Pulmonary aspiration in patients with brain lesions may result from dysfunction of the swallowing process or gastroesophageal reflux. Inadequate protection of the airway from oral secretions such as saliva may also induce aspiration. Chronic pulmonary aspiration of saliva can lead to substantial respiratory morbidity, including unexplained lung disease or recurrent pneumonia, and is an important issue in the rehabilitation unit. In particular, patients with neurologic disease who are in a long-term bedridden state can be at greater risk for development of chronic salivary aspiration and pulmonary complications [1, 2]. In contrast to aspiration during the swallowing process, continuous secretion of saliva and its aspiration are difficult to control, even through modification of food consistency or cessation of oral feeding. Use of a radionuclide salivagram to detect passive aspiration of saliva was introduced by Heyman [3] in 1989. After sublingual instillation of a small amount of radiolabeled colloid, serial images are evaluated for the presence of radiotracer uptake in the tracheobronchial tree, which is suggestive of aspiration. This test may be useful for detection of aspiration of saliva and for patients with limitations of oral feeding or poor cooperation. For these reasons, a radionuclide salivagram has been used in infants or children with neurologic diseases, for example, cerebral palsy, who have recurrent pulmonary infection [4-6]. A radionuclide salivagram can be performed under more physiological conditions without the challenge of an oral bolus for swallowing and is less invasive than a videofluoroscopic swallow study or a fiberoptic-endoscopic evaluation of swallowing [4]. There has been an increase in the use of botulinum neurotoxin A (BoNT-A) injection into salivary glands for the treatment of drooling in patients with neurologic disease, including cerebral palsy [7], Parkinson disease [8], and amyotrophic lateral sclerosis [9, 10]. Various objective or subjective methods have been used to evaluate treatment response to BoNT-A injection. However, most of the methods focus on reduction of sialorrhea or drooling itself. Few studies assess pulmonary aspiration of saliva after salivary gland injection with BoNT-A [11]. We hypothesized that a positive radionuclide salivagram could be strong evidence of aspiration of saliva and helpful to assess the indication for more intensive treatment, such as gland injection with botulinum toxin or surgical excision. In our experience with 2 patients, saliva aspiration resolved after administration of BoNT-A into salivary glands, as demonstrated on a follow-up radionuclide salivagram. A 66-year-old man with a right hemispheric stroke experienced chronic saliva aspiration and recurrent pneumonia for several months, despite nasogastric-tube feedings. He drooled constantly, and his clothing was always wet. Frequent toileting of sputum also interfered with his sleep. Radionuclide salivagram was performed for evaluation of continuous saliva aspiration. A drop of saline solution (0.1 mL) that contained 1.0 mCi of technetium 99m sulfur colloid (Techne; Fujifilm RI Pharma Co, Japan) was instilled onto the patient's tongue while the patient was in the supine position [12, 13]. Sequential images were obtained after 5 minutes and then at 10-minute intervals for 50 or 60 minutes. Pulmonary aspiration of saliva, seen as the presence of radiotracer activity in the trachea or both bronchi, was evaluated. Images also designated the region of interest (ROI) calculated as the mean counts per pixel that correspond to the right and left bronchi, and background for quantitative comparison. On the initial salivagram, radioactivity was observed in the esophageal area as well as the trachea and bilateral bronchi, which confirmed pulmonary aspiration of saliva (Figure 1A). Sequential images of a radionuclide salivagram throughout a period of 50 or 60 minutes (A, B) Case 1. (C, D) Case 2. Presence of radioactivity in the esophageal area as well as trachea and bilateral bronchi, demonstrating positivity for saliva aspiration on the initial salivagram (A, C) (arrows). There was no extraesophageal uptake of radiotracer on the follow-up salivagram (B, D) after botulinum neurotoxin A injection. After establishment of pulmonary aspiration of saliva, injection of the salivary gland with BoNT-A was conducted for control of saliva aspiration. BoNT-A (Botox; Allergan Inc, Irvine, CA) was diluted with 0.9% saline solution to 100 U per 2 mL and was then injected (total of 100 U, 25 U per gland), through a 26-gauge needle, into the bilateral parotid and submandibular glands under ultrasound guidance (5-13 MHz linear transducer; Antares, Enlargen, Germany) [2, 10]. A follow-up salivagram, performed 16 days after injection of BoNT-A, showed no extraesophageal uptake of radiotracer for pulmonary aspiration. Moreover, the increased uptake of radiotracer on the right and left bronchi had mostly disappeared in follow-up images compared with the initial study (Figure 1B). In a quantitative comparison between the initial and the follow-up salivagram after BoNT-A injection, the uptake for ROI of right and left bronchi decreased, from 0.25 and 0.65 to 0.14 and 0.16, respectively. The ratio of ROI for each bronchus to background also decreased, from 8.34 and 21.70 to 1.40 and 1.60, respectively (Figure 2A, B; Table 1). One month after injection, the severity and frequency in the drooling scoring system improved from profuse, constant drooling to mild, occasional drooling (Table 2) [14]. Clinically, pulmonary symptoms and sleep interference also improved after BoNT-A injection. The patient showed no adverse effects, and the caregiver was satisfied with the results of the BoNT-A injection. Comparison of uptake of radioactivity on both bronchi and background by using region of interest (ROI) between initial (A, C) and follow-up (B, D) salivagrams, in case 1 (A, B) and case 2 (C, D). A 26-year-old woman with quadriplegia and with cerebral palsy and hypoxic brain injury had recurrent pneumonia and lung abscess. She showed poor cooperation and remained bedridden, with percutaneous endoscopic jejunostomy feeding and a tracheostomy. Drooling was not observed because she was always in the supine position. Frequent tracheal suction of sputum, more than 10 times on average during the night-time, interfered with her sleep. Radionuclide salivagram was performed for evaluation of continuous pulmonary aspiration of saliva with the same method used in case 1. Initial salivagram showed the presence of radioactivity in the esophageal area, as well as the trachea and the right bronchus, which indicated pulmonary aspiration of saliva. BoNT-A (total, 50 U; 25 U per gland) was injected into the submandibular gland bilaterally. Because the parotid gland was small and the boundary of the gland was unclear, even on ultrasound-guided images, botulinum toxin was not injected into the parotid gland. The procedure for BoNT-A injection into the salivary gland was identical to that used in case 1. A follow-up salivagram was performed 95 days after injection of BoNT-A, and the uptake of radioactivity that was observed in the extraesophageal area in the initial study was no longer noted (Figure 1C, D). In a quantitative comparison between the initial and the follow-up salivagram after BoNT-A injection, the uptake for ROI of the right bronchus had decreased from 0.85 to 0.33 but increased in the left bronchus from 0.11 to 0.33 (Figure 2C, D; Table 1). Clinically, after BoNT-A injection, the frequency of tracheal suction was reduced to once or twice during the night. Pulmonary symptoms also were improved and maintained throughout a period of longer than 3 months. This patient also showed no adverse effect after botulinum toxin injection. This report describes 2 patients who underwent assessment of pulmonary aspiration of saliva with radionuclide salivagram and treatment with ultrasound-guided salivary gland injection of BoNT-A. Drooling or sialorrhea can be disabling for patients with neurologic disorders. In contrast to anterior drooling (ie, spillage of saliva from the mouth), posterior drooling (ie, saliva spilling over the tongue through the faucial isthmus) may increase the risk of silent aspiration for patients who are disabled and who are in a supine position for long periods of time. Various treatment options for drooling include pharmacologic therapy, such as anticholinergic agents or patches, oral motor or behavioral therapy, biofeedback, local glandular injection of botulinum toxin, irradiation, or surgery [15]. Salivary gland injection of BoNT-A has been proposed as an effective and reliable method for treatment of drooling [2, 10]. Possible indications for local application of BoNT-A into salivary glands include saliva aspiration in neurologic disorders or saliva fistulas after otolaryngologic surgery [16]. A wide spectrum of conditions could be amenable to this method of treatment to control drooling and to enhance quality of life. In contrast to anterior drooling, if there are both obvious evidence of saliva aspiration and associated clinical manifestations of recurrent pulmonary complication, more aggressive intervention, such as intraglandular injection of BoNT-A or surgery, should be considered for control of saliva aspiration. Although salivary gland injection of BoNT-A is a procedure with no serious adverse effects, in our experience, objective assessment of saliva aspiration is necessary before this intervention. However, little has been studied about objective measurement, which could help to guide for treatment with glandular injection of botulinum toxin. In previous studies, salivary flow rate or saliva production was measured by using dental rolls, suctioning, the number of napkins used daily, or chin cups for quantitative assessment. Questionnaires or scoring systems, such as drooling severity and frequency scale, the drooling impact scale, or the drooling quotient, have been used for qualitative assessment [2, 10]. Although evaluation of a large saliva pool at the entrance to the larynx by using a laryngoscope before injection has been reported, most studies focused on anterior drooling rather than posterior drooling and evaluated clinical conditions without objective assessment before the procedure [16]. The radionuclide salivagram is available for detection of aspiration of saliva, and is a more physiological and less invasive test than other tests such as a videofluoroscopic swallow study or a fiberoptic-endoscopic evaluation of swallowing because there is no intentional induction of the swallowing process with an oral bolus challenge [4]. Although a salivagram can be performed even in patients who are not cooperative, the use of the glucose oxidase test strip method or the blue dye visualization method are possible only under tracheostomy conditions. For detection of saliva aspiration itself, the use of minimal volume for oral instillation is critical so as not to interfere with the physiological condition of natural salivation without triggering the swallowing reflex. The occurrence of a positive salivagram finding may be dependent on the volume of swallowed bolus [13, 17]. If a finding on the salivagram is positive, even with a minimal volume, then pulmonary aspiration of saliva is obvious, and more aggressive intervention can be reasonable for control of saliva aspiration. In the present cases, we placed a small drop (0.1 mL) of saline solution containing radionuclide on the tongue and assumed that it was sufficient for detection of saliva aspiration itself [13]. Follow-up salivagram after BoNT-A injection showed no recurrence of the uptake of radiotracer within the bronchus. Clinical manifestations also were improved after the procedure. In a quantitative comparison of radioactivity, the uptake of both bronchi in the follow-up study was decreased except in the left bronchus in case 2. The reason is not clear. We think that the ratio of each bronchus to background may be adequate to compare between 2 different salivagrams. Unfortunately, we did not assess the uptake of initial background in case 2 and could not compare the initial and follow-up studies. The comparison of the ratio of radioactivitiy of each bronchus per background, could be helpful for evaluation of the treatment response. Further studies to clarify the quantitative comparison may be necessary. We have described 2 cases of patients whom we assessed for pulmonary aspiration of saliva by using radionuclide salivagram and treatment with ultrasound-guided salivary gland injection of BoNT-A. Although our observations have limitations, they imply the feasibility of the salivagram as an evaluation tool for the presence of pulmonary aspiration of saliva before salivary gland injection of botulinum toxin. Further complementary studies for verifying the statistical significance of the feasibility of salivagram are warranted. Additional studies will be necessary to clarify the objective indication and outcome measure for BoNT-A injection of salivary glands.
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