Original Contribution

The American Journal of Gastroenterology (2005) 100, 1844–1852; doi:10.1111/j.1572-0241.2005.41763.x

Antireflux Surgery Outcomes in Pediatric Gastroesophageal Reflux Disease

Diego M Diaz MD, MSc1, Troy E Gibbons MD2, Kurt Heiss MD3, Mark L Wulkan MD3, Richard R Ricketts MD3 and Benjamin D Gold MD1

  1. 1Pediatric Gastroenterology and Nutrition, Emory University School of Medicine, Atlanta, Georgia;
  2. 2Pediatric Gastroenterology and Nutrition, University of Arkansas, Little Rock, Arkansas;
  3. 3Pediatric Surgery, Emory University School of Medicine, Atlanta, Georgia

Correspondence: Benjamin D Gold, MD, Department of Pediatrics, Emory University School of Medicine, Division of Pediatric Gastroenterology and Nutrition, 2015 Uppergate Drive Building, Atlanta, GA 30322

Received 3 November 2004; Revised  0000; Accepted 10 March 2005.

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Abstract

OBJECTIVES:

 

Antireflux surgery is performed frequently in children with gastroesophageal reflux disease (GERD). Few comparative studies exist which assess the indications for and short- or long-term outcome of open Nissen fundoplication (ONF) and laparoscopic Nissen fundoplication (LNF) for pediatric GERD. We investigated the frequency of reoperation and factors that might influence its occurrence.

METHODS:

 

We performed a retrospective, follow up cohort study of all children less than or equal to5 years, who underwent LNF or ONF at our institution from January 1, 1997 to December 31, 2002, where five pediatric surgeons perform fundoplication. Mean follow up time was 36.2 months. The following information was obtained: surgical indications, hospital course data, and long-term surgical outcomes. Data were analyzed using univariate and multiple logistic regressions.

RESULTS:

 

Overall, 456 (150 [32.9%] ONF vs. 306 [67.1%] LNF) cases were analyzed. Reoperation was performed in 55 (12.06%), LNF 43 (14.05%), and ONF 12 (8%). The mean interim to reoperation for LNF was 11 months compared to 17 months for ONF (p= 0.007). The reoperation rate at 12 and 24 months were 10.5%, 13.4% and 4%, 6.7% respectively, when LNF was compared to ONF (p= 0.01). The multivariate analysis showed that initial LNF and prematurity were the main predictors for reoperation.

CONCLUSIONS:

 

The majority of reoperations for both LNF and ONF occurred in the first year after initial operation; LNF had a significantly higher reoperation rate than ONF. The probability of reoperation for LNF and ONF increases with the presence of comorbidities, especially prematurity and chronic respiratory conditions.

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INTRODUCTION

Gastroesophageal reflux disease (GERD) and its sequelae are increasingly recognized in the pediatric population. Recently published, evidence-based clinical practice guidelines for pediatric GERD review a number of management alternatives for children with GERD (1). These GERD management approaches included lifestyle changes, pharmacotherapeutic agents, and surgical procedures. However, the guidelines also recommend that outcome studies be performed in children with GERD, and in particular, those undergoing antireflux surgery.

Indications for antireflux surgery include primary GERD or GERD coexisting with other comorbidities, in children considered refractory to medical management. The most frequently seen GERD coexisting conditions in children undergoing fundoplication include neurological impairment, prematurity, chronic respiratory conditions, and anatomical abnormalities (2,3,4,5). Antireflux procedures are generally performed to control GERD-related symptoms, prevent complications, and permit adequate caloric intake to achieve growth.

The fundoplication technique used in the surgical management of GERD, originally described by Nissen (6), has been performed for over 45 yr. The "open" or laparotomy technique is considered a "safe" surgical procedure, but has a variable rate of reoperation ranging from less than or equal to10% to 20% in adults (7,8). Interpretation of reported operation success is variable with many studies having poorly defined case definitions or outcome/endpoints, and a lack of optimal medical management prior to surgery.

Minimally invasive surgery for GERD, performed by the laparoscopic approach, has been available in adult patients since 1991 as an alternative to surgical laparotomy (9). Comparative studies between the laparoscopic and open approach to fundoplication in adults suggested that short-term outcomes for laparoscopic Nissen fundoplication (LNF) may be superior to the traditional open Nissen fundoplication (ONF) in terms of cost, patient satisfaction, and acute complications (10,11,12).

The original reports of LNF being used in the pediatric population appeared in the literature in 1993 (13,14). The fundoplication, in particular, LNF, has recently been postulated as being the second most commonly performed surgical procedure in children in the United States (3).

Published comparative studies between the LNF and ONF in children have shown that LNF has a shorter time to initiation to feeds and length of hospital stay compared to ONF (15,16). However, reports have shown a marked variability in surgical failure rates. Reported operation failures range from 2 to almost 50% of antireflux surgery procedures, particularly in certain subsets of children. The subsets of children with increased fundoplication failure rates include those with chronic respiratory conditions, neurological impairment, repaired esophageal atresia, and infants less than 1 yr of age (17,18,19). Higher failure rates were reported by Taylor et al. (20), in a study in which a 47% failure rate and 37% reoperation rate was observed in a subset of children with neurological impairment and chronic lung disease. In 1993, Wheatley et al. (21) reported a 33% reoperation rate on 22 children with repaired esophageal atresia. Although the presence of these conditions are associated with a tendency for higher reoperation rates, there is limited knowledge as to whether other preexisting conditions concurrently confer risk to and/or whether the initial surgical approach contributes to antireflux procedure failures. Indications for a second antireflux operation include recurrence of GERD symptoms, the development of postoperative symptoms related to the surgery (i.e., gas bloat), in addition to postoperative complications related to the wrap (17,19).

There are few studies that have compared the short- and/or long-term outcome of fundoplication in the pediatric population (15,16). In addition, a multivariate analysis of previously identified risk factors for reoperation that takes into account their potential biological significance has not been reported.

We conducted a retrospective follow-up analytical examination of 456 patients that underwent Nissen fundoplication for the management of GERD at Children's Healthcare of Atlanta, Egleston Children's Hospital. Our study aimed to specifically characterize the risk factors associated with fundoplication reoperation, and to compare the short-term outcome for LNF and ONF. Unlike previous studies, we used a statistical model to potentially predict the probabilities for reoperation occurrence for new patients. Data were analyzed using univariable statistical procedures and multivariable modeling to control for confounding and establish associations.

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MATERIALS AND METHODS

We conducted a retrospective, follow up study of patients undergoing Nissen fundoplication for any indication at Children's Healthcare of Atlanta at Egleston Children's Hospital. Included in the study were 473 patients with ages ranging from newborns to 60 months. The subjects whose data were evaluated underwent Nissen fundoplication during the period of January 1, 1997 to December 31, 2002. At our institution five pediatric surgeons perform fundoplication. Exclusion criteria for data analysis were incomplete preoperative data (n = 3), acute conversion from LNF to ONF (n = 4), and children with underlying congenital anatomic anomalies of the esophagus (n = 10). Data from the hospital course and long-term surgical outcomes were retrieved from hospital charts and electronic medical records on 456 patients who underwent LNF or ONF. Demographic patient data collected on this cohort included age in months, gender, and underlying diagnoses. Hospital course data included complications such as acute intraoperative bleeding, acute respiratory problem (pneumonia, atelectasis, and bronchospasm), infection (peritonitis, surgical wound, or blood infection), and prolonged ileus (more than 48 h). The length of hospital stay (LOS) was defined as number of days from the day of operation until discharge. Included in the analysis were patients who had prolonged hospitalization for reasons unrelated to the fundoplication procedure. In such cases, hospitalization related to fundoplication was considered to be complete at the time of surgical clearance for discharge. Long-term surgical outcome was the need or lack thereof for reoperation. Mean follow-up time was 36.2 months (SD: 10.9). Outcome data on children who expired during the follow-up period (n = 9) were also included in the analysis; information collected included events occurring up until the time of death.

GERD was defined as the signs, symptoms, or complications occurring due to passage of gastric contents into the esophagus and/or oropharynx (1). Indications for surgery included persistent GERD-related symptoms, complications from GERD not resolved from medical therapy, and surgeon clinical decision. Patients were referred for surgery from both inpatient and/or outpatient pediatricians and pediatric subspecialists. Data on the type of preoperative evaluation were not available for all patients, and some were referred based on the clinical decision of the referring physician. For postoperative risk factor assessment, the diagnoses included in the analysis were those previously reported in the literature as potential risk factors for reoperation (2,3,4,17,22,23,24,25,26,27). These clinical diagnoses included prematurity, categorized as infants born at less than or equal to 29 gestational wk, and infants born between 30 and 36 gestational wk (gestational age at birth as determined by neonatology records); neurological impairment (cerebral palsy, seizure disorder, and spasticity); chronic respiratory conditions (bronchopulmonary dysplasia, persistent asthma, recurrent pneumonia, need for oxygen supplementation, and ventilator dependant patients); and cardiac disease (complex heart defects and other cardiac conditions that required medical or surgical management). Age at initial operation was categorized in three distinct strata; less than 1–5 months, 6–11 months, and 12–60 months. The study was approved and Health Insurance Portability and Accountability Act (HIPAA) authorization granted by the institutional review board at Emory University and Children's Healthcare of Atlanta.

Data Analysis

All statistical analyses were performed using the SAS 8 software package (SAS Institute, Cary, NC). All reported p values were two-sided, those <0.05 were considered as significant. Data were analyzed using univariate logistic regression, then a multiple logistic regression model was used to assess the association between the type of initial procedure and the risk of reoperation, while adjusting for the possible confounding effects of age at initial operation, and patient comorbidities that were related to this risk in previous studies. Reoperation was the primary outcome variable. Odds ratios and 95% confidence intervals (CI) were estimated for the effect of independent variables on reoperation; these measures of association were estimated before and after adjustment by using the logistic regression procedure (LOGISTIC and GENMOD). Independent variables were those considered risk factors or potential confounding factors for reoperation a priori. These variables were included in the final model, and thus plausibility due to their potential biologic significance in influencing outcomes of operation.

The independent variables were type of initial procedure (LNF vs ONF), age category at initial operation, history of prematurity, gender, cardiac disease, chronic respiratory conditions, neurological impairment, and history of reflux alone. These variables were analyzed by univariate logistic regression, and then included in the multivariate logistic regression model; statistical significance of covariates was determined by Wald's chi2 tests. Goodness-of-fit of the resulting model was evaluated by means of the Hosmer-Lemeshow test, by systematic exploration for possible interaction effects, and by evaluation of the contributions of individual subjects to the quantitative results. Furthermore, multiple logistic regression analysis was used to create a model to predict the probabilities of reoperation for LNF and ONF utilizing the independent variables studied. Survival analysis was performed by the Kaplan-Meier method to estimate reoperation rates for LNF and ONF, with comparisons based on the two-sided log-rank test. p < 0.05 was considered significant. Tests of statistical significance (p values) and 95% CI for the odds ratio and comparison of proportions were calculated by the chi2 test or Fisher's exact test, as appropriate. Because of their non-Gaussian frequency distribution, continuous data (LOS and age at initial operation) are presented as medians and ranges and evaluated by nonparametric statistics using the Wilcoxon rank-sum test.

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RESULTS

We analyzed data from 456 patients, 306 (67.1%) LNF and 150 (32.1%) ONF. The characteristics of the LNF and ONF groups are shown in Table 1. There were 190 (42%) females and 266 males (58%). The mean age at initial operation was 11.9 plusminus 13.2 months (median: 6 months, range: 1–60), and did not differ significantly between LNF and ONF. The interval between operations averaged 11.2 plusminus 9.2 months (median: 8, range: 1–47) for LNF versus 17.2 plusminus 8.9 months (median: 14.5, range: 6–36) for ONF. The shorter interval to reoperation in the LNF group was statistically different (p= 0.007). There were no operation-related deaths observed during the study period.


During the first 3 yr of the study, 222 fundoplications were performed, 100 LNF and 122 ONF; conversely, between 2000 and 2002, 206 patients underwent LNF and 28 ONF (p < 0.0001). Many patients had more than one underlying diagnosis at the time of surgery; the most common comorbidities at the time of fundoplication were chronic respiratory conditions (41.66%), neurological impairment (32.45%), and prematurity (30.04%), and their distribution did not differ significantly between LNF and ONF (Fig. 1). However, among patients with diagnosis of reflux alone, 78 (83.87%) underwent LNF compared to 15 (16.13%) from the ONF group (p= 0.0001). Children with history of prematurity were operated on primarily via LNF 95 (70%). The study included 136 ex-premature patients, 87 (64%) had the initial operation before 6 months of age, and by 1 yr of age, 111 (82%) of these former premature infants had undergone fundoplication. Children with history of prematurity had the tendency to require reoperation; 19 of 136 (14%) (OR: 1.3; 95% CI: 0.7–2.3; p= 0.4), and 13 of 19 were less than 30 wk of gestational age at birth (OR: 1.6; 95% CI: 0.82–3.2; p= 0.15) compared to 36 of 320 (11%) (OR: 0.7; 95% CI: 0.8–1.5; p= 0.41) children who were born full term. However, these observations did not reach statistical significance.

Figure 1.
Figure 1. - Unfortunately we are unable to provide accessible alternative text for this. If you require assistance to access this image, please contact help@nature.com or the author

Distribution of underlying diagnoses comparing LNF versus ONF. Bar chart depicting the distribution of underlying diagnoses between LNF and ONF, in children under 5 yr who underwent a fundoplication procedure at the Egleston Children's Hospital Campus of Children's Healthcare of Atlanta from January 1997 to December 2002. Patients can have more than one coexisting diagnosis. Results will not add up to 456. *p < 0.05.

Full figure and legend (38K)

Fifty-five (12%) of 456 patients who underwent Nissen fundoplication at our institution required reoperation; 43 (14%) in the LNF group compared to 12 (8%) for ONF (OR: 1.88; 95% CI: 0.96–3.68; p= 0.06). The frequency for reoperation by initial procedure and underlying diagnoses were not statistically significant as shown in Figure 2.

Figure 2.
Figure 2. - Unfortunately we are unable to provide accessible alternative text for this. If you require assistance to access this image, please contact help@nature.com or the author

Distribution and corresponding frequency of reoperation for underlying diagnoses comparing LNF versus ONF. Bar chart depicting the distribution and corresponding frequency of reoperation by initial procedure for underlying diagnoses for LNF and ONF in children under 5 yr who underwent a fundoplication procedure at the Egleston Children's Hospital Campus of Children's Healthcare of Atlanta from January 1997 to December 2002. Patients can have more than one coexisting diagnosis. Results will not add up to 55. * = NS; p = 0.2. LNFr = number of reoperations in the LNF group; ONFr = number of reoperations in the ONF group. % = proportion of reoperation for each comorbidity by initial approach.

Full figure and legend (38K)

Table 2 shows the frequency of acute complications following fundoplication. Overall, ONF was associated with a significantly higher frequency of acute complications; 34 (22.7%) compared to 18 (5.9%) LNF (p < 0.0001).


Table 3 shows a comparison of acute complications and long-term outcome for LNF during the two time periods (1997–1999 and 2000–2002). Overall, 4 of 310 (1.3%) laparoscopic procedures were converted to ONF. The conversion rate improved from 2% during the first 3 yr to 1% for 2000–2002 (p= 0.59). Reasons for conversion from LNF to ONF were 1 patient with hepatomegaly and difficult visualization of the surgical field, 1 patient with distended small bowel loops, and 2 patients with dense adhesions.


Table 4 depicts odds ratios for reoperation, estimated separately for each individual risk factor. Initial laparoscopic surgery, a history of prematurity, and reflux alone tended to be associated with increased risk of reoperation. However, a bivariate analysis performed showed a confounded association between primary reflux and increased risk of reoperation since this subcohort was significantly more likely to undergo LNF initially.


Table 5 shows results of the multiple logistic regression analysis using the final model; covariates included gender and risk factors for reoperation as determined by literature review. Goodness of fit was excellent, as indicated by the Hosmer-Lemeslow test (p= 0.78), and the absence of statistically significant interaction effects. The risk for reoperation tend to be higher in patients who underwent initial LNF and children with history of prematurity; however, the independent impact of these two risk factors did not reach statistical significance. The final model was used to predict the probability of reoperation depending on the type of procedure, age at initial operation, and presence of comorbidities. Overall, reoperation rates were higher for LNF, and they increased for LNF and ONF with the presence of comorbidities, especially prematurity and chronic respiratory conditions (Table 6).



Figure 3 shows the Kaplan-Meier diagram for survival time of subjects evaluated in this study. "Survival" was defined as patients who did not require reoperation. The mean follow-up time was 36.2 months (SD: 10.9); the difference in survival curves between patients who initially underwent LNF and ONF was statistically significant (p= 0.01). Table 7 shows higher reoperation rates for LNF at 12, 24, and 36 months after initial operation. The majority of reoperations for LNF and ONF occurred in the first year following the initial operation.

Figure 3.
Figure 3. - Unfortunately we are unable to provide accessible alternative text for this. If you require assistance to access this image, please contact help@nature.com or the author

Kaplan-Meier curves for reoperation in subjects who underwent LNF versus ONF. Kaplan-Meier curves of the cumulative probability of reoperation in subjects who underwent LNF or ONF. Mean follow-up time was 36.1 months; SD: 10.96; range: 12.9–59.8. A significant difference in reoperation was observed between LNF and ONF, with a log-rank chi2(1 df) = 5.44; p= 0.01.

Full figure and legend (20K)


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DISCUSSION

Although population-based studies have not been conducted, potentially preventable GERD-related complications such as erosive esophagitis appear to be rare in thriving infants who are younger than 2 yr of age. However, in children with neurological impairment or other systemic conditions, by 3 or 4 yr of age or older, reports of 20–70% describe erosive esophagitis development (1,28,29). Therefore, our study was restricted to that of younger children below 5 yr of age. Previous investigations demonstrated a number of comorbidities that either confer more risk for development of persistent GERD or occur concurrently; neurological injury being the most predominant comorbidity (25,30). In addition, studies indicate that surgical failures and/or complications are more common in those neurologically impaired (30,31). We demonstrated that LNF or ONF were done more frequently in children with neurological impairment than in other conditions, except chronic respiratory conditions (Fig. 2).

In our study, significantly fewer acute respiratory problems and prolonged ileus were encountered in LNF compared with ONF. Comparative studies recently performed concluded that LNF was a valid alternative to ONF in children (15,16,32). However, these conclusions should be interpreted with caution. Cohort sizes in these studies were small and follow-up was relatively short, ranging from 6 to 16.5 months. Bufo et al. (33) performed a larger retrospective study in which relatively smaller numbers of LNF (n = 27) versus ONF (n = 185) were used. These authors concluded that LNF was a safe and superior technique to ONF despite significant rates of immediate postoperative complications noted in LNF (37%) and an undisclosed follow-up period. Such high rates of postoperative complications for LNF are not supported by our study (5.9%). Other studies of LNF in children (10,23,30,34) and adults (35,36) have demonstrated good short-term safety and outcomes when the surgery was performed by an experienced surgeon and appropriate patient case selection was used.

Two time periods are usually evaluated in the study of relatively new surgical techniques to depict the steep "learning curve" observed early on in the experience at many large referral institutions (37,38,39). The learning curve is defined in these reports as approximately 1 yr and/or first 20–25 cases performed by each individual surgeon performing laparoscopic antireflux surgery. The pediatric surgery group at our institution started to perform LNF in 1997. We determined that by the year 2000 all five members had completed approximately 20 LNF. For example, Meehan and Georgeson (38) demonstrated a rapid decrease in complication rate after a learning phase of 20–25 patients in a review of the first 160 consecutive laparoscopic fundoplication. In our study, the overall perioperative complication rate for LNF was significantly higher during 1997–1999 (11%) compared to 2000–2002 (3%), especially the immediate postoperative complications. However, the acute intraoperative complication rate was 1% for the two periods analyzed. More importantly, the reoperation rate in our study did not decline over time. The rate of conversion from LNF to ONF was 1.3% for Esposito et al. (40), 2% for Allal et al. (41), and up to 30% for Meehan and Georgeson; this conversion rate improved to 7.5% after the first 20 cases. The conversion rate in our study was 2% for the initial 3 yr and improved to 1% during 2000–2002. Thus, the higher initial conversion rate appears to be the main reflection of the learning curve in our study. The distribution of patient comorbidities did not differ significantly; therefore the type of initial surgery did not appear to be clearly influenced by patient-related disease, and was more a factor of the training of the specific surgeons and their procedure preference. Specifically, the LNF now appears to be the procedure of choice at our institution whether or not there are preexisting comorbidities in the patient. Hence, the decision for antireflux surgery is often made on an individual surgeon's choice and selection bias was not likely to affect our study results.

One of the major benefits of LNF shown by previous studies has been the rapid postoperative recovery time compared with ONF (42,43). These observations are supported by our study with median hospital stay being 3 days for LNF compared to 5 days for ONF (p < 0.005). Previous studies were unclear as to the length of postoperative time interval considered for follow-up and/or which complications were considered as long term (33,44).

The indication for reoperation after Nissen fundoplication can be related to causes including recurrence of GERD symptoms, or postoperative symptoms such as gas bloat, dumping syndrome, and retching. In addition, reoperation has been associated with or due to transdiaphragmatic migration of the wrap, paraesophageal hernia, wrap dehiscence, loose wrap and slipped wrap into the fundus, or development of large hiatal hernia (17,19). However, there have been few studies in children documenting the indications for reoperation, and reoperation rates vary significantly between studies. The published rates range from 6% to 47% for ONF (26,27,30,45,46,47), compared to LNF approach from 2.3% to 25% (19,34). This study enabled us to characterize the long-term probability for reoperation and to perform comparative analysis between ONF and LNF. Using a statistical model that included the risk factors for reoperation, therefore taking into account their potential biological significance, the predicted probabilities of reoperation were calculated. The type of analysis performed in our study has not been previously reported.

The reoperation rate reported by Kubiak et al. (18) for infants less than 4 months at initial operation was 24%. In contrast, our study showed a predicted probability of reoperation in patients who underwent surgery within the first 5 months of life and had no comorbidities for LNF of (10.7%) compared to ONF (6.7%). Based on our study, patients with one to three comorbidities had a probability of reoperation ranging from 8% to 24% for LNF compared to ONF that ranged from 6% to 16%. These predicted probabilities can be useful to clinicians and surgeons when faced with patient selection and parental questions.

Time to reoperation in our study showed differences for both surgical approaches: for LNF, time to reoperation was 11.2 months compared to 17.2 months in ONF (p= 0.007). Most reoperations for both approaches occurred within the first 12 months. A similar time interval has been described by Kimber et al. (26) for ONF. In addition, Rothenberg (34) noted early failures in his analysis of 220 cases of laparoscopic fundoplication, and Meyer et al. (48) reported a mean time to reoperation for LNF in adults of 8 months. The reoperation rate for LNF was higher than ONF at 12, 24, and 36 months after the initial operation (p= 0.01).

There are a number of limitations to this study. Information obtained by a retrospective study is not controlled, may be incomplete, and have inaccuracies. Follow-up analysis by medical record review limits the ability to ascertain specific indications for surgery, and would be optimally performed in a prospective fashion. Procedures were performed by a group of five surgeons, and personal technique and experience with either ONF or LNF are variables that are not standardized or surgical approach protocolized. To consider technique uniformity, multicenter collaborative studies are clearly needed in order to standardize the measurement of surgical outcomes for antireflux surgery, in particular a registry of a large cohort of patients, which include large pediatric surgical practices. This would facilitate conducting prospective studies that would objectively measure indications and outcomes.

In summary, LNF was the predominant fundoplication approach used in our large series. Despite a higher reoperation rate, LNF had a shorter length of stay, fewer acute respiratory complications, and was less likely to have prolonged ileus than ONF. Based on long-term outcome, our study suggests that reoperation tends to present within the first year following the procedure for both LNF and ONF. However, the children who underwent ONF had a lower reoperation rate and lesser predicted reoperation rate as well. Thus, it is important to define for future prospective and/or multicenter studies what is considered the surgical standard of care for the definitive management of refractory GERD. Long-term prospective studies are critically needed in all the major groups of children who have GERD as a primary diagnosis or GERD secondary to some underlying conditions such as prematurity, neurological impairment, and chronic lung disease to correlate these chronic conditions with the mechanism of medical and/or surgical failure.

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Acknowledgements

The authors would like to acknowledge Daphne Pierce-Smith for critical review of this study and manuscript. Benjamin D. Gold, M.D., is supported in part by a grant from the NIH, NIDDK 53708-01.

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