Do intestinal parasitic infestations in patients with clinically acute appendicitis increase the rate of negative laparotomy? Analysis of 3863 cases from Turkey.

INTRODUCTION: Acute appendicitis is the most frequently observed disease requiring emergency surgery. The role of parasites in its pathogenesis has long been discussed. The signs of the parasitic infestations can mimic the signs of acute appendicitis. Therefore, it can cause a negative laparotomy. AIM: To evaluate the parasitic infestations of the appendix vermiformis whether increas the rate of negative laparotomy.
MATERIAL AND METHODS: The histopathology results of a total of 3863 patients who underwent appendectomy with clinically acute appendicitis were evaluated retrospectively. All appendectomy materials in which parasites were observed were evaluated with respect to the nature of the parasites and the findings of inflammation. Cases in which parasite tissue fragments and/or eggs as well as findings of inflammation were histopathologically observed in the appendix lumen were diagnosed with parasitic appendicitis.
RESULTS: Evidence of parasites was observed in 19 (0.49%) of the evaluated appendectomy materials. In 9 (47.3%) of these specimens that had evidence for parasites, findings for acute appendicitis and localized peritonitis were identified. Findings of acute appendicitis had not been identified in the other ten (52.7%) of the specimens. Enterobius vermicularis was the most frequently identified parasite.
CONCLUSIONS: In parasitic acute appendicitis, appendectomy in itself is not sufficient for treatment. Pharmacological treatment should also be administered after surgery. Patients should be evaluated prior to surgery for parasites, and diagnosis of acute appendicitis should be considered more cautiously in order to avoid negative laparotomies.

Introduction

The aetiology of acute appendicitis includes fecaliths, lymphoid hyperplasia, fruit and vegetable seeds, barium enemas and tumours. Parasites are one of the more uncommon causes of acute appendicitis. Enterobius vermicularis, Ascaris lumbricoides, Schistosoma spp. and Taenia spp. are the parasites that can lead to a clinical picture of acute appendicitis. Enterobius vermicularis is the parasite that most frequently contributes to a clinical picture of acute appendicitis [1, 2].

Material and methods

The files and electronic records of 3863 patients who underwent appendectomy at the Izmir Education and Research Hospital General Surgery Clinic between 2003 and 2012 were evaluated retrospectively. All appendectomy materials in which parasites were observed were evaluated with respect to the nature of the parasites and the findings of inflammation.

The appendectomy materials were subject to fixation with 10% formaldehyde, tissue follow-up and paraffin block embedding. The 4-micron-thick sections obtained from the paraffin blocks were stained with haematoxylin and eosin, and examined under a white light microscope. Cases in which parasite tissue fragments and/ or eggs as well as findings of inflammation were histopathologically observed in the appendix lumen were diagnosed with parasitic appendicitis (Figures 1 and 2).

Figure 1

Full thickness of appendiceal wall and two parasites located in black-lined box were seen in the lumina of the appendix (40× H + E)

Figure 2

Cut-section of the intestine of the parasite was seenin high-power magnification of the lumina of the appendix (400× H + E)

Results

A total of 3863 patients underwent surgery with clinically acute appendicitis. Parasites had been observed in 19 (0.49%) of all evaluated appendectomy materials. Of the patients with parasites in their materials, 12 (63.2%) were female and 7 (36.8%) were male. Their average age was 30.6 years (range: 17–83 years). Of these parasites, 16 (84.2%) were identified as E. vermicularis, and 3 (15.8%) were identified as Taenia saginata. Acute appendicitis and localized peritonitis had been identified pathologically in 9 (47.3%) out of a total of 19 appendectomy materials. Findings of acute appendicitis had not been identified in the other ten (52.7%) materials (Table I). None of the patients had developed any significant morbidity or mortality. All patients had been postoperatively started on anti-parasite treatment and discharged from the hospital between their 1st and 3rd postoperative days.

Table I

Demographic parameters and histological findings of the patients

No. of case	Gender	Age	Species of parasite	Acute inflammation	Negative laparotomy
1	Female	29	Enterobius vermicularis	No	Yes
2	Female	40	Enterobius vermicularis	No	Yes
3	Female	18	Enterobius vermicularis	No	Yes
4	Female	33	Enterobius vermicularis	Yes	No
5	Female	25	Enterobius vermicularis	Yes	No
6	Female	19	Enterobius vermicularis	No	Yes
7	Male	33	Enterobius vermicularis	No	Yes
8	Male	17	Enterobius vermicularis	No	Yes
9	Female	29	Enterobius vermicularis	Yes	No
10	Male	30	Enterobius vermicularis	No	Yes
11	Female	33	Enterobius vermicularis	Yes	No
12	Female	24	Enterobius	No	Yes
13	Female	32	Taenia saginata	No	Yes
14	Female	27	Taenia saginata	Yes	No
15	Male	83	Taenia saginata	Yes	No
16	Female	23	Enterobius vermicularis	Yes	No
17	Male	27	Enterobius vermicularis	Yes	No
18	Male	19	Enterobius vermicularis	No	Yes
19	Female	41	Enterobius vermicularis	Yes	No

Discussion

Acute appendicitis is the most frequently observed disease requiring emergency surgery, and it affects nearly 7% of the population. It is observed more frequently in developed countries than in developing countries. The main cause of acute appendicitis is the obstruction of the appendix lumen. The underlying cause for its greater frequency in developed countries can hence be explained by hard stools, intracolonic pressure and fecalith formation, which are caused by diet. The obstruction of the appendix causes an increase in intraluminal pressure, leading to mucosal ischaemia. In conjunction with vascular congestion, the appendix mucosa becomes hypoxic and ulcers begin to form. This in turn leads to the invasion of the appendix wall by intraluminal bacteria [3, 4].

Parasitosis is asignificant health problem in endemic countries. Although parasitic diseases are mainly observed in tropical countries, they have also started to become a significant health problem in developing countries due to increasing migration and travel [5]. Enterobius vermicularis, Ascaris lumbricoides, Schistosoma spp. and Taenia spp. are among the parasites that lead to aclinical picture of acute appendicitis. The gastrointestinal infections associated with E. vermicularis are the most frequently encountered helmintic infections worldwide [1, 6]. Although it can be observed in all ages and across all socioeconomic levels, it is seen more frequently among children and the young. The infections are generally asymptomatic in children, and the most commonly observed symptom is itching around the anus. Moreover, E. vermicularis infections may cause ileocolitis, enterocutaneous fistulas, urinary tract infections, mesenteric abscesses, salpengitis and appendicitis. The mature form of E. vermicularis is most frequently observed in the proximal section of the ascending colon, the cecum, the appendix and the terminal ileum [7, 8].The relationship between E. vermicularis and acute appendicitis was first discovered towards the end of the 19th century [9, 10]. It has been observed that E. vermicularis can cause pathological changes to the appendix, ranging from lymphoid hyperplasia to acute phlegmonous appendicitis, gangrenous appendicitis and peritonitis [1]. Appendectomy is not sufficient in itself for treatment since it is not able to resolve the main cause of the disease. To obtain the best treatment results, antihelmintic treatment should be provided following surgery [11].

Teniasis, on the other hand, is a well-known tapeworm infection characterized by the presence of Taenia saginata or Taenia solium in the human intestines. Infection generally occurs as a result of consuming raw or undercooked meat [12]. Teniasis may sporadically lead to a clinical picture of acute or subacute appendicitis or cholangitis. A clinical picture of acute appendicitis occurring in association with Taenia is a very uncommon condition [13]. In the event that Taenia is the cause of acute appendicitis, albendazole treatment is provided to the patient following surgery [12].

The identification of intraluminal parasites in appendix material is usually an accidental finding. Such findings are generally observed concomitantly with an appendix that does not display any signs of inflammation. However, the parasitic invasion of the appendix may lead to the clinical symptoms of acute appendicitis, causing colic-like repetitive pain in the right lower quadrant. As a parasitic infection is actually present within the intestinal system, the clinical and laboratory findings will be suggestive of an infection. However, acute appendicitis will not be histologically present [5]. In our study, acute appendicitis and localized peritonitis were observed in 9 (47.3%) out of a total of 19 materials. The remaining ten (52.7%%) materials did not demonstrate any findings of acute appendicitis, and the laparotomies that had been performed were hence considered as negative laparotomies.

In a study presented by Engin et al. in Turkey, parasites were observed in 9/1969 (0.45%) appendectomy materials [3]. In a study presented by Karatepe et al. in Turkey, parasites were observed in 24/5100 (0.5%) appendectomy materials, and the rate of no inflammation with appendix specimen was determined as 6/24 (25%) [4]. Similarly, Aydın 6/190 (3.15%) and 4/6 (66.6%) [5], Da Silva et al. 24/1600 (1.5%) and 12/24 (50%) [1], Sah and Bhadani 9/624 (1.62%) and 6/9 (66.6%) [14], Gialamas et al. 7/1085 (0.64%) and 6/7 (85.7%) [7], and Ramezani and Dehghani 144/5048 (2.9%) and 68/144 (47.2%) [15] reported the rates, respectively (Table II).

Table II

Data obtained from countries included in this study

Author	Country	Total materials, n	Materials with parasites
			Total, n (%)	Acute inflammation, n %	No acute inflammation, n (%)
Ramezani et al.	Iran	5048	144 (2.9)	76 (52.8)	68 (47.2)
Karatepe et al.	Turkey	5100	24 (0.5)	18 (75)	6 (25)
Aydin et al.	Turkey	190	6 (3.15)	2 (33.3)	4 (66.7)
De Silva et al.	Brazil	1600	24 (1.5)	12 (50)	12 (50)
Sah et al.	Nepal	624	9 (1.62)	3 (33.3)	6 (66.7)
Gialamas et al.	Greece	1085	7 (0.64)	1 (14.3)	6 (85.7)
Current study	Turkey	3863	19 (0.49)	9 (47.4)	10 (52.6)

The identification of parasites in 19/3863 (0.49%) of the appendix materials of cases operated with a clinically acute appendicitis in our study was consistent with the literature.

As can be seen in the literature and in our study, the rate of absence of acute inflammation in patients operated with a clinically acute appendicitis and having parasites in their appendix lumen is very high. This is indicative of the high rate of negative laparotomy that has been performed on these patients.

In conclusion, E. vermicularis is the most frequently found parasite in the appendix lumen of patients operated with a clinically acute appendicitis. In cases where parasites are present in the appendix lumen, the rate of negative laparotomy becomes higher. In order to avoid the surgical side effects associated with negative laparotomy, patients applying for complaints of abdominal pain should be examined also for intestinal parasites. Patients whose medical history as well as clinical and laboratory findings are positive should be considered and evaluated more carefully. In addition to this, patients with acute appendicitis caused by parasites should receive anti-parasitic treatment following surgery.