Surgical Site Infections after Appendectomy Performed in Low and Middle Human Development-Index Countries: A Systematic Review

Abstract

Background:

Acute appendicitis is a common surgical emergency worldwide. Early intervention is associated with better outcomes. In low and middle Human Development-Index Countries (LMHDICs), late presentation and poor access to healthcare facilities can contribute to greater illness severity and higher complication rates, such as post-operative surgical site infections (SSIs). The current rate of SSIs post-appendectomy in low- and middle-index settings has yet to be described.

Methods:

We performed a systemic review of the literature describing the incidence and management of SSIs after appendectomy in LMHDICs. We conducted qualitative and quantitative analysis of the data in manuscripts describing patients undergoing appendectomy to establish a baseline SSI rate for this procedure in these settings.

Results:

Four hundred twenty-three abstracts were initially identified. Of these, 35 studies met the criteria for qualitative and quantitative analysis. The overall weighted, pooled SSI rated were 17.9 infections/100 open appendectomies (95% confidence interval [CI] 10.4–25.3 infections/100 open appendectomies) and 8.8 infections/100 laparoscopic appendectomies (95% CI 4.5–13.2 infections/100 laparoscopic appendectomies). The SSI rates were higher in complicated appendicitis and when pre-operative antibiotic use was not specified.

Conclusions:

Observed SSI rates after appendectomy in LMHDICs are dramatically higher than rates in high Human Development-Index Countries. This is particularly true in cases of open appendectomy, which remains the most common surgical approach in LMHDICs. These findings highlight the need for SSI prevention in LMHDICs, including prompt access to medical and surgical care, routine pre-operative antibiotic use, and implementation of bundled care packages and checklists.

Acute appendicitis is a commonly encountered surgical emergency worldwide, and early intervention produces better outcomes [1, 2]. Ruptured appendicitis, a complication of delayed presentation, is associated with longer hospital stays, higher complication rates, and deaths [3, 4]. In low and middle Human Development-Index Countries (LMHDICs), late presentation and poor access to healthcare facilities may contribute to more severe presenting illness than in high Human Development-Index Countries (HHDICs) [5, 6].

Appendectomy can be performed as an open procedure or laparoscopically. Laparoscopic appendectomy is associated with lower rates of post-operative surgical site infections (SSIs), as well as better cosmesis, decreased post-operative pain, and shorter hospital stays [7, 8]. However, laparoscopic appendectomy also is associated with longer operating time, potentially higher cost to the hospital or patient, and higher rates of post-operative intra-abdominal abscess [7, 8]. Whereas laparoscopic appendectomy is now routine in HHDICs, open appendectomy continues to be the operation of choice in many LMHDICs. The advantages of laparoscopic appendectomy in resource-poor areas remains controversial, and SSIs are a well-documented complication of appendectomy, irrespective of surgical technique [3, 9].

Given the worldwide distribution of acute appendicitis, management of this disease entity has been used to assess and compare surgical quality, particularly in LMHDICs [3, 5]. Such infections may be a particularly useful metric by which to gauge access to and quality of general surgery care for healthcare providers and funding entities. The goal of this study was to review the literature on appendectomy in LMHDICs and describe the baseline post-appendectomy SSI rates observed in these settings.

Patients and Methods

We performed a systematic review of the literature describing the incidence and management of SSIs after appendectomy in LMHDICs. This review was registered prospectively in the Prospero database (Project No. 42016036658) in accordance with the Preferred Reporting Items for Systematic reviews and Meta-Analyses (PRISMA) guidelines. The PubMed, Ovid, and Web of Science databases were searched using the terms “appendicitis,” “appendectomy,” and “appendicectomy,” both alone and in combination with the countries of interest (Supplement 1). The countries included in the search terms were those recognized by the low or middle Human-Development Index by the United Nations Development Programme (UNDP) 2015 [10]. The LMHDI designation is a composite index focusing on three dimensions of human development: Life expectancy at birth, mean and expected years of schooling, and gross national income per capita [10]. All studies published between January 2000 and March 2016 found through the search criteria were included for initial review to ensure capture of all relevant papers. Studies not written in English were translated using Google Translate and included for further review.

Initial titles and abstracts from all three databases were screened for duplicates and then reviewed for relevance prior to obtaining full-text manuscripts. Eligible articles were reviewed independently by two blinded reviewers, who each evaluated the following criteria: Study location, type of study, sample size, patient age, gender, type of appendectomy, severity of appendicitis, frequency of SSI, grade of infection, use of prophylactic antibiotics, microbiological profile, morbidity and mortality rates of infection, need for re-operation, and cost of infection. Disagreement between reviewers was resolved through discussion with a third reviewer. Exclusion criteria included abstracts without full text available, studies that did not specify whether SSIs occurred, and studies describing only pediatric patients (defined as those ≤18 years of age). Complicated appendicitis was defined as perforated appendicitis, an associated abscess, or feculent peritonitis. Missing data were requested from study authors and incorporated when available. Additional studies were sought by examining the bibliographies of all studies identified during the search.

Established definitions for superficial, deep, and organ-space SSIs were used [11, 12]. For the qualitative analysis, we did not set a sample size minimum, as we did not expect to find a large number of papers. For the quantitative analysis, studies with fewer than 30 patients were excluded in concordance with the rule-of-threes sample size based on an assumed infection rate of 10% in these settings [13, 14]. For studies for which sub-populations were described, the laparoscopic and open surgery sub-groups were considered independently. Studies that did not specify which surgical procedure was performed were included in the open surgery group. Weighted pooled SSI rates and 95% confidence intervals (CIs) were calculated from the studies that met the minimum sample size requirement. Statistical analysis was performed using STATA^® (Version 14.1). This was determined to be an Institutional Review Board-exempt study, as all articles were publically available.

Results

The initial database search identified 423 abstracts (Fig. 1). Three hundred fifty-two remained after 71 duplicates were removed. Two hundred forty-five studies were excluded for non-relevance. Complete manuscripts were obtained for the remaining 107 papers (25% of the total). Of these, 72 were then excluded for the following reasons: SSI data not specific to appendectomy (n = 26), no SSI data (n = 21), pediatric sample (n = 15), unable to locate full text (n = 3), pregnant patients only (n = 3), duplicative study (n = 1), human immunodeficiency virus-infected patients only (n = 1), case report (n = 1), and patients with sickle cell disease only (n = 1). Thirty-five studies thus met the inclusion and exclusion criteria and were included in the qualitative synthesis (Table 1) [4, 5, 9, 15 –46].

FIG. 1.

Preferred Reporting Items for Systematic reviews and Meta-Analyses (PRISMA) diagram of reports describing appendectomy in low and middle Human Development-Index countries, 2000–2016.

Table 1.

Manuscripts Describing Appendectomy in Low and Middle Human Development-Index Countries Worldwide, 2000–2016

Study	Source	Design	Country	Surgical Approach	Sample No.	All SSI (%)	Deep/Organ Space (%)
Appendicitis and its surgical management experience at the University of Maiduguri Teaching Hospital Nigeria	Ali et al. 2012 [20]	Retrospective observational	Nigeria	Open only	1,257	455 (36)	48 (4)
Acute appendicitis in the developing world is a morbid disease	Kong et al. 2015 [5]	Retrospective observational	South Africa	Both open and laparoscopic	1,004	146 (15)	NR
An audit of appendicitis and appendicectomy in Kumasi, Ghana	Ohene-Yeboah et al. 2006 [28]	Prospective cohort	Ghana	Open only	638	200 (31)	36 (6)
Does Ochsner-Sherren regimen still hold true in the management of appendicular mass?	Cunnigaiper et al. 2010 [25]	Retrospective cohort	India	Both open and laparoscopic	506	7 (1)	NR
Audit of appendicectomies at Frere Hospital, Eastern Cape	Rogers et al. 2008 [39]	Retrospective observational	South Africa	Open only	436	31 (7)	NR
Evaluation of postoperative antibiotics after non-perforated appendectomy	Rafiq et al. 2015 [14]	Randomized	Pakistan	Open only	390	33 (8)	NR
A clinicopathological review of 324 appendices removed for acute appendicitis in Durban, South Africa: a retrospective analysis	Chamisa et al. 2009 [26]	Retrospective observational	South Africa	Both open and laparoscopic	324	101 (31)	3 (1)
Video-assisted laparoscopic extracorporeal appendectomy versus open appendectomy	Malik et al. 2009 [27]	Prospective case-control	Pakistan	Both open and laparoscopic^a	283	36 (13)	9 (3)
Surgical wound infection surveillance in general surgery procedures at a teaching hospital in Pakistan	Pishori et al. 2003 [45]	Prospective observational	Pakistan	Not specified	281	7 (2)	NR
Laparoscopic versus open appendectomy in West Bengal, India	Utpal et al. 2005 [30]	Randomized	India	Both open and laparoscopic^a	279	29 (10)	NR
Acute appendicitis in Lagos: a review of 250 cases	Fashina et al. 2009 [38]	Prospective observational	Nigeria	Open only	250	25 (10)	NR
Three none: A new technique for open appendectomy. Prospective non-randomized comparative study	Hussain et al. 2008 [44]	Prospective non-randomized	Yemen	Open only	240	18 (8)	NR
Laparoscopic versus open appendectomy in acute appendicitis	Batajoo et al. 2012 [34]	Retrospective cohort	Nepal	Both open and laparoscopic^a	226	18 (8)	NR
Laparoscopic appendectomy in complicated appendicitis: Is it safe?	Mohamed et al. 2013 [43]	Retrospective cohort	Egypt	Both open and laparoscopic	214	47 (22)	NR
Acute appendicitis in elderly patients: a challenge for surgeons	Pokharel et al.2011 [36]	Retrospective cohort	Nepal	Both open and laparoscopic	200	25 (13)	4 (2)
Pattern of acute appendicitis in Mekelle, Ethiopia	Hagos et al. 2015 [15]	Retrospective observational	Ethiopia	Not specified	196	49 (25)	NR
Appendicitis at Kenyatta National Hospital, Nairobi	Chavda et al. 2005 [29]	Prospective observational	Kenya	Open only	189	20 (11)	2 (1)
Laparoscopic versus open appendectomy: a comparison of primary outcome measures.	Khalil et al. 2011 [23]	Randomized	Pakistan	Both open and laparoscopic^a	147	11 (7)	NR
Acute appendicitis in the public and private sectors in Cape Town, South Africa	Yang et al. 2015 (4)	Prospective cohort	South Africa	Both open and laparoscopic	134	29 (22)	NR
Appendicitis in University of Port Harcourt Teaching Hospital, Nigeria	Dodiyi-Manuel et al. 2012 [22]	Retrospective observational	Nigeria	Open only	130	13 (10)	1 (1)
Frequency of wound infections in non-perforated appendicitis with use of single dose preoperative antibiotics	Ali et al. 2015 [33]	Prospective observational	Pakistan	Open only	121	7 (6)	NR
Laparoscopic appendicectomy for complicated appendicitis: is it safe and justified: a retrospective analysis	Khiria et al. 2011 [24]	Retrospective observational	India	Both open and laparoscopic^a	119	20 (17)	13
Laparoscopic appendectomy in a Nigerian teaching hospital	Adisa et al. 2012 [8]	Retrospective cohort	Nigeria	Both open and laparoscopic	114	9 (8)	2 (2)
Acute appendicitis in Olabisi Onabanjo University Teaching Hospital Sagamu, a three year review	Ayoade et al. 2006 [40]	Retrospective observational	Nigeria	Open only	113	16 (14)	1 (1)
A review of appendicectomy in Sokoto, North-western Nigeria	Mungadi et al. 2004 [31]	Retrospective observational	Nigeria	Open only	113	13 (12)	3 (3)
Acute appendicitis in a Kenyan rural hospital	Willmore et al. 2001 [32]	Retrospective observational	Kenya	Not specified^b	112	25 (22)	NR
Laparoscopic appendicectomy at the Aga Khan Hospital, Nairobi	Patel et al. 2003 [42]	Retrospective observational	Kenya	Laparoscopic	106	9 (8)	NR
Single-incision lift laparoscopic appendicectomy: a less expensive technique easy to learn	Gnanaraj et al. 2015 [16]	Retrospective observational	India	Laparoscopic only	104	7 (7)	NR
Comparison of rate of surgical wound infection, length of hospital stay and patient convenience in complicated appendicitis between primary closure and delayed primary closure	Khan et al 2012 (35)	Randomized	Pakistan	Open only	100	9 (9)	NR
A comparison between presenatation time and delay in surgery in simple and advanced appendicitis	Fahim et al. 2005 (41)	Prospective cohort	Pakistan	Not specified^b	96	13 (14)	NR
Short hospital stay after appendicectomy	Adesunkanmi et al. 2011 (37)	Prospective observational	Nigeria	Open only	78	7 (9)	2 (3)
Laparoscopic assisted appendicectomy in District Hospital, Joypurhat, Bangladesh	Bashar et al. 2014 (17)	Randomized	Bangladesh	Both open and laparoscopic	73	6 (8)	NR
Minilaparoscopic appendectomy using a new spiral needle	Lasheen et al. 2014 (18)	Prospective non-randomized	Egypt	Laparoscopic only	70	4 (6)	NR
Comparative study of laparoscopic versus open appendicectomy	Gundavda et al. 2012 (19)	Randomized	India	Both open and laparoscopic^a	60	7 (12)	NR
Acute appendicitis in the elderly; Pakistan Ordnance Factories Hospital, Wah Cantt. Experience	Salahuddin et al. 2012 (21)	Prospective observational	Pakistan	Both open and laparoscopic	36	9 (25)	1 (3)

Studies with sufficient data to enable sub-group analysis.

Studies where laparoscopic versus open cases were not specified but assumed to be open.

SSI = surgical site infection.

Of the 35 studies included in the qualitative analysis, 18 (51%) were prospective. Eighteen (51%) were observational studies, 8 (23%) were cohort, 6 (17%) were randomized interventions, 2 (6%) were non-randomized interventions, and 1 (3%) was a case-control study. More than half (n = 18; 51%) were conducted in African countries, 9 (26%) were carried out in Eastern Mediterranean countries, and the rest (n = 8; 23%) were conducted in Southeast Asian countries. The most commonly represented African countries were Nigeria (n = 7; 20%), South Africa (n = 4; 11%), and Kenya (n = 3; 9%). Thirty-two studies (91%) reported data from a single institution.

Twenty-three of the studies (66%) described patients who underwent open appendectomy, whereas only three studies (9%) considered exclusively patients undergoing laparoscopic appendectomy. There were seven studies (20%) that evaluated both types of intervention where the laparoscopic and open surgery sub-populations could be analyzed independently. Two studies (6%) did not specify whether laparoscopic or open appendectomy was the surgical procedure performed. These were included in the open appendectomy group. None of the studies reviewed provided data regarding the specific pathogens responsible for SSIs. Only two of the 35 papers (6%) provided data regarding the cost of managing SSIs in these LMHDI country settings. All of the studies used for the qualitative analysis had 30 or more patients, so none was excluded from the quantitative analysis.

For the quantitative analysis, the open and laparoscopic appendectomy groups were analyzed independently. The 25 studies describing predominantly open appendectomies and seven studies describing sub-populations of patients undergoing open appendectomy comprised 7,834 patients. Among the 7,089 patients with sex data reported, 3,592 (51%) were male.

A total of 1,400 SSIs were reported. The overall weighted, pooled SSI rate was 17.9 infections/100 open appendectomies (95% CI 10.4–25.3 infections/100 open appendectomies; Table 2). Of the studies that specified the depth of involvement, there were 801 (75%) superficial SSIs and 272 (25%) deep or organ-space SSIs. A total of 39 deaths were reported from 18 studies, which corresponds to an overall weighted, pooled SSI rate of 0.8 fatal infections/100 open appendectomies (95% CI 0.4–1.2 deaths/100 open appendectomies). Among these deaths, 29 were specified as resulting from generalized peritonitis secondary to perforated appendicitis and resultant multi-organ dysfunction.

Table 2.

Surgical Site Infection Rate After Appendectomy by Type of Appendectomy, Type of Appendicitis, and Use of Antibiotics Worldwide, 2000–2016

Subgroup	No. of Studies	Pooled SSI Rate (%)	95% CI	P
Type of surgery
Laparoscopic	10	8.8	4.5–13.2	<0.001
Open	32	17.9	10.4–25.3
Type of appendicitis
Uncomplicated	6	10.5	0–23.9
Complicated	7	24.9	8.5–41.2	<0.001
Pre-operative antibiotics
Always given	19	13.6	8.9–18.2	<0.001
Not specified	16	18.9	8.0–29.7

CI = confidence interval; SSI = surgical site infection.

The three studies describing exclusively patients who underwent laparoscopic appendectomy and seven studies describing sub-populations of patients undergoing laparoscopic appendectomy comprised 896 patients. Among the 797 patients with sex data reported, 491 (62%) were male; thus, there were significantly fewer female patients in the laparoscopic group (p < 0.001). A total of 79 SSIs were reported. The overall weighted, pooled SSI rate was 8.8 infections/100 laparoscopic appendectomies (95% CI 4.5–13.2 infections/100 laparoscopic appendectomies; Table 2). This weighted, pooled SSI rate was significantly lower than that in patients undergoing open appendectomy (p < 0.001). In the five laparoscopic studies that specified the depth of involvement, there were 37 (70%) superficial SSIs and 16 (30%) deep or organ-space SSIs. This frequency of superficial SSI was not significantly lower in laparoscopic surgery than in open surgery (p = 0.5). There were no peri-operative deaths in the laparoscopic surgery group.

Of the 27 studies that described the frequency of complicated and uncomplicated appendicitis, only nine had sufficient detail to allow sub-group analysis: three studies reported only cases of complicated appendicitis, two studies reported only cases of uncomplicated disease, and four studies compared outcomes after operations for complicated and uncomplicated appendicitis. Among these studies, 1,974 cases were reported, of which 1,005 (51%) were complicated. The weighted, pooled SSI rate for complicated appendicitis was 24.9 infections/100 appendectomies (95% CI 8.5–41.2 infections/100 appendectomies) for complicated appendicitis compared with a weighted, pooled SSI rate of 10.5 infections/100 appendectomies for uncomplicated appendicitis (95% CI 0–23.9 infections/100 appendectomies; Table 2).

Nineteen studies specified that pre-operative antibiotics were administered; this comprised a sub-group of 5,145 appendectomy cases. The weighted, pooled SSI rate among patients who received pre-operative antibiotics was 13.6 infections/100 appendectomies (95% CI 8.9–18.2 infections/100 appendectomies). Among the remaining studies in which pre-operative antibiotic use was not specified, the weighted, pooled SSI rate was 18.9 infections/100 appendectomies (95% CI 8.0–29.7 infections/100 appendectomies, Table 2).

Discussion

Given the worldwide distribution of appendicitis, appendectomy appears to be an excellent indicator for monitoring access to and the quality of surgical care globally. It has been examined in this setting by agencies such as the World Health Organization [47]. Establishing a baseline expected frequency of SSI after both open and laparoscopic appendectomy in these settings is critical for grading the success of future improvement efforts.

Following appendectomy in HHDICs, published SSI rates range from 1.3–3.8 infections/100 appendectomies for open operation and 0.8–2.9 infections/100 appendectomies for laparoscopic procedures [48 –51]. The weighted, pooled SSI rate of 17.9 infections/100 open appendectomies, identified from the LMHDIC studies in this analysis, is substantially higher than the HHDIC rate. Even after laparoscopic appendectomy in LMHDICs, the SSI rate was notably higher than in HHDICs at 8.8 infections/100 laparoscopic appendectomies. Some studies in HHDICs have reported higher rates of superficial SSIs after open than laparoscopic appendectomy but higher rates of intra-abdominal abscess following laparoscopic surgery [48, 49]. However, data regarding such comparative outcomes in LMHDICs are scarce; possible reasons are unavailability of such procedures, cost of cross-sectional imaging, and the infrequency of the operation. As such, consideration of this issue is outside the scope of this analysis.

The difference in SSI rates after appendectomy in HHDICs vs. LMHDICs highlights the importance of improving access to and quality of care in places where post-appendectomy SSI rates are disproportionately high. Delay in access to medical and surgical care for appendicitis can result in a greater risk of perforation prior to surgical management [52]. Supporting this is the high number of deaths resulting from sequelae of perforation. The observed mortality rate may be a result of delayed presentation and healthcare seeking, absence of effective imaging, failure of a hospital to rescue because of resource limitations, or some combination.

Consistent administration of pre-operative antibiotics in cases of acute appendicitis helps minimize SSI risk [34]. In this analysis, studies in which antibiotics were provided consistently showed a lower pooled, weighted SSI rate of 13.6 vs. 18.9 SSIs/100 appendectomies in studies where pre-operative antibiotic use was not specified. This finding underscores the potential importance of protocols and checklists in LMHDIC settings to ensure that pre-operative antibiotics are administered appropriately and in a timely fashion [53, 54].

Recently, non-operative (use of antibiotics alone) or delayed-operative (antibiotics followed by interval appendectomy once the acute inflammation and infection has resolved) management for both uncomplicated and complicated appendicitis has become increasingly common in HHDICs. Non-operative management inherently decreases the rate of SSIs [55, 56]. The optimal role for non- or delayed-operative management of appendicitis in LMHDICs has yet to be determined. Although such a strategy may seem ideal in resource-poor settings where surgical resources are limited, there are several factors complicating this assumption. First, patients treated non-operatively need to be carefully and appropriately selected, yet imaging capabilities can be limited in LMHDICs. Second, antibiotic use and the availability and quality of supportive services may be disparate. Third, reliable follow-up must be built into patient care algorithms. This often is not possible in LMHDICs, where the catchment area of a single medical facility may be hundreds of miles. Finally, there should be access to adequate surgical care for cases where non-operative or delayed-operative treatment fails.

There are multiple limitations to this study. There is selection bias, as only 11 LMHDI countries were captured. This may limit the generalizability of these findings to other LMHDI countries and regions. Second, publication bias also is likely, as surgeons may avoid publishing data showing very high rates of SSIs. Third, many of the studies did not distinguish between superficial and deep or organ-space infections; it is possible that superficial SSIs that did not require intervention would be reported infrequently, reducing the overall reported rate of SSI. Fourth, many studies did not specify whether their patient populations received pre-operative antibiotics. Although it is likely that most of the studies not reporting pre-operative antibiotic use did in fact not use them, some studies may have used pre-operative antibiotics, which would decrease the rate of infection. Fifth, the paucity of data on laparoscopic appendectomy decreases the ability to compare this sub-group with open appendectomy cases. Finally, studies with calculated odds ratios rarely reported enough data on patient populations, negating our ability to calculate pooled odds ratios.

Conclusions

Appendectomy is a common surgical procedure globally. This study describes the best available current evidence on the rate of SSIs after appendectomy in LMHDICs, which is substantially higher than that in HHDICs. These findings highlight the need for SSI prevention measures in LMHDICs, including prompt access to medical and surgical care, routine pre-operative antibiotic use, and adequate implementation of protocols and checklists. The role of laparoscopy as well as non-operative management with antibiotics in LMHDICs has yet to be determined. The SSI rate after appendectomy remains a valuable metric to evaluate the access to and quality of surgical care worldwide.

Footnotes

Author Disclosure Statement

No competing financial interests exist for any of the authors.

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