Consequences of an extreme diet in the professional sport: Refeeding syndrome to a bodybuilder

Abstract

Refeeding syndrome, as a life-threatening condition, is well known among severely malnourished or deeply metabolically stressed patients. This case presents an atypical manifestation of the syndrome to a young bodybuilder, whose extreme diet, including 5 months of insufficient nourishment before the sport competition and 6 days of carbohydrates overload afterwards, has led him to a bilateral lower - limb paralysis and drastic homeostatic disturbances. Severe hypokalemia, hypophosphatemia, hypomagnesemia and hyperglycemia with mildly elevated liver enzymes have occurred. The patient could barely move his legs and arms, and his state has been followed by a hypertensive crisis, which required an immediate intravenous treatment. Although his weight was 112,5 kg with a body mass index of 32,2 kg per square meter, and his blood serum albumin concentration resulted inside the normal range, the overall condition was corresponding to the state of extenuated and malnourished patients. This case reflects to high prevalence of eating disorders or non-adequate nutrition among weight-sensitive sport athletes. The importance of prevention and opportune diagnostics of refeeding syndrome among special vulnerable groups should be considered.

Full text

Consequences of an extreme diet in the professional sport: Refeeding
syndrome to a bodybuilder
Indr_
e Lapinskien _
e
a
, Gabija Mikulevi
cien _
e
a
,
*
, Gabija Laubner
a
, Robertas Badaras
b
a
Republican Vilnius University Hospital, Centre of Toxicology, Lithuania
b
Vilnius University, Faculty of Medicine, Centre of Toxicology, Lithuania
article info
Article history:
Received 3 September 2017
Accepted 17 October 2017
summary
Refeeding syndrome, as a life-threatening condition, is well known among severely malnourished or
deeply metabolically stressed patients. This case presents an atypical manifestation of the syndrome to a
young bodybuilder, whose extreme diet, including 5 months of insufficient nourishment before the sport
competition and 6 days of carbohydrates overload afterwards, has led him to a bilateral lower elimb
paralysis and drastic homeostatic disturbances. Severe hypokalemia, hypophosphatemia, hypomagne-
semia and hyperglycemia with mildly elevated liver enzymes have occurred. The patient could barely
move his legs and arms, and his state has been followed by a hypertensive crisis, which required an
immediate intravenous treatment. Although his weight was 112,5 kg with a body mass index of 32,2 kg
per square meter, and his blood serum albumin concentration resulted inside the normal range, the
overall condition was corresponding to the state of extenuated and malnourished patients. This case
reflects to high prevalence of eating disorders or non-adequate nutrition among weight-sensitive sport
athletes. The importance of prevention and opportune diagnostics of refeeding syndrome among special
vulnerable groups should be considered.
©2017 European Society for Clinical Nutrition and Metabolism. Published by Elsevier Ltd. All rights
reserved.
Introduction
Refeeding as a life threatening condition has been known since
the World War II [1].Itisdefined as a non-immune syndrome,
caused by metabolic disturbances, such as fluid and electrolyte
shifts, to people who happen to be severely malnourished or deeply
metabolically stressed [2,3]. It occurs when nutrition is reintro-
duced into an organism after a period of starvation or fasting [4]
and can be expressed as a mild, moderate or severe stage of
health disturbance [5]. The spectrum of presentation ranges from
nausea and vomiting, to respiratory insufficiency, cardiac arrhyth-
mias, delirium, coma and death [6]. The risk of developing the
syndrome is directly linked to the amount of weight, which is lost
during the starvation episode and the rapidity of the weight
restoration process [7]. Other risk factors, which could be also used
to recognise the syndrome, are: low baseline levels of phosphate,
potassium, magnesium, thiamine and little or no nutritional intake
for 5e10 days [8]. Refeeding syndrome is mostly common among
vulnerable groups of people, such as cancer patients (up to 25%)
and hospitalized for anorexia nervosa patients (6% in severe cases
and 22% in mild cases), hospitalized geriatric patients (around 70%)
and extremely preterm infants [9e12]. However, there are some
other special groups, for instance, professional athletes, among
whom strict dietary routine may also become a risk factor [13,14].
Case presentation
We report a case of a 28-year-old man, who was admitted to the
Emergency Department on the 20th of June 2016, due to a sudden
bilateral lower limb paralysis (Medical Research Council (MRC)
Scale for Muscle Strength eGrade 2). He had no history of injury or
trauma, as well as other previous illness or disability, remained
fully conscious (Glasgow Coma Score (GCS) 15) during the exami-
nation and had no other complaints except muscle weakness. Ac-
cording to the anamnesis and visibly pronounced general muscle
hypertrophy, the patient was a professional bodybuilder, attending
an annual international fitness competition. Two days after the
*Corresponding author. Republican Vilnius University Hospital, Siltnamiu 29, LT
04130 Vilnius, Lithuania.
E-mail address: gabija.mikuleviciene@gmail.com (G. Mikulevi
cien _
e).
Contents lists available at ScienceDirect
Clinical Nutrition ESPEN
journal homepage: http://www.clinicalnutritionespen.com
https://doi.org/10.1016/j.clnesp.2017.10.003
2405-4577/©2017 European Society for Clinical Nutrition and Metabolism. Published by Elsevier Ltd. All rights reserved.
Clinical Nutrition ESPEN xxx (2017) e1ee3
Please cite this article in press as: Lapinskien_
e I, et al., Consequences of an extreme diet in the professional sport: Refeeding syndrome to a
bodybuilder, Clinical Nutrition ESPEN (2017), https://doi.org/10.1016/j.clnesp.2017.10.003

event (where he became a vice echampion) he started to feel
annoying muscle cramps and palpitations, and after one more day a
bilateral leg paralysis and whole body weakness occurred. While
preparing for the competition, he admitted being on a special diet,
which included a suppressed nutrient income regime for one
month and then a massive consumption of carbohydrates just a few
days after the event. Although his usual diet routine consisted of
1000 g of different types of grains, plus 500 g of lean meat per day,
while preparing for the competition all carbohydrates step-by-step
were eliminated from the regime within a four-month period and
for the last month before the event patient was using no carbo-
hydrates at all. Energy requirements had to be compensated by
other nutrients eproteins and fats ealone. Fast-acting carbohy-
drates (such as chocolate bars) were used only on the competition
day and after the event e800 g of various carbohydrates eevery
day for 5 more days. The patient strongly denied using any medi-
cine or other chemical substances, only some legal dietary sup-
plements, including protein shakes and multivitamins. During the
preparations stage he lost 19 kg of body mass and on admission to
the hospital day his weight was 112,5 kg and his height e1,87 m.
Vital parameters were: arterial blood pressure (BP) 190/100 mmHg,
heart rate (HR) 86 beats per minute, peripheral oxygen saturation
96%, body temperature 37,2

C. According to the anamnesis and
clinical symptoms, refeeding syndrome was suspected as a primary
diagnosis. A broad spectrum analysis of his blood tests was chosen.
His venous blood showed severe hypokalemia (1,50 mmol/L),
hypophosphatemia (0,20 mmol/L), relatively low magnesium con-
centration (0,77 mmol/L), hyperglycemia (13,20 mmol/L or
237,60 mg/dL), elevated creatine kinase (2600 U/L) and liver func-
tion parameters (aspartate aminotransferase 92 U/L, alanine
aminotransferase 112 U/L), serum lactate 2,3 mmol/L. Other mea-
surements (pH, sodium, chloride, calcium, c-reactive protein, tro-
ponine I, serum creatinine) varied at normal ranges, serum albumin
was 47,32 g/L. According to bioimpedance analysis, an approach for
body composition, his body mass index (BMI) was 32,2 kg/m
2
, lean
tissue index (LTI) 22,5 kg/m
2
, fat tissue index (FTI) 10,1 kg/m
2
with
26 kg (23,1%) of total body fat. Electrocardiography showed U-
waves, confirming the hypokalemic state. The patient felt a whole
body weakness. He could barely move his legs (MRC muscle
strength grade 2) and the grip strength of his right (R) and left (L)
hands was correspondingly: R 40 N and L 10 N according to
dynamometric measurement, while comparing to an average grip
strength of a 24-29 year-old male: 538 N (R) and 494 N (L) [15]. The
patient was admitted to the Intensive care unit (ICU), where he was
immediately given an intravenous potassium infusion (180,5 g
totally, during the stay in ICU), as well as other electrolyte (phos-
phorus, magnesium) and fluid supplementation. Hyperglycemia
was corrected with intravenous insulin infusion (66,5 Units totally
within 34 h) and hypertensive crisis was controlled by using
nitroglycerine intravenously. A special consideration was
approached to the patient's nutrition plan. He was given a balanced
diet, composed by a clinical dietician, as well as an oral micro-
nutrient supplementation, together with injectable vitamins and
other vital microelements. Hyperglycemia and aggressive arterial
hypertension were corrected during the first 48 h hospital stay.
Fatigue and muscle strength recovered gradually (Fig. 1) in 3 days
time. After being 2 days in ICU, the patient was moved to an in-
patient department where he stayed for 2 more days and after-
wards was discharged from the hospital without any residual
outcomes. He underwent a health screening program on April 2017.
Blood serology tests (without variances from normal range) and
MRC muscle strength (grade 5) with the measured grip strength of
his right (420 N) and left (420 N) hands showed a recovery after the
syndrome.
Discussion
This is an atypical case and manifestation of refeeding syn-
drome. Bodybuilders are a specific group of people, usually having a
strict dietetic routine [16e18] . According to literature, three phases
have been described. The first phase involves few months of
hypercaloric nutrition rich in proteins, for the build-up of muscle
mass. The second phase is a period of restricted caloric intake to
reduce subcutaneous fat. The third phase, during the last week of
preparations, includes simultaneous extreme carbohydrate intake
to load muscle glycogen, sodium, and water restriction to produce
subcutaneous volume deficit and better definition of muscle con-
tours [19]. Our patient, while preparing for the competition, by
eliminating all carbohydrates from his diet before the event and
restoring their income (in sizeable amounts) right after it, has
modified the last two phases in his own way. However, the
mechanism of the process remains the same. The second phase,
especially if it lasts more than a few days, leads to a starvation ef-
fect. During starvation blood glucose level begins to fall within
24e72 h [20]. As glucose is essential to the body, organism tries to
maintain its concentration by glycogenolysis and gluconeogenesis.
Glycogen stores usually last up to 72 h [21]. and for further main-
tenance of homeostasis other substances, such as fatty acids and
0
100
200
300
400
500
600
8 p.m 11 p.m. 8 a.m 11 a.m 6 p.m 9 p.m 8 a.m 11 a.m 6 p.m 9 p.m 8 a.m 11 a.m
ht4dr3dn2ts1
R L
Fig. 1. Grip strength (Newtons) of the right (R) and left (L) hands during the 1st e4th days of hospitalisation (measured using an isometric hand grip dynamometer).
I. Lapinskien_
e et al. / Clinical Nutrition ESPEN xxx (2017) e1ee3e2
Please cite this article in press as: Lapinskien_
e I, et al., Consequences of an extreme diet in the professional sport: Refeeding syndrome to a
bodybuilder, Clinical Nutrition ESPEN (2017), https://doi.org/10.1016/j.clnesp.2017.10.003

amino acids, are being used (Krebs and Cori cycles) [22]. During this
metabolic adaptation a resultant loss of body fat and protein, as
well as depletion of elements, especially, phosphate, potassium and
magnesium, occurs [23]. Insulin stimulates the absorption of po-
tassium into the cells through the sodium-potassium ATPase pump,
which also transports glucose into the cells. Magnessium is also
taken into the cells. Stimulation of glycolysis increases formation of
phosphorylated carbohydrate compounds in liver and skeletal
muscle, which source is inorganic phosphate in the extracellular
fluid [24]. A decrease in serum levels of these elements occurs. Our
psatient, within his second phase of preparations, lost 19 kg. During
the third phase situation became even worse when a huge intake of
glucose provoked hyperinsulinemia. Insulin, by transporting
glucose into cells, has as well activated potassium transport. As
extracellular storages of potassium and other nutrients have
already been depleted during the second phase, a shift of extra-
cellular electrolytes has increased the deficit and initiated muscle
spasms and weakness, which led to the condition we have
mentioned before. Although multivitamins and other dietary sup-
plements have been used orally during the preparation stage, they
could not manage to cover the extracellular deficit because of a
disturbed homeostasis and relatively low bioavailability. In this
case manifestation of refeeding syndrome was difficult to predict as
even after a starvation period the patient's BMI and total weight
could not show the threat. One of the markers of this condition
could be a low serum albumin concentration. It usually goes along
with hypophosphatemia [25]. However, as the bodybuilder had a
well-expressed musculature and his BMI and LTI were high
(32,2 kg/m
2
and 22.5 kg/m
2
correspondingly), albumin concentra-
tion varied in normal range (47,32 g/L). This situation supports the
idea that serum albumin not always correlates with nutritional
status and has a limited value as a nutritional marker [26]. Current
studies suggest a new variable ethe importance of energy avail-
ability (EA), which describes how much energy is available for the
basic metabolic functions of a human body, such as reproduction,
immunity and skeletal homeostasis. A low EA, the state when EA
reaches <30 kcal/kg of a fat free mass and when the lower limits of
body fat (~4e5% in males) are approached, the consequences result
in muscle loss, hormonal imbalance, psychological problems,
negatively affected cardiovascular system [27]. EA could become
one of the markers that show the risk of refeeding. According to our
case, despite fasting patient's body fat was 23,1%. He did not reach
the critical limit and that, as a result, ended in a relatively milder
physiological distress, as well as a faster recovery from the syn-
drome. Treatment of refeeding syndrome depends on the imme-
diate correction of the electrolyte and fluid imbalance, as well as
other nutrients supplementation. According to the current guide-
lines, artificial nutritional support is recommended to start
together with a correction of homeostatic abnormalities [28]. Our
patient has succeeded in a quick and complete recovery after the
syndrome due to an adequate treatment, balanced diet, his physi-
ological abilities and young age. However, not all such cases are
managed to be solved without any harmful consequences.
Commonly described high prevalence of eating disorders among
athletes [29e31], especially in weight-sensitive sports, shows the
problem of underdiagnosed refeeding cases in this population. The
importance of adequate diagnostic and prevention of the syndrome
despite normal or higher BMI should be reconsidered [32] and new
possibilities to a quicker and easier screening, which could be used
on a daily basis, introduced.
Conflict of interest
The authors declare that there is no conflict of interest regarding
this publication.
References
[1] Schnitker MA, Mattman PE, Bliss TL. A clinical study of malnutrition in Japa-
nese prisoners of war. Ann Intern Med 1951;35:69e96.
[2] Mehanna HM, Moledina J, Travis. Refeeding syndrome: what it is, and how to
prevent and treat it. Br Med J 2008;336:1495e8.
[3] Doig GS, Simpson F, Heighes PT, Bellomo R, Chesher D, Peter WJ, et al.
Refeeding Syndrome Trial Investigators Group. Restricted versus continued
standard caloric intake during the management of refeeding syndrome in
critically ill adults: a randomised, parallel-group, multicentre, single-blind
controlled trial. Lancet 2015;3:943e52.
[4] Croock MA, Hally V, Panteli JV. The importance of the refeeding syndrome.
Nutrition 2001;17:632e7.
[5] Hearing SD. Refeeding syndrome. Br Med J 2004;328:908e9.
[6] Khan LU, Ahmed J, Khan S, MacFie J. Refeeding syndrome: a literature review.
Gastroenterol Res Pract 2011;2010:6.
[7] Mehler PS, Winkelmann AB, Andersen DM, Gaudiani JL. Nutritional rehabili-
tation: practical guidelines for refeeding the anorectic patient. J Nutr Metab
2010;2010.
[8] Mehler P. Anorexia nervosa in adults and adolescens: the refeeding syndrome.
Up to Date. 2016. (accessed online 2017, extrenal link: https://www.uptodate.
com/contents/anorexia-nervosa-in-adults-and-adolescents-the-refeeding-
syndrome.
[9] Gonzalez AG, Fajardo-Rodriguez A, Gonzalez-Figueroa E. The incidence of the
refeeding syndrome in cancer patients who receive artificial nutritional
treatment. Nutr Hosp 1996;11:98.
[10] Ornstein RM, Golden NH, Jacobson MS, Shenker IR. Hypophosphatemia during
nutritional rehabilitation in anorexia nervosa: for refeeding and monitoring.
J Adolesc Health 2003;32:83.
[11] Pourhassan M, Cuvelier I, Gehrke I, Marburger C, Modreker MK, Wirth R, et al.
Risk factors of refeeding syndrome in malnourished older hospitalized pa-
tients. Clin Nutr 2017. pii: S0261-5614:30219e4.
[12] Boubred F, Herlenius E, Bartocci M, Jonsson B, Vanp
ee M. Extremely preterm
infants who are small for gestational age have a high risk of early hypo-
phosphatemia and hypokalemia. Acta Paediatr 2015;104:1077e83.
[13] Mayr FB, Domanovits H. Hypokalemic paralysis in a professional bodybuilder.
Amer J Emer Med 2012;30. 1324e1324.
[14] Cheung KK, So WY, Kong AP, Ma RC, Chow FC. Life-threathening hypocalemic
paralysis in a young bodybuilder. Case Rep Endocrinol 2014;2014:483835.
[15] Mathiowetz V, Kashman N, Volland G, Weber K, Dowe M, Rogers S. Grip and
pinch strength: normative data for adults. Arch Phys Med Rehabil 1985;66:
69e72.
[16] Della Guardia L, Cavallaro M, Cena H. The risks of self-made diets: the case of
an amateur bodybuilder. J Int Soc Sports Nutr 2015;12:16.
[17] Spendlove J, Mitchell L, Gifford J, Hackett D, Slater G, Cobley S, et al. Dietary
intake of competitive bodybuilders. Sports Med 2015;45:1041e63.
[18] Gentil P, Barbosa de Lira CA, Paoli A, Barbosa dos Santos JA, Teixeira da
Silva RD, Magosso RF, et al. Nutrition, pharmacological and training strategies
adopted by six bodybuilders: case report and critical review. Eur J Transl Myol
2017 Feb 24;27(1):6247.
[19] Britschgi F, Zund G. Bodybuilding: hypokalemia and hypophosphatemia.
Schweiz Med Wochenschr 1991;121:1163e5. [article in German].
[20] Allison SP. Effect of insulin on metabolic response to injury. J Perenter Enter
Nut 1980;4:175e9.
[21] Ekberg K, Landau BR, Wnjgot A, Chandramouli V, Efendic S, Brunengraber H,
et al. Contributions by kidney and liver to glucose production in the post-
absorptive state and after 60 hours of fasting. Diabetes 1999;48:292e8.
[22] Garrett RH, Grisham CM. Principles of biochemistry with a human focus. USA:
Brooks/Cole, Thomson Learning; 2002. p. 578e85.
[23] Hill GL, Bradley JA, Smith RC, Smith AH, McCarthy ID, Morgan DB, et al.
Changes in body weight and body protein with intravenous nutrition.
J Perenter Enter Nut 1979;3:215e8.
[24] Yu ASL, Chir B, Stubbs JR. Causes of hypophosphatemia. UpToDate. 2016
(Accessed Jul, 2017, external link: https://www.uptodate.com/contents/
causes-of-hypophosphatemia.
[25] Marik PE, Bedigian MK. Refeeding hypophosphatemia in critically ill patients
in an intensive care unit. A prospective study. Arch Surg 1996;131:1043e7.
[26] Ikizler TA. The use and misuse of serum albumin as a nutritional marker in
kidney disease. Clin J Am Soc Nephrol 2012;7:1375e7.
[27] Fagerberg P. Negative consequences of low energy availability in natural male.
Bodybuilding: a review. Int J Sport Nutr Exerc Metab 2017;22:1e31.
[28] Stanga Z, Brunner A, Leuenberger E. Nutrition in clinical practicedthe
refeeding syndrome: illustrative cases and guidelines for prevention and
treatment. Eur J Clin Nutr 2008;62:687e94.
[29] Bratland-Sanda S, Sundgot-Borgen J. Eating disorders in athletes: overview of
prevalence, risk factors and recommendations for prevention and treatment.
Eur J Sport Sci 2013;13:499e508.
[30] Matzkin E, Curry EJ, Whitlock K. Female athlete triad: past, present, and
future. J Am Acad Orthop Surg 2015;23:424e32.
[31] Glazer JL. Eating disorders among male athletes. Curr Sports Med Rep 2008;7:
332e7.
[32] Martinsen M, Sundgot-Borgen J. Higher prevalence of eating disorders among
adolescent elite athletes than controls. Med Sci Sports Exerc 2013;45:
1188e97.
I. Lapinskien_
e et al. / Clinical Nutrition ESPEN xxx (2017) e1ee3 e3
Please cite this article in press as: Lapinskien_
e I, et al., Consequences of an extreme diet in the professional sport: Refeeding syndrome to a
bodybuilder, Clinical Nutrition ESPEN (2017), https://doi.org/10.1016/j.clnesp.2017.10.003