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 Table of Contents  
Year : 2015  |  Volume : 8  |  Issue : 2  |  Page : 101-106

Identification of parasitic infections in appendectomy specimens using histopathological and faecolith examinations

1 Department of Parasitology, Faculty of Medicine, Minia University, Minia, Egypt
2 Department of Pathology, Faculty of Medicine, Minia University, Minia, Egypt
3 Department of Surgery, Faculty of Medicine, Minia University, Minia, Egypt

Date of Submission04-May-2015
Date of Acceptance07-Jun-2015
Date of Web Publication27-Jan-2016

Correspondence Address:
Manal Z.M. Abdellatif
MD, Department of Parasitology, Faculty of Medicine, Minia University, Minia 61519
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/1687-7942.175007

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Appendicitis is the most common acute surgical condition of the abdomen, and appendectomy constitutes one of the most common surgical operations worldwide. Gender, age, seasonal variation and leucocytic count have been investigated in many studies, however, causative parasitic agents of appendicitis are the most important. They differ from country to country.
The present study aimed to investigate parasitic infections as causes of appendicitis among patients attending Minia University Hospital, Minia Governorate, EL Minia, Egypt.
This descriptive study was carried out during the period between October 2013 and March 2014. Among 100 patients treated by appendectomy with a prediagnosis of appendicitis, 55 were males and 45 were females. All patients with clinically prediagnosed appendicitis were subjected to an open appendectomy, in which a right Macberny incision was made, followed by delivery of the caecum, devascularisation of the appendix, base ligation and appendectomy. Removed appendices were preserved in 10% formalin, fixed, sectioned, stained with H & E and examined for histopathological changes and presence of parasites. The faecolith contents of the remaining portions of appendices were evacuated. A wet mount preparation from each specimen was subjected to light microscopic examination for detection of parasites.
Parasitic infection was detected in nine appendectomy specimens. The presence of Enterobius vermicularis worms was confirmed in three cases by both histopathological and faecolith examinations. Eggs of Ascaris lumbricoides, Ancylostoma duodenale and Hymenolepis nana were detected in one case each by faecolith examination. Bilharzial granulomas were detected in three cases by histopathology. Interestingly, E. vermicularis and the eggs of A. lumbricoides, A. duodenale and H. nana were found to be associated with obstructive acute appendicitis, whereas bilharzial granulomas were observed in chronic appendicitis.
The study concluded that parasitic infections constitute only 9% of the surgically removed appendices. Schistosoma spp. and E. vermicularis were the most common parasitic recorded. The association of H. nana with acute appendicitis appears to be a novel finding. A combination of histopathology and faecolith examinations is necessary for detection of parasitic causes of appendicitis.

Keywords: appendicitis, bilharzial granulomas, Enterobius vermicularis, faecolith, histopathology, parasitic infection

How to cite this article:
Abdellatif MZ, Abdel-Hafeez EH, Belal US, Mohamed RM, Abdelgelil NH, Abdel-Tawab N, Atiya AM. Identification of parasitic infections in appendectomy specimens using histopathological and faecolith examinations. Parasitol United J 2015;8:101-6

How to cite this URL:
Abdellatif MZ, Abdel-Hafeez EH, Belal US, Mohamed RM, Abdelgelil NH, Abdel-Tawab N, Atiya AM. Identification of parasitic infections in appendectomy specimens using histopathological and faecolith examinations. Parasitol United J [serial online] 2015 [cited 2023 Nov 29];8:101-6. Available from: http://www.new.puj.eg.net/text.asp?2015/8/2/101/175007

  Introduction Top

Acute appendicitis is a common cause of an emergent surgical intervention [1] . The prevalence of appendicitis is reported to be around 7%, being slightly higher in males. It appears to be much lower in Africa which might be due to the higher amount of fibre in the African diet compared with the refined food diet of Western Europe and North America [2] . In Egypt, as one of these African countries, appendicitis is still one of the most frequent causes for emergency operations in visceral surgery [3] . It has been reported that the cause of appendicitis is intraluminal obstruction caused by lymphoid hyperplasia, parasite-associated faecal matter and ingested foreign bodies [4] . Many parasites such as Enterobius vermicularis [5],[6] , Ascaris lumbricoides [7] , Schistosoma spp. [8],[9] and Taenia spp. [10],[11] are reported to be frequently found in the appendectomy specimens. Recently in Egypt, Hedya et al., [12] reported that the retrospective study of appendectomies revealed 11 out of 251 (4.38%) having parasitic infections; E. vermicularis (1.59%), A. lumbricoides (0.79%), Schistosoma spp. eggs (1.19%) and amoebiasis (0.79%). In 2014, Jada et al. [13] detected a wide spectrum of parasitic infections (48%) in one hundred surgically removed appendices in India. These parasitic infections included A. lumbricoides (18%), E. vermicularis (6%), A. duodenale (4%), Taenia spp. (2%), Trichostrongylous (1%) and T. trichiura (1%). Worldwide, the association between E. vermicularis infection and acute appendicitis has been reported to vary from 0.2 to 41.8% worldwide [5],[14],[15],[16] . In one, report the researchers could not provide evidence of its pathogenic effect in relation to appendicitis, but advocated that it presents with symptoms resembling true appendicitis [17] . Such evidence encouraged the argument as to whether the parasites may cause appendicitis or not [18] . Schistosoma infection is endemic in many developing countries in the world including Egypt. The presence of eggs of Schistosoma spp. in the tissues results in fibrosis, constriction and calcification of all organs reached by the eggs, including the appendix, and this leads to the formation of bilharzial granuloma in these organs [19],[20] . Therefore, the current study aimed to investigate the existence of any parasitic infections as a cause of appendicitis among patients attending the Surgical Department, Minia University Hospital, Minia Governorate, Minia, Egypt. To achieve the objective, we used two methods; histopathology and faecolith examination for screening the presence of possible parasitic infections in the surgically removed appendices.

  Patients and methods Top

Type of study: Descriptive analytical study

The study was carried out from October, 2013 to March, 2014.

Collection of appendices

Patients: One hundred patients with clinical manifestations of appendicitis underwent appendectomy at the Surgical Department of the Minia University Hospital, Minia Governorate, Minia, Egypt. After appendectomy, each appendix was immediately preserved in 10% formalin in a clean container labelled and transported to the Parasitology laboratory. The patient's consent was obtained before surgery as per norm. Data for each patient were obtained from the hospital records. All the appendix specimens delivered to the department of Parasitology were examined after obtaining consent from the institutional ethical committee.

Histopathological examination

Three transverse sections were taken from the beginning, the middle and and distal parts of the appendectomy specimens. Each section was stained with haematoxylin and eosin, and examined for inflammatory changes and the presence of any parasitic infection. The reports were grouped by pathologic features as nonobstructive acute appendicitis, obstructive acute appendicitis and chronic appendicitis [21] .

Faecolith examination

The faecal contents of the remaining portion of appendectomies were evacuated in a clean container. A wet mount preparation was prepared from each appendectomy specimen by mixing a part of faecolith with normal physiological saline (0.9%) and Lugol's iodine and examining the sediment under low and higher power microscopy for parasitic infection.

Statistical analysis

Data were fed to a computer and analysed using SPSS, version 19 (SPSS Inc., Chicago, Illinois, USA). A test of proportion (Z-test) was used to compare qualitative variables, a t-test was used to compare means and the k-test was used to determine the degree of agreement between hisopathological and faecolith examinations. The results in the mentioned procedures were considered statistically significant when the P-value was less than 5% (P < 0.05).

  Results Top

Among 100 patients who were operated on with a prediagnosis of acute appendicitis, 55 (55%) were males and 45 (45%) were females. The male : female ratio was 1.22 : 1. The mean age of patients was 26.83 ± 7.47 years among males and 23.80 ± 7.51 years among females. Both male and female patients showed marked leucocytosis of 17416 ± 1441 and 17083 ± 1605 cell/ml, respectively, as shown in [Table 1].
Table 1: Gender, age and total leucocytic count among patients with appendicitis

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In terms of the symptoms, the majority of cases subjected to appendectomy had localized right iliac pain (82%) and only a minority of patients (6%) had acute abdominal pain as their chief complaint. Diffuse abdominal pain was present in 10% of cases. Also, some patients had vomiting (5%) and fever (5%) with or without abdominal pain ([Table 2]). Furthermore, out of 100 surgically removed appendices, 6% (3 E. vermicularis), and 3 biharzial granulomas) were positive by histopathological examination. Another 6% (one case each infected with A. lumbricoides, A. duodenale, H. nana, and 3 cases with E. vermicularis) were positive by faecolith examination ([Table 3]).
Table 2: Symptoms among patients with appendicitis

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Table 3: Parasitic infection detected among patients
with appendicitis

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Histopathological examination revealed the presence of bilharzial granuloma in three cases (3%) ([Figure 1]a and b). E. vermicularis worms were detected in three cases (12, 13 and 26 years old) by both histopathological ([Figure 1]c and d) and faecolith examinations ([Figure 2]a). It is important to note that E. vermicularis was not associated with granuloma formation but it was found in the lumen of inflammed appendices. Each of A. lumbricoides, A. duodenale and H. nana eggs was detected in one case (1% each) by faecolith examination, but not by histopathological examination ([Table 3]).
Figure 1: Parasites detected by histopathological examination of appendixes.(a) Section in appendix showing normal mucosal layer (M) and the submucosal layer (S) contains several granulomas (G) each one containing a schistosomal egg. (H&E ×10) (b) A higher magnifi cation of (A) showing a parasitic submucosal granuloma with surrounding heavy lymphocytic infiltration (L), fibrosis (F) and schistosomal ova (arrows) (H&E ×40) (c) Cross sections of male and female E. vermicularis worms (arrow) (H&E ×10) (d) A higher magnifi cation of (C) showing a cross section through E. vermicularis female worm containing typical eggs (W), and surrounded by heavy lymphocytic infiltration (L). (H&E ×40).

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Figure 2: Parasites detected by faecolith examination. (a) Adult female E. vermicularis worm (arrow) surrounded by faecolith (F). (Direct smear, ×10). (b) A. lumbricoides egg. (Direct smear, ×40). (c) A. duodenale egg. (Direct smear, ×40).(d) H. nana egg. (Direct smear, ×40).

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In addition, most of the cases (65%) showed a picture of nonobstructive acute appendicitis in which inflammation commenced either in the mucous membrane or in the lymph follicles and terminated either as resolution, ulceration, suppuration or fibrosis. The mucosa was partially ulcerated with infiltration by acute inflammatory cells mainly formed of neutrophilis and pus cells. The inflammatory cellular infiltrate reached the submucosa and muscularis propria. Fifteen cases (15%) showed obstructive acute appendicitis. The obstruction was considered to be either because of parasites in the lumen, which was in the form of E. vermicularis (three cases) or other causes as faecolith, and food particles in the appendicular wall (12 cases). Products of inflammation proceeded more rapidly and more certainly to perforation. Perforation occurred most commonly at the site of impacted faecolith or parasite. The escaping purulent contents caused periappendicitis in the form of inflammation of tissues around the appendix with the formation of a cyst outside the appendicular wall. This occurred in a few cases. Twenty cases (20%) showed chronic appendicitis in the form of transmural infiltration by chronic inflammatory cells in the form of lymphocytes, eosinophils, plasma cells and macrophages. The mucosa was either ulcerated, especially when the parasite was seen, or intact. The submucosa showed congested vascular spaces and three cases showed granuloma formation around a calcified Schistosoma spp. egg ([Figure 1]a and b). Some cases showed hyperplasia of the lymphoid follicles present in the submucosa. Interestingly, the bilharzial granulomas were particularly associated with chronic obstructive appendicitis, while the E. vermicularis worms and eggs of A. lumbricoides, A. dudenale, H. nana were found to occur in the obstructive acute appendicitis cases.

  Discussion Top

Appendicitis is the most common acute surgical circumstance of the abdomen [20] and appendectomy is one of the most common surgical operations worldwide [16] . Gender, age, seasonal variation and leucocytic count have been investigated in many studies. Parasitic causes differ from country to country [24],[25] . Therefore, the present study examined 100 surgically removed appendices from Minia University hospital patients by both histopathology and faecolith examination to verify the association between appendicitis and parasitic infections. Study of patients' characteristics showed that 55% of them were males and 45% were females. The male : female ratio of 1.22 : 1. This ratio approximately coincided with that obtained by Ramezani and Dehghani [26] . In contrast, Helmy et al. [27] reported that the male : female ratio among patients previously diagnosed with appendicitis in Cairo was 1 : 2. Our recorded age ranges of both males and females appendiceal patients were 12-41 and 12-37 years, respectively, but the most affected age group for both sexes was between 12 and 30 years. This result was nearly comparable with that obtained by others [27],[28] .

As the appendix is a vestigial organ, it can be easily infiltrated by numerous intestinal contents such as vegetable fibres, faecolith, parasites and their eggs. These foreign particles can lead to the obstruction of the appendiceal lumen. If the lumen is obstructed, the continuous mucosal secretion and proliferation of bacteria and/or the presence of parasites may cause an increase in the intraluminal pressure. Increased pressure hinders the blood supply of the appendix wall and mucosal damage may cause bacterial invasion, inflammation, sepsis and finally necrosis. The inflammation of all appendices included in our study was anticipated before histopathological examination because all of the studied patients showed leucocytosis. With obstruction of the lumen, the resulting, pain can be partially or exclusively reported at the umbilicus, and can be difficult to localize at the beginning of the inflammatory condition [29],[30],[31],[32],[33],[34] . Results of our study showed that most of the patients included had right iliac pain, whereas some had acute abdominal pain, vomiting and fever. The latter condition may be explained by the late attendance of the patients to the department of surgery.

The causes of appendicitis are apparently numerous. As reported previously, parasitic infections are one of these causes [5-11]. Our results showed that '9%' of surgically removed appendices were positive for parasitic infections, revealing E. vermicularis, Shistosoma spp., A. lumbricoides, A. duodenale and H. nana eggs. In another study in Cairo city, Helmy et al. [27] reported that parasites were detected in 14.8% of surgically removed appendices. Our identification of E. vermicularis male and female worms in 3% of the appendectomies by both faecolith and histopathological examinations coincides with reported results by Arca et al. [5] in a study conducted in USA. Our results also coincide with the findings recorded by Ramezani and Dehghani [26] , who identified E. vermicularis in 2.9% of surgically removed appendices from an Iranian population. In Turkey, several studies recorded the presence of E. vermicularis in 3.15% [28] and 3.8% [29],[30] of surgically removed appendices from a Turkish population. In Nepal, E. vermicularis was identified in 1.62% of Nepalese patients with clinically diagnosed appendicitis [37] . A 4% incidence of entrobiasis was described in another study from Denmark [38] . In other reports on enterobiasis, slightly higher incidences of 10% were recorded in Egyptian patients [27] and 12% in patients from India [13] . The wide range of these percentages indicates that the association between E. vermicularis and appendicitis differs from country to country [2],[25] . This can be explained on the basis that parasitic diseases affect four billion individuals worldwide, especially in communities that have lower hygiene and sanitation, socio-economical status, education and living conditions [39] . Wiebe [38] reported that there was a highly significant difference in the incidence of E. vermicularis in normal appendices than in inflamed ones. The researcher suggested that the presence of this parasite in the appendix can lead to the symptoms of acute appendicitis or this parasite leaves or does not enter an inflamed appendix [32] . In our findings, E. vermicularis was found in inflamed appendices.

Interestingly, histopathological examination of the appendix specimens revealed bilharzial granulomas that clearly contained eggs of Schistosoma spp. Previous records implicated S. haematobium [8],[9],[20] and S. mansoni [40] in the granulomatous reactions in the appendix. The 3 pateints who had bilharzial granulomas were associated with chronic obstructive appendicitis. This result is somewhat close to three other cited records [12],[27],[41] in which shistosomiasis was recorded in 6.3%, 1.6% and 1.19% of the appendectomies by histopathology, respectively. The 3% granulomas noted in our study and the recorded percentage (6.3%) in another Egyptian study [27] were much higher than that recorded by others (0.95%) [42] . This highlighted the role played by schistosomiasis as an aetiological agent of chronic appendicitis necessitating surgical intervention in Egypt. As previously stated, the majority of the recorded cases of appendiceal shistosomiasis were case reports [20],[40] . This can be attributed to the ecology of shistosomiasis worldwide.

In our study, faecolith examination successfully detected eggs of A. lumbricoides (1%), A. duodenale (1%) and H. nana (1%) in the appendectomies examined, whereas histopathological examination failed to detect them. This confirmed the value of the combination of histopathological and faecolith examinations for laboratory diagnosis of the parasitic aetiology of appendicitis. Our record of A. lumbricoides is nearly similar to the 0.79% obtained by other Egyptian researchers [12] and is contradictory to the 18% result obtained by Indian researchers [13] . Similarly the incidence of A. duodenale in our study is not compatible with the 4% result obtained by the same Indian researchers [13] . Interestingly our result of the association of H. nana with acute appendicitis is a novel finding as no available literature reported a similar result.

The majority (80%) of the appendix specimens examined showed acute appendicitis 65% of which were non obstructed while the remaining (15%) were obstructed. It is noteworthy that E. vermicularis worms (3%) and the eggs of A. lumbricoides, A. duodenale and H. nana were found to be associated with obstructive acute appendicitis. Other causes of obstruction of the appendices were due to faecolith or undigested food particles.

On the hand, the smaller number (20%) of studied appendix specimens showed chronic appendicitis. The bilharzial granulomas (3%) were observed only in the chronic appendicitis cases.

It can be concluded that infections of the appendix by schistosomiasis and enterobiasis are important agents in the pathogenesis of appendicitis in Egypt; thus, early diagnosis as well as treatment of these infestations are indicated to avoid the development of appendicitis, with subsequent appendectomy. Our study also concluded the importance of post-surgical investigation of the appendix specimens by both histopathological and faecolith examinations to detect the various aetiological agents of appendicitis and prescribe the appropriate anti-parasitic treatment.

  Acknowledgements Top

Author contribution: MZM Abdellatif proposed the research idea and shared with EH Abdel-Hafeez in writing the manuscript. US Belal shared with RM Mohamed and AM Atiya in sample collection. They also shared with NH Abdelgelil and N Abdel-Tawab in performing laboratory parasitological and histopathological studies and in results interpretation.

Conflicts of interest

There are no conflicts of interest.

  References Top

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  [Figure 1], [Figure 2]

  [Table 1], [Table 2], [Table 3]

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