MATERIAL AND METHODS
Chemicals
Dexamethasone (micronized) and poloxamer 407 NF were purchased from Spectrum Chemicals. Acepromazine, ketamine and xylazine were from MWI Veterinary. OTO-104 consisted of a sterile suspension containing dexamethasone in 16% poloxamer 407 manufactured under GMP conditions.
Animal Studies
All animal studies were conducted in accordance with the policies and recommendations of the United States Department of Agriculture, the National Institute of Health guidelines for the handling and use of laboratory animals and received approval from the Institutional Animal Care and Use Committees of Otonomy Inc and MPI Research Inc.
Pharmacokinetic studies in guinea pigs
Female guinea pigs (Charles River) weighing 200-300g, of approximately 6-8 weeks of age were used (N = 4 per time point). Prior to any procedure, animals were anesthetized using a combination of xylazine (10 mg/kg), ketamine (40 mg/kg) and acepromazine (0.75 mg/kg) for up to an hour via the intramuscular route. If needed, an intraoperative booster was administered intraperitoneally representing one-tenth of the original dose.
Intratympanic injection – Each animal was positioned so that the head was tilted at an angle to favor injection towards the round window niche. Briefly, under visualization with an operating microscope, 50 µl of the formulation was injected using a 27G or 30G needle through the tympanic membrane into the superior posterior quadrant behind which the round window niche is located. Using this approach, the formulation specifically targeted the round window membrane and minimized the presence of the gel in other areas. During the procedure and until recovery, animals were placed on a temperature controlled (40 ⁰C) heating pad. After consciousness was regained, animals were returned to the vivarium.
Perilymph sampling procedure - The skin behind the ear of anesthetized guinea pigs was shaved and disinfected with povidone-iodine. An incision was then made behind the ear, and muscles were carefully retracted from over the bulla. A hole was drilled though the bulla using a dental burr so that the middle ear was exposed and accessible. The cochlea and the round window membrane were visualized under a stereo surgical microscope. Mucosal tissues of the cochlea were removed and the area washed carefully to remove any potential drug contaminants. A unique microhole was hand drilled through the bony shell of the cochlea (otic capsule) adjacent to the round window. Perilymph (5 µl) was then collected using a microcapillary inserted into the cochlear scala tympani.
Pharmacokinetic studies in sheep
Female sheep (Buckham Sheep Farm, Kalamazoo, MI) weighing 50-65kg, of approximately 2-4 years of age were used (N=1, 2 ears per time point). Prior to any procedure, animals were anesthetized using a combination of xylazine (0.22 mg/kg), glycopyrrolate (0.01 mg/kg) and ketamine (15 mg/kg) administered IM in addition to isoflurane by inhalation.
Intratympanic injection – Each intubated animal was immobilized and placed laterally in reverse trendelenburg position, with the rostrum slightly elevated to ensure access to the round window. Following ear cleaning (using Otocalm and warm saline), and under otoscopic visualization, 600 µl of the formulation was injected using a 25G or 27G needle through the tympanic membrane into the posterior inferior quadrant towards the round window niche. After dosing, the animal was left on an incline with its head up for approximately 30min to allow the dosing solution to settle into the tympanic cavity. Procedure was then repeated for the opposite ear.
Perilymph sampling procedure – The animal was intubated and placed in lateral recumbency. A post-auricular skin incision was made and the post-auricular vein located and ligated. Cautery was performed to expose the bulla and temporal bone. The middle ear was accessed using a nitrogen powered drill and a round-tipped bur. The middle ear ossicles were pushed to the side, with care taken to avoid damaging the round window membrane. Mucosal tissues of the cochlea were removed and the area washed carefully to remove any potential drug contaminants. Using a 0.5-1 mm round-tipped burr, a hole was hand drilled into the basal turn of the cochlea until the bone was thin enough to pierce with a modified sewing needle. Perilymph (50µl) was then collected using Hamilton syringe connected to a 28-32G needle inserted into the cochlear scala tympani.
Acute ototoxicity
Male (n=5 per group) and female (n=5 per group) guinea pigs weighing 200-300g, of approximately 6-8 weeks of age were used. Prior to any procedure, animals were anesthetized using a combination of xylazine (2.5 or 5 mg/kg) and ketamine (75 mg/kg) for up to an hour via the intramuscular route. Anesthesia was maintained via isoflurane inhalation during the intratympanic injection procedures.
Intratympanic injection –All animals were injected bilaterally. Each animal was positioned so that the head was tilted at an angle to favor injection towards the round window niche. Briefly, under visualization with an operating microscope, 50 µl of the formulation was injected using a 27G or 30G needle through the tympanic membrane into the superior posterior quadrant behind which the round window niche is located. During the procedure and until recovery, animals were placed on a temperature controlled (40 ⁰C) heating pad. After consciousness was regained, animals were returned to the vivarium.
Auditory Brainstem Responses (ABR) assessment – During the procedure, additional anesthetic (xylazine and ketamine) was administered if needed to maintain anesthesia depth sufficient to insure immobilization and relaxation. ABRs were recorded in an electrically and acoustically shielded chamber. Needle electrodes were placed at the vertex (active) and immediately below the pinna of the test ear (reference) and contralateral ear (ground). Tucker Davis Technologies (TDT) System III hardware and SigGen/BioSig software (TDT, Alachua, FL USA) were used to present the stimulus and record the ABR responses. Tones were delivered through a Tucker-Davis EC1 driver (aluminum-shielded enclosure made in house), with the speculum placed just inside the tragus. Acoustic calibration was performed with TDT software (SigCal) and thresholds are expressed as dB SPL. Stimulus presentation (15 ms tone bursts, with 1 ms rise/fall times) were presented 10 per second. Up to 1024 responses were averaged for each stimulus level. Responses were collected for stimulus levels in 10 dB steps at higher stimulus levels, with additional 5 dB steps near threshold. Thresholds were interpolated between the lowest stimulus level where a response was observed, and 5 dB lower, where no response was observed.
Middle ear assessment – At necropsy, a visual examination of the middle ear was conducted using a dissecting microscope. The middle ear was opened by removing regions of the temporal bone in order to reveal the ossicles. A forceps was used to gently apply pressure to the ossicles and mobility was noted. The presence of fibrous tissue, edema /swelling and erythema (discrete reddened areas with or without presence of fluids) was scored as follows: (0) not present, (1) minimal, (2) moderate, or (3) severe.
Plasma collection method - Blood samples (1ml) were collected via the orbital sinus intoheparin coated tubes. No fasting was conducted prior to collection.
Acute dermal toxicity (local tolerance)
Male (n=5) and female (n=5) guinea pigs weighing 200-300g, of approximately 6-8 weeks of age were used. On the day prior to dosing, the hair from no less than 15% of the total body surface area (BSA) was clipped from the back of the animal. It was determined by that 1.0 ml of the test article was sufficient to cover an area of approximately 40 cm2. The following formula was used to calculate the area:
BSA2 = 9*W2/3
where “A” was the estimated area in square centimeters and “W” was the body weight in grams. 20% OTO-104 was applied by gentle inunction to the animals back with a glass stirring rod, and distributed evenly over an area starting at the scapular region and continuing caudally over the test site. The test article was then held in contact with the skin by gauze dressing and nonirritating tape. Following a 24 h exposure period, the dressing was removed.Observations for clinical signs (morbidity, mortality and injury) were conducted at approximately 30 min, 2 and 4 h post-dose and once daily for the remainder of the study. The test site was evaluated at each clinical observation for the presence of reddened areas.
Skin sensitization by Buehler method (Delayed hypersensitivity)
Male and female guinea pigs weighing 200-300g, of approximately 6-8 weeks of age were used. The vehicle group (n=5 per gender) was administered 0% OTO-104 during the induction phase, and 20% OTO-104 during the challenge phase. The positive control group (n=5 per gender) received Hexyl Cinnamic Acid (HCA) during both induction and challenge periods. The test article group (n=10 per group) received 20% OTO-104 during the induction and challenge phases.
Induction phase - At least 24 h prior to dosing, the left shoulder surface area was shaved from each animal in anamount to equal approximately one-fourth of the animal’s back and side. On each day ofdosing (day 1, 8, and 15), each animal received one application to the same shaved leftshoulder region. The amount (0.4 ml) of the vehicle (0% OTO-104), positive control (HCA), or 20% OTO-104 formulation was placed into a Hill Top Chamber and was secured with 2 to 3 inch 3M Health Care tape, covered with clear plastic wrap that was folded in thirds, woundaround the torso of each animal, and secured with Vetrap tape. The chamberwas then considered applied and the time was documented. After at least 6 h of exposure, thetape and chambers were removed and the application sites were washed with a Wypallandtepid tap water. After the last induction, the animals were left untreated for 2 weeks until the challenge phase.
Challenge phase - All animals exposed during the induction phase were challenged 2 weeks after the last induction exposure. Approximately 24 h prior to dosing, the left flank surface of the side and back of each animal was shaved. On the day of dosing (day 29), each animal received one application to the shaved left flank region. The formulation (0.4 mL) was placed into a Hill Top Chamber and was secured with 2 to 3 inch 3M Health Care tape, covered with clear plastic wrap that was folded in thirds and wound around the torso of each animal, and secured with Vetrap tape. At this point, the chamber was considered applied and the time was documented. After at least 6 h of exposure, the tape and chambers were removed and the application sites were washed with a Wypall and tepid tap water.
Sensitization scoring - Each site was scored for irritation at approximately 24 and 48 h after patch removal. At least 8 h prior to the initial skin evaluation, all animals were depilated. The scoring scale was as follows: (0) no visible change, (0.5) very faint erythema usually patchy, (1) faint erythema usually confluent, (2) moderate erythema and (3) severe erythema with or without edema. To interpret the responses, a severity index (SI) and a sensitization index (SII) were developed.
SI = Sum of grades at interval / total number of animals
SII = (number of animals showing a positive response at 24-48h / total number of animals) * 100
Histology
Guinea pigs received vascular perfusion through the heart with an isotonic saline solution followed by fixative containing 4% paraformaldehyde (PFA) in phosphate buffer. Left and right temporal bones were removed and trimmed. Cochleae of the left ear were fixed by intrascalar perfusion with 4%PFA. The temporal bones were then placed in 4% pPFA for approximately 1 hour and transferred to a vial containing 0.5% PFA in phosophate buffer. The right temporal bones were trimmed, and then each was placed in a cassette containing of 5% EDTA in phosphate buffer. The cassettes were placed into a PELCO 3451 Microwave System, running constantly for 3-5 days. Ears were then dehydrated in EtOH and processed in JB-4 Glycol Methacrylate resin, placed into molds containing the resin and polymerized at ~4 ⁰C for ~12h. Blocks containing cochleae were trimmed and five micrometer sections were cut with a Leica RM2165 Microtome and stained with Paragon stain. Sections were examined under bright field optics. Middle ear sections were assessed for tissue reaction and inflammatory response. Mild tissue reaction was defined as small increases in the thickness of the tissue associated with mucosal linings with some possible vesiculation. Mild – moderate tissue reaction was defined as small regions of new tissue growth or inflammatory response. Moderate tissue reaction was defined as larger tissue growth often associated with an inflammatory response. Moderate to large tissue reaction was defined as several regions with large amounts of new tissue growth and cells associated with inflammatory response. Large response was defined as a large tissue growth and inflammatory response associated with much to all of the middle ear often with new bone growth. Sections with paramodiolar profiles through the cochlea were assessed for appearance of the organ of Corti, spiral ganglion neurons and stria vascularis / lateral wall tissues.
The cochleae were carefully removed from left temporal bones and then further dissected, first removing the bony otic capsule, followed by removal of lateral wall tissues, including spiral ligament and stria vascularis. The tectorial membrane was then removed and the cochleae placed in a solution of rhodamine labeled phalloidin, diluted 1:100 in phosphate buffered saline (PBS), for 30-120 mins, in the dark, followed by two washes in PBS. The cochlear sensory neural epithelium was then dissected away from the modiolus, starting at the apex, to produce surface preparations of the cochlear spiral. Each segment was mapped for location and placed on a slide. A quantitative assessment of presence or absence of hair cells was then carried out, beginning at apex and proceeding to the base, to produce a cycocochleogram, with presence or absence or hair cells mapped by position along the cochlear spiral.
Analytical method
Determination of dexamethasone concentrations was performed using high pressure liquid chromatography (HPLC) combined with mass spectrometry detection (MS). The limit of detection of the method was 1.0 ng/ml. Samples (perilymph, plasma and CSF) were extracted by liquid-liquid extraction using dichloromethane:hexane:MTBE (1:1:1, v/v/v). The organic portion was then dried and the extracts reconstituted with a water:methanol solution (1:1, v/v). The samples were analyzed by reversed phase HPLC (1100 series, Agilent) using an Atlantis dC18 column maintained at 40 ⁰C. The mobile phase was nebulized using heating nitrogen in a Z-spray source/interface and the ionized compounds detected using MS/MS (Tandem quadrupole mass spectrometer, Quattro Ultima, Waters). Peak heights of dexamethasone were determined using MassLynx software (Waters). The calibration curves were obtained by fitting the peak height ratios of analyte / internal standard and the standard concentrations to a suitable equation using MassLynx. Sample dexamethasone concentrations were then interpolated using the equations derived from the calibration curves.
Data Analysis
Results are presented as mean + standard error to the mean (SEM) whenever possible. Pharmacokinetic parameters are calculated using conventional non-compartmental pharmacokinetic methods. A metric to estimate the time during which dexamethasone concentrations remained above therapeutic levels in the perilymph (0.04 µg/ml) was developed and termed Terminal Exposure Time (TET). A non linear regression approach was taken to derive TET, using the exponential decay equation:
Y = span * e(-k.x) + plateau
Where Y is the concentration of dexamethasone in the perilymph, span the difference between Y0 and plateau, k is the rate constant equal to the reciprocal of the time, and x is the time.
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