Swallowing abnormalities in HIV infected children: an important cause of morbidity
© Nel and Ellis; licensee BioMed Central Ltd. 2012
Received: 1 November 2011
Accepted: 5 June 2012
Published: 14 June 2012
Swallowing disorders, well recognised in adults, contribute to HIV-infection morbidity. Little data however is available for HIV-infected children. The purpose of this study is to describe swallowing disorders in a group of HIV-infected children in Africa after the introduction of combined anti-retroviral therapy.
We describe 25 HIV-infected children referred for possible swallowing disorders. Clinical and videofluoroscopic assessment of swallowing (VFSS), HIV stage, and respiratory and neurological examination were recorded.
Median age was 8 months (range 2.8-92) and 15 (60%) were male. Fifteen (60%) were referred for recurrent respiratory complaints, 4 (16%) for poor growth, 4 (16%) for poor feeding and 2 (8%) patients for respiratory complaints and either poor growth or feeding. Twenty patients (80%) had clinical evidence of swallowing abnormalities: 11 (44%) in the oral phase, 4 (16%) in the pharyngeal phase, and 5 (25%) in both the oral and pharyngeal phases. Thirteen patients had a videofluoroscopic assessment of which 6 (46%) where abnormal. Abnormalities were detected in the oral phase in 2, in the pharyngeal phase in 3, and in the oral and pharyngeal phase in 1; all of these patients also had evidence of respiratory involvement. Abnormal swallowing occurred in 85% of children with central nervous system disease. CNS disease was due to HIV encephalopathy (8) and miscellaneous central nervous system diseases (5). Three of 4 (75%) patients with thrush had an abnormal oral phase on assessment. No abnormalities of the oesophagus were found.
This report highlights the importance of swallowing disorders in HIV infected children. Most patients have functional rather than structural or mucosal abnormalities. VFSS makes an important contribution to the diagnosis and management of these patients.
Swallowing disorders, often unrecognized in AIDS and other chronic diseases, significantly reduce quality of life  and increase morbidity and mortality: nutrition is adversely affected , the ability to take medication is reduced  and serious complications such as aspiration pneumonia  may occur. The causes of swallowing disorders are multi-factorial and include infections of the mouth, pharynx and esophagus, functional abnormalities of swallowing, and structural abnormalities of the oral cavity, pharynx and esophagus. Early diagnosis and treatment of these disorders may improve the outcome of HIV infected patients .
A wide range of swallowing difficulties occurs in HIV infected adults. Almost 80% of adults in an HIV clinic in South Africa  reported symptoms of swallowing disorders that adversely affected quality of life. Odynophagia and difficulty swallowing specific foods were common: the oral, pharyngeal, and oesophageal phases of swallowing were involved. Although patients with lower CD4 counts had more severe symptoms, even patients who were not severely immune compromised often had swallowing abnormalities.
Videofluoroscopic studies of HIV infected adults  with dysphagia show abnormalities in the oral and pharyngeal phases of swallowing, often in the absence of signs of oesophagitis or local pathology of the mouth or pharynx. Aspiration, that is often silent, is common and may lead to pneumonia.
The limited pediatric data that is available precedes the introduction of combination anti-retroviral therapy (cART). Forty-five percent of children with AIDS in a case-series preceding the introduction of cART had dysphagia . Of these, 24% had thrush, 48% had developmental delay, and 12% had progressive encephalopathy. Most patients had improved oral intake and weight gain with manipulations such as postural changes during feeds and dietary changes. However, little is known about swallowing disorders after the introduction of combined anti-retroviral treatment (cART) or in HIV-infected children in Africa.
We describe our experience with HIV-infected children referred for assessment of swallowing at Tygerberg Children’s Hospital in Cape Town, South Africa, a referral unit in a high HIV prevalence area. It is estimated that 16% of women attending antenatal clinics in the Western Cape Province in South Africa are HIV infected  and that 1.1% of children between 2 and 14 years are HIV infected .
Twenty-five HIV infected children were referred for suspected swallowing disorders from June 2006 through March 2009. Clinical details (HIV stage, presence of neurological disease, HIV encephalopathy, lung disease) were obtained from patient records.
Clinical assessment of feeding, as described by Logemann [8, 9], was performed. This assessment includes examination of oral anatomy for malformations or muscle weakness, of posture and the presence of reflexes of swallowing, coughing or gagging. The speech and language therapist also observes the patient for signs of aspiration during feeding and swallowing. Patients were referred for a videofluoroscopic swallow study (VFSS) if a pharyngeal swallowing abnormality or aspiration were suspected.
Standard videofluoroscopy equipment was used. Children were positioned supine or standing depending on age and motor skills. Every child received a routine upper gastrointestinal series prior to the videofluoroscopy to assess the upper gastrointestinal tract. Children were given Omnipague® first to assess for aspiration before thin barium was given. Thin barium (diluted with water) was given via syringe or bottle depending on the feeding skills of the child. In children older than 3 months, thickened barium was also presented as a puree or syrup consistency with a spoon.
After the videofluoroscopy, the radiologist and speech and language therapist commented on the oral and pharyngeal phases, timing of swallow, and aspiration (silent or symptomatic). Specific strategies to promote oral feeding and other long-term feeding options were suggested.
HIV infection was diagnosed by HIV RNA PCR in children below age 15 months and HIV-specific antibodies by ELISA in children over 15 months. CD4 counts are expressed as absolute counts and percentages. Clinical and immunological staging are according to the World Health Organisation (WHO) guidelines for immunological and clinical classification for children with confirmed HIV infection (2006) .
Results are summarized as medians with ranges. A Chi-squared test was used to compare categorical variables. Where the expected value of one of more cells was less than 5, the Fisher exact test was used. Medians were compared with the Mann- Whitney U Test. Statistical analysis was performed with Statistica® version 9 (Statsoft Inc.).
This study was carried out in compliance to the Helsinki Declaration and permission to conduct the study was granted by the Human Ethics Research Committee of the Faculty of Health Sciences of Stellenbosch University.
The median age of the 25 children was 8 months (range 2.8-92) and 15 (60%) were male. Fifteen (60%) were referred for recurrent respiratory complaints, 3 (12%) for poor growth, 4 (16%) for poor feeding and 2 (8%) patients for respiratory complaints and poor growth and 1 (4%) for poor feeding and respiratory complaints. No specific swallowing disorder was identified in any of the patients prior to referral.
Clinical features of patients with results of assessment
Indication for assessment
Recurrent respiratory infections (n = 18)*
Poor feeding (n = 5)
Growth failure (n = 5)
Thirteen patients had a VFSS of which 6 (46%) were abnormal; all of these also had an abnormal clinical assessment. Abnormalities were detected in the oral phase in 2, in the pharyngeal phase in 3, and in the oral and pharyngeal phase in 1 (Table 1).
Six (24%) patients aspirated during assessment: 4 patients during clinical assessment (2 of these also had radiological evidence of aspiration); 1 patient aspirated during VFSS without symptoms of aspiration (silent aspiration); and 1 patient aspirated after an episode of gastroesophageal reflux. Five of the 6 (83%) patients with aspiration had been referred for recurrent respiratory infections and the other was subsequently found to have radiological evidence of lung disease.
Sixteen patients were receiving cART at the time of initial assessment for a median of 55 days (Range 11–392 days). Thirteen of these (81%) had swallow disorders in comparison to 7 of 9 (78%) patients who were not yet on cART (NS). There was no difference in the CD4 counts (expressed as a percentage of total T-cells and as an absolute count) between those patients on and off cART.
Presence of swallowing disorders by clinical and immunological staging of patients
Swallowing disorder present
No swallowing disorder
Clinical stage (n = 25)
Stage 3: 3
4 Stage 3;
Stage 4: 17
Stage 4: 4
21 Stage 4
Immunological stage (n = 19)
None 3; Mild 2;
Absolute CD4 count
(7-4573) (n = 19)
(n = 16)
(n = 3)
Cd4 count percentage
(n = 16)
(n = 3)
(n = 19)
Thirteen of 25 patients had central nervous system disease: 8 with HIV encephalopathy and 5 with miscellaneous central nervous system diseases (cerebral palsy, seizures after meningitis, developmental delay). Of these, 11 (85%) had abnormal swallowing: 9 in the oral phase and 7 in the pharyngeal phase (5 patients have abnormalities in both the oral and pharyngeal phases). Patients with neurological abnormalities were not more likely to have swallowing abnormalities than those without (p = 0.64).
Three of 4 (75%) patients with thrush had an abnormal oral phase: 2 with clinical assessment only, and 1 with clinical assessment and VFSS. One patient also had symptoms of aspiration. No anatomic abnormalities of the oesophagus were demonstrated with contrast studies.
This case-series highlights the importance of assessing HIV-infected children for swallowing disorders, in particular those with recurrent respiratory tract infections and neurological disease.
The spectrum of patients described reflects the referral pattern to our swallowing disorder clinic. The most common indication for referral was recurrent lung infections. The majority of these patients (88%) had abnormal swallowing and a third of them aspirated during assessment. This is similar to the finding of Halvorsen  that almost half of adults assessed with VFSS aspirated. Clinical assessment underestimates the true number of patients in whom aspiration occurs. In our study, VFSS identified 2 patients with aspiration in whom it was not suspected clinically and significantly changed their management. The importance of silent aspiration in the development of lung disease in HIV infected children is unknown, it should however be considered as a possible contributing factor in those with chronic or recurrent lung disease of uncertain etiology [11, 12].
Another explanation for the high prevalence of swallowing abnormalities in children referred with recurrent lung infections is that both lung infections and swallowing disorders are more likely to occur in patients with advanced HIV infection. Bladon  found that patients with low CD4 counts were more likely to have swallowing disorders. There was however no difference in the CD4 counts or clinical stage of HIV infection of those patients with or without swallow disorders in our series. This may be because patients with swallowing disorders were more likely to be referred for assessment and the small number of patients included. The relatively short duration of treatment prior to assessment may explain the apparent lack of effect of cART on the CD4 count. The short duration of cART in most patients was possibly also too short to make a clinical difference. While improvements in immunological status, weight gain, and well-being are observed within the first weeks of treatment, improvement in neurological and intestinal disease are often delayed.
Dysphagia is common in children with severe neurological disease [13–16]. The characteristics of swallowing disorders found in these children are similar to those found in non-HIV infected children with neurological impairment. Although most of the children with neurological disease in this series had some swallowing abnormality, this was not significantly more common than in children without signs of neurological disease.
Most swallowing abnormalities were due to functional disturbances of swallowing. These findings are consistent with studies in adults that showed abnormalities in all phases of swallowing in the absence of local pathology . It should however be noted that esophagoscopy was not performed on any of these patients.
We describe all HIV infected referred for feeding and swallowing assessment over a period of 33 months. The HIV clinic in the hospital manages approximately 400 children with HIV infection. However, the present study does not allow us to estimate the prevalence of swallowing disorders in HIV infected children in our service. The spectrum of patients referred is also subject to a strong referral bias as children with respiratory disease and neurological abnormalities were more likely to be referred for evaluation. This bias may also account for the absence of any association between immunological and clinical stage of HIV infection and the presence of swallowing disorders.
In this report of we bring attention to the importance of swallowing disorders in HIV infected children. In particular, children with recurrent lung infections often had swallowing disorders. Most patients had functional abnormalities rather than structural or mucosal abnormalities. VFSS makes an important contribution to the diagnosis and management of these patients.
- Bladon KL, Ross E: Swallowing difficulties reported by adults infected with HIV/AIDS attending a hospital outpatient clinic in Gauteng, South Africa. Folia Phoniatr Logop. 2007, 59: 39-52. 10.1159/000096549.View ArticlePubMedGoogle Scholar
- Kirby M, Noel RJ: Nutrition and gastrointestinal tract assessment and management of children with dysphagia. Semin Speech Lang. 2007, 28: 180-189. 10.1055/s-2007-984724.View ArticlePubMedGoogle Scholar
- Bobba RK, El-Dika SS, Arsura EL: Dysphagia in a HIV patient: concern for the etiology?. South Med J. 2007, 100: 61-62. 10.1097/SMJ.0b013e31802e3e0f.View ArticlePubMedGoogle Scholar
- Halvorsen RAJ, Moelleken SMC, Kearney AT: Videofluoroscopic evaluation of HIV/AIDS patients with swallowing dysfunction. Abdom Imaging. 2003, 28: 244-247. 10.1007/s00261-002-0034-2.View ArticlePubMedGoogle Scholar
- Pressman H, Morrison SH: Dysphagia in the pediatric AIDS population. Dysphagia. 1988, 2: 166-169. 10.1007/BF02424936.View ArticlePubMedGoogle Scholar
- Stinson K, Boulle A, Smith PJ, Stringer EM, Stringer JS, David C: Coverage of the prevention of mother-to-child transmission programme in the Western Cape, South Africa using cord blood surveillance. [published online ahead of print Feb 16 2012]. J Acquir Immune Defic Syndr. 10.1097/QAI.0b013e31824d985e. Accessed April 12, 2012
- Shisana O, Rehle T, Simbayi LC, Zuma K, Jooste S, Pillay-van-Wyk V, Mbelle N, Van Zyl J, Parker W, Zungu NP, Pezi S, the SABSSM III Implementation Team (2009) the SABSSM III Implementation Team: South African National HIV Prevalence, Incidence, Behaviour and Communication Survey, 2008: A turning of the tide among teenagers?. 2009, HSRC Press, Cape TownGoogle Scholar
- Logemann J: Chapter 3. Evaluation and Treatment of Swallowing Disorders. 1998, PRO-ED,INC, Austin Texas, 53-62.Google Scholar
- Logemann JA: Role of the modified barium swallow in management of patients with dysphagia. Otolaryngol Head Neck Surg. 1997, 116: 335-338. 10.1016/S0194-5998(97)70269-9.View ArticlePubMedGoogle Scholar
- WHO: WHO Case Definitions of HIV for Surveillance and Revised Clinical Staging and Immunological Classification of HIV-Related Disease in Adults and Children. 2006, WHO, GenevaGoogle Scholar
- Schindler A, Ginocchio D, Ruoppolo G: What we don't know about dysphagia complications?. Rev Laryngol Otol Rhinol (Bord). 2008, 129: 75-78.Google Scholar
- Lefton-Greif MA, Carroll JL, Loughlin GM: Long-term follow-up of oropharyngeal dysphagia in children without apparent risk factors. Pediatr Pulmonol. 2006, 41: 1040-1048. 10.1002/ppul.20488.View ArticlePubMedGoogle Scholar
- Mirrett PL, Riski JE, Glascott J, Johnson V: Videofluoroscopic assessment of dysphagia in children with severe spastic cerebral palsy. Dysphagia. 1994, 9: 174-179. 10.1007/BF00341262.View ArticlePubMedGoogle Scholar
- Wright RE, Wright FR, Carson CA: Videofluoroscopic assessment in children with severe cerebral palsy presenting with dysphagia. Pediatr Radiol. 1996, 26: 720-722. 10.1007/BF01383388.View ArticlePubMedGoogle Scholar
- Calis EA, Veugelers R, Sheppard JJ, Tibboel D, Evenhuis HM, Penning C: Dysphagia in children with severe generalized cerebral palsy and intellectual disability. Dev Med Child Neurol. 2008, 50: 625-630. 10.1111/j.1469-8749.2008.03047.x.View ArticlePubMedGoogle Scholar
- Erkin G, Culha C, Ozel S, Kirbiyik EG: Feeding and gastrointestinal problems in children with cerebral palsy. Int J Rehabil Res. 2010, 33 (3): 218-224. 10.1097/MRR.0b013e3283375e10.View ArticlePubMedGoogle Scholar
- The pre-publication history for this paper can be accessed here:http://www.biomedcentral.com/1471-2431/12/68/prepub
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.