Grey parrot (Psittacus erithacus) beak papillae and nerves identified using novel 2-D and 3-D imaging modalities

Emily J. Lessner Department of Earth and Space Sciences, Denver Museum of Nature and Science, Denver, CO

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M. Scott Echols Medical Center for Birds, Oakley, CA
Scarlet Imaging, Murray, UT

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Joanne R. Paul-Murphy Department of Medicine and Epidemiology, School of Veterinary Medicine, University of California-Davis, Davis, CA

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Brian L. Speer Medical Center for Birds, Oakley, CA

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Casey M. Holliday Department of Pathology and Anatomical Science, School of Medicine, University of Missouri, Columbia, MO

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Abstract

OBJECTIVE

The avian beak is a complex organ containing bone, neurovascular tissue, and keratinized covering (rhamphotheca). Nerve-rich papillae extend through bone into rhamphotheca providing sensory input from the beak tip. Beak trimming is a common procedure in avian species and is used for corrective, cosmetic, and behavioral modification purposes. Yet, practitioners are not well versed in complete beak anatomy, and therefore, beak trimming often disregards neurovasculature, injuring the patient and hampering recovery. Here, using comprehensive anatomical description, we aim to provide recommendations on how to safely perform beak trimming without damaging underlying sensory papillae.

ANIMALS

Here, we evaluated beaks of 2 deceased grey parrots (Psittacus erithacus).

PROCEDURES

In one, we used a novel stain and microcomputed tomography to visualize papillae in the upper and lower beaks. In a second, we hand isolated the upper and lower beak dermal papillae and used high-resolution photography plus traditional paraffin histology.

RESULTS

Papillae and their nerves were easily identified in these 2- and 3-dimensional approaches. This allowed us to determine the approximate lengths of papillae within the upper and lower beak.

CLINICAL RELEVANCE

Based on these findings, the authors recommend lateral radiographs of the bird’s head and beak to identify the location of the underlying bone relative to the overlying rhamphotheca before performing beak trims. Specifically in grey parrots, the authors recommend the upper and lower beak should not be trimmed closer than 8 to 10 mm from the underlying bone. Further work is needed to support these recommendations and provide guidelines for other species.

Abstract

OBJECTIVE

The avian beak is a complex organ containing bone, neurovascular tissue, and keratinized covering (rhamphotheca). Nerve-rich papillae extend through bone into rhamphotheca providing sensory input from the beak tip. Beak trimming is a common procedure in avian species and is used for corrective, cosmetic, and behavioral modification purposes. Yet, practitioners are not well versed in complete beak anatomy, and therefore, beak trimming often disregards neurovasculature, injuring the patient and hampering recovery. Here, using comprehensive anatomical description, we aim to provide recommendations on how to safely perform beak trimming without damaging underlying sensory papillae.

ANIMALS

Here, we evaluated beaks of 2 deceased grey parrots (Psittacus erithacus).

PROCEDURES

In one, we used a novel stain and microcomputed tomography to visualize papillae in the upper and lower beaks. In a second, we hand isolated the upper and lower beak dermal papillae and used high-resolution photography plus traditional paraffin histology.

RESULTS

Papillae and their nerves were easily identified in these 2- and 3-dimensional approaches. This allowed us to determine the approximate lengths of papillae within the upper and lower beak.

CLINICAL RELEVANCE

Based on these findings, the authors recommend lateral radiographs of the bird’s head and beak to identify the location of the underlying bone relative to the overlying rhamphotheca before performing beak trims. Specifically in grey parrots, the authors recommend the upper and lower beak should not be trimmed closer than 8 to 10 mm from the underlying bone. Further work is needed to support these recommendations and provide guidelines for other species.

The avian beak has long been an object of interest, studied in the context of general anatomy,16 mechanics,7 beak health,8,9 tactile foraging,1014 sensory structures,1527 and beak trimming.2831 The beak’s use as a tool for food manipulation and preening has been noted, and thus, importance has been placed on beaks in relation to avian welfare. Beak trimming is a widely used practice, spanning from the poultry industry (ie, in chickens and ducks) to companion bird species (ie, parrots) and those housed in zoological institutions.

In the poultry industry, the practice is often used to prevent feather pecking and cannibalism and removes rostral portions of the upper and lower beak, therefore negatively impacting the local sensory structures.2831 In birds kept under human care, beak-trimming procedures are commonplace when keratin overgrowth occurs from improper husbandry, malnutrition, trauma, congenital and other anomalous malformations, or disease.32,33 These rhamphothecal malformations can be trimmed and shaped manually using handheld tools (eg, Dremel) when natural grinding and abrasion alone are insufficient to correct the problem. 34 During trimming, sensory receptors may be removed, removing somatosensory capabilities; in addition, free nerve endings are left exposed, increasing nociception. Over-trimming can result in reduced feeding and obvious discomfort.32,35,36

There is little consensus as to the appropriate extent of trimming or anatomical landmarks to follow. Careful investigation into the anatomy of parrot beaks has described sensory papillae extending from the premaxillary bone and through the rhamphotheca associated with delicate manipulation of objects,6,25 but no guidance for trimming is provided. Few recent studies have focused on the presence of sensory structures with the exception of an investigation37 of the Senegal parrot (Poicephalus senegalus) in which 7 pairs of sensory pits within the rhamphotheca can be seen along the tomium of the rhinotheca, with a single pit at the bill tip. Here we describe, in 3 dimensions (3-D), the anatomy of the sensory structures at the tip of the grey parrot (Psittacus erithacus) beak to provide guidance and suggestions for beak trimming best practices.

Materials and Methods

A 20- to 30-year female grey parrot (MUVC AV347; Psittacus erithacus) was donated postmortem to the Comprehensive Anatomy Research Project, and the body was treated with Scarlet Tissue Stain (Scarlet Imaging; https://www.scarletimaging.com). The parrot was an outside breeder bird and had a history of weight loss and sitting at the bottom of the cage. The parrot died on the way to the hospital for evaluation (MSE). Postmortem CT scan resulted in the following diagnoses: obesity with decreased pectoral muscle mass, mild to moderate diffuse osteoporosis, mild stifle osteoarthritis, moderate pulmonary edema and multifocal lung parenchymal mineralizations, severe multifocal atherosclerosis with vascular mineralizations, ascites, and thyroid enlargement.

In preparation for soft tissue staining, the sternum was removed, and a 20-g IV catheter was placed into the left ventricle. Next, 140 cc of Scarlet Imaging Animal Preservation-Prep solution was flushed through the IV catheter (Scarlet Imaging; https://www.scarletimaging.com). This step was followed by the administration of 300 cc of distilled water. Finally, 300 cc of Scarlet Tissue Stain was administered through the IV catheter.

The parrot was CT scanned again to confirm good stain distribution. Poststaining CT readily identified atheromas within affected vessels and showed good stain distribution except in the cerebrum. There appeared to be a thrombus within the base of the cerebrum that prevented good stain distribution within this portion of the brain only and was the suspected cause of death (severe ischemic cerebral stroke).

The tissue stain allowed for contrast enhancement for differentiation between hard and individual soft tissue structures (eg, bone, cartilage, muscle, tendon, vasculature, nerve) upon CT scanning.38 The isolated head was initially micro-CT scanned at the University of Texas High-Resolution X-Ray CT Facility on an NSI scanner at a resolution of 36.3 μm (voxel size). A second scan imaged a subvolume focusing on the beak at a resolution of 9.75 μm. TIFFs were imported into Avizo Lite (Thermo Fisher Scientific), where measurements and images were collected. Videos were captured in Avizo (Supplementary Videos S1S5). All counts and measurements are specific to this specimen.

A second deceased grey parrot (MUVC AV043) was donated to the Comprehensive Anatomy Research Project. No history or cause of death was provided. For histology, the lower beak was removed from this grey parrot specimen using a rotary Dremel tool. Dermal papillae were isolated by hand removal of the epidermal keratin using a scalpel, prepared for traditional paraffin histology, and stained using a modified Masson’s trichrome stain. Detailed histological methods follow Bailleul et al.39 Photographs were taken using an Accu-Scope 3000 LED Microscope and an Excelis HD Camera (AU-600-HDS). Additional photography was taken of the upper beak of MUVC AV043, which was prepared using a scalpel. Photographs were taken using a Nikon SMZ100 microscope, Nikon Digital Sight U2/L2 camera, and NIS-Elements F v 4.30.01 software.

Results

The avian beak is a multilayered structure, and various publications detail the anatomy using several overlapping terms (Table 1). Internally to externally, the beak comprises an inner layer of bone, which facilitates passage of neurovasculature, a layer of dermis containing neurovascular components and collagen, and the keratinous rhamphotheca, the characteristic cornified layer of the epidermis (Figure 1).2,33 The rostral edge of the bony beak is perforated with about 3 foramina on the premaxilla (dorsal bony beak) and 10 on the dentary (ventral bony beak) in our specimen (MUVC AV347; Figure 2). Neurovascular components pass through these foramina into the dermis. Numerous extensions of the dermis (papillae), ranging from 1 mm to 4 mm and increasing in length rostrally, are present along the edge of the beak deep to the tomia (cutting edges of the rhamphotheca; Figures 13).33 These dermal papillae are present within both the keratinous upper and lower beak (rhinotheca and gnathotheca, respectively), rostral to the dorsally and ventrally angled sections that originate caudally at the rictus (angle of the mouth to caudal tomia).33 As with the dermis of the body, mechanosensitive Herbst and Grandry corpuscles are known to be present within the papillae, although we only noted Herbst corpuscles (Figure 2).8,9 These elongated papillae pass through the epidermal layer toward the tomium, terminating within the epidermis at the origins of the soft keratinous canals discussed below (Figure 3).37

Table 1

Table of equivalent terms.

Menzel and Lüdicke6 Van Hemert et al8 Genbrugge et al3 Speer and Powers33
Epidermal layers Stratum corneum Stratum corneum Stratum corneum Stratum corneum
Stratum germinativum Stratum germinativum
Stratum transitivum Stratum transitivum
Stratum intermedium Stratum spinosum
Stratum cylindricum Stratum basale Stratum basale
Regions Schutzhorn (protective) Dorsal and lateral surface Covering-type keratin
Deckhorn/Traghorn contact (covering/supporting) Lateral sharp (tomial) edge Tomium
Mundhöhlenhorn (oral) Horny palate Pressure-bearing occlusal rhino/gnathotheca
Figure 1
Figure 1

Rostral grey parrot beak in right lateral (A–D) and right rostrolateral (E and F) views with illustration of 3 main layers (A), 3-D rendering of contrast-enhanced micro-CT data with keratinous rhamphotheca rendered transparent revealing extent of dermal papillae (B), 3-D rendering of contrast-enhanced micro-CT data with keratinous rhamphotheca and dermal layers rendered transparent revealing extent of bony beak (C), midsagittal contrast-enhanced CT cross-section with relevant anatomical structures labeled (D), 3-D rendering of contrast-enhanced micro-CT data with all structures rendered transparent revealing nerve locations (E), and 3-D reconstruction of isolated nerves (F).

Citation: American Journal of Veterinary Research 84, 7; 10.2460/ajvr.23.03.0059

Figure 2
Figure 2

Grey parrot (MUVC AV347) head in right lateral view, reconstructed from contrast-enhanced micro-CT data (A). Lower beak of grey parrot in right lateral view with keratinous rhamphotheca removed, revealing dermal papillae (B). Bony lower beak of grey parrot in dorsal view revealing foramina through which neurovasculature supplies dermal papillae (C). Histological images of grey parrot dermal papillae from lower beak of MUVC AV043 (D) with close-ups of individual papillae marked in D (E and F). Upper beak of MUVC AV043 with lateral section removed showing a relationship between soft epidermal canal and pit and dermal papilla (G).

Citation: American Journal of Veterinary Research 84, 7; 10.2460/ajvr.23.03.0059

Figure 3
Figure 3

3-D renderings of contrast-enhanced micro-CT data (A and D) and accompanying illustrations (B and E). Grey parrot beak in dorsal view with upper beak mostly removed revealing soft epidermal canals and dermal papillae within keratinous rhamphotheca of the lower beak (A and B) accompanied by coronal contrast-enhanced CT cross-section of the upper beak (location indicated in B) with relevant anatomical structures labeled (C). Grey parrot beak in ventral view revealing dermal papillae and soft epidermal canals leading to pits at their rostral extent of the upper beak (D and E). Left lateral radiograph indicating bony and keratinous features (F).

Citation: American Journal of Veterinary Research 84, 7; 10.2460/ajvr.23.03.0059

The epidermal layer (rhamphotheca) is divided into germinative and superficial layers, known as the stratum germinativum and stratum corneum, respectively (Table 1; Figures 1 and 3).8 The epidermal canals through which the papillae pass are lined with stratum germinativum and do not extend to the tomial surface of the stratum corneum. The stratum corneum can be further divided by function and location.3,6,40,41 An important distinction is that a transition between these layers is evident at the tomium. Menzel and Lüdicke6 describe areas of the psittacine beak associated with the oral rhamphotheca along the tomium (Traghorn) in which the layered lamellae of keratin are loose and very soft (Figure 3). Similar packets of uncornified cells are described by Genbrugge et al.3 We observed these canals in cross-section (Figures 2 and 3), and they likely function to transmit mechanosensory signals from the tomium to the papillae sheathed by the epidermis. The rostral extents of these soft, keratinous epidermal canals are visible as pits at the beak tip.37

These layers are readily visible in the CT data (Figures 1 and 3). The high density of the bone and germinative layers make these structures the most evident. For the first time, we can provide a whole, 3-D examination of these layers, structures, and their interactions. At the beak tip in the upper beak of MUVC AV347, the bone is 5.89 mm from the furthest extent of the dermal papillae, and the papillae are 8.22 mm from the furthest extent of the keratinous rhamphotheca (which appears overgrown in this specimen; Figure 1). In the lower beak, the bone is 6.62 mm from the furthest extent of the dermal papillae, and the papillae are 4.01 mm from the furthest extent of the keratinous rhamphotheca. Similar measurements were not possible from the hand-dissected specimen (MUVC AV043) due to the method of preparation.

Discussion

Knowledge of the sensory structures at the rostral aspect of the beak provides guidance for beak-trimming best practices. Although measurements are unique to this individual (MUVC AV347) and grey parrots, they provide new insight into the 3-D anatomy of this clinically significant region. Additionally, beak tips are subject to numerous maladies such as beak deviations, mandibular prognathism, fractures, and avulsions.33 In the treatment of these maladies, careful consideration of the extent of the dermal papillae is necessary because of their highly neurovascular nature. Damage to these structures can be detrimental to the animal’s well-being because of increased sensitivity and nociception and/or loss of object and food manipulation abilities, feeding, preening, and social behaviors.35,36

Based on these pilot study findings, the authors recommend lateral radiographs of the head and beak of avian species requiring beak trims to determine the location of the underlying bone in relation to the overlying rhamphotheca. Although x-ray images will not reveal the precise location of neurovascular tissue, neurovascular extent can be estimated, as contrast-enhanced CT imaging is only an option for deceased animals. In grey parrots (Psittacus erithacus), we recommend the rostral tomia (upper and lower beaks) should not be trimmed closer than 8 to 10 mm from the underlying bone. Avian anatomy and behavior are highly variable among individuals of a species and between species. Because of the limited sample and monospecific nature of this anatomy-focused study, further studies will need to be performed to confirm these findings; adjust for weight, age, size, and behavioral differences; and make similar and more precise trimming recommendations for the lateral tomia of grey parrots and other species.

Supplementary Materials

Supplementary materials are posted online at the journal website: avmajournals.avma.org.

Acknowledgments

Dr. Echols is the creator of Scarlet Tissue Stain, Scarlet Imaging Animal Preservation solutions and owns Scarlet Imaging. The other authors have nothing to declare.

We thank the University of Texas High-Resolution X-Ray CT Facility (UTCT) and M. Colbert and J. Maisano for image acquisition and processing and C. Toupadakis Skouritakis for illustrations. We thank Stephen. A. Fronefield, DVM, DABVP, of ABC Animal & Bird Clinic in Sugar Land, Texas for providing the donor grey parrot used with the Scarlet Tissue Stain and Crystal Wilcox, BS, LVT, VTS (CP-Exotic Companion Animal), Julianna Stevens, and the staff and management of Parrish Creek Veterinary Hospital and Diagnostic Center in Centerville, UT for their facilities and CT scanner. For funding, we thank the National Science Foundation Integrative Organismal Systems (IOS) 1457319 (CMH) and Earth Sciences (EAR) 1762458 (UTCT), Society of Vertebrate Paleontology (EJL), The Tia Greenberg Foundation for Exotic Animal Research (MSE), and the Richard M. Schubot Parrot Wellness and Welfare Program at the School of Veterinary Medicine at University of California-Davis (MSE and JPM).

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  • Figure 1

    Rostral grey parrot beak in right lateral (A–D) and right rostrolateral (E and F) views with illustration of 3 main layers (A), 3-D rendering of contrast-enhanced micro-CT data with keratinous rhamphotheca rendered transparent revealing extent of dermal papillae (B), 3-D rendering of contrast-enhanced micro-CT data with keratinous rhamphotheca and dermal layers rendered transparent revealing extent of bony beak (C), midsagittal contrast-enhanced CT cross-section with relevant anatomical structures labeled (D), 3-D rendering of contrast-enhanced micro-CT data with all structures rendered transparent revealing nerve locations (E), and 3-D reconstruction of isolated nerves (F).

  • Figure 2

    Grey parrot (MUVC AV347) head in right lateral view, reconstructed from contrast-enhanced micro-CT data (A). Lower beak of grey parrot in right lateral view with keratinous rhamphotheca removed, revealing dermal papillae (B). Bony lower beak of grey parrot in dorsal view revealing foramina through which neurovasculature supplies dermal papillae (C). Histological images of grey parrot dermal papillae from lower beak of MUVC AV043 (D) with close-ups of individual papillae marked in D (E and F). Upper beak of MUVC AV043 with lateral section removed showing a relationship between soft epidermal canal and pit and dermal papilla (G).

  • Figure 3

    3-D renderings of contrast-enhanced micro-CT data (A and D) and accompanying illustrations (B and E). Grey parrot beak in dorsal view with upper beak mostly removed revealing soft epidermal canals and dermal papillae within keratinous rhamphotheca of the lower beak (A and B) accompanied by coronal contrast-enhanced CT cross-section of the upper beak (location indicated in B) with relevant anatomical structures labeled (C). Grey parrot beak in ventral view revealing dermal papillae and soft epidermal canals leading to pits at their rostral extent of the upper beak (D and E). Left lateral radiograph indicating bony and keratinous features (F).

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