Vitamin a Deficiency Due to Selective Eating As a Cause of Blindness in A

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Vitamin A Deficiency Due to Selective Silvia Martini, MD,a Angela Rizzello, MD,a Ilaria Corsini, MD,a Benedetta Romanin, MD,a EatingMichelangelo Fiorentino, as PhD, ba Sara Cause Grandi, MD,a Rosalba of Bergamaschi, Blindness MDa in a High-Income Setting abstract Vitamin A is a fat-soluble micronutrient involved in the regulation of several physiologic functions, such as visual acuity, epithelial tissue integrity, immune response, and gene expression, thus playing a crucial role in childhood growth and development. Although vitamin A deficiency (VAD) in resource-limited settings is still an actual issue and represents the leading cause of preventable childhood blindness, its occurrence in high- income countries is rare, although possibly underdiagnosed because of its a b nonspecific early manifestations. A good awareness of VAD symptoms and Pediatric Emergency Unit and Pathology Service, Addarii Institute of Oncology, St. Orsola-Malpighi Hospital, risk factors could aid its early diagnosis, which is fundamental to undertake University of Bologna, Bologna, Italy a prompt treatment and to prevent ocular complications. Nevertheless, Drs Martini, Rizzello, and Romanin collected the role of restrictive dietary habits, increasingly common in developed and reviewed the patient’s data and wrote the countries, is often overlooked in infants and children. We present a case first draft of the manuscript; Drs Bergamaschi, of VAD with permanent ocular sequelae in a 5-year-old girl from a high- Corsini, and Grandi actively contributed in the clinical management of the patient and critically income country. In the case described, VAD ensued from a highly restricted revised the manuscript; Dr Fiorentino performed diet, mainly limited to oat milk, which had been followed for more than 2 the histological evaluation and critically revised years. This child presented with ocular symptoms, opportunistic infection, the manuscript; and all authors approved the final manuscript as submitted and agree to be anemia, poor growth, and a diffuse squamous metaplasia of the bladder; accountable for all aspects of the work. after commencing retinol supplementation, a gradual healing of clinical VAD DOI: https://doi.org/10.1542/peds.2016-2628 manifestations occurred, with the exception of the ocular sequelae, which Accepted for publication Jun 15, 2017 resulted in irreversible visual loss. Address correspondence to Silvia Martini, MD, Neonatal Intensive Care Unit, St. Orsola-Malpighi University Hospital, Via Massarenti 11, 40138 Bologna, Italy. E-mail: [email protected] Vitamin A is a fat-soluble vitamin countries, childhood VAD is thought PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, involved in crucial physiologic to be rare and primarily related to 1098-4275). processes, including organogenesis, underlying medical conditions5 (eg, Copyright © 2018 by the American Academy of tissue differentiation, visual1 function, malabsorption, liver diseases ), Pediatrics and immune response, thus playing whereas other possible risk factors, FINANCIAL DISCLOSURE: The authors have a key role in growth and development such as adherence to selective diets for indicated they have no financial relationships during childhood. either sociocultural,6 environmental, relevant to this article to disclose. or health reasons,7 are rarely taken FUNDING: No external funding. In resource-limited settings, vitamin into account. Although an early POTENTIAL CONFLICT OF INTEREST: The authors A deficiency (VAD) is mainly due to diagnosis is fundamental to undertake have indicated they have no potential conflicts of chronic malnutrition and is estimated a prompt retinol supplementation and interest to disclose. to affect up to2 50% of preschool- to prevent permanent blindness, VAD aged children ; in this population, can present a diagnostic challenge to To cite: Martini S, Rizzello A, Corsini I, et al. Vitamin A VAD represents the leading3 cause pediatricians. Its early symptoms, such Deficiency Due to Selective Eating as a Cause of of preventable blindness and is as xerophthalmia and hemeralopia, are Blindness in a High-Income Setting. Pediatrics. 2018; 141(s5):e20162628 associated with increased rates4 subtle and nonspecific 3and are thus of morbidity and mortality. On frequently overlooked. Furthermore, the other hand, in high-income the progressive impairment of multiple Downloaded from www.aappublications.org/news by guest on September 28, 2021 PEDIATRICS Volume 141, number s5, April 2018:e20162628 CASE REPORT TABLE 1 Anthropometric Measures, Blood Tests, and Urinalysis Results During Hospital Stay and at Follow-up Evaluation Time From Diagnosis, d Admission Diagnosis Follow-up Reference Valuesa −28 0 30 60 180 360 Weight, kg (percentile) 14.5 (<3°) 15 (<3°) 15.5 (<3°) 17 (3–10°) 18 (10°) 22 (>25°) Height, cm (percentile) 105 (<3°) 105 (<3°) 105 (<3°) 105 (<3°) 106 (3°) 112 (3–10°) White blood cell count, n/mmc 22 200 12 480 6920 6460 10 010 6920 4200–9000 Neutrophils, % 74.3 44.4 31.7 36.6 27.5 30.2 40–74 Lymphocytes, % 20.5 46.1 57.6 53.7 61.8 58.2 19–48 Hemoglobin, g/dL 9.3 8.8 9.9 10.1 12.3 12.6 12–15 C-reactive protein, mg/dL <0.03 0.3 <0.03 <0.03 <0.03 0.04 <0.8 Albumin, g/dL 2.6 2.9 4.3 4.5 4.2 4.4 3.5–5.5 Total cholesterol, mg/dL 63 58 108 159 195 — <200 HDL, mg/dL 37 6 42 53 67 — >45 LDL, mg/dL 17 26 60 — — — <130 Iron, μg/dL 36 16 38 18 20 70 35–145 Ferritin, ng/mL 107 74 18 6 6 7 15–140 Vitamin A, mmol/L — 1.1 1.4 1.3 1.7 1.4 1.1–2.3 RBP, mg/dL — 3.5 4.8 — — — 3–6 Vitamin B12, pg/mL — 1406 1281 457 — 488 145–914 PT 1.24 1.25 1.15 1.11 1.07 1.09 <1.2 aPTT 0.89 0.85 1.06 1.04 1.01 1.09 0.82–1.25 Thyrotropin, mcIU/mL — 52.1 1.4 1.5 1.54 1.14 0.27–4.2 FT3, pg/mL — 2.4 6.4 5.6 4.3 5.6 2.2–5.5 FT4, pg/mL — 6.3 14.7 15.6 17.5 15.7 9–17 Zinc, μmol/mL — 18.9 — — — — 9.8–16.8 Urinalysis Leukocytes Leukocytes Normal Normal Normal Normal Bacteria Bacteria Squamous cells Squamous cells aPTT, activated partial thromboplastin; FT3, free T3; FT4, free T4; HDL, high-density lipoprotein; LDL, low-density lipoprotein; PT, prothrombin time; —, not applicable. a Reference values used in our laboratory.

organ systems (sensory organs, discharge unresponsive to topical (PN) was started on day 7 of endocrine and immune systems, bone antibiotics. hospitalization. marrow, skin, and mucosae) associated Combined antibiotic and antifungal At admission, the patient also with the worsening of vitamin A status eye drops were also administered, presented with thin scalp hair, can be misdiagnosed as other more8 but no improvement in ocular dystrophic skin covered with lanugo, common pathologic conditions, thus symptoms occurred over the first and diffuse muscle atrophy. Blood potentially contributing to delayed week. Ultrasound biomicroscopy, tests revealed moderate anemia, diagnosis and treatment. performed on day 9, revealed right hypoalbuminemia, and significantly corneal thinning and left corneal We report a case of VAD with low levels of total and low-density perforation, requiring corneal patch multisystem involvement in a high- lipoprotein cholesterol (see Table 1), graft repair. income 5-year-old girl, caused by a whereas the urinalysis revealed ’ persistent selective diet and ensuing pyuria, bacteriuria, and abundant A catheter urine culture, collected in permanent visual loss. squamous cells. The girl s weight Pseudomonasin view of persistent aeruginosa pyuria and bacteriuria, was positive for CASE REPORT and height at admission were well below the third percentile for age; ; therefore, both birth weight and target height on day 6, treatment with ceftazidime were above the 75th percentile, but was undertaken. In the following This 5-year-old girl was admitted other anthropometric data were not days, however, the urine turned to the Pediatric Department of St. available. progressively turbid and bladder Orsola-Malpighi University Hospital ultrasound revealed a thickening (Bologna, Italy) with fever and severe From the time of admission, the of the bladder wall and gross, keratoconjunctivitis. Photophobia patient showed irritability and hyperechoic particles suspended and epiphora were reported to have feeding refusal, which the parents within its lumenP aeruginosa (Fig 1). Because first appeared 1 year before and to ascribed to her poor physical urine cultures were persistently have gradually worsened to bilateral condition; because of the persistence positive for , after conjunctival injection and purulent of this behavior, parenteral nutrition a 7-day course, ceftazidime was Downloaded from www.aappublications.org/news by guest on September 28, 2021 S440 MARTINI et al gradually increased, whereas vitamin B12 had returned to normal. Anthropometric measurements and laboratory test results at follow-up evaluations are shown in Table 1. The patient continued on a varied diet, and serum retinol FIGURE 1 remained within the normal range. Bladder ultrasound evaluation showing thick ening of the bladder wall and hyperechoic par As thyroid function progressively ticles within the lumen. normalized, substitutive therapy was discontinued after 9 months. Satisfactory catch-up growth gradually occurred; at the 2-year changed to meropenem and evaluation, height and weight teicoplanin. On day 20, while still had reached the 25th and 50th on antibiotics, the patient flushed percentiles, respectively. Although out in the urine a whitish tissue most of the VAD-related clinical fragment, which on histologic features completely recovered, FIGURE 2 examination was found to be entirely Squamous metaplasia of bladder mucosa. A, a worsening of the ocular composed of acellular keratin Cystoscopic appearance. B, Histologic evidence symptoms occurred despite retinol material. A cystoscopy evaluation of metaplastic urothelium with extensive hyper supplementation. The patient was thus performed on day 25, keratinization and shedding of acellular keratin developed irreversible retinal material. showing a diffuse white patch of atrophy in the left eye, whereas bladder mucosa (Fig 2A); histology the right corneal thinning was revealed squamous metaplasia complicated by a severe infection of the urothelium with extensive to chase possible overlooked with ensuing phthisis bulbi, hyperkeratinization (Fig 2B). information: a significantly restricted eventually resulting in permanent The combination of bladder diet, consisting mainly of oat milk bilateral visual loss. metaplasia, ocular symptoms, and and ongoing for over 2 years, was DISCUSSION the opportunistic infection eventually eventually revealed by the parents. led us to consider VAD. On day 28, A psychosocial evaluation of the serum vitamin A levels were thus whole family was consequently This case describes the occurrence determined as 1.1 mmol/L (PN performed, disclosing a conflictual of VAD resulting from a prolonged, ongoing for 21 days). Furthermore, mother-daughter relationship and an strictly selective diet in a high- serum levels of vitamin B12 were unsupportive family environment; income child. remarkably high, whereas zinc, iron, therefore, both psychological and After oral intake, vitamin A is and ferritin fell within normal ranges nutritional rehabilitation were absorbed by enterocytes and (see Table 1). A significant elevation undertaken. metabolized into its predominant of thyrotropin (52.1 mcIU/mL) circulating form, retinol, which was also noticed, with evidence of In the following weeks, the patient combines with its carrier, retinol- an enlarged thyroid gland at neck improved, her urine gradually binding protein (RBP), and ultrasound. In view of these findings, ’ 9 µ cleared, and urine culture results transthyretin. By binding specific parenteral supplementation of µ became negative. Under a dietician s cell or nuclei receptors, the resulting vitamin A (retinol, 1000 g/day) and guidance, she progressively adopted complex regulates several functions, oral levothyroxine (6.25 g/day) a varied and nutritionally balanced including visual acuity, epithelial were started. diet, which allowed PN to be tissue integrity, immune1 competence, The main causes of malabsorption discontinued 1 month after VAD and gene expression. In the presence diagnosis and an intravenous-to- (celiac disease, pancreatic µ of VAD, or in the case of impaired insufficiency, intestinal bowel oral switch of retinol administration RBP synthesis, these processes are disease, intestinal infections, (1500 g/day). After a 3-month inadequately supported and multiple immunodeficiency) were hospitalization, the patient was clinical manifestation may develop, ’ investigated, yielding negative discharged in good condition and the most common being ocular results. The patient s dietary habits on oral retinol supplementation; at symptoms, anemia, and increased10 were thus thoroughly reexamined discharge, vitamin A serum levels had susceptibility to infections. These Downloaded from www.aappublications.org/news by guest on September 28, 2021 PEDIATRICS Volume 141, number s5, April 2018 S441 findings were all present in the case rapidly increase. Hence, the normal to the following dietary features: described; additionally, squamous RBP values observed in the present strict exclusion of meat, eggs, and metaplasia of the bladder, a rare case are consistent with parenteral dairy products, which is becoming but characteristic condition ensuing vitamin A administration, which at increasingly 27common (eg, unbalanced from the VAD-related impairment11,12 the time of measurement had been vegan diets) ; the so-called cafeteria of epithelial regeneration, was ongoing for 3 weeks. diet, increasingly popular in the observed. By reducing nocturnal In the case described, VAD ensued modern society, which consists growth hormone secretion, VAD can from a persistent selective diet, of energy-dense, low-quality lead to significant growth restriction, consisting mainly of oat milk. food providing large amounts of 28 usually responsive13 to vitamin A Storage processes for oat milk carbohydrates and vegetable lipids ; supplementation ; this is consistent extreme dietary protein restriction cause significant22 losses of vitamins with the significant catch-up growth A and B12‍ ; nevertheless, some that, though rare in high-income observed in this patient after of the main products currently countries,25 can result in functional undertaking VAD treatment. Vitamin available, such as the 1 the patient VAD by affecting RBP synthesis. A is also known to influence the 14 consumed, are fortified with the In the present case, the abnormal pituitary-thyroid axis ; although the 23 latter but not with the former. eating behavior was attributed to high thyrotropin levels observed in These data are consistent with the an impaired maternal relationship this patient might be first ascribed high serum levels of vitamin B12 and family functioning, which are to her poor clinical condition, a observed in the present case, which reported as the main psychosocial concomitant role for VAD could be progressively normalized after oat causes underlying selective eating hypothesized. 29 milk discontinuation. The effects of in preschool-aged children. Other this diet were further evidenced by conditions, such as multiple food Serum retinol levels are frequently β 30,31 32 the low cholesterol levels, consistent allergies, ‍ mental disorders,33 and used to determine individual with the properties of oat -glucan, poor socioeconomic status have vitamin A status; current cutoff which hampers the intestinal uptake also been associated with selective values defining15 VAD are 0.7 of dietary cholesterol and enhances diets and ensuing micronutrient mmol/L, whereas values <1.05 ’ its hepatic24 conversion into bile deficiencies and thus need to be mmol/L identify subjects16 with acids. Oat milk products are also investigated at the patient s history. a marginal status. Although among the nondairy plant-based The case described provides a real the clinical manifestations in the milk substitutes with the lowest 23 example of how VAD can affect present case were suggestive of protein content ; the ensuing ’ different systems and organs, severe VAD, serum retinol was not protein malnutrition, highlighted by thus resulting in a diagnostically significantly reduced; this finding the patient s hypoalbuminemia, may challenging entity even in high- might be explained by the fact have contributed to worsen VAD income settings, where diagnostic that, at the time of measurement, symptoms by affecting liver synthesis 25 resources are easily accessible PN had already been ongoing of RBP, which is crucial for retinol and available. To avoid permanent for 21 days, providing vitamin A cellular intake. μ complications, the varied range intake equal to the recommended17 dietary allowance (400 g/day ). To the best of our knowledge, this of VAD clinical manifestations Consistent with its homeostatic case is the first report of VAD with should be kept in mind not only control mechanisms, however, serum permanent sequelae resulting from by pediatricians but also by the retinol reflects vitamin A stores severe selective eating in early subspecialty physicians potentially childhood and reveals how restrictive involved in the differential diagnosis; only when they are either18 extremely high or severely depleted ; hence, dietary habits can place children at to this end, a multidisciplinary between these extremes, it may not risk for VAD even in high-income discussion of complex cases such reliably correlate with individual settings. as the 1 described soon after vitamin A status or clinical signs The main sources of preformed hospital admission may contribute of deficiency. RBP has also been vitamin A are animal liver, egg yolk, to optimize and shorten the related diagnostic process. proposed as19 a surrogate for VAD whole milk, and dairy products, assessment. RBP, however, has a whereas fruit and green leafy CONCLUSIONS short half-life and20 previous studies and yellow vegetables are rich26 on both animal21s and malnourished in provitamin A carotenoids. children on PN have shown that, Hence, if VAD is suspected, the A good awareness of VAD signs, soon after undertaking vitamin A nutrition history should be carefully symptoms, and risk factors is supplementation, its serum levels examined, with particular reference fundamental for early diagnosis Downloaded from www.aappublications.org/news by guest on September 28, 2021 S442 MARTINI et al 6. Kersting M, Alexy U, Schürmann the Prevalence of Vitamin A Deficiency S. Critical dietary habits in early in Populations. Geneva, Switzerland: in infants and children from low- childhood: principles and practice. World Health Organization; 2011 World Rev Nutr Diet. 2016;115:24 35 prevalence settings to prevent the – 19. Baeten JM, Richardson BA, Bankson establishment of ocular sequelae 7. Couroucli XI. Vitamin A deficiency in DD, et al. Use of serum retinol-binding that can persist even after adequate adolescents: rare or underdiagnosed? protein for prediction of vitamin A vitamin A status is restored. Lancet. 2016;387(10013):94 deficiency: effects of HIV-1 infection, ACKNOWLEDGMENTS 8. Balint JP. Physical findings in protein malnutrition, and the acute nutritional deficiencies. Pediatr Clin phase response. Am J Clin Nutr. 2004;79(2):218 225 North Am. 1998;45(1):245–260 – We acknowledge Prof Massimo 9. Gibson RS. Principles of Nutritional 20. Muto Y, Smith JE, Milch PO, Goodman Busin, who has managed the patient Assessment. 2nd ed. Oxford, United DS. 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