Splenic injuries following upper endoscopic procedures: a systematic review of cases

Introduction

Background

The spleen is a highly vascularized, intraperitoneal organ found in the left upper quadrant (LUQ) of the abdomen, underlying ribs 9–11. Splenic injuries can occur when forces, whether penetrating, blunt, or indirect, disrupt the splenic capsule or associated blood vessels. These injuries can result in significant arterial bleeds that may go undetected due to the large holding capacity of the peritoneum (1). Although splenic injuries are most commonly due to traumatic events, such as motor vehicle accidents, falls, or gunshot wounds, they can also be iatrogenic (1). Iatrogenic injuries can result from indirect forces sustained in abdominal procedures such as colonoscopies, colectomies and nephrectomies (2). Of these procedures, colonoscopy has been the most widely reported and studied cause.

Rationale and knowledge gap

Splenic injury following upper endoscopic procedures is an exceedingly rare complication that has been documented primarily through case reports. Upper endoscopic procedures include esophagogastroduodenoscopy (EGD), endoscopic ultrasound (EUS), and endoscopic retrograde cholangiopancreatography (ERCP). These procedures are generally well tolerated with a low rate of complications. The majority of EGD and EUS complications are sedation-related, but can also include perforation of the gastrointestinal tract, bleeding, and infection (3). In addition to the above complications, ERCP can also cause acute pancreatitis and cholangitis (4). While splenic injuries following colonoscopies have been thoroughly investigated (5), less is known about the clinical course of splenic injuries following upper endoscopic procedures. Various mechanisms of injury have been proposed, with the most common being that the endoscope may damage the spleen when direct or sheering forces are transmitted through the greater curvature of the stomach, particularly when the scope is held in a tense, bowed position, such as when intubating the pylorus (6,7).

Objective

We seek to perform a systematic review of case reports and series documenting splenic injuries following upper endoscopic procedures to explore potential commonalities in cases by comparing the patient characteristics, clinical presentations, modes of diagnosis, treatment modalities, and outcomes. To our knowledge, this will be the first systematic review of cases of splenic injury following upper endoscopic procedures. Although this complication is rare, we hope that our review will raise awareness of these injuries and elucidate their typical presentation and management. We present this article in accordance with the PRISMA reporting checklist (8) (available at https://tgh.amegroups.com/article/view/10.21037/tgh-24-93/rc).

Methods

The protocol for this study was prospectively registered with PROSPERO (ID: CRD42023445504).

Eligibility criteria

Studies were included if they were case reports or case series, including conference abstracts, that were published in English and documented a splenic injury following an upper endoscopic procedure.

Studies were excluded if they were not published in English; dealt with splenic injuries not following an upper endoscopy procedure, including colonoscopy; documented a later complication of an upper endoscopic procedure, such as a migrating stent; not case reports or case series, such as review articles, database studies, etc.

Information sources and search strategy

A systematic search of literature was conducted on PubMed, Embase, and Web of Science for cases of splenic injury following an upper endoscopic procedure. The dates searched were inception to 14 July 2023. We used the terms ‘splenic rupture’ or ‘splenic hematoma’ or ‘splenic injury’ or ‘splenic tear’ or ‘splenic laceration’ and ‘endoscopy’ or ‘esophagogastroduodenoscopy’ or ‘endoscopic retrograde cholangiopancreatography’ or ‘endoscopic ultrasound’ for our search. We also included Medical Subject Headings (MeSH terms). The reference lists of included studies were searched by hand to look for additional eligible studies.

Selection process

The studies obtained through our search were imported into Covidence, which automatically screened for duplicates (9). Two independent researchers (B.J.B. and A.J.T.) screened the title and abstracts of studies, excluding irrelevant ones. The same two researchers then screened the full-texts of the remaining studies, examining their adherence to eligibility criteria. Disagreements during the screening process were settled through discussion, with a third author (B.M.B.) available to resolve any persistent disagreements.

Data collection process and data items

Two independent researchers (B.M.B. and B.J.B.) then extracted data from included studies, consisting of the basic characteristics of included studies and a description of the subsequent clinical course. The last name of the first author, year of publication, country where the case report came from, demographics of the patient(s) the reports centered around (including age, gender, and history of chronic pancreatitis or prior abdominal procedures), and the type of upper endoscopic procedure and its indication were the basic characteristics of interest. Clinical course included: reported procedural difficulty, time since procedure that symptoms developed; specific splenic injury; presenting symptoms; diagnostic modality that identified the splenic injury; treatment; and final outcome for the patient.

Study risk of bias assessment

The Joanna Briggs Institute (JBI) critical appraisal tools for case reports was used to assess the quality of included studies (10). This tool assesses the comprehensiveness of detail inclusion by the case report across eight domains: demographics of the patient; patient’s history; current clinical condition of the patient; diagnostic tests or assessment methods and their results; intervention or treatment procedures; post-intervention clinical condition; adverse or unanticipated events; and take-away lessons. Each question was answered for all included reports as either “Yes”, “No”, “Unclear”, or “Not Applicable”. Case series were treated as separate individual case reports for the purpose of bias assessment. Studies with ≤1 domain receiving “No” were determined to be high quality and at low risk of bias, while those receiving 2 domains were deemed intermediate. Studies with ≥3 domains receiving “No” were determined to be low quality and at high risk of bias.

Effect measures and synthesis methods

Due to the cases coming from different facilities, variations in the data reported were observed. To account for these variations, frequencies were calculated using the number of studies that reported the specific parameter as the denominator, with the specific injury, symptom, diagnostic test, or treatment type as the numerator. For symptoms, all reported symptoms were used in the frequencies, representing the prevalence of all symptoms across the included cases. This differs from the reporting of the specific splenic injuries and treatment. When multiple injuries were reported, the most prominent splenic injury was used. For instance, if a case reported “splenic laceration with perisplenic hematoma”, then only splenic laceration was used. For treatment, the definitive treatment of the splenic injury was used, such as splenectomy or embolization. We excluded other aspects of the treatment course, such as blood transfusions and medications, due to the wide variation in reporting of these measures. However, cases in which no procedural treatment was utilized were reported as “conservative management”. Median, mean, and range were used for time to presentation or diagnosis, while mean, median and range were used for age.

Timing methods: only reports with explicit, numerical times to the onset of symptoms were included in the analysis, except for case reports that described an immediate onset of symptoms (these were given a time of 0 hours). Excluded from the analysis were reports of symptom onset such as “several hours later”, “soon after”, or “later that evening”. This resulted in the exclusion of 17 of the 52 cases.

Results

Study selection

The literature search yielded 2,313 articles across the three databases: PubMed (n=494), Embase (n=1,739), and Web of Science (n=80). Covidence removed 465 duplicates prior to the title and abstract screening. After screening the title and abstract of the remaining 1,848 studies, 1,707 were deemed irrelevant for the aim of this study. The full-texts of the remaining 141 studies were obtained and adherence to eligibility criteria was assessed. This resulted in the exclusion of 94 studies, with 47 being used in this review. The reasons for exclusion were: the injury occurring not after an upper endoscopic procedure, including colonoscopy (n=50); wrong study design, i.e., not a case report (n=20); duplicate articles (n=10); no splenic injury was reported (n=6); study was not in English (n=5); or the case report documented a long-term complication of an upper endoscopic procedure, such as a migrating stent (n=3). An additional 3 studies meeting inclusion criteria were identified by manual search of the reference lists of included studies, for a total of 50 studies in this review. These studies are listed in Table 1. This process is summarized in the PRISMA flowchart in Figure 1.

Figure 1 Study screening process.

Study characteristics

There were 50 total included studies. Of these, two were case series with two patients each, for a total of 52 cases (Table 1). The studies were published between 1955 and 2023. They were published in fifteen different countries, with the United States (n=27), United Kingdom (n=5), and Canada (n=3) being the most common. Three countries (Australia, Germany, and China) accounted for two reports each, while nine other countries each accounted for one.

The median age of presentation was 55 years, with a mean of 56, and a range of 21–86 years (Table 1). The reports included a roughly equal number of males (25/52) and females (27/52). Prior EGDs or ERCPs were reported in 21% of cases (11/52), while prior abdominal surgeries were reported in 31% of cases (16/52). Chronic pancreatitis was reported in 15% of cases (9/52). Of the included cases, 71% occurred following ERCP (37/52). Of the ERCPs, 81% were therapeutic (30/37) and 19% were diagnostic (7/37). The remaining procedures were upper endoscopic procedures not involving ERCP. Of these procedures, 40% were therapeutic (6/15), and 60% were diagnostic (9/15). EUS was used in 6% of cases overall (3/52).

Procedural difficulty and/or prolonged procedure times were reported in 21% of cases (11/52). Reported procedural difficulties included difficulty cannulating the common bile ducts (3/11), difficulty cannulating the hepatopancreatic ampulla (1/11), a patient moving during the procedure due to inadequate sedation (1/11), and unspecified (6/11).

Risk of bias in studies

Overall, 28 studies received a perfect score on the JBI critical appraisal tool, as they were not found to be deficient in any of the eight domains. Another 9 studies had only one domain that was found to be lacking data, for a total of 37 studies being deemed high quality with a low risk of bias. On the other hand, 2 studies were deemed to have deficiencies in three domains and another 2 across four domains, for a total of four studies that were low quality with a high risk of bias potential. The remaining 11 studies had deficiencies across two domains, placing them at intermediate quality and risk of bias.

The most commonly deficient JBI questions were questions 1 and 2, which investigate the patient’s demographics and history. These details were absent int 13 and 14 studies, respectively. This stemmed from poor or incomplete presentations of the past medical history of the patients. The third most commonly deficient was question 8, regarding whether the report provides take-home points, which were absent in 12 studies. Questions 3, 6, and 7 were found to be deficient in 4, 2, and 1 studies, respectively. Questions 4 and 5, regarding diagnostic tests and treatment interventions, were met in all studies.

Results of syntheses

The mean time to the onset of initial symptoms was 21 hours, with a median of 4 hours, and a range from 0 to 144 hours. The distribution was positively-skewed by several patients with late presentations, including two patients who presented after four days, and another who presented after six days. Across our cases, we found the occurrence of the following symptoms: 79% reported abdominal pain (41/52), 15% reported pain radiating to the left shoulder (positive Kehr’s sign) (8/52), 67% reported hypotension and/or tachycardia (35/52), and 58% reported postoperative anemia or drops in hemoglobin (30/52). The median recorded drop in hemoglobin was 4.1 g/dL (interquartile range 3.7–5.5 g/dL).

The reported modes of diagnosis were computed tomography (CT) (69%, 36/52), laparotomy (17%, 9/52), ultrasonography (10%, 5/52), and CT angiography (4%, 2/52). The reported treatment modalities were splenectomy (59%, 31/52), partial splenectomy with cystectomy (2%, 1/52), splenic artery embolization (10%, 5/52), splenic artery embolization with splenectomy (2%, 1/52), splenic artery ligation (2%, 1/52), splenic drain placement (2%, 1/52), and various modes of conservative treatment (23%, 12/52).

Full recovery occurred in 82% of cases (42/51). Complications occurred following 18% of cases (9/51). Mortality occurred following two of these cases, with a third patient documented as being in hospice following a multi-organ failure (6%, 3/51). The two cases of mortality followed splenectomy, while the multi-organ failure followed splenic artery embolization. Complications without mortality occurred in the 6 remaining cases (6/48). Of these complications, 4 followed splenectomy, with those complications being post-op PE [1], atelectasis and pneumonia [2], nosocomial pneumonia [3], and prolonged postoperative hospitalization for unspecified reasons [4]. One complication followed conservative treatment, which was splenic abscess formation. One complication followed splenic drain placement, which was recurrence of the splenic abscess that the drain was placed for. The clinical outcome wasn’t reported in one of the cases (2%, 1/52). These results are summarized in Table 2.

Reporting biases

Since the case reports came from different facilities, there was a lack of standardization in their diagnostic and procedure capabilities, which may have skewed the frequencies. Additionally, the reporting bias from so many different authors could have skewed results. Finally, because these cases represent a procedure complication, reporting bias is possible due to intentional under-reporting or misrepresentation of the case, both of which could benefit the physicians who performed the case.

Discussion

Key findings

Across 52 cases, we found a roughly equal incidence of injuries among males and females. The majority of patients were middle aged, with a mean age of 56 years, but a broad age range was represented (21–86 years old). Prior abdominal surgeries were reported in 31% of patients, prior upper endoscopic procedures in 21%, and chronic pancreatitis in 15%. Most of the cases occurred following ERCP (71%). The majority of these ERCPs were therapeutic (81%). Procedural difficulty was reported in 21% of cases. The mean time to onset of symptoms was 21 hours after the procedure ended, with a median time of 4 hours, and a range from 0–144 hours. Many cases reported an immediate onset of symptoms, while others took several days to develop any symptoms. The most common symptom was abdominal pain (79%), usually in the LUQ or epigastric region, however several cases reported generalized abdominal pain. Kehr’s sign, or pain radiating to the left shoulder, is a pathognomonic finding that was reported in a handful of cases (8%) (1). The next most common symptoms were hypotension and/or tachycardia, present in 67% of cases. These were likely reflective of the hypovolemia resulting from bleeding. Anemia or clinically significant drops in hemoglobin were reported in 58% of cases. The average recorded drop in hemoglobin was 4.34 g/dL. Nausea, vomiting, altered mental status or lethargy, diaphoresis, peritonitis, and respiratory distress were reported in a minority of cases. Many patients described worsening symptoms, or had additional symptoms appear over time. Diagnosis was obtained primarily through CT scan (69%), although some injuries were diagnosed during laparotomy (17%) or with ultrasonography (10%). The majority of injuries were treated with various types of splenectomy (63%), followed by various modes of conservative treatment (23%) and splenic artery embolization (10%). Most patients who underwent splenectomy had reported hemodynamic instability (82%). Across all cases, full recovery was reported in 81%, while complications and mortality were reported in 17% and 6%, respectively.

Strengths and limitations

One strength of our study is the relative high-quality of case reports included, as shown through the JBI critical appraisal results. A majority of studies showed no deficiencies across the eight domains, and 92% had sufficient information provided across at least six of the eight domains. Another strength is that our study had a decent sample size with 52 cases. These two factors allowed for a complete and robust analysis of the clinical course of splenic injuries following upper endoscopic procedures. We also performed a comprehensive literature search and meticulously reviewed the reference lists of included studies, likely ensuring that we included all eligible case reports that have been published to date. Further, we extracted a significant amount of data from all included studies, which allowed us to be specific and complete in the findings that we reported. Most of our variables were reported consistently and objectively across the case reports.

However, our study is also not without limitations. Given that we relied on published case reports for our data, reporting bias cannot be ignored. Further, the case reports included in our review varied greatly in terms of length and format, and some of our variables weren’t reported uniformly across cases. For example, pre- and post-operative hemoglobin was not reported in all case reports. This limited our ability to accurately depict the clinical course, as well as our ability to pursue subgroup analyses with past medical histories, procedure difficulties, age, gender, and others. Additionally, we included conference abstracts in our data analysis to increase our sample size, which may have led to an increase in bias through the JBI checklist, which assesses the completeness of case reports. Furthermore, the number of reported cases remains low given the rarity of this phenomenon, which limited our sample size. As a result, our analysis was limited to descriptive statistics. Although this review has been carried out systematically, it is important to recognize that the above factors could impact the generalizability of our findings. When considered in the framework of evidence-based medicine, systematic reviews of case reports are lower on the hierarchy of validity when compared to observational studies and randomized controlled trials (58).

Comparison with similar researches

Although this is the first systematic review of splenic injuries following all manner of upper endoscopic procedures, we can compare our results to a prior systematic review of injuries following colonoscopy (5). The colonoscopy group reported a higher proportion of patients with prior abdominal or pelvic surgeries, with 64% of cases compared to our 31%. The rate of reported procedural difficulty was slightly higher, with 35% compared to our 21%. The mean time to onset of symptoms was similar, with 16.9 hours compared to our 21 hours, with a similarly broad range. The most common symptom in both groups was abdominal pain. The trend in diagnostic modalities were similar, with most cases being diagnosed with CT, followed by laparotomy and then ultrasonography. Splenectomy was the most common treatment modality for both groups. The overall mortality rate was similar.

The potential for delayed onset of symptoms in splenic injury has now been documented for both upper endoscopic procedures, colonoscopy (59), and trauma (60). Amongst our cases, many of the patients with delayed onset of symptoms had already been discharged from the hospital following their procedures, requiring them to re-present to the office or emergency department. This was the case for one patient who presented four days after their procedure, and another for the patient who presented six days after. It’s also worth noting that we analyzed the time to the onset of any symptoms, rather than the time to presentation, maximal symptoms, or diagnosis. Many cases described a gradual progression of symptoms with some symptoms only appearing later in the course. The large variability in symptom onset and progression, including the potential for a significantly delayed onset, contributes to the overall challenge in diagnosing these injuries.

Explanations of findings

While the precise mechanism underlying splenic injuries during these procedures is unknown, several mechanisms have been proposed. These injuries may result from excessive forces being placed on the greater curvature of the stomach by the endoscope in the long position, especially when intubating the pylorus, which can cause the scope to adopt a tense, bowed position (6,7). The scope can then transmit forces either directly to splenic tissues or transmit shearing forces across surrounding tissue. These forces have the potential to avulse the nearby splenic vasculature or damage the splenic capsule. This phenomenon is more likely to occur when operators have trouble advancing into the duodenum, causing them to make repeated attempts at entry or employ greater amounts of force. The injuries might also result from excessive torquing of the scope when intubating the ampulla during ERCP (31).

It has been suggested that the risk for splenic injury may increase with procedural difficulty or prolonged procedure times, especially when the scope is being held in the long position for greater lengths of time (6,7,54). However, in our review, just 21% of cases reported procedural difficulty or prolonged procedure times. It is possible that procedural difficulty or prolonged procedure times have been under-reported in the literature, however several cases explicitly denied having either risk factor. This could suggest that the damaging maneuvers are too subtle to be perceived by the operators.

Another risk factor that has been proposed is chronic pancreatitis, which can result in the calcification and fibrosis of suspensory ligaments between the pancreas and spleen (26,43,54). This can reduce the relative mobility of the stomach and spleen, causing forces to be translated more readily between the two. Our review found that 15% of patients had a reported history of chronic pancreatitis. Prior abdominal surgeries have been implicated for similar reasons, due to their ability to cause intra-abdominal adhesions that reduce the mobility of the spleen (26,43,54). These surgeries also have the potential to alter the intra-abdominal anatomy, which can result in longer procedure times and the need for greater manipulations of the endoscope. Our review found that 31% of patients had a reported history of intra-abdominal surgeries. However, it’s possible that these factors are merely coincidental, as patients with histories of chronic pancreatitis or intra-abdominal procedures are more likely to undergo upper endoscopic procedures at baseline.

The diagnostic modality of choice for splenic injuries is a CT scan. Ultrasonography can also be used, and is often employed in trauma settings as a rapid screening tool that can be followed by CT. However, ultrasound is less sensitive overall, and can fail to detect splenic injuries without significant intraperitoneal fluid or visibly distorted architecture (61,62). Ultrasound was used to make the diagnosis in just 10% of our cases.

Splenic injuries can be graded from 1 to 5, in order of increasing severity. Grade 1 corresponds to a laceration of the splenic capsule <1 cm in depth, or a hematoma involving less than 10% of the surface area. Grade 2 is a laceration 1–3 cm in depth, or a hematoma involving 10–50% of the surface area. Grade 3 is either a laceration >3 cm in depth, a laceration involving a trabecular blood vessel, a hematoma of >50% of the surface area, a hematoma expanding over time, or a hematoma that has ruptured. Grade 4 is a laceration of a hilar or segmental blood vessel with either partial devascularization, or involvement of >25% of the spleen. Grade 5 is a ruptured or entirely devascularized spleen (1). Many cases reported splenic rupture, which would qualify as a grade 5 injury automatically. However, the majority of cases reporting splenic lacerations or hematomas failed to comment on the depth of the laceration, or the surface area of the hematoma, making them ineligible for grading. Due to the inconsistencies in reporting, no further analysis of the relationship between injury grade and other variables was pursued.

Splenic injuries can be treated conservatively, operatively, or through splenic artery embolization. Splenectomy is generally indicated for patients with hemodynamic instability, signs of peritonitis, and active bleeding (1). Splenic artery embolization is an endoscopic intervention that may be used to reduce splenic perfusion pressure and bleeding, either in preparation for splenectomy or as a standalone measure (63). The latter represents a less invasive treatment option that can preserve splenic tissue due to the organ’s collateral blood flow (63). Standalone embolization may be performed for hemodynamically stable patients with moderate-to-severe splenic injuries (grades 3–5) with ongoing bleeding (1). Stable patients with low-grade splenic injuries can be treated conservatively, with serial abdominal exams and transfusions as-needed (1).

Implications and actions needed

Clinicians should keep splenic injury in their differential when assessing patients with abdominal pain and/or hemodynamic instability in the setting of a recent upper endoscopic procedure. While many cases noted a prompt or immediate onset of symptoms, there was significant variability in the onset of symptoms, with some patients presenting as late as six days post-procedure. We hope that our findings will assist clinicians in diagnosing and treating this rare complication of upper endoscopic procedures, as delays in diagnosis can cause significant morbidity and mortality. Future studies should attempt to find a precise mechanism for these injuries, which could help clinicians avoid damaging maneuvers during endoscopy. Given the rarity of these injuries, the unclear mechanism of injuries, and the overall limitations of our study, we are limited in our ability to suggest preventative strategies or procedural modifications. However, our research suggests that patients may benefit from shorter procedural times and the avoidance of tension-inducing maneuvers or repeated attempts at duodenal cannulation, whenever possible for operators. Further delineation of risk factors could help identify patients at a higher-risk for these injuries, which could assist with their diagnosis. Finally, future studies could analyze the outcomes of various treatment modalities, including surgical splenectomy, splenic artery embolization, or conservative management, with the hopes of establishing formal guidelines for treatment.

Conclusions

To our knowledge, this is the first systematic review of the clinical course of splenic injuries following upper endoscopic procedures. Although rare, this complication should be reviewed due to its potential for morbidity and mortality. Clinicians should consider these injuries in patients presenting with post-operative abdominal pain, signs of hemodynamic instability, or acute drops in hemoglobin. Increased suspicion should be given to patients with a history of chronic pancreatitis, prior abdominal surgeries, or who underwent prolonged or technically difficult procedures. Prompt diagnosis can allow for successful treatment via splenectomy, splenic artery embolization, or conservative measures.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the PRISMA reporting checklist. Available at https://tgh.amegroups.com/article/view/10.21037/tgh-24-93/rc

Peer Review File: Available at https://tgh.amegroups.com/article/view/10.21037/tgh-24-93/prf

Funding: None.

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://tgh.amegroups.com/article/view/10.21037/tgh-24-93/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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