Objective
We sought to analyze the published literature on bowel injuries in patients undergoing gynecologic robotic surgery with the aim to determine its incidence, predisposing factors, and treatment options.
Data Sources
Studies included in this analysis were identified by searching PubMed Central, OVID Medline, EMBASE, Cochrane, and ClinicalTrials.gov databases. References for all studies were also reviewed. Time frame for data analysis spanned from November 2001 through December 2014.
Study Eligibility Criteria
All English-language studies reporting the incidence of bowel injury or complications during robotic gynecologic surgery were included. Studies with data duplication, not in English, case reports, or studies that did not explicitly define bowel injury incidence were excluded.
Study Appraisal and Synthesis Methods
The Guidelines for Meta-Analyses and Systematic Reviews of Observational Studies were used to complete the systematic review with the exception of scoring study quality and a single primary reviewer.
Results
In all, 370 full-text articles were reviewed and 144 met the inclusion criteria. There were 84 bowel injuries recorded in 13,444 patients for an incidence of 1 in 160 (0.62%; 95% confidence interval, 0.50–0.76%). There were no significant differences in incidence of bowel injury by procedure type. The anatomic location of injury, etiology, and management were rarely reported. Of the bowel injuries, 87% were recognized intraoperatively and the majority (58%) managed via a minimally invasive approach. Of 13,444 patients, 3 (0.02%) (95% confidence interval, 0.01–0.07%) died in the immediate postoperative period and no deaths were a result of a bowel injury.
Conclusion
The overall incidence of bowel injury in robotic-assisted gynecologic surgery is 1 in 160. When the location of bowel injuries were specified, they most commonly occurred in the colon and rectum and most were managed via a minimally invasive approach.
Introduction
Gynecologic indications are among the most common reasons for surgery in the United States, with approximately half a million hysterectomies conducted every year. Minimally invasive surgery (MIS) has become a common approach when performing gynecologic surgeries based on evidence that it is associated with less postoperative pain, faster return of bowel function, lower intraoperative blood loss, fewer wound infections, and shorter length of hospital stay. Robotic surgery is currently a standard approach when performing minimally invasive procedures for both benign and oncologic indications.
One of the potential complications associated with MIS is bowel injury. Bowel injury during abdominal entry for laparoscopy may be difficult to recognize or repair, and delayed treatment of these injuries can be fatal. The rate of such complications is usually increased in patients with a history of multiple prior surgeries where the risk of adhesion formation increases substantially and in morbidly obese patients. Most common bowel injuries occur upon initial trocar entry; however, other injuries may occur from bowel dissection during lysis of adhesions, from thermal injury when using monopolar or bipolar energy, or from inadequate tissue tension during dissection. Unfortunately, a high percentage of bowel injuries go unrecognized at the time of surgery and thus lead to significant morbidity or even mortality. Although it is difficult to establish accurate numbers on the rate of bowel injury during MIS, it is estimated that over all gynecologic procedures, it occurs in 1 of 769 conventional laparoscopic gynecologic surgeries and the associated case fatality rate (number of deaths per bowel injury) is 1 in 125 women.
A recent report evaluated the incidence of bowel injury in nonrobotic gynecologic laparoscopy. In that study, the authors compiled data from 90 studies totaling 474,063 patients. The incidence of bowel injuries was 0.13%. The rate of bowel injury specifically after hysterectomy was 1 in 256 cases. The authors found that the small intestine was the most frequently damaged portion of the gastrointestinal tract and that most bowel injuries occurred during abdominal access and insufflation. Delayed recognition of bowel injury occurred in 375 of the 604 injuries, and all of the 5 deaths were attributed to delayed recognition of bowel injury.
To date, there is a paucity of data regarding the rate of bowel injuries specifically associated with robotic gynecologic surgery. The purpose of our review was to analyze all the published literature on bowel injuries when performing robotic surgery for gynecologic procedures with the ultimate goal to determine its incidence, predisposing factors, and potential treatment options.
Materials and Methods
Sources
We conducted a systematic review of robotic gynecologic surgery by searching PubMed Central, OVID Medline, EMBASE, the Cochrane database, and ClinicalTrials.gov databases. Searches were conducted using the terms “robotic” or “robotics,” “intraoperative complications” or “postoperative complications” or “intestinal perforation” or “bowel injury” or “colon injury,” and “gynecologic surgical procedures.” Searches were limited to English-language articles, without restriction on initial publication date and published from November 2001 through December 31, 2014. There were no initial limitations in regards to study design. Additional studies were deemed relevant by reviewing the references of included articles.
Study selection
The Guidelines for Meta-Analyses and Systematic Reviews of Observational Studies (MOOSE) was used to complete the systematic review with the exception of scoring study quality and a single primary reviewer. The identified abstracts and the additional references were reviewed by one of the authors (T.P., a gynecology resident) for inclusion. Another author (N.L.S., a senior epidemiologist) also reviewed a subset (n = 82) of abstracts and articles that the data abstractor (T.P.) found questionable; full agreement on the decision regarding inclusion occurred. N.L.S. also reviewed all included articles for a subset of analyzed indices. Manuscript authors were not contacted.
Abstracts were evaluated for relevance after identification utilizing the search criteria listed above. Articles were included if they were published in refereed journals and mentioned bowel or colon injury or gynecologic surgical complications in the title and/or abstract. The full text of relevant abstracts was then reviewed in detail. For inclusion in the review, articles had to report the incidence of injury to the gastrointestinal tract. If articles commented on multiple other complications but did not include bowel injuries, it was assumed no bowel injuries occurred. Articles only including isolated complications (ie, cystotomy) that were not bowel injuries were excluded.
In the articles included in the review, bowel injury definitions varied, together with but not limited to: serosal abrasion, bowel perforation or tear, enterotomy, or bowel injuries for which the details were not further specified. We report on all of the cases as best possible, although details such as surgical indication, etiology, and management were not specified for most of the study subjects experiencing injury. The authors were not contacted to more precisely categorize these indices because the lack of original manuscript specificity reflects information that was either unavailable to them or that was not abstracted or recorded by them. Articles using national databases, case reports, data presented in review articles, and duplicate data presented in multiple manuscripts were also excluded to avoid double-counting.
Fisher exact test and odds ratios (OR) with 95% confidence intervals (CIs) are presented for all incidence rate comparisons given the varied study designs and uncommon occurrence of bowel injury. The Wilson method for proportions was used to calculate 2-tailed 95% CIs and P values for incidence. As surgical procedure and anatomic location play such potentially important roles in the incidence of bowel injury, exact OR are presented for analyses stratified by these variables, using the most precise classifications possible based on the reviewed articles, comparing the incidence rates to the most common procedure (which was procedures not otherwise specified), with P ≤ .05 considered statistically significant. The data were also analyzed by study design. All analyses were conducted using Stata (Version 11.0; StataCorp, College Station, TX) except for basic incidence rates that were calculated using the Excel (Microsoft Corp, Redmond, WA)data abstraction database for which 2 authors (T.P. and N.L.S.) developed a variable-specific coding scheme.
Materials and Methods
Sources
We conducted a systematic review of robotic gynecologic surgery by searching PubMed Central, OVID Medline, EMBASE, the Cochrane database, and ClinicalTrials.gov databases. Searches were conducted using the terms “robotic” or “robotics,” “intraoperative complications” or “postoperative complications” or “intestinal perforation” or “bowel injury” or “colon injury,” and “gynecologic surgical procedures.” Searches were limited to English-language articles, without restriction on initial publication date and published from November 2001 through December 31, 2014. There were no initial limitations in regards to study design. Additional studies were deemed relevant by reviewing the references of included articles.
Study selection
The Guidelines for Meta-Analyses and Systematic Reviews of Observational Studies (MOOSE) was used to complete the systematic review with the exception of scoring study quality and a single primary reviewer. The identified abstracts and the additional references were reviewed by one of the authors (T.P., a gynecology resident) for inclusion. Another author (N.L.S., a senior epidemiologist) also reviewed a subset (n = 82) of abstracts and articles that the data abstractor (T.P.) found questionable; full agreement on the decision regarding inclusion occurred. N.L.S. also reviewed all included articles for a subset of analyzed indices. Manuscript authors were not contacted.
Abstracts were evaluated for relevance after identification utilizing the search criteria listed above. Articles were included if they were published in refereed journals and mentioned bowel or colon injury or gynecologic surgical complications in the title and/or abstract. The full text of relevant abstracts was then reviewed in detail. For inclusion in the review, articles had to report the incidence of injury to the gastrointestinal tract. If articles commented on multiple other complications but did not include bowel injuries, it was assumed no bowel injuries occurred. Articles only including isolated complications (ie, cystotomy) that were not bowel injuries were excluded.
In the articles included in the review, bowel injury definitions varied, together with but not limited to: serosal abrasion, bowel perforation or tear, enterotomy, or bowel injuries for which the details were not further specified. We report on all of the cases as best possible, although details such as surgical indication, etiology, and management were not specified for most of the study subjects experiencing injury. The authors were not contacted to more precisely categorize these indices because the lack of original manuscript specificity reflects information that was either unavailable to them or that was not abstracted or recorded by them. Articles using national databases, case reports, data presented in review articles, and duplicate data presented in multiple manuscripts were also excluded to avoid double-counting.
Fisher exact test and odds ratios (OR) with 95% confidence intervals (CIs) are presented for all incidence rate comparisons given the varied study designs and uncommon occurrence of bowel injury. The Wilson method for proportions was used to calculate 2-tailed 95% CIs and P values for incidence. As surgical procedure and anatomic location play such potentially important roles in the incidence of bowel injury, exact OR are presented for analyses stratified by these variables, using the most precise classifications possible based on the reviewed articles, comparing the incidence rates to the most common procedure (which was procedures not otherwise specified), with P ≤ .05 considered statistically significant. The data were also analyzed by study design. All analyses were conducted using Stata (Version 11.0; StataCorp, College Station, TX) except for basic incidence rates that were calculated using the Excel (Microsoft Corp, Redmond, WA)data abstraction database for which 2 authors (T.P. and N.L.S.) developed a variable-specific coding scheme.
Results
A total of 467 abstracts and 370 full-text articles were reviewed, of which 144 ( Table 1 ) met our inclusion criteria ( Figure 1 ). The robotic procedures were performed from November 2001 through April 2014. In the review, 88 studies were retrospective, 53 prospective, 2 both retrospective and prospective, and only 1 was a randomized controlled trial. A total of 13,444 robotic-assisted procedures were recorded, including 3584 hysterectomies for malignant indications, 2361 benign hysterectomies, 1945 sacrocolpopexies with or without concurrent hysterectomy, 746 hysterectomies for mixed indications meaning the authors did not specify whether the surgical indication was for benign or malignant disease processes (ie, they reported them as a single category), 681 myomectomies, 109 pure adnexal surgeries, and 97 robotic staging procedures. Additionally, to most completely report the data, 3921 robotic gynecologic surgeries for which the exact procedure was not specified or with what procedure the bowel injury occurred are reported ( Table 2 ).
Citation | Study design | Country | Dates of data collection | Robotic surgeries, no. | Bowel injuries, no. | Bowel injuries |
---|---|---|---|---|---|---|
Abunnaja et al | Retrospective cohort | United States | February 2010 through April 2011 | 215 | 1 | 0.47% |
Advincula et al | Retrospective cohort | United States | December 2001 through April 2004 | 35 | 0 | 0.00% |
Anand et al | Retrospective cohort | United States | January 2007 through December 2009 | 50 | 2 | 4.00% |
Anger et al | RCT | United States | N/A | 40 | 0 | 0.00% |
Ascher-Walsh and Capes | Retrospective cohort | United States | July 2005 through July 2008 | 75 | 0 | 0.00% |
Awad et al | Retrospective cohort | Israel | April 2011 through April 2012 | 40 | 0 | 0.00% |
Ayav et al | Prospective cohort | France | June 2002 through June 2003 | 17 | 1 | 5.88% |
Backes et al | Retrospective cohort | United States | May 2006 through December 2009 | 503 | 2 | 0.40% |
Barakat et al | Retrospective cohort | United States | January 2008 through December 2009 | 89 | 0 | 0.00% |
Barboglio et al | Retrospective cohort | United States | May 2010 through August 2012 | 127 | 3 | 2.36% |
Bell et al | Retrospective cohort | United States | 2005 through June 2007 | 40 | 0 | 0.00% |
Bell et al | Retrospective cohort | United States | March 2005 through January 2007 | 100 | 2 | 2.00% |
Benson et al | Retrospective cohort | United States | July 2005 through June 2009 | 33 | 0 | 0.00% |
Bernardini et al | Prospective cohort | Canada | November 2008 through November 2010 | 45 | 1 | 2.22% |
Beste et al | Retrospective cohort | United States | November 2001 through December 2002 | 11 | 0 | 0.00% |
Boggess et al | Retrospective cohort | United States | May 2005 through May 2008 | 152 | 1 | 0.66% |
Boggess et al | Prospective cohort | United States | June 2005 through December 2007 | 103 | 1 | 0.97% |
Borahay et al | Retrospective cohort | United States | January 2011 through August 2012 | 20 | 0 | 0.00% |
Brown et al | Retrospective cohort | United States | January 2009 through December 2013 | 26 | 0 | 0.00% |
Burnett et al | Prospective | United States | N/A | 6 | 0 | 0.00% |
Cadiere et al | Prospective cohort | Belgium/France/Mexico | March 1997 through February 2001 | 28 | 0 | 0.00% |
Cantrell et al | Retrospective cohort | United States | June 2005 through July 2008 | 63 | 0 | 0.00% |
Cardenas-Goicoechea et al | Retrospective cohort | United States | Penn December 2007 through April 2010; WPMC May 2005 through December 2009 | 187 | 4 | 2.14% |
Cela et al | Prospective cohort | Italy | October 2011 through April 2012 | 12 | 0 | 0.00% |
Chan et al | Retrospective cohort | Hong Kong | 2007 through May 2010 | 16 | 0 | 0.00% |
Chen et al | Retrospective cohort | Taiwan | N/A | 24 | 0 | 0.00% |
Chong et al | Retrospective cohort | Korea | January 2008 through March 2011 | 50 | 0 | 0.00% |
Cohen et al | Both retrospective and prospective cohort | United States | January 2013 through April 2014; January through April 2014 | 8 | 0 | 0.00% |
Collinet et al | Retrospective cohort | International | 2008 through 2012 | 164 | 2 | 1.22% |
Coronado et al | Retrospective cohort | Spain | 2007 through June 2011 | 71 | 0 | 0.00% |
Corrado et al | Retrospective cohort | Italy | August 2010 through December 2012 | 30 | 0 | 0.00% |
Crane et al | Retrospective cohort | United States | January 2009 through December 2011 | 231 | 1 | 0.43% |
Desille-Gbaguidi et al | Retrospective cohort | France | 2008 through December 2011 | 30 | 0 | 0.00% |
Dharia Patel et al | Prospective cohort | United States | February 2003 through January 2004 | 18 | 0 | 0.00% |
Di Marco et al | Retrospective cohort | United States | June 2003 | 5 | 0 | 0.00% |
Eichelberger et al | Retrospective cohort | United States | January 2006 through December 2009 | 19 | 0 | 0.00% |
El Hachem et al | Prospective cohort | United States | March 2011 through March 2012 | 39 | 0 | 0.00% |
Elliot et al | Prospective cohort | United States | September 2002 through Acc May 2007 | 42 | 0 | 0.00% |
Estape et al | Prospective cohort | United States | August 2006 through April 2008 | 32 | 0 | 0.00% |
Fader and Escobar | Retrospective cohort | United States | 2009 | 4 | 0 | 0.00% |
Fagotti et al | Both retrospective and prospective cohort | Italy | N/A | 3 | 0 | 0.00% |
Fanning et al | Prospective cohort | United States | N/A | 20 | 0 | 0.00% |
Fastrez et al | Prospective cohort | Belgium | January 2008 through–? | 8 | 0 | 0.00% |
Feuer et al | Retrospective cohort | United States | March 2008 through April 2009 | 55 | 0 | 0.00% |
Field et al | Retrospective cohort | United States | January 2001 through August 2006 | 41 | 1 | 2.44% |
Fiorentino et al | Prospective cohort | United States | November 2003 through December 2004 | 18 | 0 | 0.00% |
Gallo et al | Retrospective cohort | United States | September 2006 through October 2010 | 442 | 6 | 1.36% |
Gargiulo et al | Retrospective cohort | United States | February 2007 through September 2009 | 174 | 0 | 0.00% |
Geisler et al | Prospective cohort | United States | January 2007 through June 2008 | 30 | 0 | 0.00% |
Ghomi et al | Prospective cohort | United States | October through December 2010 | 20 | 0 | 0.00% |
Giep et al | Retrospective cohort | United States | August 2007 through June 2009 | 237 | 0 | 0.00% |
Göçmen et al | Retrospective cohort | Turkey | October 2008 through April 2009 | 25 | 0 | 0.00% |
Göçmen et al | Retrospective cohort | Turkey | 2009 through 2010 | 12 | 0 | 0.00% |
Göçmen et al | Prospective cohort | Turkey | October 2008 through November 2009 | 10 | 0 | 0.00% |
Göçmen et al | Prospective cohort | Turkey | January 2008 through August 2010 | 15 | 0 | 0.00% |
Göçmen et al | Prospective cohort | Turkey | March 2009 through January 2010 | 10 | 0 | 0.00% |
Halliday et al | Prospective cohort | Canada | January 2008 through December 2009 | 16 | 0 | 0.00% |
Hemal et al | Prospective cohort | India | August 2006 through October 2007 | 7 | 0 | 0.00% |
Holtz et al | Retrospective cohort | United States | November 2005 through July 2006 | 13 | 0 | 0.00% |
Hoogendam et al | Prospective cohort | Netherlands | February 2008 through July 2013 | 104 | 0 | 0.00% |
Hsiao et al | Retrospective cohort | Taiwan | June 2010 through October 2011 | 20 | 1 | 5.00% |
Joubert et al | Retrospective cohort | France | January 2008 through January 2013 | 17 | 0 | 0.00% |
Jung et al | Prospective cohort | Korea | May 2006 through January 2009 | 28 | 0 | 0.00% |
Kannisto et al | Retrospective cohort | Germany | February 2011 through December 2012 | 116 | 2 | 1.72% |
Kim et al | Retrospective cohort | Korea | January 2008 through May 2013 | 23 | 0 | 0.00% |
Kimmig et al | Prospective cohort | Germany | N/A | 26 | 0 | 0.00% |
Kimmig et al | Prospective cohort | Germany | N/A | 42 | 0 | 0.00% |
Ko et al | Retrospective cohort | United States | August 2006 through August 2007 | 16 | 0 | 0.00% |
Lambaudie et al | Prospective cohort | France | February through September 2007 | 32 | 0 | 0.00% |
Landeen et al | Retrospective cohort | United States | January 2003 through December 2008 | 562 | 0 | 0.00% |
Lau et al | Prospective cohort | Canada | December 2007 through March 2010 | 143 | 2 | 1.40% |
Lee et al | Retrospective cohort | Taiwan | July 2007 through August 2008 | 6 | 0 | 0.00% |
Lee et al | Retrospective cohort | United States | July 2010 through December 2012 | 200 | 0 | 0.00% |
Lee et al | Prospective cohort | South Korea | March 2011 through June 2012 | 28 | 0 | 0.00% |
Lenihan et al | Retrospective cohort | United States | June 2005 through March 2007 | 113 | 0 | 0.00% |
Lim et al | Prospective cohort | United States | March 2008 through July 2010 | 122 | 2 | 1.64% |
Lönnerfors and Persson | Prospective cohort | Sweden | October 2005 through December 2011 | 1000 | 5 | 0.50% |
Louis-Sylvestre and Herry | Prospective cohort | France | April 2008 through January 2012 | 90 | 1 | 1.11% |
Lowe et al | Retrospective cohort | United States | April 2003 through August 2008 | 42 | 0 | 0.00% |
Lowe et al | Retrospective cohort | United States | April 2003 through January 2009 | 405 | 4 | 0.99% |
Madhuri et al | Prospective cohort | United Kingdom | December 2009 through December 2011 | 104 | 2 | 1.92% |
Manchana et al | Retrospective cohort | Thailand | 2011 through 2014 | 30 | 0 | 0.00% |
Marchal et al | Prospective cohort | Belgium/France | September 1999 through July 2003 | 30 | 0 | 0.00% |
Martinez-Maestre et al | Prospective cohort | Spain | January 2008 through December 2009 | 51 | 0 | 0.00% |
Matthews et al | Prospective cohort | United States | June 2008 through January 2010 | 48 | 2 | 4.17% |
Matthews et al | Retrospective cohort | United States | July 2007 through June 2009 | 49 | 0 | 0.00% |
Mok et al | Retrospective cohort | Singapore | August 2008–? | 34 | 0 | 0.00% |
Moreno Sierra et al | Prospective cohort | Spain | November 2006 through May 2008 | 31 | 0 | 0.00% |
Mourik et al | Retrospective cohort | Netherlands | June 2009 through April 2011 | 50 | 0 | 0.00% |
Myers et al | Retrospective cohort | United States | September 2008 through December 2011 | 169 | 1 | 0.59% |
Nash et al | Retrospective cohort | United States | September 2008 through March 2010 | 27 | 0 | 0.00% |
Nawfal et al | Retrospective cohort | United States | January 2008 through November 2010 | 202 | 0 | 0.00% |
Nevadunsky et al | Retrospective cohort | United States | August 2006 through January 2009 | 102 | 0 | 0.00% |
Nezhat et al | Retrospective cohort | United States | January 2008 through January 2009 | 40 | 0 | 0.00% |
Nezhat et al | Retrospective cohort | United States | January 2006 through August 2007 | 87 | 0 | 0.00% |
Ng et al | Retrospective cohort | Singapore | N/A | 40 | 0 | 0.00% |
Nosti et al | Retrospective cohort | United States | 1999 through 2010 | 262 | 0 | 0.00% |
Oehler | Prospective cohort | Australia | August 2008 through May 2010 | 71 | 0 | 0.00% |
Oleszczuk et al | Prospective cohort | Germany | November 2007 through May 2008 | 12 | 0 | 0.00% |
Orasanu et al | Retrospective cohort | United States | N/A | 6 | 0 | 0.00% |
Paley et al | Prospective cohort | United States | May 2006 through December 2009 | 1000 | 1 | 0.10% |
Payne and Dauterive | Retrospective cohort | United States | February 2006 through January 2007 | 100 | 0 | 0.00% |
Payne and Dauterive | Retrospective cohort | United States | January 2007 through February 2008 | 100 | 0 | 0.00% |
Peiretti et al | Prospective cohort | Italy | November 2006 through October 2008 | 77 | 0 | 0.00% |
Pitter et al | Retrospective cohort | United States | N/A | 40 | 0 | 0.00% |
Ploumidis et al | Retrospective cohort | Belgium | April 2006 through December 2011 | 95 | 0 | 0.00% |
Pluchino et al | Retrospective cohort | Italy | June 2009 through December 2011 | 43 | 0 | 0.00% |
Ramirez et al | Retrospective cohort | United States | December 2006 through February 2008 | 5 | 0 | 0.00% |
Rebeles et al | Prospective cohort | United States | June through November 2007 | 100 | 0 | 0.00% |
Reynolds and Advincula | Retrospective cohort | United States | December 2001 through December 2004 | 16 | 1 | 6.25% |
Reynolds et al | Retrospective cohort | United States | August 2002 through May 2004 | 7 | 0 | 0.00% |
Saceanu et al | Retrospective cohort | Italy | January 2008 through December 2010 | 100 | 0 | 0.00% |
Salamon et al | Prospective cohort | United States | June 2009 through May 2010 | 120 | 0 | 0.00% |
Sangha et al | Retrospective cohort | United States | January 2005 through June 2009 | 100 | 0 | 0.00% |
Sarlos et al | Prospective cohort | Switzerland | June 2007 through May 2009 | 40 | 0 | 0.00% |
Scheib and Fader | Prospective cohort | United States | June 2013 through March 2014 | 40 | 0 | 0.00% |
Schreuder et al | Prospective cohort | Netherlands | August 2006 through January 2008 | 13 | 0 | 0.00% |
Sendag et al | Retrospective cohort | Turkey | April 2012 through May 2013 | 36 | 0 | 0.00% |
Seror et al | Prospective cohort | France | January 2008 through November 2010 | 20 | 0 | 0.00% |
Sert and Abeler | Retrospective cohort | Norway | November 2005 through November 2009 | 35 | 0 | 0.00% |
Shariati et al | Retrospective cohort | United States | May 2003 through October 2005 | 77 | 1 | 1.30% |
Shashoua et al | Retrospective cohort | United States | May 2005 through November 2007 | 26 | 0 | 0.00% |
Siddiqui et al | Retrospective cohort | United States | UNC March 2006 through March 2007, DUKE April 2007 through April 2009 | 125 | 0 | 0.00% |
Siesto et al | Prospective cohort | Italy | July 2007 through December 2012 | 235 | 1 | 0.43% |
Smith et al | Retrospective cohort | United States | November 2009 through November 2010 | 116 | 0 | 0.00% |
Smorgick et al | Retrospective cohort | United States | July 2004 through June 2010 | 30 | 0 | 0.00% |
Soliman et al | Retrospective cohort | United States | January 2007 through November 2010 | 34 | 0 | 0.00% |
Subramaniam et al | Retrospective cohort | United States | March 2006 through March 2009 | 73 | 0 | 0.00% |
Sundaram et al | Prospective cohort | Malaysia | N/A | 5 | 0 | 0.00% |
Tan et al | Retrospective cohort | Taiwan | March 2009 through February 2011 | 60 | 0 | 0.00% |
Tang et al | Retrospective cohort | United States | June 2007 through February 2010 | 129 | 5 | 3.88% |
Tan-Kim et al | Retrospective cohort | United States | November 2004 through January 2009 | 43 | 0 | 0.00% |
Tinelli et al | Retrospective cohort | Italy | January 2003 through May 2010 | 23 | 0 | 0.00% |
Unger et al | Retrospective cohort | United States | 2006 through 2012 | 145 | 3 | 2.07% |
Vergote et al | Prospective cohort | Belgium | October 2007 through January 2008 | 5 | 0 | 0.00% |
Vitobello et al | Retrospective cohort | Italy | July 2008 through–? | 11 | 0 | 0.00% |
Vizza et al | Prospective cohort | Italy | August 2010 through July 2012 | 25 | 0 | 0.00% |
Vizza et al | Prospective cohort | Italy | December 2011 through June 2012 | 15 | 0 | 0.00% |
Wechter et al | Retrospective cohort | United States | March 2004 through December 2009 | 1155 | 14 | 1.21% |
Woelk et al | Retrospective cohort | United States | January 2007 through December 2009 | 325 | 7 | 2.15% |
Xylinas et al | Prospective cohort | France | N/A | 12 | 0 | 0.00% |
Yim et al | Prospective cohort | Korea | May 2006 through May 2011 | 65 | 1 | 1.54% |
Yoo et al | Prospective cohort | Korea | December 2013 through August 2014 | 6 | 0 | 0.00% |
Zapardiel et al | Retrospective cohort | Italy | January through August 2009 | 81 | 0 | 0.00% |