Bariatric surgery, in which the gastrointestinal (GI) tract is surgically manipulated with the goal of decreasing caloric absorption and ultimately causing weight loss, is relevant to neuro-ophthalmologists for 2 reasons. First, it is a treatment option we may discuss with our patients who have weight-associated neuro-ophthalmic disorders, and, second, because neuro-ophthalmic symptoms and signs may result from the nutrient deficiencies that can accompany altered caloric absorption. A challenge in reviewing the relevant literature on bariatric surgery is that it spans numerous specialties including general surgery, obesity, endocrinology, nutrition, psychiatry, ophthalmology, neurology, and even neurosurgery. There is heterogeneity in the literature because bariatric surgery encompasses multiple distinct surgical procedures, and some of these are also used for nonbariatric indications. Another barrier is the relative rarity of the associated neuro-ophthalmic conditions, which makes both definitive epidemiological and treatment studies challenging.
BARIATRIC SURGERY—WHO GETS IT?
Guidelines for the management of obesity, most recently published by the American College of Cardiology, American Heart Association, and the Obesity Society, recommend consideration of bariatric surgery in patients who are motivated and who have not responded to behavioral weight loss treatment (with or without pharmacotherapy) based on body mass index (BMI = [weight in kilograms]/[height in meters]2) and the presence of weight-related comorbidities (1). The 2 categories warranting consideration are BMI ≥40 kg/m2 or BMI ≥35 kg/m2 with weight-related comorbidity.
What is considered to be comorbidity varies from study to study. The most widely referenced bariatric surgery outcome scale includes hypertension, cardiovascular disease, type 2 diabetes, sleep apnea, obesity/hyperventilation syndrome, osteoarthritis, and infertility as major comorbid conditions (2). In this scale, idiopathic intracranial hypertension (IIH), venous stasis, gastro-esophageal reflux disease, and urinary stress incontinence are considered to be minor comorbid conditions. A more recent scale, which also includes IIH, does not distinguish between major and minor comorbid conditions and is administered based on patient self-report (3). This scale incorporates severity of each comorbidity using an integer rating from 0 to 5, where 0 means no symptoms, 1 or 2 means symptoms, and 3 to 5 mean diagnosis with varying levels of treatment. Consequently, a person can have a rating of 2 for IIH by reporting headaches even if no other testing has been performed. How the severity of any comorbid conditions might impact surgical decision making is not yet clear.
Although classified as weight-related comorbidity in the bariatric surgery literature, IIH remains a relatively rare disease in this population. In a prospective evaluation of comorbidities (assessed by interview) in 226 candidates for gastric bypass surgery, only 1 (0.4%) reported a diagnosis of IIH, whereas 201 had psychosocial impairment, 173 had musculoskeletal disease, 106 had hypertension, and 50 had diabetes (3). Two studies have evaluated the prevalence of IIH in patients undergoing bariatric surgery evaluation using a protocol of nonmydriatic fundus photographic screening followed by full neuro-ophthalmic evaluation and appropriate clinical workup for those with photographic abnormalities. Krispel et al (4) reported 7 of 1,148 screened subjects (0.6%) had a history of IIH. Seventeen of 606 patients with interpretable fundus photographs (none with a history of IIH) had possible optic disc edema, and 4 of 11 had confirmed mild papilledema with normal vision on subsequent examination. Three patients had complete workup with lumbar puncture and opening pressures of 24, 25, and 32 cm H2O, respectively. The authors concluded that IIH was present in this population with a prevalence of 3 of 606 (0.5%), although this excluded 7 subjects with suspicious photographs who could not be completely followed up. In a similar study, Hamdallah et al (5) reported 4 of 1,084 screened subjects (0.4%) had a previous diagnosis of IIH. Sixteen of 532 subjects with interpretable photographs had possible optic disc edema, and 27 had other ophthalmic findings. 4/11 had Frisén Stage 1 disc edema on clinical examination, and IIH was subsequently diagnosed in 3 (further specifics not given). Of note, 2 patients photographed with a previous diagnosis of IIH did not have disc edema. Also, 2 of the patients newly diagnosed with IIH with papilledema were asymptomatic. This casts doubt on any conclusions that are drawn from studies based solely on a survey of symptoms and patient self-report.
BARIATRIC SURGERY—WHAT IS BEING DONE?
Approximately 113,000 bariatric surgical procedures are performed annually in the United States (6). Weight loss is achieved through restricted food intake, malabsorption (i.e., bypassing a length of intestine), maldigestion (i.e., less exposure to stomach acids), and combinations thereof. There are multiple surgical techniques in use and these techniques are in constant evolution (Fig. 1).
An adjustable gastric band (Lap Band, the band) involves laparoscopic placement of an adjustable band around the upper stomach. This restricts food intake and facilitates a feeling of satiety, which helps to reduce food consumed by the patient. Neither digestion nor absorption is affected. The band is adjustable via injection of saline through a subcutaneous port and is removable (7). Hospital stay is short (outpatient or 24 hours), and the frequency of complications is reported to be 1%–3% in the hands of an experienced surgeon (1).
Sleeve gastrectomy (the sleeve) involves laparoscopic removal of the greater curvature of the stomach to create a sleeve-like pouch. This restricts food intake and alters hormone patterns to promote satiety. It also impacts digestion of food. Hospital stay is typically 2 days, and complication rates range between those of gastric band and gastric bypass procedures (7).
Roux-en-Y gastric bypass surgery (gastric bypass, RGB) involves dividing the GI tract at the stomach and at the jejunum, anastomosing the proximal stomach to the distal jejunum and attaching the removed section (distal stomach and proximal jejunum) approximately 1 m further down the small intestine. This restricts food intake, alters hormone patterns, and decreases absorption in the proximal small intestine (7). It can be performed laparoscopically with a complication rate of 4%–5% (major complications) and 2%–18% (all complications) (1).
Biliopancreatic diversion (BPD) with or without duodenal switch involves the creation of a tubular stomach (similar to sleeve gastrectomy) and dividing the GI tract at 2 points, specifically the duodenum proximal to the first division is anasatomosed to the ileum distal to the second division. The bypassed section (consisting of 3/4 of the small intestine) is attached, as a blind pouch, approximately 1 m distal to the second division. The procedure can be performed laparoscopically. BPD restricts food intake, alters hormone patterns, alters digestion, and substantially decreases absorption (7). Perioperative complication rates range from 2% to 8% (1).
Guidelines for the perioperative nutritional, metabolic, and nonsurgical support of bariatric surgery patients were last published in 2013 by the American Association of Clinical Endocrinologists, the Obesity Society, and the American Society for Metabolic & Bariatric Surgery (8). These include recommendations for preoperative psychosocial, nutritional, and cardiopulmonary assessment. Postoperative meal initiation should be supervised by a registered dietitian, and patients should receive counseling regarding appropriate food intake. Patients having undergone a gastric banding should receive supplementation with a multivitamin containing minerals (including iron, folate, and thiamine), calcium, and vitamin D. In addition, patients' status after other surgical procedures should receive a second daily multivitamin with minerals and vitamin B12. Patients status post-BPD also should receive zinc supplementation. Supplementation can be oral with the possible exception of vitamin B12, which may require sublingual, parenteral, intramuscular, or subcutaneous formulations to ensure adequate absorption. Vitamin B12 and urinary calcium should be monitored in all patients. In addition, folate, iron, parathormone (parathyroid hormone), and vitamin D should be monitored after RGB and BPD, and vitamin A should be monitored after BPD. Thiamine, selenium, zinc, and copper should be evaluated based on clinical findings (e.g., rapid weight loss, vomiting, or symptoms attributable to deficiency). However, studies show that, in practice, testing does not meet these guidelines. One study based on claims analysis found that only 50% of patients had been tested for vitamin B12 and iron status postoperatively (9). The practice of vitamin supplementation also varies widely (10).
BARIATRIC SURGERY OUTCOMES
Patients typically achieve a weight loss of 20%–35% 2–3 years after surgical procedures. This degree of weight loss is 14%–37% greater than comparable nonsurgical cohorts (1). Evidence for longer-term success rates is less compelling because there is a tendency for some weight to be regained by 10 years. Studies suggest that patients exhibiting similar weight loss after 2–3 years do better at 10 years after gastric bypass than gastric banding.
Idiopathic Intracranial Hypertension
Fridley et al (11) published a meta-analysis of 62 patients (11 case series and case reports) who had IIH and underwent bariatric surgery. Lumbar puncture opening pressure was reported in 55 patients, ranging from 20 to 55 cm H2O. Of 58 patients with documented preoperative funduscopy, 42 had papilledema. Of 39 who had documented visual field testing, 25 had preoperative field defects. The majority of patients (89%) had RGB with a minority undergoing gastroplasty (6%) or gastric banding (5%). Five patients did not experience any improvement in their symptoms, but the remainder did. Only 1 of 35 patients with preoperative papilledema and a postoperative eye examination did not demonstrate resolution of the papilledema. The earliest documented resolution of papilledema occurred at 6 months postoperatively. Twelve patients who had both preoperative and postoperative visual field testing demonstrated stabilization or improvement in their visual fields. The authors noted that this remains Class IV evidence for treatment of IIH with bariatric surgery and stressed the possibility of publication bias, meaning that case reports and series could be skewed toward those with positive outcomes.
When treating IIH, alternative treatments including medical and surgical management should be considered as well as nonsurgical approaches to weight loss. Timelines, complications, and effectiveness should all be considered when making individual treatment recommendations (12).
The recent guidelines of obesity management indicate that, in concert with weight loss after successful surgery, diabetic markers decrease, diabetic remissions increase, and diabetes incidence decreases. Similarly, there is a decrease in use of blood pressure medication, hypertension remission increases, cholesterol levels improve, and health-related quality of life improves. All of these effects are found, both within subjects and in comparison to subjects undergoing nonsurgical treatments for weight loss (1). There may even be a mortality benefit in persons undergoing bariatric surgery compared with obese subjects who did not undergo surgery (8,13). Additional trials published since the 2013 guidelines provide further evidence regarding the association of bariatric surgery with improvement in weight-associated diseases such as diabetes (13). There may be some variation in the degree of improvement based on the type of procedure—malabsorption procedures generally giving better results than purely restrictive procedures—although the level of evidence for this is poor.
In contrast to the long-term improvements seen in weight-associated metabolic diseases, there may be negative effects in the short term, particularly with regard to diabetic complications. Relevant to neuro-ophthalmologists is the evidence that short-term improvements in glycemic control may be associated with paradoxical worsening of diabetic retinopathy (DR). A meta-analysis of 4 case series with 148 patients found that 7.5% of patients developed DR after bariatric surgery, 57.4% of patients with DR preoperatively had no change, 19.2% of patients had improvement, and 23.5% of patients had progression (14). Murphy et al (15) reported similar findings in their retrospective study of over 300 diabetic patients who underwent bariatric surgery: 73% had no change in DR, 11% had regression, and 16% had progression of DR after bariatric surgery. Male gender, higher-level preoperative DR grade, and larger magnitude of postoperative HbA1c reduction were associated with higher-level postoperative DR grade.
After bariatric surgery, drug pharmacokinetics are potentially altered via the same mechanisms that reduce nutrient absorption. Although this has not been extensively studied, potential mechanisms include altered breakdown of drug salts resulting from exposure to a different pH in the GI tract, altered first-pass metabolism due to bypass of certain intestinal components, and altered processing of extended-release pharmaceutical products. Some examples include decreased phenytoin levels and increased atorvastatin levels after bypass-type surgeries (16). Monitoring therapeutic effects and drug levels after bariatric surgery is advised. The use of extended-release or sustained-release drug formulations is not advised in patients who have had bariatric surgery, particularly those of the bypass variety. As of September 2014, PubMed did not list studies examining common neuro-ophthalmic medications (acetazolamide, topiramate, and prednisone). Nonsteroidal anti-inflammatory drugs should be avoided in patients with restrictive type procedures because of potential direct irritation of the gastric lining (17).
Vitamin and mineral absorption is altered after bariatric surgery via the same mechanisms that reduce caloric absorption. Contributing factors include maldigestion, malabsorption, and intake deficiency (e.g., decreased fat intake as recommended after bypass surgery). Although the literature describing and studying laboratory deficiencies is fairly comprehensive, that dealing with symptomatic deficiencies is less robust.
Interestingly, many patients have vitamin and mineral deficiencies before bariatric surgery. One study documented that of 232 patients 49% had a deficiency of at least 1 micronutrient preoperatively, with vitamin B12, zinc, vitamin D, and selenium being the most common (18). Another study of 267 patients found deficiencies of vitamins D, A, and iron in 67.9%, 16.9%, and 18.8% of patients, respectively (19). Zinc and selenium were deficient preoperatively in less than 5% of patients. After surgery, nutrient deficiencies are more common in patients with a bypass component to their operation (9,20). The type of bypass surgical intervention also has an effect. A study of 141 patients after bariatric surgery found copper deficiency in 50.6% of BPD patients, but only 3.8% of RGB patients (21). Zinc deficiency was also more common in the BPD group.
Although multivitamins are routinely recommended after surgery, these are often inadequate to prevent laboratory deficiencies. Gasteyger et al (22) found that, of 137 patients who had undergone RGB and who were taking a standard multivitamin preparation, 98% required additional nutritional supplements by 2 years postoperatively. The most common deficiencies were vitamin B12, iron, vitamin D (in >50% of patients), folic acid (45% of patients), zinc, vitamin B6, magnesium (12%–13% of patients), and vitamin B1 (4% of patients). This study excluded patients with preoperative deficiencies and those noncompliant with follow-up. Brolin et al (23) have suggested that some deficiencies such as iron are poorly remediated with oral supplementation. In contrast to these reports, Papamargaritis et al (24) noted no significant change in the prevalence of serum levels of copper, zinc, and selenium before and after surgery in 437 patients taking multivitamin–mineral supplements.
Despite the high prevalence of laboratory nutrient deficiencies, and the well-described neurological consequences of vitamin and mineral deficiencies (25–29) (Table 1), the majority of laboratory nutrient deficiencies after bariatric surgery seem to be asymptomatic. Brolin et al (23) reported in 348 patients who had undergone RGB, including 37% with laboratory-proven vitamin B12 deficiency, that no patient was symptomatic. In a report of 141 patients after RGB procedures with a high frequency of copper and zinc deficiency on the basis of blood levels, none had neurological symptoms (21).
Data regarding prevalence of symptomatic vitamin deficiencies after bariatric surgery is limited. Thaisetthawatkul et al (30) examined neurological complications after bariatric surgery, with a focus on peripheral neuropathy. Based on medical record review at a single institution, they found that 16% of patients developed symptomatic, electrodiagnostically-confirmed peripheral neuropathy after bariatric surgery, compared with 4% of patients after cholecystectomy. Features of jejunoileal bypass surgery (no longer performed) and prolonged nausea/vomiting/dumping/diarrhea were associated with development of neuropathy, whereas vitamin B12 injections, multivitamin supplementation, calcium supplementation, and attendance at a nutritional clinic were inversely associated with neuropathy development in patients having undergone bariatric surgery.
Even less data are available regarding the prevalence of neuro-ophthalmic symptoms after bariatric surgery. In a prospective series of 500 neurologically normal patients followed over 20 months after RGB (n = 457) and gastroplasty (n = 43), Abarbanel et al (31) reported neurologic complications in 23 patients (4.6%). Diagnosis of complications was based on neurological examinations and testing prompted by patient complaint. One patient had acute severe neuropathy, electrical myotonia, nystagmus, and facial diplegia, one had a myotonic syndrome, 2 each had burning foot syndrome, Wernicke–Korsakoff encephalopathy, and posterolateral myelopathy, 3 had meralgia paresthetica, and 12 had symmetric polyneuropathy. This corresponds to a roughly 0.8% incidence of neuro-ophthalmic presentations in 20 months after surgery. A report of 90 patients attributed a 40%–70% prevalence of night blindness symptoms 6 months after RGB to vitamin A deficiency (32). However, this study did not include examination findings or visual function testing sufficient to confirm the etiology of these symptoms; therefore, it is difficult to be certain of these results.
The reasons why only some patients develop symptomatic vitamin deficiency and many remain asymptomatic are unknown. Case reports of neuro-ophthalmic syndromes after bariatric surgery offer some insight. Multiple concurrent nutrient deficiencies are reported in many symptomatic patients, suggesting that the aggregate effect may be stronger than individual effects (33,34). Zinc excess is well known to potentiate copper deficiency, and this likely contributed symptomatic copper deficiency in 1 reported gastric bypass patient who used zinc containing denture cream (35). Comorbid nonnutritional risk factors may lower the threshold for vitamin deficiencies to become symptomatic, as demonstrated in a report of a patient found to have post–bariatric surgery optic neuropathy with both vitamin deficiency and Leber hereditary optic neuropathy 11,778 mutation (36). Cerebrospinal fluid (CSF) oligoclonal bands were detected in conjunction with nutritional deficiency in 2 patients with optic neuropathy and additional 2 patients with myelopathy 6 months to 6 years after bariatric surgery (37). The CSF oligoclonal bands may represent comorbid disease or may be a marker of vitamin deficiency–associated inflammation that facilitates development of symptoms.
The best-characterized syndrome relevant to neuro-ophthalmology is that of Wernicke encephalopathy related to thiamine (vitamin B1) deficiency, the body stores of which can be depleted in a matter of weeks. In 2007, Singh and Kumar (38) surveyed the literature and identified 37 cases of Wernicke encephalopathy occurring after bariatric surgery: 21 of these had the complete triad of confusion, ataxia, and nystagmus, 7 lacked confusion, 4 lacked nystagmus, and 1 lacked ataxia. One patient only had nystagmus. Onset occurred between 2 and 78 weeks after various bariatric surgical procedures, with most presenting within 12 weeks. Many cases were associated with other neurological symptoms, most commonly sensory neuropathy. In addition, 3 cases had third nerve palsies, 2 had sixth nerve palsies, and 2 had papilledema. The diagnosis was clinical in the majority of cases, with thiamine levels being reported in only 6 patients (and low in only 4). Erythrocyte transketolase levels were reported in 2 patients (but were low in only one), thus highlighting that thiamine serum levels do not reflect body stores of this nutrient. After repletion, approximately half of the patients had recovery. These observations reinforce the importance of vigilance for thiamine depletion as a cause of a wide range of neurological symptoms after bariatric surgery and the importance of effectiveness of empiric therapy even in the absence of laboratory confirmation of deficiency.
Optic neuropathy can be caused by copper, vitamin B12, and/or thiamine deficiency after bariatric surgery. Optic neuropathy because of thiamine deficiency typically develops in weeks to months after surgery with other associated symptoms. In contrast, vitamin B12 deficiency usually manifests over 1 year after surgery (37) and copper deficiency typically manifests over 3 years (even over 20 years) after surgery (39). The reason for this delay is that it takes years to deplete body stores of these nutrients. Optic neuropathy induced by both vitamin B12 and copper deficiencies can recover with treatment. Therefore, it is important to screen for deficiency of either and replete deficiencies in symptomatic patients. In patients with suspected copper deficiency, it is also important to screen for zinc excess because this can potentiate copper deficiency states (35).
Other neuro-ophthalmic presentations are nyctalopia due to vitamin A and/or zinc deficiency (32) and ophthalmoparesis due to vitamin E deficiency. In addition, many other neurological and ophthalmic symptoms and signs can occur as a result of vitamin deficiency (Table 1). Delayed deficiency can also result from late noncompliance with nutritional supplements. Because of the variety of presentations and frequent overlap of multiple deficiencies, it is important for the neuro-ophthalmologist to maintain a broad differential diagnosis in patients who have previously had bariatric surgery, even in the distant past.
Bariatric surgery is a safe and effective treatment for weight loss in obese individuals. There is Level I evidence that it is associated with improvement in common weight-associated comorbidities such as diabetes mellitus and hypertension and Level IV evidence that it is associated with improvement in IIH. Bariatric surgery does not preclude nonsurgical weight loss treatment or directed treatment of comorbid conditions including IIH. Guidelines for selection of patients and for preoperative and postoperative management are published regularly by professional organizations and are an excellent resource for the nonbariatric specialist. Laboratory nutrient deficiencies after bariatric surgery are common and associated with the type of procedure performed and the type of nutrient supplementation. Clinical syndromes of nutrient deficiency after bariatric surgery are relatively rare, and definitive diagnosis can be challenging because of limitations of laboratory testing, overlap of clinical presentations, and coincident morbidities.
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