Zakaria, Ossama M.a,b
Background: Controversy still exists regarding the relationship between parasitic infections and acute appendicitis.
Aim: To investigate the role of parasitic infections in the etiology of acute pediatric appendicitis.
Patients and methods: A two-center retrospective study included 1500 pediatric and adolescent patients who had undergone surgical therapy for a diagnosis of acute appendicitis over a period of 8 years from January 2001 to December 2008 in the Suez Canal University hospitals and Alexandria Health Insurance Sporting Hospital for School Students and children. The patients’ records were reviewed thoroughly to gather the demographic data on age, sex, and residence. Clinical data including the chief complaints on admission, duration of symptoms, history of similar attacks, previous hospitalization, and history of any chronic inflammatory diseases and drug history, if any, were analyzed. Laboratory and imaging studies were also reviewed. A thorough study of operative data was conducted, including a descriptive review of the operative findings during surgery. Postoperative complications, if any, and the histopathology reports of the removed appendices were also studied. Patients were divided into two groups according to the presence or the absence of parasites in the appendix lumen. In group I (n=98), parasitic infection was observed, whereas in group II (n=1402), no parasitic infection was present.
Results: Parasites were reported in 98 patients out of the 1500 patients included in the study (6.5%). Of those 98 parasitic infestations, 40 (40.8%) were Enterobaisis, 23 (23.5%) were Schistosomiasis, 15 (15.3%) were Ascaris lumbricoides, 12 (12.2%) were Trichuris trichiura, and eight (8.2%) were Taenea saginata. All patients showed a single parasitic infection. The percent of patients with suppurative, gangrenous, or perforated appendicitis was similar in both groups, with no statistical significance irrespective of the presence or the absence of parasitic infection.
Conclusion: Intestinal parasitic infection may not be considered as a risk factor for the development of acute appendicitis among the studied patients, and the low prevalence of parasites among the appendectomy specimens does not support the notion that parasites are a major cause of appendicitis in pediatric patients. However, parasitic infections could mimic the clinical picture of acute appendicitis, which need verification before the diagnosis of acute appendicitis.
Acute appendicitis is the most common acute surgical condition in children. It is usually caused by intraluminal obstruction and secondary infection of the appendix. Parasitic infections may cause symptoms mimicking acute appendicitis; however, their role in the causation of acute appendicitis remains speculative. Sporadic cases of appendicitis have been attributed to parasitic infections 1–3.
Parasitic infections are ubiquitous on a worldwide basis and are seen in high numbers in developing countries. Although the role of parasitic infections in relation to appendicitis is controversial, intestinal parasites may cause significant morbidity and mortality 4. It has been documented that Enterobius vermicularis (pin worm) infections of the gastrointestinal tract occur in 4–28% of children worldwide 4–10. Pin worms have been found in multiple locations in the gastrointestinal tract, including the appendix. Its most common manifestation is perianal pruritus 11–15. The association of E. vermicularis infection with acute appendicitis varies from 0.2 to 41.8% worldwide 3. Recent literature regarding appendiceal parasites focuses primarily on the pathologic changes induced by the presence of intraluminal parasites. The current retrospective study is aimed to assess the role of parasitic infections as an important factor in the etiology of pediatric appendicitis.
Patients and methods
This is a retrospective study reviewing the medical files of all pediatric and adolescent patients who were admitted and surgically treated for acute appendicitis in the Suez Canal University Hospital and Alexandria Health Insurance Sporting’s Students Hospital in the period of January 2001 to December 2008. The ethical considerations were fulfilled through the approval of the ethical committees in both centers. Data confidentiality was maintained through the whole study.
Patients’ records were studied thoroughly to gather the demographic data on age, sex, and residence. Clinical data including the chief complaints on admission, duration of symptoms, history of similar attacks, previous hospitalization, and history of any chronic inflammatory diseases and drug history, if any, were analyzed. Laboratory and imaging studies were also reviewed.
A thorough study of operative data was conducted, including a descriptive review of the operative findings during surgery. Postoperative complications, if any, and the histopathology reports of the removed appendices were also studied.
The collected data were tabulated and analyzed statistically. All statistically analyzed data were categorical and were tested using the χ2-test and Yate’s correction when necessary. A P-value of <0.05 was considered significant.
Patients (N=1500) were divided into two groups according to the presence or the absence of parasites in the appendix lumen. In group I (n=98), parasitic infection was observed, whereas in group II (n=1402), no parasitic infection was present. The age of our patients ranged from 1 to 17 years, with a mean age of 7.8±2.3 years.
Out of a total of 1500 patients, 822 (54.8%) were girls and 678 (45.2%) were boys, with an F/M ratio of 1.2 : 1. The percentage of parasitic infections was almost the same among patients living in urban and suburban areas (6.6%) and in those living in rural areas (6.5%) (Table 1).
One-thousand three hundred and thirty patients (88.7%) complained only of lower right quadrant abdominal pain. In contrast, the remaining 170 patients (11.3%) complained of right lower quadrant pain in association with diarrhea in 93 patients (54.7%); 32 patients (18.8%) had associated vomiting and fever, and 45 patients (26.5%) suffered from associated attacks of constipation preceded by diarrhea.
Open appendectomy was performed in 1387 patients (92.5%), whereas 113 patients (7.5%) underwent laparoscopic appendectomy. The operative findings showed acute edematous congested appendix in 1250 patients (83.3%), perforated appendix in 33 patients (2.2%), obstructed appendix in 41 patients (2.7%), gangrenous appendicitis in 46 patients (3.1%), and apparently normal appendix in 130 patients (8.7%). The operative time ranged from 22 to 94 min, with a median of 31 min.
The associated intra-abdominal findings included Meckel’s diverticulum that was not inflamed in six patients (0.4%), perforation of the appendix with Ascaris worm seen in the peritoneal cavity in three patients (0.2%), pin worm perforation of the appendix in four patients (0.3%), and ovarian cyst torsion in four patients (0.3%).
Postoperative complications included pelvic collection in seven patients (0.5%), wound infection and dehiscence in 35 patients (2.3%), and postoperative chest infection in three patients (0.2%).
In 548 specimens (36.5%), the appendix showed an acute catarrhal inflammation. Eosinophilic infiltration was seen microscopically in 43 specimens that also showed different parasitic infiltration, whereas neutrophil infiltration was noted in 1343 specimens (89%).
Six hundred and eighty specimens (45.3%) showed acute diffuse suppuration of the appendix. In 23 specimens (1.5%), different parasitic and eosinophilic infiltrations were recorded.
The appendix was found to be normal in 157 (10.5%) of the studied specimens and acutely gangrenous in 115 specimens (7.7%).
A total of 98 (6.5%) specimens showed parasitic infection. Out of these specimens, 66 (67.3%) were histopathologically proved to be acute appendicitis. The 98 appendiceal specimens with parasitic infection included Enterobaisis in 40 (40.8%) specimens, Schistosomiasis in 23 (23.5%) specimens, Ascaris lumbricoides in 15 (15.3%) specimens, Trichuris trichiura in 12 (12.2%) specimens, and Tinea saginata in eight specimens (8.2%). All patients showed a single parasitic infection, with no mixed parasitic infections. (Tables 2–4).
Normal Appendix (on histopathological examination) was significantly more common in cases associated with parasitic infection (group I) than in cases without parasitic infection (group II), as more than 90% of the patients without parasitic infections had inflamed appendices, whereas only 67% of the patients with parasitic infections had inflamed appendices (Table 5). This observation suggests that parasitic infections may mimic appendicitis in a considerable number of patients, who may not need appendectomy.
Gastrointestinal infection due to parasitic infection occurs worldwide. Its role in the etiology of acute appendicitis has been controversial.
The annual report of the two local referring health centers during our study period showed the prevalence of common parasite infections to be 46.3% among children between 1 and 18 years old. The percentages of parasite types were as follows: E. vermicularis in 22.9%, A. lumbricoides in 19.8%, Schistosomas in 10.2%, whereas T. trichiura and Taenia spp. showed a percentage of 1.4%. E. vermicularis (pin worm) is considered to be the most common helminthes infection 16. It has been documented to infect the gastrointestinal tract in 4–28% of children worldwide 4–10.
There was no difference in the percentage of parasitic infections between rural, urban, and suburban patients. This may be interesting, with the expectation to find a high percentage of parasitic infections in those living in the rural areas of a developing country, due to the better health services in urban and suburban areas, which help in diagnosing many cases that may be missed or neglected in the rural areas.
In the current study, 98 appendices with parasites were recorded out of a total of 1500 appendectomies. It was present in 66 (4.4%) inflamed appendiceal specimens and in 32 (2.1%) specimens of apparently normal appendices. These data are contradicted by Dorfman, who reported parasitic infection with a normal appendix in 7.2% and with an inflamed appendix in 8.9% 16.
E. vermicularis infection with acute appendicitis varies from 0.2 to 41.8% worldwide 3. It was often associated with uninflamed appendices and with inflamed appendices, and mucosal invasion was not seen; therefore, it seems unlikely that these parasites cause acute appendicitis. However, E. vermicularis may be a cause of symptoms resembling appendicitis, because a significantly higher proportion of patients with symptoms had E. vermicularis compared with patients who had an incidental appendicectomy 1–3. Although seen in all ages and socioeconomic levels, it is most common in children aged from 5 to 14 years 3.
Of the parasitically infected patients, 66% were above the age of 6 years up to 17 years, whereas 34% were below the age of 6. E. vermicularis was reported in 40 cases (2.7%) out of a total of 1500 appendisectomized patients; this could be compared with some reported literature of 1549 appendectomies with 1.4% specimens containing E. vermicularis. It can also be compared with other published data 2 where parasites were present in 62 (7.46%) cases out of a total of 830 appendectomy specimens. Nevertheless, in the literature review of appendiceal Enterobiasis infections, it represented about 4.5% in appendectomies 16–21.
The cause of acute appendicitis is generally considered to be an obstruction at the base of the appendix. An appendix affected by Schistosomiasis shows considerable fibrosis, which may have led to the obstruction 22.
Schistosomas were seen in 1.5% of our studied specimens; this coincides with some published data that showed the percentage of Schistosomal appendicitis to be 1.6% 23. It has been recorded to be only 0.2% in Hong Kong 24. Others reported percentages of Schistosomal appendicitis recorded as 2.3 and 1.3%, respectively 25,26.
A percentage of 1.0 and 0.9% for A. lumbricoides and T. trichiura were respectively recorded. This can be compared with previous data of Dorfman et al. 16 which showed a similar percentage of 1.1%.
Except for Taenia saginata, the prevalence rate of parasitic infections is significantly higher among the normal appendix than in the Appendicitis group for every single species and for total infestation (P<0.01). Prevalence of T. trichiura was still higher among the normal group with border-line significance (Table 3).
Laparoscopy was initiated to diagnose 43 (2.9%) patients with persistent abdominal pain out of a total of 113 who underwent laparoscopic procedures. It showed free pin worms in three patients and also free Ascaris in the abdominal cavity in one patient.
Moreover, laparotomy showed free pin worms in the peritoneal cavity due to appendiceal perforation in one patient. These data coincide with a literature report of three cases in which pin worms were set free into the abdominal cavity during laparoscopic appendectomy 27. It has been recommended that surgeons should exercise caution when performing laparoscopic appendectomy, using the endoloop technique to ensure that the pin worms are not released into the peritoneum upon amputation of the appendix 3–28.
Parasitic infection of the appendix was found to be associated with acute appendicitis or even ruptured appendicitis, especially in cases of Enterobius and Ascaris infestation. These parasitic infections, however, have also been found in symptom-free patients. Although our patients did not receive any antiparasitic treatment during their hospital stay, it is imperative that patients with parasitic infections receive the appropriate antiparasitic treatment before being discharged from the hospital, because an appendectomy treats a consequence and not the root cause of the disease. Parasitic infection was found in patients with appendicitis, and yet, it does not prove that it caused the disease. However, a larger group of parasites may cause appendicitis as shown by the histological changes in the resected specimens. The presence of pin worms may be an incidental finding, as they may cause symptoms mimicking appendicitis as reported in other studies 3.
In conclusion, intestinal parasitic infection may not be considered as a risk factor for the development of acute appendicitis among the studied patients, and the low percentage of parasites among the appendectomy specimens (6.5%) does not support the notion that parasites are a major cause of appendicitis in pediatric patients. However, the diagnosis of parasitic infections should be considered in any child with a right lower quadrant pain that is suspected to be appendicitis, especially in developing countries with limited resources. In these situations, a stool analysis should be performed as part of the routine investigatory tools.
The author would like to acknowledge Professor Hesham F el- Sayed, Professor of Paediatric Medicine, Suez Canal University and WHO epidemiology consultant for his advice and help in review of this manuscript.
Conflicts of interest
There are no conflicts of interest.
1. Karatepe O, Adas G, Tukenmez M, Battal M, Altiok M, Karahan S. Parasitic infestation as cause of acute appendicitis. G Ghir. 2009;30:426–428
2. Dorfman S, Cardozo J, Dorfman D, Del Villar A. The role of parasites in acute appendicitis of pediatric patients. Invest Clin. 2003;44:337–340
3. Arca MJ, Gates RL, Groner JI, Hammond S, Caniano DA. Clinical manifestations of appendiceal pinworms in children: an institutional experience and a review of the literature. Pediatr Surg Int. 2004;20:372–375
4. Waseem M, Simha S. Appendicitis: a rare cause. J Emerg Med. 2011;41:e9–e11
5. Gatti S, Lopes R, Cevini C, Ijaoba B, Bruno A, Bernuzzi AM, et al. Intestinal parasitic infections in an institution for the mentally retarded. Ann Trop Med Parasitol. 2000;94:453–460
6. Henley M, Sears JR. Pinworms: a persistent pediatric problem. MCN Am J Matern Child Nurs. 1985;10:111–113
7. Lee DS, Chung BH, Lee NS, Nam HW, Kim JH. A survey of helminthic infections in the residents of rural areas near Ulaanbaatar, Mongolia. Korean J Parasitol. 1999;37:145–147
8. Weller PF, Nutman TBIsselbacher KJ, Martin JB. Intestinal nematodes. Harrison’s principles of internal medicine. 199413th ed. New York McGraw-Hill:919
9. Yoon HJ, Choi YJ, Lee SU, Park HY, Huh S, Yang YS. Enterobius vermicularis
egg positive rate of pre-school children in Chunchon, Korea (1999). Korean J Parasitol. 2000;38:279–281
10. Ball MT, Hay J. Simultaneous demonstration of eosinophilic granulocytes and mast cells in tissue sections containing helminths. Ann Trop Med Parasitol. 1990;84:195–196
11. Bredesen J, Falensteen Lauritzen A, Kristiansen VB, Sorensen C, Kjersgaard P. Appendicitis and enterobiasis in children. Acta Chir Scand. 1988;154:585–587
12. Sterba J, Vlcek M. Appendiceal enterobiasis – its incidence and relationships to appendicitis. Folia Parasitol (Praha). 1984;31:311–318
13. Still GF. Oxyuriasis vermicularis
in children. Br Med J. 1899;1:898–900
14. Williams DJ, Dixon MF. Sex, Enterobius vermicularis
and the appendix. Br J Surg. 1988;75:1225–1226
15. Sridhar R, Kapila K, Verma K. Cytologic diagnosis of Enterobius vermicularis
eggs in an enterocutaneous fistula. Indian J Pathol Microbiol. 1999;42:355–357
16. Dorfman S , Talbot IC, Torres R, Cardozo J, Sanchez M. Parasitic infestation in acute appendicitis. Ann Trop Med Parasitol. 1995;89:99–101
17. Tolstedt GE. Pinworm infestation of the appendix. Am J Surg. 1968;116:454–455
18. Budd JS, Armstrong C. Role of Enterobius vermicularis
in the aetiology of appendicitis. Br J Surg. 1987;74:748–749
19. Gupta SC, Gupta AK, Keswani NK, Singh PA, Tripathi AK, Krishna V. Pathology of tropical appendicitis. J Clin Pathol. 1989;42:1169–1172
20. Dalimi A, Khoshzaban F. Comparative study of two methods for the diagnosis of Enterobius vermicularis
in the appendix. J Helminthol. 1993;67:85–86
21. Batistatou A, Zolota V, Scopa CD. Images in pathology: Oxyuris
in human cecum and appendix. Int J Surg Pathol. 2002;10:58
22. Meshikhes AWN, Chandrashekar CJ, Al Daolah Q, Al Saif O, Al Joaib AS, Al Habib SS, et al. Schistosomal appendicitis in the Eastern Province of Saudi Arabia: a clinicopathological study. Ann Saudi Med. 1999;19:12–14
23. Satti MB, Tamimi DM, Al Sohaibani MO, Al Quorain A. Appendicular schistosomiasis: a cause of clinical acute appendicitis? J Clin Pathol. 1987;40:424–428
24. Chan KW, Fu KH, Ling J. The pathology of the appendix in Hong Kong. Br J Clin Pract. 1988;42:241–244
25. Adebamowo CA, Akang EE, Ladipo JK, Ajao OG. Schistosomiasis of the appendix. Br J Surg. 1991;78:1219–1221
26. Abu Eshy SA, Malik GM, Khan AR, Khan GM, Al Shehri MY. Schistosomal appendicitis. Ann Saudi Med. 1995;15:347–349
27. Saxena AK, Springer A, Tsokas J, Willital GH. Laparoscopic appendectomy in children with Enterobius vermicularis.
Surg Laparosc Endosc Percutan Tech. 2001;11:284–286
28. Symmers WS. Pathology of oxyuriasis; with special reference to granulomas due to the presence of Oxyuris vermicularis
) and its ova in the tissues. AMA Arch Pathol. 1950;50:475–516