Reduced dietary intake

To determine if there are changes in dietary intake, several studies investigated the impact of different bariatric procedures on overall energy intake. A recent meta-analysis observed that caloric intake decreased significantly after sleeve gastrectomy (weighted mean difference: 939·8 kilocalories (kcal)/d; 95% CI 647·66–1231·10) and Roux-en-Y gastric bypass (weighted mean difference: 1215·16 kcal/d; 95% CI 887·66–1542·67)^{(Reference Janmohammadi, Sajadi, Alizadeh and Daneshzad30)}. The reduction in caloric intake goes hand in hand with a reduction in micronutrient intake. Inadequate intake of various micronutrients has been extensively investigated by different research groups after both sleeve gastrectomy and Roux-en-Y gastric bypass (Table 1)^{(Reference Bavaresco, Paganini and Lima31–Reference Warde-Kamar, Rogers, Flancbaum and Laferrere45)}. Importantly, different research methods and recommendations have been applied throughout these studies, although they do indicate inadequate micronutrient intake as a challenge after bariatric surgery⁽⁴⁶⁾. While there is still some uncertainty regarding the dietary mechanisms underpinning this reduction in micronutrient intake, decreased portion sizes and altered food preferences are recognised as important players^{(Reference Al-Najim, Docherty and le Roux47)}. Evidently, the size of the gastric pouch or sleeve acts as a physical barrier for (excessive) eating initially after surgery^{(Reference Laurenius, Larsson and Bueter48)}. Therefore, specific eating behaviours are recommended, including but not limited to eating at a slow pace (specific dietary recommendations are reviewed elsewhere)^{(Reference Dagan, Goldenshluger and Globus49)}. In addition, post-operative changes in appetite, smell and taste may drive changes in food preference^{(Reference Makaronidis, Neilson and Tymoszuk50)}. Food cravings may be exacerbated in cases of nutritional deficiencies, whereby the patient desires essential nutrients. Interestingly, food urges has been identified as one of the strongest predictors of weight regain^{(Reference Odom, Zalesin and Washington51)}.

Table 1. Micronutrient intake after bariatric surgery

Abbreviations: AI, adequate intake; ASMBS, American Society for Bariatric and Metabolic Surgery; DRI, dietary reference intake; EAR, estimated average requirements; IOM, Institute of Medicine; RDA, recommended dietary allowance; RYGB, Roux-en-Y gastric bypass; SG, sleeve gastrectomy.

Legend: ⁽¹⁾Dietary intake refers to micronutrient intake from food, while total intake refers to micronutrient intake from food and nutritional supplements.; ⁽²⁾Adequate intake refers to a recommended average daily intake level based on observed or experimentally determined approximations or estimates of nutrient intake by a group (or groups) of apparently healthy people that are assumed to be adequate.; ^{(Reference Wells, Sawaya and Wibaek3)}Dietary reference intake refers to a set of nutrient-based reference values that can be used for planning and assessing diets.; ^{(Reference Ames4)}Estimated average requirements refers to the average daily intake value that is estimated to meet the nutrient requirements in 50% of the individuals in a particular life stage and gender group.; ^{(Reference Astrup and Bugel5)}Recommended dietary allowance refers to the average daily intake value that is estimated to meet the nutrient requirements in 97–98% of the individuals in a particular life stage and gender group.⁽⁴⁶⁾

Food intolerance and aversion

Beyond food portions and preferences, some food items may be harder to tolerate, which may lead to the avoidance of specific food groups. Consequently, food intolerance and aversion may contribute to the reduced micronutrient intake after bariatric surgery^{(Reference Zarshenas, Tapsell, Neale, Batterham and Talbot52)}. Given its subjective nature, research on dietary intolerance varies widely due to differences in the applied definition of intolerance and the given research methodology^{(Reference Freeman, Overs, Zarshenas, Walton and Jorgensen53–Reference Overs, Freeman, Zarshenas, Walton and Jorgensen65)}. In general, most reported intolerances are bread, cereals, dairy, fibrous vegetables, meat, pasta and rice^{(Reference Zarshenas, Tapsell, Neale, Batterham and Talbot52)}. Some of these intolerances may impose a risk on diet quality. For instance, avoidance of red meat may imply a lower iron intake, whereas other intolerances may improve diet quality by avoiding specific food items^{(Reference Nicoletti, de Oliveira and Barbin66)}. For instance, dumping syndrome may restrain patients from consuming energy-dense food items after surgery. The ingestion of refined sugar and fat triggers an exaggerate release of gut hormones (especially GLP-1) and the rapid entry of water into the intestinal lumen. This phenomenon of post-prandial hyperinsulinaemic hypoglycaemia is characterised by the occurrence of non-specific symptoms including a broad spectrum of presentations related to Whipple’s triad for hypoglycaemia (e.g. symptomatic hypoglycaemia, documented low plasma glucose level, and resolution of symptoms after glucose administration). For hypoglycaemia, symptoms are categorised as autonomic (e.g. sweating, tremor and palpitation) or neuroglycopenic (e.g. confusion, weakness, light-headedness, dizziness, blurred vision, disorientation and eventually loss of consciousness)^{(Reference Tack and Deloose67–Reference Eisenberg, Azagury, Ghiassi, Grover and Kim69)}. From a patient’s perspective, dumping syndrome has been described as an unpleasant protection mechanism to avoid the consumption of energy-dense food items^{(Reference Laurenius and Engström70)}. The effect on micronutrient intake may be rather small as energy-dense foods are often poor in micronutrient content^{(Reference Monsivais and Drewnowski71)}. Overall, food tolerance improves over time after both sleeve gastrectomy and Roux-en-Y gastric bypass^{(Reference Sherf Dagan, Keidar and Raziel56–Reference Novais, Junior, Shiraga and de Oliveira60,Reference Coluzzi, Raparelli and Guarnacci62,Reference Harbottle63)} . On the basis of these individual physiological responses, efforts should be made to work towards personalising dietary recommendations based on physiological and tolerance response.

Non-compliance with dietary and supplementation recommendations

Another nutritional aspect that negatively affects nutrient intake is non-compliance with dietary recommendations and follow-up^{(Reference Smelt, Pouwels, Smulders and Hazebroek72,Reference Luca, Nicolas, Marina, Sarah and Andrea73)} . Dietetic counselling and nutritional supplementation is recommended to prevent nutritional complications after bariatric surgery^{(Reference Mechanick, Apovian and Brethauer74,Reference Busetto, Dicker and Azran75)} . However, the majority of research on non-compliance focuses on dietary recommendations and Roux-en-Y gastric bypass^{(Reference Elkins, Whitfield and Marcus76,Reference James, Lorentz and Collazo-Clavell77)} . Regarding nutritional supplementation, non-compliance is frequently encountered in clinical practice. A recent systematic review and meta-analysis observed that guideline compliance rate for nutritional supplementation does not exceed 20% after bariatric surgery^{(Reference Ha, Kwon and Kwon78)}. However, research indicates that supplementation compliance is associated with more favourable biochemical assessments of nutritional status^{(Reference Henfridsson, Laurenius and Wallengren79,Reference Ledoux, Calabrese and Bogard80)} . Previously, increasing age and medicine intake were identified as positive predictors of compliance. While experiencing barriers was identified as a negative predictor of compliance. Most common barriers for supplement use are forgetfulness, price of supplements and experience of side effects^{(Reference Steenackers, Vandewynckel and Boedt81)}.

The ‘bariatric’ gastrointestinal tract at a glance

Traditionally, the presence of nutritional deficiencies after bariatric surgery was solely attributed to the mechanical aspects of inducing ‘restriction’ and ‘malabsorption’. However, this mechanical hypothesis does not provide an adequate explanation for why some nutritional deficiencies are equally common after sleeve gastrectomy and Roux-en-Y gastric bypass^{(Reference Moize, Andreu and Flores41,Reference Kwon, Kim and Menzo84)} . In theory, it is plausible to assume that the drastic anatomical alterations of bariatric procedures influence gastrointestinal physiology. In turn, the anatomical and supposed physiological alterations imposed by the different types of bariatric procedures define the type and extent of nutritional deficiencies^{(Reference Syn, Cummings and Wang85)}. An overview of potential physiological alterations is visualised in Fig. 3 and reviewed elsewhere^{(Reference Steenackers, Vanuytsel and Augustijns21)}.

Fig. 3. Potential physiological alterations of sleeve gastrectomy (left) and Roux-en-Y gastric bypass (right).

The ability of the gastrointestinal tract to digest food and absorb nutrients might be compromised by the profound anatomical and physiological alterations of bariatric surgery. Regarding digestion, the stomach needs an acidic environment for the initiation of macronutrient digestion (e.g. pepsinogen activation for protein digestion) and optimising micronutrients for absorption (e.g. releasing vitamin B₁₂ from protein, optimising calcium and iron solubility and reducing ferric iron into the absorbable ferrous form)^{(Reference Pohl, Fox and Fried86)}. It is plausible that the resection and bypass of the oxyntic glands of the stomach affects digestion and nutrient absorption after surgery. In addition, this may as well reduce gastric secretion of intrinsic factor and, as such, affect vitamin B₁₂ absorption further on in the ileum^{(Reference Marcuard, Sinar, Swanson, Silverman and Levine87)}. Moreover, a reduced gastric mixing and accelerated gastric emptying delivers partially undigested nutrients rapidly into the small intestine. This could delay protein, carbohydrate and lipid digestion until the ingested food reaches the pancreatic and biliary fluids that only appear in the common limb after Roux-en-Y gastric bypass. As a consequence, malabsorption of fat-soluble vitamins can occur that in turn affect other nutrients (e.g., vitamin D–calcium interaction). Beyond delaying digestion, a major area for nutrient absorption with transporters is bypassed after Roux-en-Y gastric bypass as visualised in Fig. 4. Altogether, changes in gastrointestinal physiology have serious implications for digestion and nutrient absorption.

Fig. 4. Gastrointestinal micronutrient absorption after sleeve gastrectomy (left) and Roux-en-Y gastric bypass (right).

Iron deficiency

Microcytic and hypochromic erythrocytes are considered the hallmark finding of iron deficiency, which reduces the oxygen-carrying capacity of the erythrocytes^{(Reference Steenackers, Van der Schueren and Mertens94)}. Symptoms and signs of iron deficiency with/without anaemia include fatigue, lethargy, reduced concentration, dizziness, paleness, dry skin, dry hair, alopecia, koilonychia and atrophic glossitis, but can be asymptomatic as well^{(Reference Pasricha, Tye-Din, Muckenthaler and Swinkels105)}. A recent systematic review and meta-analysis observed that the risk of developing iron deficiency is comparable after sleeve gastrectomy and Roux-en-Y gastric bypass (relative risk (RR) 1·27; 95% CI 0·98–1·64; P = 0·069)^{(Reference Kwon, Ha and Lee106)}. Increased divalent metal transporter expression may increase the absorptive capacity of the remaining nutrient-exposed intestine to compensate for the bypassed biliopancreatic limb with its nutrient transporters after Roux-en-Y gastric bypass^{(Reference Marambio, Watkins and Castro107)}. Iron status monitoring and daily nutritional supplementation is recommended independently of the type of procedure. In case of deficiency, oral supplementation should be increased or replaced by intravenous administration for patients with severe intolerance or refractory iron deficiency^{(Reference Mechanick, Apovian and Brethauer74)}.

Vitamin B₁₂ deficiency

Another frequent cause of nutritional anaemia is vitamin B₁₂ or cobalamin deficiency. Given vitamin B₁₂ body stores can last for 3–5 years, vitamin B₁₂ deficiency usually only becomes clinically relevant several years after bariatric surgery^{(Reference Bal, Finelli, Shope and Koch108)}. Contrary to iron deficiency, the risk of post-operative vitamin B₁₂ deficiency is higher after Roux-en-Y gastric bypass compared with sleeve gastrectomy (RR 1·86; 95% CI 1·15–3·02; P = 0·012)^{(Reference Kwon, Ha and Lee106)}. Severe vitamin B₁₂ deficiency is characterised by macrocytic erythrocytes, leading to megaloblastic anaemia^{(Reference Stover109)}. Symptoms and signs of vitamin B₁₂ with/without anaemia resemble the symptoms of iron deficiency (anaemia) including fatigue and glossitis. Beyond haematological complications, vitamin B₁₂ deficiency can contribute to neurological complications such as myelopathy, neuropathy, paraesthesia and ataxia. As the morphological features of vitamin B₁₂ deficiency are camouflaged in case of iron deficiency and symptoms are similar, vitamin B₁₂ status should always be monitored in combination with iron status^{(Reference Nuzzo, Czernichow and Hertig101,Reference Bal, Finelli, Shope and Koch108,Reference Hunt, Harrington and Robinson110)} .

Vitamin B₉ or folate deficiency

Although less common, folate deficiency is another potential cause of nutritional anaemia. Folate absorption can occur along the entire small intestine, which explains the low incidence of folate deficiency, especially when supplemented with folic acid. The risk of developing folate deficiency is comparable after sleeve gastrectomy and Roux-en-Y gastric bypass (RR 0·79; 95% CI 0·47–1·35; P = 0·391)^{(Reference Kwon, Ha and Lee106)}. Similar to vitamin B₁₂, severe folate deficiency is characterised by macrocytic erythrocytes that lead to megaloblastic anaemia^{(Reference Stover109)}. Symptoms include weakness, anorexia and weight loss^{(Reference Bal, Finelli, Shope and Koch108)}. Considering the risk of neural tube defects in the foetus, it is advised that women who underwent a bariatric procedure receive between 400 and 1000 µg of folic acid in the peri-conceptional period^{(Reference Mechanick, Apovian and Brethauer74,Reference Vynckier, Ceulemans and Vanheule111)} .

Calcium and vitamin D deficiency

Bone fragility has emerged as a common and severe complication of bariatric surgery. Different mechanisms have been proposed to contribute to bone fragility, including (i) micronutrient malabsorption, (ii) mechanical unloading and (iii) changes in sex, gut and adipose-derived hormones^{(Reference Corbeels, Verlinden and Lannoo112)}. Among micronutrients, calcium and vitamin D are essential to ensure bone health. After surgery, malabsorption of calcium and vitamin D may cause a hypocalcaemic state. As a result, the parathyroid glands will secrete higher levels of parathyroid hormone. Under the control of parathyroid hormone, urinary calcium secretion is decreased and skeletal calcium is mobilised to maintain serum calcium^{(Reference Bal, Finelli, Shope and Koch108,Reference Corbeels, Verlinden and Lannoo112)} . In the short term, the clinical symptoms of calcium and vitamin D deficiency include muscle weakness, muscle cramps and back pain^{(Reference Bal, Finelli, Shope and Koch108,Reference Bouillon, Manousaki and Rosen113)} . In the long term, bone loss can manifest and translate into fracture risk. Fracture risk seems to increase following mixed restrictive and malabsorptive bariatric procedures with a predominance of fractures at osteoporotic sites (RR 1·4–2·3 depending on the study). Mounting data indicate that fracture risk manifests in the long term, whereas bone remodelling already occurs within the first year after surgery^{(Reference Saad, Ghezzawi, Habli, Alami and Chakhtoura114,Reference Gagnon and Schafer115)} . To date, it remains unclear whether sleeve gastrectomy has the same effect on skeletal health as Roux-en-Y gastric bypass^{(Reference Krez and Stein116)}. Due to the multifactorial skeletal effect of bariatric surgery, a multidisciplinary approach of screening and supplementation is recommended^{(Reference Beavers, Greene and Yu117)}.

Water-soluble vitamins B₁, B₉ and B₁₂

Vitamin B₁ or thiamine is an essential micronutrient for myelin formation in the nerve cells with limited body storage. Encephalopathy is a major nutritional complication of vitamin B₁ deficiency that mainly develops in the first week or first months after surgery. After surgery, inadequate dietary intake or vomiting can lead to depleted stores. In turn, severe thiamine deficiency results in selective neuronal cell death that can culminate into acute and chronic encephalopathy. Wernicke’s encephalopathy is an acute neurological condition that is characterised by a triad of symptoms including ophthalmological problems, ataxia and consciousness disturbances. When left untreated, Wernicke’s encephalopathy can progress to Korsakoff syndrome, which is characterised by a chronic state of mental dysfunction with permanent memory impairment^{(Reference Landais118)}. In severe cases, thiamine deficiency may result in death^{(Reference Haid, Gutmann and Crosby119)}. Another rare complication associated with vitamin B₁ deficiency is acute polyradiculoneuropathy. It presents as pain in the lower limbs, followed by ascending paralysis, ataxia, areflexia and sensory loss, which resembles Guillain–Barré syndrome^{(Reference Yasawy and Hassan120,Reference AlShareef, Albaradei, AlOtaibi, Alanazy and Abuzinadah121)} . Although the risk of thiamine deficiency is highest in the first months after surgery, it can present lifelong, especially in combination with inadequate intake due to persisting vomiting and supplementation non-compliance or alcohol abuse^{(Reference Oudman, Wijnia, van Dam, Biter and Postma122)}. In addition to thiamine, other water-soluble vitamins can result in neurological complications. Although uncommon, folate deficiency may lead to peripheral neuropathy or restless leg syndrome, while vitamin B₁₂ deficiency can manifest neurologically by presenting as myelopathy, neuropathy, paraesthesia and ataxia^{(Reference Berger123)}.

Fat-soluble vitamins A and E

Given that fat-soluble vitamins require bile acids for absorption, deficiencies of fat-soluble vitamins with neurological manifestations may arise after bariatric surgery. Due to its role in photoreceptor function, vitamin A deficiency can result in optic neuropathy, xerophthalmia and night blindness^{(Reference Spits, De Laey and Leroy124,Reference Lee, Hamilton, Harris and Schwab125)} . Vitamin E is essential for normal neurological functioning and for protecting neural cell membranes from oxidative damage. After bariatric surgery, the clinical presentation of vitamin E deficiency is rarely documented. However, vitamin E deficiency may present as peripheral neuropathy, skeletal myopathy, gait disturbances, head titubation, decreased sensation, ataxia, ophthalmologic disorders and nystagmus^{(Reference Sherf-Dagan, Buch, Ben-Porat, Sakran and Sinai126)}.

Copper and zinc deficiency

Mineral and trace-element deficiencies have seldom been described after bariatric surgery. Although human cases are rare, copper deficiency can manifest neurologically as myelopathy and peripheral neuropathy after bariatric surgery^{(Reference Kumar, McEvoy and Ahlskog127)}, while zinc deficiency can manifest as a myeloneuropathy-like disorder with spastic gait and sensory ataxia^{(Reference Bal, Finelli, Shope and Koch108)}.