What is CBS?
In 1769, Charles Bonnet––a Swiss biologist, naturalist and philosopher––first described symptoms of hallucination in his elderly, cognitively intact and visually impaired grandfather, Charles Lullin.1-12 Mr. Lullin reported vivid visions of men, women, birds, buildings, carriages and other images that he knew were not real.1-8,11,12

Charles Bonnet suffered from vision loss when he was very young. By age 40, he was severely visually impaired. Following retirement, he experienced visual hallucinations similar to those reported by his grandfather.1,4,6,11,13-16

Visual hallucinations are subjective experiences that occur “without external stimulation of the relevant sensory organ.”1-5,7,8,17,18 CBS has been termed a “pseudohallucination,” because the individual is aware that the sensory experience is unreal.2,3,5,18

The exact cause of the visual hallucinations is unknown, and not entirely understood by researchers and health care providers.1,2,4,7,8,18

An awareness and basic understanding of CBS is important to properly screen patients who may be suffering in silence from the condition, and reassure them that their anxiety and distress is unnecessary. 
 
     
Visual hallucinations can be a disturbing experience, particularly in patients who already have a vision problem. Visually impaired individuals, who are otherwise psychologically normal, may experience vivid hallucinations yet fail to report them to their primary care physician or eye care professional for fear of being labeled “insane.”

When an individual consciously recognizes the fictitious nature of the hallucination, and when other senses are not involved and there is no other etiology for the event, the condition is termed Charles Bonnet syndrome (CBS). Here, we review the case of an 88-year-old psychologically normal male who experienced visual hallucinations in his left eye for two years.

We include a discussion of possible pathophysiologies and potential treatment options for Charles Bonnet syndrome, as well as introduce a useful screening tool to help identify visually impaired patients who may be experiencing visual hallucinations.

Case Report

History
An 88-year-old white male presented with a chief complaint of intermittent hallucinations in his left eye that had persisted for two years. He reported seeing visions of a red brick wall with mortar. At other times, he saw pineapples. Both of these visions appeared at random times throughout the day. He did not notice any significant changes in the hallucinations during the past two years.

The patient reported that the images appeared more vivid when he covered his right eye, faded binocularly and disappeared completely when the left eye was covered. He was well aware that the wall and the pineapples were not real. His ocular history was remarkable for a blast injury to the left eye during military service in 1945. This caused impaired vision, flash burns and abrasions, as well as necessitated muscle repair performed in 1947.

Slit-lamp findings were significant for bilateral pseudoexfoliation and cataracts (OS > OD). His medical history was significant for benign hypertension, hypothyroidism, cardiomyopathy, hyperlipidemia and a mitral valve disorder. He previously suffered a near-syncopal episode and bradycardia, for which he underwent a CT scan and MRI. His current medications included levothyroxine sodium, low-dose (81mg) aspirin, simvastatin, chondroitin/glucosamine, metoprolol and a multivitamin.

CT scans and MRIs/MRAs of his brain and Circle of Willis were performed during the timeframe of the hallucinations and were remarkable only for mild, microvascular white matter ischemic changes, but no acute infarct. Blood work during the same time frame was remarkable for a slightly reduced epidermal growth factor receptor and elevated triglycerides. In addition, a prior neurology consult revealed no evidence of a neurological event.

Diagnostic Data
On examination, best-corrected visual acuity measured 20/30 OD and 20/400 OS, which was stable since his ocular injury over 60 years earlier. He was alert and well oriented, scoring a 10 on the Hodkinson Abbreviated Mental Test. Pupils, ocular motility and finger-counting fields were normal.

Intraocular pressure measured 14mm Hg OD and 12mm Hg OS. Slit-lamp examination showed mild nuclear sclerotic and cortical cataracts in the right eye, with a trace central and inferior nasal posterior subcapsular cataract. Significant nuclear sclerotic and cortical cataracts were observed in the left eye, with a grade 4 posterior subcapsular cataract. Pseudoexfoliative material was noted on both lenses. Dilated examination revealed a cup-to-disc (C/D) ratio of 0.30 x 0.35 (horizontal by vertical) in the right eye, with a trace epiretinal membrane overlying the macula. No hypertensive changes were noted, and the peripheral retinal examination was unremarkable.

Due to dense cataracts in the left eye, the posterior pole could not be visualized. The periphery appeared normal and intact. Previous dilated examinations of the left eye showed a C/D ratio of 0.40 round. A cross-sectional B-scan obtained via optical coherence tomography revealed a hazy vitreous and intact retina OS.

Treatment
At subsequent visits over a six-month period, the patient’s central and peripheral vision continued to decline in his left eye secondary to cataracts. The visual hallucinations, however, remained the same. He was referred for a surgical consultation.

At his cataract evaluation, the patient’s vision was 20/30 OD and counting fingers at two feet OS. The surgeon performed cataract extraction in his left eye. Several weeks after the procedure, the patient sent a letter reporting that he was extremely satisfied with the outcome of his surgery. His peripheral vision was much improved; it was much brighter, colors were more vivid. He also stated he was able to read the wall clock with his left eye, and his visions of the brick wall and pineapples had completely disappeared.

Diagnosis
Based on the ocular and medical exams, as well as the postoperative outcome, we diagnosed the patient with CBS.

Discussion
Charles Bonnet syndrome has been regarded as a diagnosis of exclusion. Typically, it presents as an occurrence or recurrence of persistent, vivid, complex images in an individual with impaired vision but normal psychological and neurological status. The images tend to be only visual in nature and most often consist of geometric patterns or people.1-3,5,6,8,15,17-21

In some cases, the images appear to blend into the surrounding environment––making it difficult for the patient to determine if the visions are genuine or pseudo-hallucinations. According to several published reports, approximately 20% of patients initially believe that the hallucinations are real.3,6,8,19

Visual hallucinations may be either simple or complex. Simple images include flashes of light and geometric patterns, such as circles and squares. However, in our clinical population, patients have described significantly more complex images, including brick walls, pineapples, butterflies, trains moving through the landscape, bulls-eyes, windows with flowing curtains, miniature people in row boats, and children wearing checkered shirts and dungarees. Despite poor vision, patients tend to describe these visions as vivid and clear––as though no visual impairment exists.1,3,8 Further, such hallucinations are more often described by individuals who have experienced sudden, profound vision loss or bilateral visual impairment.1,3,8

The hallucinations may persist for seconds to hours, days, months or even years. At a meeting of the visually impaired support group at our VA hospital, when asked, almost all patients claimed to have experienced hallucinations that they knew weren’t real. However, the majority also stated that their hallucinations disappeared over time, and they no longer saw anything “interesting” in their vision. Approximately 71% of patients report neutrality toward their hallucinations.17

This is because patients often have no emotional connection with the images in question, and they are not necessarily associated with any of the individual’s past history. Our patient was previously a brick layer and when asked what he thought about his hallucinations, he reported being fascinated by the detail in the brick wall, and could even describe the shape, color and positioning of various bricks.The prevalence of complex visual hallucinations in patients with visual impairment ranges between 10% and 40%.1-3,5,6,8-10,17,19,20

Multiple reports indicate that CBS typically occurs in patients with best-corrected vision between 20/40 and 20/1600, with a higher overall incidence in patients who exhibit an acuity worse than 20/300.8,19 CBS is more common in elderly patients, with a typical age of onset between 75 and 80 years (likely because of a higher incidence of visual loss with increased age). However, there have been reports of visually impaired children (secondary to retinopathy of prematurity) experiencing symptoms of CBS.3 Take note that there is no correlation between hallucination complexity and vision loss severity.8,9,20

Thus, a patient suffering from moderate visual impairment may experience a more complex hallucination, whereas a patient with profound vision loss may only see simple shapes.

Pathophysiology

Macular degeneration is the most commonly associated ocular pathology, likely due to its increased prevalence among the elderly. However, CBS has been associated with ocular pathologies located anywhere along the visual pathway. In our eye clinic, CBS-style hallucinations have been reported by patients who are blind from cataracts, bilateral macula-off retinal detachments, ischemic optic neuropathy, glaucoma and––in our patient’s case––ocular trauma. Other ocular pathologies include macular holes, optic neuritis, central retinal artery occlusion, corneal scarring and occipital lobe infarctions.1,3,8,10

In the case of glaucoma and infarction, which may result in peripheral field loss, hallucinations may occur in the area of the scotoma.8 This would explain why hallucinations tend to appear straight ahead in CBS patients with macular degeneration.

The true pathophysiology of CBS is not completely understood, and there are several hypotheses regarding the underlying cause of the syndrome. But, two primary explanations largely stand apart from others: sensory deprivation and release.1,3,5-9

• Sensory deprivation implies that the visual sensory cortex––when deprived of normal afferent input––exhibits spontaneous independent activity, resulting in conscious images.
• Release refers to the idea that when neurons transmit electrochemical impulses from the retina, defective impulses are released along with normal impulses. A defect in impulse processing is what causes visual hallucinations.

Hallucinations correlate with the area of the brain that is being stimulated. Functional MRI studies have shown that particular parts of the brain are activated while hallucinations are occurring. For example, colored hallucinations are associated with activity localized to the posterior fusiform gyrus in the area corresponding to the color center, whereas gray-scale hallucinations are associated with activity located both behind and above the region.13,15 Additionally, faces are associated with activity in the middle left fusiform gyrus, while other shapes and objects are linked to the middle right fusiform gyrus.13,15

In our patient, the textured brick walls would correlate to an increased signal in the collateral sulcus, the area of the brain that responds to visual textures.

Examination and Testing

New-onset visual hallucinations in any patient generally require a complete physical examination, including blood work, a review of medications and a baseline neurological evaluation.1 Although an ocular pathology could be the cause of immediate visual impairment, you must rule out the presence of an underlying ocular or systemic etiology that could be responsible for the hallucination. In general, a baseline psychological examination should be performed. In this case, we evaluated our patient with the Hodkinson Abbreviated Mental Test Score (AMTS) to screen for dementia.16

The Hodkinson AMTS is useful to quickly assess the cognitive function of elderly patients. A score greater than 6 suggests that the patient’s mental faculties are normal; a score of 3 to 6 indicates moderate impairment; and a score of less than 3 signifies severe impairment. However, remember that this test only screens for the presence or absence of dementia and not other causes of hallucinations.

Any patient who exhibits moderate or severe cognitive impairment should be referred to their primary care physician immediately to rule out medication-induced hallucinations and/or psychiatric conditions. Should an individual achieve a normal cognitive function score on the Hodkinson AMTS and exhibit pathognomonic symptoms of CBS, be sure to alert the patient’s PCP. Depending upon the complexity of the patient’s medical history––including previous systemic work-ups, lab tests and CT scans––further investigation might not be warranted.

Our patient underwent CT scans, laboratory tests and neurological work-ups during the time that he was experiencing the hallucinations. So, no further investigation was necessary. Many conditions and circumstances can cause visual hallucinations, which is why it’s important to rule out other, more serious pathologies. Common causes of visual hallucinations include metabolic or toxic disorders secondary to vitamin deficiency, endocrine disease, uremia, and infectious or inflammatory diseases.1

Drug and alcohol withdrawal, as well as the use of LSD, also may cause visual hallucinations. Further, the use of antidepressants, analgesics, anticonvulsants and NSAIDs may produce medication-induced hallucinations.1,3,5,6,8,18,22 Common neurological causes of visual hallucinations include Parkinson’s disease, migraine, Lewy body dementia, epilepsy and tumors.1 Additionally, psychiatric disorders that frequently cause visual hallucinations include schizophrenia, delirium, acute psychoses and post-traumatic stress disorder.1,3,5,6,8,18,22

The fundamental difference between hallucinations caused by the aforementioned disorders and those that result from CBS is the lack of other sensory involvement in Charles Bonnet syndrome. For example, CBS patients typically do not interact with their hallucinations whereas schizophrenia patients may report that a person or object in their hallucination may talk to or interact with them.3,22

  CBS Screening Questionnaire2
1. Have you ever had any unusual visual experiences? (If no response is elicited, proceed to question 2. If the patient reports hallucinations, proceed to question 3.)
2. Have you ever seen objects or things in your vision that are you know are not real?
3. What objects/images do you see?
4. How long have they been present?
5. How often do they occur, and how long do they last?
6. Do they move? How so?
7. Are they colored or black and white?
8. Do they make any noises or sounds?
9. Were you aware that they are not real?
10. Is there anything that you can do to make the visions appear?
11. Have you tried anything to make them disappear? If so, what?
12. Do the images/visions upset you?
13. Have you told anyone about these images/visions?
   
Therefore, be sure to ask these patients about the specific nature of their hallucinations (see “CBS Screening Questionnaire,” left). Important questions to ask include: What do the hallucinations look like? Are you aware that they are not real? Does the image talk or interact with you? Does the vision bother or threaten you?

In suspected cases of visual hallucination, it is essential to uncover any potential visual problems. Initially, these individuals may be reluctant to inform you or their PCPs about the hallucinations. If they do not claim to see any unusual images, then you may wish to educate them about CBS, reassure them that it is common in patients with vision loss, and potentially readdress the question about seeing hallucinations. Should the patient subsequently mention their hallucination (or unusual visual experience), the remainder of the questionnaire can be completed. Of significant importance is question eight, which is intended to determine involvement of any other senses. Sensory involvement is uncharacteristic of CBS—so, if a patient answers “yes,” other causes of visual hallucination should be explored.

Ending the Visions

There are numerous triggers and inhibitors of visual hallucinations; however, in CBS patients, the hallucinations may begin and end without any trigger at all. Hallucinations may be precipitated by fatigue, stress, dim lighting conditions, general sensory reduction, increased visual impairment level, rate of vision loss and social isolation. Hallucination inhibitors include repeatedly closing or opening the eyes, increased illumination, talking to or shouting at the hallucinations, and increased social interaction.1,3,4,5,8,9,17

In one case at our clinic, a patient who experienced detailed hallucinations of children stated that, in the privacy of his home, he would swat at the images with his cane to make them disappear because he knew they were not real. But in public places, he dared not swat at these visions for fear they might be real children playing. Our patient determined that he simply had to cover or close his left eye to eliminate the appearance of visions. Currently, there is no accepted treatment modality for CBS. Patient education and reassurance is the mainstay therapy. The goal of most treatments is to improve visual function. Thus, CBS patients require a careful refraction, increased peripheral vision, decreased glare, and increased illumination and contrast.1,3,4,5,7-9,14,18

In CBS patients with visual impairment secondary to cataracts, surgical intervention may eliminate visual hallucinations.1,3,8,9,20 In our eye clinic, an older man who was legally blind secondary to cataracts complained of seeing cockroaches, bulls-eyes, and blue and yellow butterflies in his vision for years. Due to his cardiovascular history, he was not considered a good surgical candidate. Eventually, however, he underwent cataract extraction and achieved a postoperative acuity of 20/20 OU. Six weeks after surgery, he reported not experiencing any visions since the procedure. CBS also has been reported to improve in some macular degeneration patients following successful management.12,23

On the other hand, progression to complete vision loss can also halt hallucinations, as does a longer duration of visual impairment.1 Several isolated reports have indicated that off-label treatment with certain pharmacologic agents effectively eliminates visual hallucinations in some patients. These include haloperidol and olanzapine (antipsychotic agents), carbamazepine (an anti-seizure medication) and donepezil (a cholinesterase inhibitor).1,4,8,9,24

One study published in 2007 described the case of a 78-year-old woman with CBS who was treated successfully with venlafaxine, a selective serotonin and norepinephrine reuptake inhibitor.24 Due to systemic complications, she was switched to citalopram and continued to be symptom free. The authors suggested that, in CBS patients, these medications somehow “change neuronal excitability in the occipital areas responsible for hallucinations.”24 Keep in mind that these medications may not work for all patients with CBS.Charles Bonnet syndrome remains an under-reported, underdiagnosed and poorly understood condition. This can be explained, in part, by some patients’ fear of being labeled “insane” by a health care professional. Eye care clinicians interact with the blind and visually impaired on a daily basis. So, we’re in a unique position to openly discuss the troubling––and even frightening––nature of CBS symptoms. No matter the case, our primary goal is to reassure affected patients that they are indeed sane, provide them relief from the distress associated with the hallucinations, and help them live with the condition.

Drs. Dunatov, Gruosso and Miller are staff optometrists at the Bay Pines VA Health Care System in Florida. Dr. Cantrell is chief of optometry at the Bay Pines VA.

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