K, Ahmed I, Khatri AM, Ur-Rehman S (2015) The frequency of Enterobius vermicularis infections in patients diagnosed with acute appendicitis in Pakistan. Glob J Health Sci 7(5):196–201

    Article  PubMed  PubMed Central  Google Scholar 

  • Ajao OG, Jastniah S, Malatani TS, Morad N, el Tayeb EN, Saif SA, Al-Ghamdi AS (1997) Enterobius vermicularis (pin worm) causing symptoms of appendicitis. Trop Dr 27(3):182–183

    CAS  Google Scholar 

  • Akbulut S, Tas M, Sogutcu N, Arikanoglu Z, Basbug M, Ulku A, Semur H, Yagmur Y (2011) Unusual histopathological findings in appendectomy specimens: a retrospective analysis and literature review. World J Gastroenterol 17(15):1961–1970

    Article  PubMed  PubMed Central  Google Scholar 

  • Akhigbe T, Smith F, Adeyemo A, Adeyanju T, Condon E, Waldron D (2013) Pinworm and appendicitis in children. Internet J Surg 30(3):1–4

  • Arca MJ, Gates RL, Groner JI, Hammond S, Caniano DA (2004) Clinical manifestations of appendiceal pinworms in children: an institutional experience and a review of the literature. Pediatr Surg Int 20(5):372–375

    Article  PubMed  Google Scholar 

  • Aydin Ö (2007) Incidental parasitic infestations in surgically removed appendices: a retrospective analysis. Diagn Pathol 2:16

    Article  PubMed  PubMed Central  Google Scholar 

  • Bahadoran M, Rezaian M, Nikian Y (1996) A survey of prevalence of intestinal parasites in primary and junior high schools of Isfahan City during the year 1993. J Kerman Univ Med Sci 3(2):73–79 (In Persian)

    Google Scholar 

  • Boulos PB, Cowie AG (1973) Pinworm infestation of the appendix. Br J Surg 60(12):975–976

    Article  CAS  PubMed  Google Scholar 

  • Budd JS, Armstrong C (1987) Role of Enterobius vermicularis in the aetiology of appendicitis. Br J Surg 74(8):748–749

    Article  CAS  PubMed  Google Scholar 

  • Çallı G, Özbilgin M, Yapar N, Sarıoğlu S, Özkoç S (2014) Acute appendicitis and coinfection with enterobiasis and taeniasis: a case report. Turkiye Parazitol Derg 38(1):58–60

    Article  PubMed  Google Scholar 

  • Cerva L, Schrottenbaum M, Kliment V (1991) Intestinal parasites: a study of human appendices. Folia Parasitol 38(1):5–9

    CAS  PubMed  Google Scholar 

  • Chamisa I (2009) A clinicopathological review of 324 appendices removed for acute appendicitis in Durban, South Africa: a retrospective analysis. Ann R Coll Surg Engl 91(8):688–692

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cook GC (1994) Enterobius vermicularis infection. Gut 35(9):1159–1162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dahlstrom JE, Macarthur EB (1994) Enterobius vermicularis: a possible cause of symptoms resembling appendicitis. Aust N Z J Surg 64(10):692–694

    Article  CAS  PubMed  Google Scholar 

  • Dalimi A, Khoshzaban F (1993) Comparative study of two methods for the diagnosis of Enterobius vermicularis in the appendix. J Helminthol 67(1):85–86

    Article  CAS  PubMed  Google Scholar 

  • Dorfman S, Talbot IC, Torres R, Cardozo J, Sanchez M (1995) Parasitic infestation in acute appendicitis. Ann Trop Med Parasitol 89(1):99–101

    Article  CAS  PubMed  Google Scholar 

  • Dorfman S, Cardozo J, Dorfman D, Del Villar A (2003) The role of parasites in acute appendicitis of pediatric patients. Investig Clin 44(4):337–340

    Google Scholar 

  • Duran-Jorda F (1957) Appendicitis and enterobiasis in children; a histological study of 691 appendices. Arch Dis Child 32(163):208–215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Engin O, Calik S, Calik B, Yildirim M, Coskun G (2010) Parasitic appendicitis from past to present in Turkey. Iran J Parasitol 5(3):57–63

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fallah E, Dehgani A (2008) A study on Entrobius vermicularis infection in a appendices removed by surgery in Tabriz hospitals. IJPD 4(1):1–5

    Google Scholar 

  • Figueiredo J, Santos Â, Clemente H, Lourenço A, Costa S, Grácio MA et al (2014) Schistosomiasis and acute appendicitis. Acta Medica Port 27(3):396–399

    Article  Google Scholar 

  • Flasar MH, Goldberg E (2006) Acute abdominal pain. Med Clin North Am 90(3):481–503

    Article  PubMed  Google Scholar 

  • Flum DR, Koepsell T (2002) The clinical and economic correlates of misdiagnosed appendicitis: nationwide analysis. Arch Surg 137(7):799–804

    Article  PubMed  Google Scholar 

  • Gatti S, Lopes R, Cevini C, Ijaoba B, Bruno A, Bernuzzi AM, de Lio P, Monco A, Scaglia M (2000) Intestinal parasitic infections in an institution for the mentally retarded. Ann Trop Med Parasitol 94(5):453–460

    Article  CAS  PubMed  Google Scholar 

  • Gialamas E, Papavramidis T, Michalopoulos N, Karayannopoulou G, Cheva A, Vasilaki O, Kesisoglou L, Papavramidis S (2012) Enterobius vermicularis: a rare cause of appendicitis. Turkiye Parazitol Derg 36(1):37–40

    Article  PubMed  Google Scholar 

  • Goldmann DA, Wilson CM (1997) Pinworm infestations. In: Hoekelman RA (ed) Primary pediatric care, 3rd edn. Mosby, St. Louis, p 1519

    Google Scholar 

  • Gupta SC, Gupta AK, Keswani NK, Singh PA, Tripathi AK, Krishna V (1989) Pathology of tropical appendicitis. J Clin Pathol 42(11):1169–1172

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hafezi Ahmadi M, Seifmanesh H (2011) Taeniasis caused appendicitis without local tenderness: a rare case. Hospital Chronicles 6(4):207–209

    Google Scholar 

  • Hamdona SM, Lubbad AM, Al-Hindi AI (2016) Histopathological study of Enterobius vermicularis among appendicitis patients in Gaza strip, Palestine. J Parasit Dis 40(1):176–183

    Article  PubMed  Google Scholar 

  • Herd ME, Cross PA, Dutt S (1992) Histological audit of acute appendicitis. J Clin Pathol 45(5):456–458

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ilhan E, Senlikci A, Kızanoglu H, Ustüner MA, Vardar E, Aykas A, Yeldan E, Yıldırım M (2013) Do intestinal parasitic infestations in patients with clinically acute appendicitis increase the rate of negative laparotomy? Analysis of 3863 cases from Turkey. Prz Gastroenterol 8(6):366–369

    PubMed  PubMed Central  Google Scholar 

  • Jafariyan R (2013) Holy City of Qom: past and present. Mashhad: imam Reza network, available at. http://www.Imamreza.Net/eng/imamreza.Php?Id=3026. Accessed 28.08.13

  • Karaman Ü, Türkmen E, Iraz M, Karataş T, Çolak C (2010) Parasitosis in appendectomy cases. Eur J Gen Med 7(3):317–320

    Google Scholar 

  • Karatepe O, Adas G, Tukenmez M, Battal M, Altiok M, Karahan S (2009) Parasitic infestation as cause of acute appendicitis. G Chir 30(10):426–428

    CAS  PubMed  Google Scholar 

  • Kazemzadeh H, Afshar-Moghadam N, Meamar AR, Rahimi HR, Kia EB (2008) Enterobius vermicularis and the appendix: report of five cases. Iran J Parasitol 3(3):54–55

    Google Scholar 

  • Kelly AOJ (1899) The pathogenesis of appendicitis. Phil Med J 21:119–137

    Google Scholar 

  • Khoshzaban F, Dalimi Asal A, Jamali Zavareh M, Karimi A (1999) A study on Enterobius vermicularis infection in appendices removed by surgery in Tehran hospitals. Daneshvar Med 6(23):33–38 (In Persian)

    Google Scholar 

  • Kucik CJ, Martin GL, Sortor BV (2004) Common intestinal parasites. Am Fam Physician 69(5):1161–1168

    PubMed  Google Scholar 

  • Lala S, Upadhyay V (2016) Enterobius vermicularis and its role in paediatric appendicitis: protection or predisposition? Aust N Z J Surg 86(9):717–719

    Article  Google Scholar 

  • Lally KP, Cox CS, Andrassy RJ (2004) The appendix. In: Townsend CM, Beauchamp RD, Evers BM, Mattox KL (eds) Sabiston textbook of surgery, 17th edn. WB Saunders, Philadelphia, pp 1381–1399

    Google Scholar 

  • Lamps LW (2004) Appendicitis and infections of the appendix. Semin Diagn Pathol 21(2):86–97

    Article  PubMed  Google Scholar 

  • Lejbkowicz F, Abel AB, Tsilman B, Cohen HI (2002) Taenia infestation in the appendix: a report of two cases. J Med Microbiol 51(1):90–91

    Article  PubMed  Google Scholar 

  • Mogensen K, Pahle E, Kowalski K (1985) Enterobius vermicularis and acute appendicitis. Acta Chir Scand 151(8):705–707

    CAS  PubMed  Google Scholar 

  • Mowlavi G, Massoud J, Mobedi I, Rezaian M, Solaymani Mohammadi S, Mostoufi NE, Gharaguzlo MJ (2004) Enterobius vermicularis: a controversial cause of appendicitis. Iran J Public Health 33(3):27–31

    Google Scholar 

  • Ng WT, Sze SY, Hui SK (2003) Port placement for laparoscopic appendectomy with the best cosmesis and ergonomics. Surg Endosc 17(1):166–167

    Article  CAS  PubMed  Google Scholar 

  • Nordback I, Harju E (1988) Inflammation parameters in the diagnosis of acute appendicitis. Acta Chir Scand 154(1):43–48

    CAS  PubMed  Google Scholar 

  • Nordstrand IA, Jayasekera LK (2004) Enterobius vermicularis and clinical appendicitis: worms in the vermiform appendix. Aust N Z J Surg 74(11):1024–1025

    Article  Google Scholar 

  • Panidis S, Paramythiotis D, Panagiotou D, Batsis G, Salonikidis S, Kaloutsi V, Michalopoulos A (2011) Acute appendicitis secondary to Enterobius vermicularis infection in a middle-aged man: a case report. J Med Case Rep 5:559

    Article  PubMed  PubMed Central  Google Scholar 

  • Pasupati TM, Yothasamutr K, Wah MJ, Sherif SET, Palayan K (2008) A study of parasitic infections in the luminal contents and tissue sections of appendix specimens. Trop Biomed 25(2):166–172

    Google Scholar 

  • Prystowsky JB, Pugh CM, Nagle AP (2005) Current problems in surgery. Appendicitis Curr Probl Surg 42(10):688–742

    Article  PubMed  Google Scholar 

  • Ramezani MA, Dehghani MR (2007) Relationship between Enterobius vermicularis and the incidence of acute appendicitis. Southeast Asian J Trop Med Public Health 38(1):20–23

    PubMed  Google Scholar 

  • Rostami M, Tohidi F, Sharbatkhori M, Taherkhani H, Eteraf A, Mohammadi R, Maghsoodloorad F (2012) The prevalence of intestinal parasitic infections in primary school students in Gorgan, Iran. Med Lab J 6(2):42–46 (In Persian)

    Google Scholar 

  • Sah SP, Bhadani PP (2006) Enterobius vermicularis causing symptoms of appendicitis in Nepal. Trop Dr 36(3):160–162

    Google Scholar 

  • Saravi KH, Fakhar M, Nematian J, Ghasemi M (2016) Co-infection with Enterobius vermicularis and Taenia saginata mimicking acute appendicitis. J Infect Public Health 9(4):519–522

    Article  PubMed  Google Scholar 

  • Sartorelli AC, da Silva MG, Rodrigues MA, da Silva RJ (2005) Appendiceal taeniasis presenting like acute appendicitis. Parasitol Res 97(2):171–172

    Article  PubMed  Google Scholar 

  • Saxena AK, Springer A, Tsokas J, Willital GH (2001) Laparoscopic appendectomy in children with Enterobius vermicularis. Surg Laparosc Endosc Percutan Tech 11(4):284–286

    Article  CAS  PubMed  Google Scholar 

  • Sforza M, Andjelkov K, Zaccheddu R, Ivanov D, Krstić S, Paganelli A (2011) An unusual case of ascariasis of the appendix. Srp Arh Celok Lek 139(11–12):809–811

    Article  PubMed  Google Scholar 

  • Shahabi S (1996) Prevalence of oxyuriasis in students aged 6-13 years in Torkaman port city in the province Mazandaran and comparing the effectiveness of medications mebendazole and piruinium pamoate in Oxyuris patients. Teb Tazkiyeh 5(3):17–21 (In Persian)

    Google Scholar 

  • Siavoshi MR, Sattari M, Pilevar M (1999) Histopatholoy and relative frequency of parasitic appendicitis in the main treatment centers of Hamadan City. J Guilan Univ Med Sci 8(29–30):63–68 (In Persian)

    Google Scholar 

  • da Silva DF, da Silva RJ, da Silva MG, Sartorelli AC, Rodrigues MA (2007) Parasitic infection of the appendix as a cause of acute appendicitis. Parasitol Res 102(1):99–102

    Article  PubMed  Google Scholar 

  • Singh I, Collins RE (2005) Right iliac fossa pain. Br J Hosp Med 66(11):76–78

    Article  Google Scholar 

  • Sodergren MH, Jethwa P, Wilkinson S, Kerwat R (2009) Presenting features of Enterobius vermicularis in the vermiform appendix. Scand J Gastroenterol 44(4):457–461

    Article  PubMed  Google Scholar 

  • Stĕrba J, Vlcek M (1984) Appendiceal enterobiasis—its incidence and relationships to appendicitis. Folia Parasitol 31(4):311–318

    PubMed  Google Scholar 

  • Stĕrba J, Vlcek M, Noll P, Vorel F (1985) Contribution to the question of relationships between Enterobius vermicularis (L.) and inflammatory processes in the appendix. Folia Parasitol 32(3):231–235

    PubMed  Google Scholar 

  • Still GF (1899) Observations on Oxyuris vermicularis in children. Br Med J 1(1998):898–900

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Symmers WS (1950) Pathology of oxyuriasis; with special reference to granulomas due to the presence of Oxyuris vermicularis (Enterobius vermicularis) and its ova in the tissues. AMA Arch Pathol 50(4):475–516

    CAS  PubMed  Google Scholar 

  • To KK, Cheng VC, Hung IF, Tang BS, Wong SS, Yuen KY (2006) Caecal-caecal intussusception caused by Trichuris trichiura in a young healthy adult. Scand J Infect Dis 38(9):813–815

    Article  PubMed  Google Scholar 

  • Wiebe BM (1991) Appendicitis and Enterobius vermicularis. Scand J Gastroenterol 26(3):336–338

    Article  CAS  PubMed  Google Scholar 

  • Williams DJ, Dixon MF (1988) Sex, Enterobius vermicularis and the appendix. Br J Surg 75(12):1225–1226

    Article  CAS  PubMed  Google Scholar 

  • Yabanoğlu H, Aytaç HÖ, Türk E, Karagülle E, Calışkan K, Belli S, Kayaselçuk F, Akın Tarım M (2014) Parasitic infections of the appendix as a cause of appendectomy in adult patients. Turkiye Parazitol Derg 38(1):12–16

    Article  PubMed  Google Scholar 

  • Yildirim S, Nursal TZ, Tarim A, Kayaselcuk F, Noyan T (2005) A rare cause of acute appendicitis: parasitic infection. Scand J Infect Dis 37(10):757–759

    Article  PubMed  Google Scholar 

  • Zakaria OM, Zakaria HM, Daoud MY, Al Wadaani H, Al Buali W, Al-Mohammed H (2013) Parasitic infestation in pediatric and adolescent appendicitis: a local experience. Oman Med J 28(2):92–96

    Article  PubMed  PubMed Central  Google Scholar 

  • Ziaei Hezarjaribi H, Dalimi A, Ghasemi M, Esmaeili Reykande S, Fakhar M (2013) Study on verminous appendicitis and its histopathologic lesions at teaching hospitals of Mazandaran University of Medical Sciences during 2005-2009. J Mazandaran Univ Med Sci 23(Suppl 2):31–37 (In Persian)

    Google Scholar 

  • Zoorob RJ (1996) Appendiceal colic caused by Enterobius vermicularis. J Am Board Fam Pract 9(1):57–59

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We acknowledge the co-operation of Prof. I. Moubedi from the Department of Medical Parasitology and Mycology, School of Public Health, Tehran University of Medical Sciences (TUMS), Tehran, Iran, and Dr. F. Sharifi from the Medical Laboratory of Nekoii Hospital, Qom University of Medical Sciences, Qom, Iran. The authors are also grateful to Mr. A. Khosh Nezhad and Mrs. T. Shahbazi, Z. Vesali Jamshid, F. Farrokhi, and S. Ghiasi for their assistance in reviewing histopathology reports and recorded demographic data of patients. This study financially supported by Mazandaran University of Medical Sciences, Sari, Iran (project No: 2305).

Author information

Authors and Affiliations

  1. Department of Microbiology, Blood Transfusion Research Center, High Institute for Research and Education in Transfusion Medicine, Tehran, Iran

    Ahmad Mardani

  2. Qom University of Medical Sciences, Qom, Iran

    Fatemeh Feizi

  3. Molecular and Cell Biology Research Center, School of Medicine, Department of Parasitology, Mazandaran University of Medical Sciences, Km 18, Farah-Abad Road, P.O Box: 48175-1665, Sari, Iran

    Mahdi Fakhar

  4. School of Paramedicine, Qom University of Medical Sciences, Qom, Iran

    Hossein Barani Beyranvand & Mohsen Farrokhi

  5. Medical Laboratory of Nekoii Hospital, Qom University of Medical Sciences, Qom, Iran

    Mohammad Abbasi

  6. Student Research Committee, Department of Parasitology and Mycology, School of Medicine, Mazandaran University of Medical Sciences, Sari, Iran

    Shabnam Asfaram

Authors
  1. Ahmad Mardani
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fatemeh Feizi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mahdi Fakhar
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hossein Barani Beyranvand
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mohsen Farrokhi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mohammad Abbasi
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Shabnam Asfaram
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mahdi Fakhar.

Ethics declarations

Funding

This study was funded by Mazandaran University of Medical Sciences (grant number 2305).

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Conflict of interest

The authors declare that they have no conflicts of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mardani, A., Feizi, F., Fakhar, M. et al. Enterobius vermicularis infection among appendectomy specimens in Qom Province, Central Iran: a retrospective study. Comp Clin Pathol 26, 1213–1219 (2017). https://doi.org/10.1007/s00580-017-2512-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00580-017-2512-5

Keywords

Search

Navigation