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Feeding problems and weight gain in Duchenne muscular dystrophy
ARTICLE IN PRESS E U R O P E A N J O U R N A L O F PA E D I AT R I C N E U R O L O G Y
10 (2006) 231 – 236
Official Journal of the European Paediatric Neurology Society
Original article
Feeding problems and weight gain in Duchenne muscular dystrophy Marika Panea, Isabella Vastaa, Sonia Messinaa,b, Domenica Sorletic, Annie Aloysiusd, Federico Sciarrae, Fortunato Mangiolae, Maria Kinalid, Enzo Riccif,g, Eugenio Mercuria,d, a
Department of Child Neurology, Policlinico Gemelli, Largo Gemelli 00168, Roma, Italy Department of Neurosciences, Psychiatry and Anaesthesiology, University of Messina, Italy c Department of Paediatrics, University of Messina, Italy d Dubowitz Neuromuscular Centre, Department of Paediatrics, Imperial College, Hammersmith Hospital, London e UILDM Unione Italiana Lotta Distrofia Muscolare Rome, Italy f Department of Neurology Catholic University Rome, Italy g Fondazione Don Carlo Gnocchi Rome, Italy b
art i cle info
A B S T R A C T
Article history:
The aim of the study was to conduct a survey using a dedicated questionnaire to estimate
Received 28 July 2006
feeding difficulties, gastrointestinal involvement and weight gain in a population of 118
Received in revised form
Duchenne muscular dystrophy (DMD) patients (age range 13.80–35.8 years). All the answers
24 August 2006
were entered in a database and the data analysed subdividing the cohort into age groups
Accepted 25 August 2006
(3–9, 9–13, 13–18, 18–24, 24–30, 30–36 years). The results indicate that chewing difficulties are frequent and become increasingly present with age, associated with a progressive
Keywords:
increase of the duration of meals. Episodes of choking or other clinical signs of swallowing
Duchenne muscular dystrophy
difficulties are in contrast much less frequent even after age 18. Aspiration pneumonia
Feeding difficulties
were also not very frequent and only occurred in 7/118.
Swallowing Dysphagia
Clinical signs of gastroesophageal reflux requiring treatment were only found in 5 while 43/118 complained of constipation requiring treatment. Very few of our patients had their weight above 2 SD (n ¼ 4) and this was always found in patients between 9 and 18 years while after this age there was an increasing number of patients with weight below 2 SD. The results of our survey suggest that although choking is one of the most feared complications in patients with DMD, clinical signs of swallowing abnormalities are infrequent when collecting clinical information retrospectively. Further studies using an objective evaluation such as videofluoroscopy are needed to identify minor signs that may not be obvious on clinical examination. & 2006 European Paediatric Neurology Society. Published by Elsevier Ltd. All rights reserved.
Corresponding author. Department of Child Neurology, Policlinico Gemelli, Largo Gemelli 00168, Roma, Italy. Tel.: +39 06 30155340; fax: +39 06 30154363. E-mail address: [email protected] (E. Mercuri). 1090-3798/$ - see front matter & 2006 European Paediatric Neurology Society. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.ejpn.2006.08.008
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1.
E U R O P E A N J O U R N A L O F PA E D I AT R I C N E U R O L O G Y
Introduction
Duchenne muscular dystrophy (DMD) is the most frequent neuromuscular disorder, clinically characterised by progressive muscle weakness leading to loss of ambulation by age 13 years. Frequent complications are progressive respiratory, heart involvement and scoliosis. It has also been reported that nutritional problems are also frequent after the first decade.1 These mainly involve feeding difficulties, gastrointestinal dysfunction and excessive or reduced weight gain. Chewing and swallowing difficulties have been reported in both ambulant and non-ambulant DMD patients2 and this has been related to increased weakness of the masticatory muscles, malocclusion or other abnormalities of the oropharyngeal phase. As a consequence of this, patients may be at risk of food aspiration and aspiration pneumonias. The involvement of gastrointestinal smooth muscle has also been reported.3,4 Gastroparesis and gastric distension can contribute to delayed gastric emptying, gastroesophageal reflux and subsequent nutritional disturbances such as meteorism.5 Constipation is also frequent and may also contribute to a reduced appetite and therefore oral intake.6 Other studies have reported the evolution of weight in DMD. Excessive weight is more common around the time of loss of ambulation and reaches the highest prevalence before 13 years of age. Excessive weight may negatively impact on an already progressively reduced motor function and increase the risk for developing scoliosis. Older patients, in contrast, show a progressive weight loss which is more often noted by 18 years.7 This has been related to several factors including feeding difficulties, inability to self-feed due to progressive weakness and progression of respiratory insufficiency.8 The aim of this study was to conduct a survey using a questionnaire on feeding difficulties, gastrointestinal involvement and weight gain in a large cohort of DMD patients of age ranging between 3 and 35 years and to correlate these findings with other variables such as age, level of motor impairment, use of ventilatory support and other aspects of clinical management.
2.
10 (2006) 231 – 236
cohort of 20 patients with DMD before the beginning of the study and they all appeared to have a good understanding of the questions and completed the questionnaire without any problem. Feeding difficulties were subdivided according whether these were related to the extrabuccal (opening mouth), anterior (keeping food in mouth, chewing) or posterior (choking, repeat attempt to swallow, food aspiration) phases of chewing and swallowing. Dietary modifications including changes in the consistency or quantity of administered food were also recorded. The following part of the questionnaire included questions related to gastrointestinal function, collecting information on presence and frequency of nausea, vomiting, reflux, meteorism and constipation. We also collected data on frequency of chest infections, ventilatory support and gastrostomy placement. Medication or supplements intake was also recorded. Weight, measured in kilograms, was converted in standard deviations and Z-scores according to CDC’s (Centre for Disease Control) growth charts.9
3.
Results
We analysed questionnaires of 118 consecutive DMD patients who all agreed to take part in the survey. Their age ranged from 3.4 to 35.8 years (mean 17.578.3). The cohort was subsequently subdivided into 6 groups according to age (details in Table 1). Thirty-two of the 118 patients were walking independently and 86 were constant wheelchairs users at the time of the survey.
3.1.
Weight
Table 1 shows details of the mean weight and standard deviations in the 6 groups subdivided according to age. All the patients below the age of 9 (groups 1) had weights between 72 SD compared with the standard weight on age appropriate charts for boys. In 6 patients the weight was above 2 SD and these were in group 2 (n ¼ 4) and 3 (n ¼ 2). Thirty-three patients showed a weight below 2 SD with an increasing prevalence with age.
Patients and methods 3.2.
The survey was conducted from January 2005 to January 2006. Participants included patients with diagnosis of DMD, confirmed by muscle biopsy and/or genetic analysis followed at the Paediatric Neurology Unit of the Catholic University and at the main center for diagnosis and rehabilitation of muscle disorders (UILDM Unione Italiana Lotta Distrofia Muscolare) of Rome. Patients were sent a preliminary letter asking for their approval to be part of the study. DMD patients and parents were interviewed by one paediatric neurologists (MP) and one paediatrician (IV) using a semi-structured questionnaire. The study was approved by the Research Ethical Committee of the Catholic University. The questionnaire was designed by a consensus of neurologists, paediatricians and speech and physiotherapists and included questions on weight, feeding abilities and gastrointestinal function. The questionnaire was tested in a small
Feeding difficulties
Difficulties in mouth opening were identified in 12 patients (10%) and were more frequently found in patients older than 24 years (7/29 ¼ 24%, group 5 and 6). Chewing difficulties were reported in 24 patients (20%) and were progressively more frequent with age. Episodes of choking were reported in 21 patients (18%) and they were also more frequent in older patients. Five patients had episodes of choking for both solids, liquids and semisolids, 12 for solids only and 4 for liquids only. The patients reported that choking was not present at each meal and on average, occurred once a week or even less frequently. Dietary changes, mainly consisting in cutting the food in smaller pieces or preference for smooth food were recorded in 31 patients and were also more frequent in older patients. Duration of meal time also progressively increased with age.
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Table 1 – Details on age and weight of DMD patients
Number Age range, (mean-SD) Weight, range, (mean-SD) No. of patients below 2 SD No. of patients above 2 SD
Group 1
Group 2
Group3
Group 4
Group 5
Group 6
19 3.4–8.7 (6.571.8) 15–38 (24.176.5) 0 0
22 9–12.5 (10.770.22) 19–61 (41.9711.0) 1 4
26 13–17.7 (15.171.4) 24–100 (57.5719.3) 4 2
22 18–23.7 (21.571.5) 28–80 (55.8713.9) 10 0
20 24–29.9 (27.471.5) 30–85 (48.0717.1) 13 0
9 30–35.8 (32.371.5) 39.2–80 (51.9712.9) 5 0
Table 2 – Feeding difficulties of DMD patients
Age Number Meal time in minutes (mean-SD) Difficulty opening mouth Difficulty chewing Choking with liquids only Choking with semisolids Choking with solids only Choking on both liquids and solids Dietary modifications Gastrostomy Aspiration pneumonia
Group 1
Group 2
Group 3
Group 4
Group 5
Group 6
3–9 19 18.4 (77.1) 0 1 0 0 1 0 3 0 0
9–13 22 20.9 (711.1) 2 3 0 0 1 0 3 0 0
13–18 26 24.2 (78.3) 1 3 0 0 2 1 4 0 2
18–24 22 25.4 (714.9) 2 6 1 1 3 2 7 2 1
24–30 20 31.4 (718.1) 4 6 3 0 2 1 9 4 2
30–36 9 31.7 (722.9) 3 5 0 0 3 0 5 4 2
Table 3 – Gastrointestinal symptoms of DMD patients
Age Number Gastroesophageal reflux Constipation Meteorism
Group 1
Group 2
Group 3
Group 4
Group 5
Group 6
3–9 19 0 3 0
9–13 22 0 2 3
13–18 26 1 4 3
18–24 22 1 13 7
24–30 20 1 15 10
30–36 9 2 6 4
Only 7 patients (6%) reported episodes of proven aspiration pneumonia. Details of feeding difficulties are shown in Table 2.
3.3.
Gastrointestinal symptoms
In our cohort gastrointestinal symptoms were reported by 56 subjects (47%). Although the majority of patients complained of occasional episodes of heartburn, gastroesophageal reflux requiring pharmaceutical treatment was reported by 5 patients (4%). Forty-three patients complained of constipation (36%) and it was more frequently reported in patients older than 18 years. Constipation was managed with lactulose in 13 of the 43 patients (30%) and with a combination of lactulose and rectal enemas in another 16 patients (37%). Meteorism was reported by 27 patients (23%). Details of gastrointestinal symptoms are shown in Table 3.
3.4.
Treatment with steroids
Thirty-three patients in group 1, 2 and 3 were (n ¼ 29) or had been (n ¼ 4) on intermittent steroids for over a year. None of the patients in group 4 or 5 had been on steroids.
3.5.
Ventilatory support
Twenty-three patients had tracheotomy at mean age of 22.7 (6 in group 4 and 17 in group 5 and 6) and 10 had non-invasive ventilation at mean age of 21.5 (1 in group 3, 3 in group 4, 6 in group 5). Details of ventilatory support are shown in Table 4.
3.6.
Gastrostomy
Gastrostomy was placed in 10/118 (8%) patients at mean age of 23.6 years (range 20–29 yr) (2 in group 4 and 8 in group 5
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Table 4 – Ventilatory support of DMD patients Group1
Group 2
Group 3
Group 4
Group 5
Group 6
3–9 19 0 0
9–13 22 0 0
13–18 26 0 1
18–24 22 6 3
24–30 20 10 6
30–36 9 7 0
Age Number Tracheo NIV
and 6). All 10 had gastrostomy inserted within one year of tracheotomy and were all still regularly having food by mouth.
100% 90% PEG choking normal
80%
3.7.
Steroids and weight
None of the patients in group 1 had a weight below or above 2 SD. Eleven of them were or had been on steroids for at least 1 year. Four of the 22 patients in group 2 had weight above 2 SD, 2 of 4 were on steroids. Another 14 patients in group 2 were or had been on steroids for at least one year and their weight was within 2 SD. Two of the 26 patients in group 3 had weight above 2 SD and none were on steroids. Another 5 patients in group 3 were or had been on steroids for at least 1 year and their weight was within 2 SD. None of the patients in groups 4, 5 and 6 had been on steroids.
70% 60% 50% 40% 30% 20% 10% 0% tracheo (n=23)
3.8.
NIV (n=10)
no ventilation (n=18)
Ventilatory support and feeding difficulties
Fig. 1 shows the prevalence of gastrostomy and choking episodes in patients with no ventilatory support, on nocturnal non invasive ventilation and in those with tracheotomy.
Fig. 1 – Ventilatory support and feeding difficulties. NIV ¼ non invasive ventilation.
100% 90%
3.9.
Ventilatory support and weight
<2SD
80%
>2SD
Fig. 2 shows the percentage of weight within 2 SD, above and below 2 SD in patients with no ventilatory support, on nocturnal non-invasive ventilation and in those with tracheotomy.
70%
within 2SD
60% 50% 40%
4.
Discussion
30% 20%
Although in the last few years increasing attention has been devoted to the assessment and management of feeding difficulties in patients with neuromuscular disorders, only a few studies have systematically assessed feeding difficulties in patients with DMD.3,8,10,11 Even less has been reported regarding their management and treatment. As a consequence of this, DMD patients and their families are often anxious about the possible onset of such problems that have been reported as a common complication of DMD.12 The aim of our study was to evaluate the prevalence of feeding problems in a population of DMD patients of different ages. Problems included difficulty chewing food, abnormal swallowing and presence of gastrooesophageal reflux. We were also interested to establish the presence of poor and excessive weight gain and the possible associations with feeding problems and with age.
10% 0% tracheo (n=23)
NIV (n=10)
no ventilation (n=18)
Fig. 2 – Ventilatory support and weight. NIV ¼ non invasive ventilation. Feeding problems were overall present in less than 28% of the patients with chewing difficulties being the most frequently observed problem (20%). They were relatively uncommon in patients younger than 18 and their presence progressively increased with age. In most cases chewing difficulties were associated with difficulties in opening the mouth. Such difficulties have been previously explained by masticatory muscles weakness, that has been reported in
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clinical11 and electrophysiological studies and may also be attributed to secondary malocclusion patterns.13,14 or to macroglossia that have not been systematically assessed in our cohort. Most patients above the age of 18 perceived meals as stressful because of fear of choking but choking episodes and subjective symptoms of swallowing difficulties were only present in 21 of the 118 patients interviewed (18%). Our prevalence is much lower of those reported in a previous study reporting abnormal choking in approximately 30% of DMD patients even if their cohorts only included patients younger than 25 years.4,7 Swallowing difficulties mainly consisted of episodes of choking on solids as well as on liquids in 4 cases. Evidence of choking on liquids only was rare. Food aspiration is the most feared consequence associated with choking, due to the associated strong risk of aspiration pneumonia. Children with severe neurological disability have been reported as having a high prevalence of aspiration at 68–70%15,16 but the prevalence of these episodes has not been previously assessed in DMD. None of our patients had videfluoroscopy that is the gold standard in the diagnosis of swallowing disorder17 and we therefore cannot establish whether and to what extent the choking episodes correlate to pharyngeal weakness, silent aspiration4 or to abnormalities of the oral phase that have been reported in patients affected by other forms of myopathies.18 It is of interest however that in all these patients choking was only occasional (once a week or less) and chest infections were usually secondary to upper respiratory infections with only 7 having clear evidence of aspiration pneumonia. The results of chest radiographs however were not always available as the acute episodes were usually seen at local hospitals, and we cannot exclude that other episodes may have occurred in other patients. The length of meal time also increased with age ranging from a mean of 18 min in younger patients to a mean of 32 min in the older patients. The increasing length was probably related to a combination of increasing weakness of the masticatory muscles and difficulties in chewing and swallowing difficulties. The increased length of meal time with age was also associated with an increased number of patients who introduced dietary modifications. Many of the patients and their families were aware of these symptoms as a part of their condition and even in absence of choking episodes or other signs of possible swallowing difficulties, had introduced dietary modifications including cutting the food in small pieces or preference for pure´ed food in order to facilitate chewing and reduce meal time. Another possible variable that may have influenced meal time length is the ability self feeding but this was not considered at the time of data collection. Gastric emptying delay and/or acute gastrointestinal dilatation have been shown to characterize the clinical disease course in DMD.19,20 Surprisingly, relatively few of our patients complained of recurrent signs of gastroesophageal reflux that is often promoted by gastroparesis and gastric distension.5 In contrast, over 60% of the patients older than 18 had constipation suggesting gastric and bowel motility derangement possibly due to an altered function of smooth muscle cells.6
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235
Failure to thrive or increased weight gain were frequently observed in our cohort (33%) though there were different trends of weight gain in different age bands. Previous studies have reported that 44–54% of dystrophic children are obese by the age of 13.7,21 Although a direct comparison with the previous studies cannot be made because of different inclusion criteria and methods, it is of interest that only 6 patients in the whole cohort (5%) had a weight for age above 2 SD compared with the standard weight for age chart for boys. Most of the boys with weight above 2 SD were between 9 and 13 years and the lower incidence of weight gain in our cohort compared to previous studies is even more surprising considering that 17 out of 22 of the patients included in this age range were on intermittent regime of steroids. The same studies also suggest that approximately 50% of DMD patients are underweight by the age of 18.7,21 In our cohort the number of patients between 13 and 18 who had a weight below 2 SD for their age was much smaller (4/26 ¼ 26% in the age band) but the percentage raises to 45% in the group between 18 and 24 and further progressively increases with age. Our results clearly suggest that there is an increasing weight loss with age. This can be attributed not only to the progressive loss of muscle bulk and to increasing feeding difficulties but also to other factors such as progressive respiratory impairment, both as recurrent chest infections and nocturnal hypoventilation that have been reported to affect weight gain. These results should therefore be interpreted with caution as the assessment and management of some of these aspects has dramatically improved over the years and the dramatic failure to thrive observed in our older patients probably also reflect differences of clinical management over the years. While younger patients are routinely assessed with spirometry and overnight sleep studies of oxygen saturation and are referred for non-invasive ventilation as soon as the first signs of respiratory failure is detected, before 1998 a similar management was not routinely available and this may have played an important role in their failure to thrive. With increasing survival22 other aspects of management have also improved and while in the past gastrostomy was rarely performed, often in combination with tracheotomy, there is now increasing evidence suggesting that this is an option to be considered not only in patients with unsafe swallowing but also in those with severe failure to thrive. Although the aim of our study was to have a general overview of feeding problems, nevertheless our results suggest a few considerations. Although swallowing problems are one the most feared complicances even in young DMD patients, in our cohort overt clinical signs of swallowing difficulties appear to be relatively rare, especially before the age of 18, as suggested by the low prevalence of choking difficulties and aspiration pneumonia. Clinical evaluation is necessary for determining comprehensive feeding strategies and recommendations23,24 but may fail to detect penetration and aspiration and is not able to assess accurately the pharyngeal and oesophageal stages of swallowing.25–30 Further prospective studies using a more systematic approach with chest radiography at the time of acute chest infections and video fluoroscopy in the cases with suspicious
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clinical signs are needed to objectively assess swallowing problems. Our results also suggest that a multidisciplinary team approach, including speech therapist, dietician, neurologist, pneumologists is needed to evaluate and managing feeding problems. A systematic evaluation of weight gain feeding abilities and respiratory function should be part of the routine medical examination in order to identify early signs of failure to thrive and the best options of management. At present the main treatment options for feeding problems are dietary manipulation, such as altering the consistency of food, adopting safe swallowing techniques, surgical interventions and enteral feeding but no systematic randomised study has been performed to establish the value of these or other options, as recently highlighted by a Cochrane review on management and therapy for dysphagia in chronic muscle disease.12 Further prospective interventional studies are therefore needed to establish which intervention is most effective in managing swallowing difficulties in DMD and other neuromuscular disorders. R E F E R E N C E S
1. Dubowitz V. Muscle disorders in childhood, 2nd ed. London: Saunders; 1995. 2. Willig TN, Paulus J, Lacau Saint Guily J, Beon C, Navarro J. Swallowing problems in neuromuscular disorders. Arc Phys Med Rehab 1994;75:1175–81. 3. Nowak TV, Ionasesku V, Ingman E, et al. Gastrointestinal manifestation of muscular dystrophies. Gastroenterology 1982;82:800–10. 4. Jaffe KM, Mc Donald CM, Ingman E, Haas J. Symptoms of upper gastrointestinal dysfunction in duchenne muscular dystrophy. Case-control study. Arch Phys Med Rehab 1990;71:742–4. 5. Orlando RC. Pathogenesis of gastroesophageal reflux disease. Am J Med Sci 2003;326:274–8. 6. Borrelli O, Salvia G, Mancini V. Evolution of gastric electrical features and gastric emptying in children with Duchenne and Becker Muscular Dystrophy. Am J Gastroenterol 2005;100(3):695–702. 7. Willig TN, Carlier L, Legrand M, et al. Nutritional assessment in Duchenne Muscular Dystrophy. Dev Med Child Neurol 1993;35:1074–82. 8. Willig TN, Gilardeau C, Kazandjian, et al. Dysphagia and nutrition in neuromuscular disorders. In: Bach JR, editor. Pulmonary rehabilitation: the obstructive and paralytic conditions. Philadelphia: Hanley and Belfus; 1996. p. 353–69. 9. Kuczmarski RJ, Ogden CL, Guo SS, et al. CDC growth chart for the United States: Methods and Development. Vital Health Stat; 11 (246) National Center for Health statistics, 2002. 10. Hamada T, Kobayashi M, Kawazoa Y. Electromyographic activity of masticatory muscles in patients with progressive muscular dystrophy (Duchenne type): relation between integrated electromyographic activity and biting force. Spec Care Dentist 1981;1:37–8.
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11. Hamada T, Kawazoa Y, Imada K, Kobayashi M, Ii K, Yamada S. Maximum biting forces in the patients with progressive muscular dystrophy. J Hiroshima Univ Dent Soc 1975;7:159–61. 12. Hill M, Hughes T, Milford C. Treatment for swallowing difficulties (dysphagia) in chronic muscle disease. Cochrane Database Systemat Rev 2005(4). 13. Ghafari J, Clark RE, Shofer FS, Bermen PH. Dental and occlusal characteristics of children with neuromuscular disease. Am J Orthop Dentofac Orthop 1988;93:126–32. 14. Ertu¨rk N, Dogan S. The effect of neuromuscular disease on the development of dental and occlusal characteristics. Quintessence Int 1991;22:317–21. 15. Griggs GA, Findley LJ, Suratt PM, Esau SA, Wilhoit SC, Rochester DF. Prolonged relaxation rate of inspiratory muscles in patients with sleep apnea. Am Rev Respir Dis 1989;140:706–10. 16. Mirrett PL, Riski JE, Glascott J, Johnson V. Videofluoroscopic assessment of dysphagia in children with severe spastic cerebral palsy. Dysphagia 1994;9:3174–9. 17. De Matteo C, Matovich D, Hjartarson A. Comparison of clinical and videofluoroscopic evaluation of children with feeding and swallowing difficulties. Dev Med Child Neurol 2005;47:149–55. 18. Philpot J, Bagnall A, King C, Dubowitz V, Muntoni F. Feeding problems in meosin deficient congenital muscular dystrophy. Arch Dis Child 1999;80:542–7. 19. Barohn RJ, Levine EJ, et al. Gastric hypo motility in Duchenne’s Muscular Dystrophy. N Engl J Med 1988;319:15–8. 20. Leon SH, Schuffler MD, Kettler M, et al. Chronic intestinal pseudo obstruction as complication of Duchenne’s Muscular Dystrophy. Gastroenterology 1986;90:455–9. 21. McDonald CM, Abresch RT, Carter GT, et al. Profiles of neuromuscular diseases Duchenne muscular dystrophy. Am J Phys Med Rehab 1995;74:S70. 22. Eagle M, Baudonin SV, Chaudler C, et al. Survival in Duchenne muscular dystrophy: improvements in life expectancy since 1967 and the impact of home nocturnal ventilation. Neuromuscular disorder 2002;12:926–9. 23. Bacon MJ, Smith C. Videofluoroscopic evaluation of swallowing. AJR Am J Roentgenol 1994;163:223–5. 24. Sheckman B, Manno CJ. Dysphagia in infants and children with oral-motor deficits: assessment and management. Semin Speech Lang 1996;17:283–309. 25. Linden P. Videofluoroscopy in the rehabilitation of swallowing disfunction. Dysphagia 1989;3:189–91. 26. Zerilli KS, Stefans VA, DiPietro MA. Protocol for the use of videofluoroscopy in pediatric swallowing dysfunction. Am J Occup Ther 1990;44:441–6. 27. Groher ME. The detection of aspiration and videofluoroscopy. Dysphagia 1994;9:147–8. 28. Zenner PM, Losinski DS, Mills RH. Using cervical auscultation in the clinical dysphagia examination in long-term care. Dysphagia 1995;10:27–31. 29. Wright RE, Wright FR, Carson CA. Videofluoroscopy assessment in children with severe cerebral palsy presenting with dysphagia. Pediatr Radiol 1996;26:720–2. 30. Leder SB. Videofluoroscopic evaluation of aspiration with visual examination of the gag reflex and velar movement. Dysphagia 1997;12:21–3.
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Official Journal of the European Paediatric Neurology Society
Original article
Feeding problems and weight gain in Duchenne muscular dystrophy Marika Panea, Isabella Vastaa, Sonia Messinaa,b, Domenica Sorletic, Annie Aloysiusd, Federico Sciarrae, Fortunato Mangiolae, Maria Kinalid, Enzo Riccif,g, Eugenio Mercuria,d, a
Department of Child Neurology, Policlinico Gemelli, Largo Gemelli 00168, Roma, Italy Department of Neurosciences, Psychiatry and Anaesthesiology, University of Messina, Italy c Department of Paediatrics, University of Messina, Italy d Dubowitz Neuromuscular Centre, Department of Paediatrics, Imperial College, Hammersmith Hospital, London e UILDM Unione Italiana Lotta Distrofia Muscolare Rome, Italy f Department of Neurology Catholic University Rome, Italy g Fondazione Don Carlo Gnocchi Rome, Italy b
art i cle info
A B S T R A C T
Article history:
The aim of the study was to conduct a survey using a dedicated questionnaire to estimate
Received 28 July 2006
feeding difficulties, gastrointestinal involvement and weight gain in a population of 118
Received in revised form
Duchenne muscular dystrophy (DMD) patients (age range 13.80–35.8 years). All the answers
24 August 2006
were entered in a database and the data analysed subdividing the cohort into age groups
Accepted 25 August 2006
(3–9, 9–13, 13–18, 18–24, 24–30, 30–36 years). The results indicate that chewing difficulties are frequent and become increasingly present with age, associated with a progressive
Keywords:
increase of the duration of meals. Episodes of choking or other clinical signs of swallowing
Duchenne muscular dystrophy
difficulties are in contrast much less frequent even after age 18. Aspiration pneumonia
Feeding difficulties
were also not very frequent and only occurred in 7/118.
Swallowing Dysphagia
Clinical signs of gastroesophageal reflux requiring treatment were only found in 5 while 43/118 complained of constipation requiring treatment. Very few of our patients had their weight above 2 SD (n ¼ 4) and this was always found in patients between 9 and 18 years while after this age there was an increasing number of patients with weight below 2 SD. The results of our survey suggest that although choking is one of the most feared complications in patients with DMD, clinical signs of swallowing abnormalities are infrequent when collecting clinical information retrospectively. Further studies using an objective evaluation such as videofluoroscopy are needed to identify minor signs that may not be obvious on clinical examination. & 2006 European Paediatric Neurology Society. Published by Elsevier Ltd. All rights reserved.
Corresponding author. Department of Child Neurology, Policlinico Gemelli, Largo Gemelli 00168, Roma, Italy. Tel.: +39 06 30155340; fax: +39 06 30154363. E-mail address: [email protected] (E. Mercuri). 1090-3798/$ - see front matter & 2006 European Paediatric Neurology Society. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.ejpn.2006.08.008
ARTICLE IN PRESS 232
1.
E U R O P E A N J O U R N A L O F PA E D I AT R I C N E U R O L O G Y
Introduction
Duchenne muscular dystrophy (DMD) is the most frequent neuromuscular disorder, clinically characterised by progressive muscle weakness leading to loss of ambulation by age 13 years. Frequent complications are progressive respiratory, heart involvement and scoliosis. It has also been reported that nutritional problems are also frequent after the first decade.1 These mainly involve feeding difficulties, gastrointestinal dysfunction and excessive or reduced weight gain. Chewing and swallowing difficulties have been reported in both ambulant and non-ambulant DMD patients2 and this has been related to increased weakness of the masticatory muscles, malocclusion or other abnormalities of the oropharyngeal phase. As a consequence of this, patients may be at risk of food aspiration and aspiration pneumonias. The involvement of gastrointestinal smooth muscle has also been reported.3,4 Gastroparesis and gastric distension can contribute to delayed gastric emptying, gastroesophageal reflux and subsequent nutritional disturbances such as meteorism.5 Constipation is also frequent and may also contribute to a reduced appetite and therefore oral intake.6 Other studies have reported the evolution of weight in DMD. Excessive weight is more common around the time of loss of ambulation and reaches the highest prevalence before 13 years of age. Excessive weight may negatively impact on an already progressively reduced motor function and increase the risk for developing scoliosis. Older patients, in contrast, show a progressive weight loss which is more often noted by 18 years.7 This has been related to several factors including feeding difficulties, inability to self-feed due to progressive weakness and progression of respiratory insufficiency.8 The aim of this study was to conduct a survey using a questionnaire on feeding difficulties, gastrointestinal involvement and weight gain in a large cohort of DMD patients of age ranging between 3 and 35 years and to correlate these findings with other variables such as age, level of motor impairment, use of ventilatory support and other aspects of clinical management.
2.
10 (2006) 231 – 236
cohort of 20 patients with DMD before the beginning of the study and they all appeared to have a good understanding of the questions and completed the questionnaire without any problem. Feeding difficulties were subdivided according whether these were related to the extrabuccal (opening mouth), anterior (keeping food in mouth, chewing) or posterior (choking, repeat attempt to swallow, food aspiration) phases of chewing and swallowing. Dietary modifications including changes in the consistency or quantity of administered food were also recorded. The following part of the questionnaire included questions related to gastrointestinal function, collecting information on presence and frequency of nausea, vomiting, reflux, meteorism and constipation. We also collected data on frequency of chest infections, ventilatory support and gastrostomy placement. Medication or supplements intake was also recorded. Weight, measured in kilograms, was converted in standard deviations and Z-scores according to CDC’s (Centre for Disease Control) growth charts.9
3.
Results
We analysed questionnaires of 118 consecutive DMD patients who all agreed to take part in the survey. Their age ranged from 3.4 to 35.8 years (mean 17.578.3). The cohort was subsequently subdivided into 6 groups according to age (details in Table 1). Thirty-two of the 118 patients were walking independently and 86 were constant wheelchairs users at the time of the survey.
3.1.
Weight
Table 1 shows details of the mean weight and standard deviations in the 6 groups subdivided according to age. All the patients below the age of 9 (groups 1) had weights between 72 SD compared with the standard weight on age appropriate charts for boys. In 6 patients the weight was above 2 SD and these were in group 2 (n ¼ 4) and 3 (n ¼ 2). Thirty-three patients showed a weight below 2 SD with an increasing prevalence with age.
Patients and methods 3.2.
The survey was conducted from January 2005 to January 2006. Participants included patients with diagnosis of DMD, confirmed by muscle biopsy and/or genetic analysis followed at the Paediatric Neurology Unit of the Catholic University and at the main center for diagnosis and rehabilitation of muscle disorders (UILDM Unione Italiana Lotta Distrofia Muscolare) of Rome. Patients were sent a preliminary letter asking for their approval to be part of the study. DMD patients and parents were interviewed by one paediatric neurologists (MP) and one paediatrician (IV) using a semi-structured questionnaire. The study was approved by the Research Ethical Committee of the Catholic University. The questionnaire was designed by a consensus of neurologists, paediatricians and speech and physiotherapists and included questions on weight, feeding abilities and gastrointestinal function. The questionnaire was tested in a small
Feeding difficulties
Difficulties in mouth opening were identified in 12 patients (10%) and were more frequently found in patients older than 24 years (7/29 ¼ 24%, group 5 and 6). Chewing difficulties were reported in 24 patients (20%) and were progressively more frequent with age. Episodes of choking were reported in 21 patients (18%) and they were also more frequent in older patients. Five patients had episodes of choking for both solids, liquids and semisolids, 12 for solids only and 4 for liquids only. The patients reported that choking was not present at each meal and on average, occurred once a week or even less frequently. Dietary changes, mainly consisting in cutting the food in smaller pieces or preference for smooth food were recorded in 31 patients and were also more frequent in older patients. Duration of meal time also progressively increased with age.
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Table 1 – Details on age and weight of DMD patients
Number Age range, (mean-SD) Weight, range, (mean-SD) No. of patients below 2 SD No. of patients above 2 SD
Group 1
Group 2
Group3
Group 4
Group 5
Group 6
19 3.4–8.7 (6.571.8) 15–38 (24.176.5) 0 0
22 9–12.5 (10.770.22) 19–61 (41.9711.0) 1 4
26 13–17.7 (15.171.4) 24–100 (57.5719.3) 4 2
22 18–23.7 (21.571.5) 28–80 (55.8713.9) 10 0
20 24–29.9 (27.471.5) 30–85 (48.0717.1) 13 0
9 30–35.8 (32.371.5) 39.2–80 (51.9712.9) 5 0
Table 2 – Feeding difficulties of DMD patients
Age Number Meal time in minutes (mean-SD) Difficulty opening mouth Difficulty chewing Choking with liquids only Choking with semisolids Choking with solids only Choking on both liquids and solids Dietary modifications Gastrostomy Aspiration pneumonia
Group 1
Group 2
Group 3
Group 4
Group 5
Group 6
3–9 19 18.4 (77.1) 0 1 0 0 1 0 3 0 0
9–13 22 20.9 (711.1) 2 3 0 0 1 0 3 0 0
13–18 26 24.2 (78.3) 1 3 0 0 2 1 4 0 2
18–24 22 25.4 (714.9) 2 6 1 1 3 2 7 2 1
24–30 20 31.4 (718.1) 4 6 3 0 2 1 9 4 2
30–36 9 31.7 (722.9) 3 5 0 0 3 0 5 4 2
Table 3 – Gastrointestinal symptoms of DMD patients
Age Number Gastroesophageal reflux Constipation Meteorism
Group 1
Group 2
Group 3
Group 4
Group 5
Group 6
3–9 19 0 3 0
9–13 22 0 2 3
13–18 26 1 4 3
18–24 22 1 13 7
24–30 20 1 15 10
30–36 9 2 6 4
Only 7 patients (6%) reported episodes of proven aspiration pneumonia. Details of feeding difficulties are shown in Table 2.
3.3.
Gastrointestinal symptoms
In our cohort gastrointestinal symptoms were reported by 56 subjects (47%). Although the majority of patients complained of occasional episodes of heartburn, gastroesophageal reflux requiring pharmaceutical treatment was reported by 5 patients (4%). Forty-three patients complained of constipation (36%) and it was more frequently reported in patients older than 18 years. Constipation was managed with lactulose in 13 of the 43 patients (30%) and with a combination of lactulose and rectal enemas in another 16 patients (37%). Meteorism was reported by 27 patients (23%). Details of gastrointestinal symptoms are shown in Table 3.
3.4.
Treatment with steroids
Thirty-three patients in group 1, 2 and 3 were (n ¼ 29) or had been (n ¼ 4) on intermittent steroids for over a year. None of the patients in group 4 or 5 had been on steroids.
3.5.
Ventilatory support
Twenty-three patients had tracheotomy at mean age of 22.7 (6 in group 4 and 17 in group 5 and 6) and 10 had non-invasive ventilation at mean age of 21.5 (1 in group 3, 3 in group 4, 6 in group 5). Details of ventilatory support are shown in Table 4.
3.6.
Gastrostomy
Gastrostomy was placed in 10/118 (8%) patients at mean age of 23.6 years (range 20–29 yr) (2 in group 4 and 8 in group 5
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Table 4 – Ventilatory support of DMD patients Group1
Group 2
Group 3
Group 4
Group 5
Group 6
3–9 19 0 0
9–13 22 0 0
13–18 26 0 1
18–24 22 6 3
24–30 20 10 6
30–36 9 7 0
Age Number Tracheo NIV
and 6). All 10 had gastrostomy inserted within one year of tracheotomy and were all still regularly having food by mouth.
100% 90% PEG choking normal
80%
3.7.
Steroids and weight
None of the patients in group 1 had a weight below or above 2 SD. Eleven of them were or had been on steroids for at least 1 year. Four of the 22 patients in group 2 had weight above 2 SD, 2 of 4 were on steroids. Another 14 patients in group 2 were or had been on steroids for at least one year and their weight was within 2 SD. Two of the 26 patients in group 3 had weight above 2 SD and none were on steroids. Another 5 patients in group 3 were or had been on steroids for at least 1 year and their weight was within 2 SD. None of the patients in groups 4, 5 and 6 had been on steroids.
70% 60% 50% 40% 30% 20% 10% 0% tracheo (n=23)
3.8.
NIV (n=10)
no ventilation (n=18)
Ventilatory support and feeding difficulties
Fig. 1 shows the prevalence of gastrostomy and choking episodes in patients with no ventilatory support, on nocturnal non invasive ventilation and in those with tracheotomy.
Fig. 1 – Ventilatory support and feeding difficulties. NIV ¼ non invasive ventilation.
100% 90%
3.9.
Ventilatory support and weight
<2SD
80%
>2SD
Fig. 2 shows the percentage of weight within 2 SD, above and below 2 SD in patients with no ventilatory support, on nocturnal non-invasive ventilation and in those with tracheotomy.
70%
within 2SD
60% 50% 40%
4.
Discussion
30% 20%
Although in the last few years increasing attention has been devoted to the assessment and management of feeding difficulties in patients with neuromuscular disorders, only a few studies have systematically assessed feeding difficulties in patients with DMD.3,8,10,11 Even less has been reported regarding their management and treatment. As a consequence of this, DMD patients and their families are often anxious about the possible onset of such problems that have been reported as a common complication of DMD.12 The aim of our study was to evaluate the prevalence of feeding problems in a population of DMD patients of different ages. Problems included difficulty chewing food, abnormal swallowing and presence of gastrooesophageal reflux. We were also interested to establish the presence of poor and excessive weight gain and the possible associations with feeding problems and with age.
10% 0% tracheo (n=23)
NIV (n=10)
no ventilation (n=18)
Fig. 2 – Ventilatory support and weight. NIV ¼ non invasive ventilation. Feeding problems were overall present in less than 28% of the patients with chewing difficulties being the most frequently observed problem (20%). They were relatively uncommon in patients younger than 18 and their presence progressively increased with age. In most cases chewing difficulties were associated with difficulties in opening the mouth. Such difficulties have been previously explained by masticatory muscles weakness, that has been reported in
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clinical11 and electrophysiological studies and may also be attributed to secondary malocclusion patterns.13,14 or to macroglossia that have not been systematically assessed in our cohort. Most patients above the age of 18 perceived meals as stressful because of fear of choking but choking episodes and subjective symptoms of swallowing difficulties were only present in 21 of the 118 patients interviewed (18%). Our prevalence is much lower of those reported in a previous study reporting abnormal choking in approximately 30% of DMD patients even if their cohorts only included patients younger than 25 years.4,7 Swallowing difficulties mainly consisted of episodes of choking on solids as well as on liquids in 4 cases. Evidence of choking on liquids only was rare. Food aspiration is the most feared consequence associated with choking, due to the associated strong risk of aspiration pneumonia. Children with severe neurological disability have been reported as having a high prevalence of aspiration at 68–70%15,16 but the prevalence of these episodes has not been previously assessed in DMD. None of our patients had videfluoroscopy that is the gold standard in the diagnosis of swallowing disorder17 and we therefore cannot establish whether and to what extent the choking episodes correlate to pharyngeal weakness, silent aspiration4 or to abnormalities of the oral phase that have been reported in patients affected by other forms of myopathies.18 It is of interest however that in all these patients choking was only occasional (once a week or less) and chest infections were usually secondary to upper respiratory infections with only 7 having clear evidence of aspiration pneumonia. The results of chest radiographs however were not always available as the acute episodes were usually seen at local hospitals, and we cannot exclude that other episodes may have occurred in other patients. The length of meal time also increased with age ranging from a mean of 18 min in younger patients to a mean of 32 min in the older patients. The increasing length was probably related to a combination of increasing weakness of the masticatory muscles and difficulties in chewing and swallowing difficulties. The increased length of meal time with age was also associated with an increased number of patients who introduced dietary modifications. Many of the patients and their families were aware of these symptoms as a part of their condition and even in absence of choking episodes or other signs of possible swallowing difficulties, had introduced dietary modifications including cutting the food in small pieces or preference for pure´ed food in order to facilitate chewing and reduce meal time. Another possible variable that may have influenced meal time length is the ability self feeding but this was not considered at the time of data collection. Gastric emptying delay and/or acute gastrointestinal dilatation have been shown to characterize the clinical disease course in DMD.19,20 Surprisingly, relatively few of our patients complained of recurrent signs of gastroesophageal reflux that is often promoted by gastroparesis and gastric distension.5 In contrast, over 60% of the patients older than 18 had constipation suggesting gastric and bowel motility derangement possibly due to an altered function of smooth muscle cells.6
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Failure to thrive or increased weight gain were frequently observed in our cohort (33%) though there were different trends of weight gain in different age bands. Previous studies have reported that 44–54% of dystrophic children are obese by the age of 13.7,21 Although a direct comparison with the previous studies cannot be made because of different inclusion criteria and methods, it is of interest that only 6 patients in the whole cohort (5%) had a weight for age above 2 SD compared with the standard weight for age chart for boys. Most of the boys with weight above 2 SD were between 9 and 13 years and the lower incidence of weight gain in our cohort compared to previous studies is even more surprising considering that 17 out of 22 of the patients included in this age range were on intermittent regime of steroids. The same studies also suggest that approximately 50% of DMD patients are underweight by the age of 18.7,21 In our cohort the number of patients between 13 and 18 who had a weight below 2 SD for their age was much smaller (4/26 ¼ 26% in the age band) but the percentage raises to 45% in the group between 18 and 24 and further progressively increases with age. Our results clearly suggest that there is an increasing weight loss with age. This can be attributed not only to the progressive loss of muscle bulk and to increasing feeding difficulties but also to other factors such as progressive respiratory impairment, both as recurrent chest infections and nocturnal hypoventilation that have been reported to affect weight gain. These results should therefore be interpreted with caution as the assessment and management of some of these aspects has dramatically improved over the years and the dramatic failure to thrive observed in our older patients probably also reflect differences of clinical management over the years. While younger patients are routinely assessed with spirometry and overnight sleep studies of oxygen saturation and are referred for non-invasive ventilation as soon as the first signs of respiratory failure is detected, before 1998 a similar management was not routinely available and this may have played an important role in their failure to thrive. With increasing survival22 other aspects of management have also improved and while in the past gastrostomy was rarely performed, often in combination with tracheotomy, there is now increasing evidence suggesting that this is an option to be considered not only in patients with unsafe swallowing but also in those with severe failure to thrive. Although the aim of our study was to have a general overview of feeding problems, nevertheless our results suggest a few considerations. Although swallowing problems are one the most feared complicances even in young DMD patients, in our cohort overt clinical signs of swallowing difficulties appear to be relatively rare, especially before the age of 18, as suggested by the low prevalence of choking difficulties and aspiration pneumonia. Clinical evaluation is necessary for determining comprehensive feeding strategies and recommendations23,24 but may fail to detect penetration and aspiration and is not able to assess accurately the pharyngeal and oesophageal stages of swallowing.25–30 Further prospective studies using a more systematic approach with chest radiography at the time of acute chest infections and video fluoroscopy in the cases with suspicious
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clinical signs are needed to objectively assess swallowing problems. Our results also suggest that a multidisciplinary team approach, including speech therapist, dietician, neurologist, pneumologists is needed to evaluate and managing feeding problems. A systematic evaluation of weight gain feeding abilities and respiratory function should be part of the routine medical examination in order to identify early signs of failure to thrive and the best options of management. At present the main treatment options for feeding problems are dietary manipulation, such as altering the consistency of food, adopting safe swallowing techniques, surgical interventions and enteral feeding but no systematic randomised study has been performed to establish the value of these or other options, as recently highlighted by a Cochrane review on management and therapy for dysphagia in chronic muscle disease.12 Further prospective interventional studies are therefore needed to establish which intervention is most effective in managing swallowing difficulties in DMD and other neuromuscular disorders. R E F E R E N C E S
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