O’Loughlin, Edward V.*; Somerville, Helen*; Shun, Albert†; Gangemi, Rachel*; La Hei, Erik†; Desphande, Aniruddh†; O’Loughlin, Timothy F.‡
Gastrooesophageal reflux disease (GERD) is common in children and adults with neurological impairment (1–3). Complications, including reflux oesophagitis and recurrent pulmonary aspiration, cause significant morbidity and mortality. This adds to the burden of care for both affected children and adults and their caregivers. GERD often accompanies dysphagia in patients with neurological impairment, which in turn contributes to malnutrition and recurrent pulmonary aspiration. Gastrostomy tube feeding, when used in the setting of poor nutrition or recurrent aspiration with eating, may aggravate the problems associated with gastrooesophageal reflux (4). Thus, clinicians working in the disability setting are often confronted with children and adults with multiple comorbidities such as GERD, chronic suppurative lung disease, and chronic malnutrition because of inadequate intake. Effective treatment of GERD and nutritional rehabilitation are important outcomes of management. Although acid suppression therapy is effective in the treatment of reflux oesophagitis, antireflux surgery is often required to prevent reflux-associated morbidity such as recurrent aspiration.
Nissen fundoplication is the standard surgical therapy for GERD, but there are no randomised controlled trials attesting to its efficacy in children or adults with neurological impairment (5). Case series suggest higher mortality and surgical complication rates in this group of patients (6), leading to a reluctance on the part of some surgeons to undertake this procedure. Indeed, a recent cohort study of antireflux surgery in children in the United States indicates that rates of surgery are static for normal children but have fallen over time for children with neurological impairment (7). Gastrojejunal feeding has been recommended by some as an effective therapy for reflux and aspiration in this group (8) but is not favoured by our clinic because it commits the caregiver to continuous pump feeding to avoid dumping, and tube blockage and jejunal intussusception commonly complicate this technique (personal observation).
An important consideration for clinicians when developing management strategies for children with neurological impairment is the attitudes and perceptions of caregivers. Parental/caregiver perceptions of their childrens’ mealtimes and eating often differ from those of involved physicians and allied health professionals. Morrow et al (9) compared parental and health professional perceptions of quality of life in children with spastic quadriplegic cerebral palsy and severe feeding difficulties. Health professionals placed more emphasis on physical and medical aspects of well-being in contrast to caregivers who were more concerned about emotional well-being and socialisation. These differences in perception not infrequently led to miscommunication between health professionals and caregivers and occasionally a perceived deterioration in quality of life from medical interventions such as gastrostomy insertion. Two previous studies examined caregiver perceptions of their child's quality of life following antireflux surgery in neurologically impaired children, although neither enquired about attitudes to the surgical intervention (10,11). Thus, the aims of the present study were to report parent and caregiver perceptions of symptoms following Nissen fundoplication (with gastrostomy) in a group of patients with severe neurological impairment and to describe the complications of surgery.
Patients and Clinical Variables
Patients were seen at tertiary referral multidisciplinary clinics established for the management of dysphagia and nutritional problems in children and adults with severe neurological impairment. The clinic structure and this patient group have been described in detail previously (2). Children up to and including age 18 years were seen at the Children's Hospital Westmead and patients older than 18 were seen at Westmead Hospital. All of the patients were seen by a developmental paediatrician, clinic nurse, speech-language pathologist, dietician, and paediatric gastroenterologist in the paediatric clinic and all but the gastroenterologist at the adult clinic. Patients were included if fundoplication was performed since 1994 and follow-up occurred in 1 of the clinics until December 2009.
Study design was a retrospective cohort study except the questionnaire, which was conducted as a cross-sectional survey. Clinical information was obtained from a variety of sources including referring physicians, involved clinicians, and hospital electronic medical records. Data of interest was entered into a clinic database and updated with each clinic visit. Patient variables included demographic data, diagnoses, growth data, comorbidities (GERD, respiratory symptoms or disease, epilepsy, and use of anticonvulsants), results of clinic investigations (upper endoscopy and biopsy, high-resolution computed tomography of the chest, and barium videofluoroscopy), age at and type of surgery, presence or absence of gastrostomy, and surgical complications.
Dysphagia was defined as difficulty swallowing as reported by parent/caregiver (coughing and choking with eating, aversion to eating) and/or proven aspiration on vidoefluoroscopy. Gastrooesophageal reflux included a history of frequent regurgitation or vomiting, pain behaviour such as neck arching, frequent nighttime waking, or proven GERD (endoscopy with biopsy-proven oesophagitis). Respiratory disease was defined as ≥2 episodes of respiratory infection requiring antibiotic therapy and/or admission to hospital for treatment of pneumonia or recurrent wheezing requiring bronchodilators (frequently misdiagnosed as asthma). Pulmonary aspiration was suspected in patients with recurrent chest infections and/or the presence of chronic suppurative lung disease and proven only when demonstrated on videofluoroscopy. We previously described our approach to the medical management of dysphagia, GERD, and undernutrition (2).
Indications for fundoplication surgery in children with neurological impairment and dysphagia included proven reflux oesophagitis (or symptoms suggestive of gastrooesophageal reflux) associated with recurrent chest infections or established chronic suppurative lung disease. Patients with dysphagia and recurrent chest infections without a history suggestive of GERD and with negative endoscopy and biopsy were sometimes managed with gastrostomy and nil per os initially. If chest symptoms persisted, patients subsequently underwent fundoplication. Although a proportion of patients had gastrostomy before first attendance at a dysphagia clinic, the decision to insert a gastrostomy was taken in patients with severe dysphagia, leading to either aspiration with eating or undernutrition. The decision to proceed to fundoplication was made in consultation with clinic physicians (H.S. and E.V.O’L.) and surgeon undertaking the procedure. Initial surgery was undertaken at a single centre (the Children's Hospital at Westmead). Standard Nissen fundoplication was performed by open or laparoscopic technique. Hiatal repair was performed using nonabsorbable sutures followed by creation of a loose 360-degree fundal wrap (Nissen fundoplication). Since 2004, to minimise the failure of the hiatal repair, we chose to reinforce the hiatal repair using a bioprosthetic patch (Surgisis, Cook Urological, Spencer, IN).
Because there is no validated questionnaire for this group of patients, we adapted the Infant Gastrooesophageal Reflux Questionnaire Revised (I-GERQ-R) (12). Parents were contacted by the clinic nurse coordinator (R.G.). The questionnaire was administered in the clinic by the nurse coordinator or by telephone for those unwilling to return to clinic. Four children lived in long-term residential care and the questionnaires were completed by 1 clinician (H.S.) who obtained the information from their caregivers at the residential facility.
Parents or caregivers were asked the following questions:
1. With regard to
2. weight gain
3. the number of chest infections
4. the frequency of vomiting
5. feed tolerance (ie, the ability to ingest, via mouth or tube, recommended daily intake)
6. pain and distress with feeds, that is, behaviour around mealtimes such as crying, agitation, wriggling, which you think is related to pain
7. the amount of gagging and retching
8. disturbed sleep pattern
could you please rate the symptom on a scale from 1 to 5 where 1 is much better, 2 is better, 3 is no change, 4 is worse, and 5 is much worse. After answering the questions about symptoms, the parent/caregiver was asked, “How do you feel about your decision to agree to a fundoplication for your child?” Parents of children who died before the questionnaire was administered were not contacted.
Surgical complications were defined as severe if the surgery resulted in death, required surgical intervention, or redo surgery due to failure of the fundoplication, or resulted in a protracted admission or readmission to hospital.
Data are depicted as median (and interquartile range) or percentage of total unless otherwise indicated. Mean weight z scores measured before surgery and at last follow-up visit were compared by paired t test. Study protocols were approved by the ethics committee, Children's Hospital at Westmead.
Fundoplication surgery was performed in 122 children. Table 1 depicts the primary clinical diagnoses for their neurological impairment. Seventy-seven of 122 (63%) had spastic quadriplegic cerebral palsy. The majority of children, 112 of 122 (92%), were immobile and totally dependent on their caregivers—gross motor function classification system (GMFCS) V. Epilepsy was common, with 81 of 122 (66%) taking at least 1 anticonvulsant medication when last reviewed in 1 of the dysphagia clinics.
Dysphagia was present in 109 of 122 (89%) children. A history of vomiting suggestive of GER was present in 83 of 122 (73%) and proven oesophagitis (endoscopy and biopsy) in 72 of 122 (59%) children. Recurrent chest infections were present in 95 of 122 (78%) with a diagnosis of chronic suppurative lung disease in 44 of 122 (31%) based on history of recurrent chest infections, physical signs (finger clubbing), and/or abnormal computed tomography chest (36 patients). Pulmonary aspiration was suspected in the majority of children with recurrent chest infections but was only identified in 39 of 90 children who had an oesophageal videofluoroscopy. Poor weight gain not responding to dietary supplementation and oral feeds necessitating insertion of gastrostomy occurred in 82 of 122 (67%) children. Weight z score at the time of surgery was −2.54 ± 0.15 (mean ± SE, n = 93). Children usually suffered from multiple comorbidities such that no patient underwent fundoplication surgery for a single indication.
Nissen fundoplication was performed at a median age 74 months (interquartile range 29–124) by laparoscopic technique in 77 of 122 (63%) and open fundoplication in the remainder. Gastrostomy was inserted in a total of 117 of 122 (96%) patients because of poor weight gain or concerns about recurrent aspiration with swallowing. Ninety-six (79%) had gastrostomy inserted at the time of fundoplication, 21 (17%) patients had gastrostomy initially but underwent fundoplication at a later date because of worsening GERD or recurrent aspiration pneumonia, and 5 (4%) had fundoplication but never had gastrostomy.
Twenty patients (16%) died during the course of the present study. Thirteen patients died of pneumonia mostly because of recurrent aspiration, 1 from central hypoventilation because of degenerative neurological disorder (Alexander disease), and 3 from seizures (1 of whom aspirated during a grandmal seizure). There were 3 patients in whom the exact cause of death could not be ascertained. There were no deaths directly attributable to either fundoplication surgery or gastrostomy insertion (death within 1 month of surgery), and there were no deaths from subsequent gastrostomy button replacement. Thirteen patients (11%) had moved and could not be contacted by the clinic nurse and thus were lost to follow-up.
Questionnaires were completed by parents (85) or caregivers (4) of 89 patients (89/122 [73%] of patients who had fundoplication); median duration of time from fundoplication to questionnaire was 77 months (43–89). Eighteen of 89 (20%) patients answered the questionnaire at a clinic visit and 71 of 89 (80%) by telephone. Eighty-three of 89 (93%) caregivers responding to the questionnaire reported that weight gain was better or much better following fundoplication with a median score of 1 (Table 2). Weight z score also increased significantly (−2.57 ± 0.16 to −1.65 ± 0.20, P < 0.00005 paired t test, n = 85 pairs) during the study period supporting the parent/caregiver observations of weight improvement. More than two thirds of care givers reported that chest infections, feed tolerance, and vomiting were better or much better, but there was less improvement in the symptoms of pain and distress with feeds, gagging and retching, and sleep disturbance. Parents and caregivers were also asked for their general comments about fundoplication/gastrostomy. The majority reported some level of satisfaction with the surgery and only 2 of 89 (2%) commented that they would not consent to surgery if they had their time over again.
Complications are depicted in Table 3. There were no deaths directly attributable to fundoplication surgery or gastrostomy insertion/change of gastrostomy button. No surgical complications could be identified in 83 of 122 (74%) patients undergoing fundoplication. Severe complications occurred in 12 of 122 (10%) patients. Four patients underwent repeat surgery, which included redo fundoplication in 3 for either slipped fundoplication wrap (27, 26 and 24 months after initial surgery) or development of a large hiatus hernia resulting in recurrence of symptoms and reversal of fundoplication with gastropexy (13) in 1 with intractable gagging and retching (92 months after initial surgery). One patient who had a redo fundoplication subsequently underwent an oesophagojejunostomy with gastric disconnection (29 months after initial surgery). Gastropexy was recommended in another patient (99 months after initial surgery) who had intractable retching and gagging following fundoplication, but consent was refused by the child's parents. One each developed postoperative wound dehiscence, postoperative pneumonia requiring admission to intensive care, postoperative pain lasting 6 weeks, and a perforated duodenum requiring surgery following a change from gastrostomy to jejunostomy. Mild-to-moderate complications occurred in 36 of 122 (30%). The fundoplication wrap slipped in 3 children resulting in the development of hiatus hernia and recurrence of symptoms. One of these patients developed recurrent peptic stricture. All have responded to medical therapy and have not yet required surgical repair. Twenty-five of 122 (20%) patients have complained of gagging and retching postfundoplication at clinical review, which was severe enough to require investigation and medical intervention (5 converted from gastrostomy to jejunostomy and the remainder became less symptomatic with changes in feeding regimes and time or with sedative medication). Dumping has been proven in 4 with abnormal glucose tolerance tests and 4 complained of gas bloat, which settled with regular venting of the gastrostomy.
The present study reports a single-centre experience with antireflux surgery and gastrostomy in children with severe neurological impairment. The majority of children were immobile and totally dependent on their caregivers for their day-to-day needs attesting to the severity of their neurological impairment. Parents and caregivers reported significant improvements in symptoms for which the surgery was originally undertaken such as poor weight gain and recurrent chest infections, vomiting and pain, and discomfort with feeds. Caregivers responding to the questionnaire also expressed high level of satisfaction with the results of surgery, only 2 of 89 who answered the questionnaire reporting that they would not consent to surgery if they had to make the decision again. There were no deaths attributable to the surgery and serious surgical complications were uncommon; however, a significant minority complained of persistent postoperative symptoms likely because of fundoplication.
Children with neurological impairment presenting for fundoplication are a heterogeneous group, with underlying diagnoses ranging from spastic quadriplegic cerebral palsy to rare degenerative and metabolic disorders (2,14,15). Poor coordination of swallowing resulting in undernutrition and recurrent aspiration is common. This often necessitates gastrostomy feeding for nutritional rehabilitation and/or to reduce the risk of aspiration. Several studies attest to the efficacy of gastrostomy feeding in the nutritional rehabilitation of children with a severe developmental disability (16–18); however, gastrostomy feeding may aggravate reflux and pulmonary aspiration (4,19,20), although this has not been reported by all of the observers (21). GERD may also affect quality of life (symptomatic oesophagitis, peptic stricture, recurrent pneumonia) and often requires specific therapy.
Antireflux surgery is the only available therapy for stopping gastrooesophageal reflux (22). Motility agents have no proven efficacy in the childhood population, and acid suppression therapy improves oesophagitis but does not stop reflux. Randomised clinical trials of antireflux surgery compared with proton pump inhibitor in adult patients with GERD show similar efficacy in controlling oesophagitis, although quality of life is significantly improved in patients undergoing surgery (23). A recent Cochrane review failed to identify any randomised controlled trial of antireflux surgery in children with neurological impairment, although several case series attest to the efficacy of surgical treatment (14,15,24–27). One large cohort study also demonstrated reduced rates of reflux-related hospitalisation (aspiration, GERD, and respiratory failure) for 12 months following antireflux surgery (28), although rates of pneumonia did not decrease; however, there has been increasing reluctance to undertake this procedure in children (6,7) despite the lack of effective alternative therapies and the serious comorbidities associated with GER in neurologically impaired children.
Approximately one-fourth of the patients who had surgery died or were lost to follow-up; however, most of the surviving patients in this series continued to attend for follow-up and/or could be contacted by telephone (89/122, 73%). Caregivers responding to the questionnaire reported improvements in most of the symptoms for which the surgery was being undertaken and a high degree of satisfaction overall with the surgery. The data are in keeping with 2 previous studies examining caregiver perceptions following antireflux surgery in neurologically impaired children (10,11). O’Neill et al (10) surveyed 25 caregivers following their child's antireflux surgery (with gastrostomy in 23/25 patients) presurgery and at 6 months and 2 years postsurgery. Parents reported significant improvements in feeding indices, perceptions of the child's comfort and child's quality of life, but no improvement in the caregiver quality of life. Interestingly, caregivers indicated that respiratory health was not altered by surgery. In another study, Srivastava et al (11) surveyed 43 caregivers on the child's quality of life at baseline and 1 month after antireflux surgery (100% with gastrostomy). They reported improvements in several domains in quality of life as measured by the Child Health Questionnaire parental form 50 but found little improvement in caregiver quality of life, although caregivers were not questioned about their perceptions of the surgical intervention. How much of the benefit can be ascribed to antireflux surgery versus gastrostomy is difficult to ascertain because gastrostomy feeds have previously been shown to enhance aspects of the neurologically impaired child's health (29–31) and caregiver quality of life (29,30). These limited data suggest high levels of caregiver satisfaction with the results of antireflux surgery and gastrostomy despite reported failure and complication rates of fundoplication. Considering the complex medical problems associated with feeding, the limited life expectancy of patients with neurological impairment (32,33), and the difficulty in assessing symptoms in this group, caregiver perceptions of efficacy should be an important outcome measure when assessing invasive interventions in this group.
Serious surgical morbidity was modest (redo fundoplication or gastropexy, prolonged hospitalisation or readmission) in our study and there were no deaths directly attributable to the surgery; however, a significant percentage of children developed symptoms such as gagging and retching (20%) and gas bloat. Gagging and retching is frequently a worrisome symptom for caregivers. Richards et al (34) have suggested that these symptoms are caused by hyperactive vagal emetic reflexes resulting from reduced central inhibition of peripheral reflexes in the neurologically impaired and are a preexisting problem in a subgroup of patients with neurological impairment. We identified only 1 patient in our series who had gagging and retching prefundoplication but may have missed this in others and ascribed their symptoms to GER; however, in the majority, the symptom emerged or became a significant issue for caregivers after surgery, and in 1 patient did not develop for some years postsurgery. We postulate that surgical scarring and/or the fundoplication wrap irritates the vagal trunks, which run along the serosal surface of the distal oesophagus inducing sensory-motor reflexes. This symptom postsurgery was so intractable in one of our patients that the fundoplication was taken down and replaced by vertical gastropexy with resolution of symptoms.
There are several limitations affecting the interpretation of our results. The study reports a single-centre experience limiting extrapolation to other units especially given the variable management approaches in the field and the range of surgical expertise undertaking surgery in this challenging group of patients. The survey used a nonvalidated questionnaire (because there are none available for this group of patients). Recall bias could confound the questionnaire results given that it was performed as a cross-sectional survey with variable and, in some patients, an extended period of follow-up between timing of surgery and administration of the questionnaire. In addition, the majority of patients had both fundoplication and gastrostomy (96%) at the time of the latest follow-up, making it difficult to determine to what degree fundoplication surgery alone provided the observed benefit. Nevertheless, despite these limitations, there was a surprising degree of parent/caregiver acceptance to the surgery, particularly in light of recent negative reviews of this treatment (6,7).
In conclusion, our experience with Nissen fundoplication and gastrostomy in patients with a neurological impairment indicates high levels of caregiver satisfaction with the results of surgical intervention when measured 6 years after surgery and low risk of serious surgical complications. Properly conducted clinical trials are needed to clarify the issue of risk versus benefit with this surgery in patients with neurological impairment and GERD. The lack of such trials to date is testament to the difficulty in conducting prospective studies in this group of children.
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