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B Workshop Papers Concerns About the Effects of Military Environments on Mineral Metabolism and Consequences of Marginal Deficiencies to Performance Karl E. Friedl U.S. Army Research Institute of Environmental Medicine, Natick, Massachusetts OVERVIEW Statement of the Problem Mineral requirements to sustain soldier performance in stressful conditions have been considered in military nutrition studies for many decades but rarely as the primary focus of the studies (Johnson, 1986; Sauberlich, 1984). These stud- ies, which were often underpowered, only descriptive, or not designed to address specific hypotheses in this area, raised questions that remained unresolved. The primary concern is the inability to-date to determine if there is a problem related to mineral metabolism (especially iron, calcium, zinc, and magnesium) that im- pairs health and performance in some soldiers in any field conditions. This should be considered from at least the following two perspectives: (a) does the military environment produce somewhat unique derangements or specifically change min- eral intake requirements that affect performance? and (b) are marginally defi- cient individuals (regardless of the reason for their deficiency) impaired relative to the demands of military performance? Answers to these questions are also 240

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APPENDIX B 241 important as they will help the Army address persistent suggestions about using mineral supplemention for soldiers that arise from health advocates and inter- ested entrepreneurs. Military Stressors Key stressors in the military environment include thermoregulatory chal- lenges, hard work and exercise, inadequate rest and energy intakes, and psycho- logical stress. Inadequate food intake is a problem in field environments, where soldiers typically underconsume by 25 percent of their energy requirements, and it can be worsened by the loss of appetite in hot or hypoxic environments; underconsumption is also a consequence of strictly enforced body fat standards, possibly with a larger effect on service women than men because women are more likely to exceed the standards and restrict their food intake. High sweat rate and water turnover is an important feature of hot work environments. Psycho- logical stressors range from trauma (e.g., exposure to traumatic injuries and death, exposures to populations living in poverty and ruin, and feelings of help- lessness in some peacekeeping operations) and anxiety (e.g., worry about per- sonal safety and family separation), to information overload (e.g., managing complex data from multiple sources). The extent to which these exposures are manifested in various stress responses depend on the resilience of the individual as well as leadership, unit cohesion, and other stress mitigators. Some unique environments and exposures (e.g., cold, altitude, enclosed en- vironments, blast overpressure in field artillery units, noise and toxic chemicals around military vehicles and aircraft, radiofrequency radiation in communica- tions centers) may also have to be considered when recommending optimal min- eral intakes. A previous Committee on Military Nutrition Research (CMNR) concluded that none of these special environments had been adequately charac- terized as producing higher oxidative stress burdens to soldiers than that for the healthy active U.S. population (IOM, 1999). Health and Performance Outcomes Soldiers are likely to be involved in demanding physical tasks that require strength and endurance; most physical tasks require lifting and carrying heavy loads. There are also significant mental demands that come with increased speed, complexity, and lethality of modern warfare; in this regard, every individual soldier may be called upon for rapid decision making and judgment calls, may require fine psychomotor performance (e.g., marksmanship), spatial mapping ability, pattern recognition, etc. Mood and motivation are important underlying aspects of soldier mental performance at all times. Even momentary lapses in mental and physical performance may have catastrophic effects in today's mili- tary environment.

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242 MINERAL REQUIREMENTS FOR MILITARY PERSONNEL Practical tests that adequately reflect militarily-relevant performance have been elusive but various test paradigms have provided useful measures in mili- tary studies, such as repeated box lifts (strength endurance), simulated sentry duty (vigilance, judgment, psychomotor performance), and simulated mission control center (multiple cognitive domains). The Army is increasingly turning to realistic training simulators that include electronic "combat" games and new markmanship trainers; these systems can also be converted to research tools that unobtrusively assess performance. In addition to cognition abilities, a fully responsive immune system is criti- cal to maintain the health and optimal health needed to face the demands of military lifestyle. Regardless of how good our vaccines may be, soldiers are not likely to be protected against all the endemic and deliberate infectious threats that may determine success or failure of a mission, nor will they have equipment and drugs to fully prevent inflammatory responses to physical demands and other physical and chemical threats. This highlights one more broad outcome of interest to the Army, optimizing a soldier's resistance to disease and injury. Some of the host defense systems that determine immunological and inflamma- tory responses appear to be importantly affected by mineral status. RANGER TRAINING AS A STRESS MODEL In the early 1990s, the Army had concerns about the high prevalence of infectious illnesses (pneumococcal pneumonia and soft tissue infections such as cellulitis) occurring in healthy young men undergoing 65 days of Ranger train- ing with multiple stressors, including extreme food and sleep restriction and hot humid conditions. This concern led to a request to determine if we could just provide "an iron pill or a vitamin" to prevent soldiers from getting sick while subjected to the same high level of stressful training. Initially we conducted a descriptive study to quantify the stressors (1,000 kcal/day energy deficits; 3.6 hr/ day sleep) and their effects; this was followed by a study that increased feeding by only 400 kcal/day, which was associated with marked improvement in im- mune function and reduction in infection rates (Kramer et al., 1997). Most of the men lost all of their fat reserves and the main adverse outcomes due to the semistarvation were in the cognitive and immune function (Friedl, 2003; Friedl et al., 2001). In addition, soldiers were hyperphagic and had sleep disturbances for several weeks after the course but were fully recovered six months later. During the initial planning of these experiments, we worried repeatedly about what would happen to iron and hematological parameters in association with the extreme privation. It was assumed that at some point hemoglobin and hematocrit would become low enough that it would not be safe or ethical to continue to draw blood from the test volunteers. This never happened and the significant changes in iron status that were observed occurred in the first few

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APPENDIX B 243 weeks of the course and corrected by the end of the course (Figure B-1). The observed changes were ascribed to acute phase responses, with no changes in iron, zinc, or copper status between baseline and the end of the course (Moore et al., 1993; Shippee et al., 1993). One possible explanation for the absence of a progressive decline in iron status is that periodic re-feeding that occurred at the end of each two week phase through the four training phases of this course replenished any deficiencies (sampling was done at the end of each phase of restriction and before the re-feeding began). The loss of muscle mass in this study would have also provided a steady supply of minerals and nutrients into the circulation. These findings matched those in the 1973 biomedical studies of Ranger training, with comparable weight loss and also no significant changes in hematological parameters and iron status across the training period. Thus, we did not detect overt mineral deficiencies in one of the most stressful models we could ethically study. However, only iron was targeted for study a priori and periodic re-feeding provided a less challenging intermittent replenishment. MILITARY QUESTIONS Is There a Problem (#1)?: Stress of Initial Entry Training and Iron Status in Young Women Iron became a subject of interest after a 1979 study identified deficiencies in female West Point cadets; this was observed again in the decennial 1989 study, despite the high prevalence of mineral and vitamin supplement use (Friedl et al., 1991; Kretsch et al., 1986). The observation was attributed to "just part of the stress of West Point," rather than being considered a medical concern, a treatable condition, or an important performance issue. However, in 1993, a comprehen- sive study of womens' health and performance in the last gender-segregated Army basic training class also suggested a high incidence of iron deficiency anemia compared to the U.S. population (Westphal et al., 1995). We noted inad- equate intakes of several minerals compared to established RDAs, a slight wors- ening of iron status through the course, and a correspondence between poor iron status and physical fitness test run time (Westphal et al., 1995). Several subse- quent studies attempted to followup on these findings as part of the 1994 De- fense Women's Health Research Program (DWHRP). One followed a select population of new female officers, comparing iron and hematological status to treadmill measured aerobic performance at the beginning and end of their officer basic course. This group was uniformly well nourished and fit, and offered no significant correlation between measures of iron and hematological status and aerobic performance (Cline et al., 1998); this sample was probably not represen- tative of the majority of female soldiers. The second study was a cross sectional examination of three populations of female soldiers, with iron and hematological

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244 MINERAL REQUIREMENTS FOR MILITARY PERSONNEL Hemoglobin Hematocrit 160 40 140 35 120 (g/L) 100 30 80 25 Hemoglobin 60 40 20 Baseline wk 2 wk 4 wk 6 wk 8 Baseline wk 2 wk 4 wk 6 wk 8 Ferritin Iron 240 14 12 190 10 (ug/L) 8 140 (umol/L) 6 Ferritin Iron 90 4 2 40 0 Baseline wk 2 wk 4 wk 6 wk 8 Baseline wk 2 wk 4 wk 6 wk 8 FIGURE B-1 Changes in iron status indicators status during Ranger training under severe food restriction and other stressors. SOURCE: Moore et al. (1993). B-1 new data that suggested a worsening status through their initial training (IOM, 1995). The cross sectional design presented a significant weakness in this study, and because of different locations, feeding regimens, and stressors, it was difficult to draw conclusions about the nature of this apparent decline in health status. A clinical study investigated the prevalence of iron deficiency in women referred to a military gastroenterology clinic, concluding that the majority of asymptom- atic iron deficiency anemia cases, including several already diagnosed by spe- cialists as having excess blood loss related to menstrual flow, actually had a high prevalence of significant endoscopy findings (Kepzyk et al., 1999). A fourth study funded in the DWHRP examined the benefits to neurocognitive perfor- mance from zinc and iron repletion in marginal deficiency. In preliminary analy- ses, many cognitive and psychometric tests were apparently improved (Sandstead, 2001); however, the results have not yet been reported.

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APPENDIX B 245 Is There a Problem (#2)?: Calcium Requirements and Bone Health Calcium intakes have been given more attention in military studies in the past decade because of research initiatives on prevention of stress fractures, particularly in female recruits. As part of the DHWRP, the CMNR convened a special review of women's body composition, nutrition and health which in- cluded a major review of stress fractures in the military (IOM, 1998). The subse- quent Bone Health and Military Medical Readiness (BHMMR) research pro- gram was shaped by the recommendations from this review and from the DRI report on calcium, vitamin D, and related nutrients (IOM, 1997). One important DWHRP project demonstrated that energy deficit, not in- tense exercise, was a key determinant of menstrual disturbances (Loucks and Thuma, 2003), refuting earlier concepts of a "female athlete triad" of intense exercise, menstrual abnormalities and osteoporosis. This was consistent with findings that high functioning women, such as Olympic athletes, exercising in- tensively but not restricting their diet had normal rates of oligomenorrhea. As a follow up effort supported by the BHMMR, experimental manipulations of the energy deficit that exceeded thresholds and caused alterations in LH (luteinized hormone) pulsatility, produced changes in bone mineral metabolism consistent with demineralization (Ihle and Loucks, 2004). Another important study, currently underway, is testing the hypothesis that 2,000 mg of calcium along with 800 IU of Vitamin D can substantially reduce the acute occurrence of stress fracture in a study of 5,200 young women during eight weeks of recruit training at the Great Lakes Naval Base. Part of the hypoth- esis and assumptions are that young women still have not attained peak bone mass, recruit training stimulates new bone formation, calcium intakes are nor- mally low in this population, and substantial sweat calcium losses occur in this training (Lappe, 2003). Special populations such as submariners living for extended periods in closed environments and away from sunlight have reduced plasma levels of 25-(OH) Vitamin D and special challenges in calcium metabolism (Sack et al., 1986). Two studies in progress in the BHMMR program are defining Vitamin D needs in relation to ethnicity and skin pigmentation, following up on a research gap identified in the review of calcium, vitamin D, and related nutrients (IOM, 1997). Are We Missing a Performance Enhancing Benefit (Or Are Some Supplements a Health or Performance Risk)? Some military studies have raised questions about the effects of stressors on mineral requirements and/or effects of supplementation on mitigation of stress responses. For example, as part of an important series of starvation and limited intake studies to determine minimum requirements for 10-day patrols, the 1968

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246 MINERAL REQUIREMENTS FOR MILITARY PERSONNEL Panama study measured intakes and losses for sodium, potassium, calcium, and magnesium, including sweat and urine excretion rates (Consolazio et al., 1979). The authors concluded that magnesium intakes were deficient but there was no biomedical evidence of a decline in magnesium levels. In a study at the Uni- formed Services University of Health Sciences (USUHS), magnesium balance in anaerobic exercise was considered. Another study tested specific performance benefits of zinc combined with Vitamin E on exhaustive running in women, based on hypothesized antioxidant actions, but found no effect of acute dosing (Singh et al., 1999). However, there has been no concerted effort through a carefully planned program of studies to determine benefits and risks of mineral supplements in military populations. Most service members report using supplements of some kind; this is cur- rently being resurveyed to improve estimates of specific supplement use. Young soldiers are at high risk for the use of supplements with putative performance enhancement because of the ready availability of these products in military com- missaries and stores, and because of perceptions that military training and opera- tional demands somehow drive a higher intake requirement, as well as the strate- gically seeded suggestions of performance enhancement in popular fitness magazines and the prevalent belief that such claims could not be made if they were not true (Friedl et al., 1992). A potentially important question that has never been addressed in military research studies is whether or not higher than usual intakes of certain supplements, including minerals, produce a deficiency state from withdrawal that is likely to occur when soldiers leave them behind for a field exercise or operational deployment. Another concern would be individual and population bases of upper limits of intakes, such as the obvious problem of iron overload if supplements are provided across military groups, for men and women or to all women regardless of their iron status. SUMMARY Constant discoveries of new roles of minerals in integrated physiological processes, where a mineral deficiency may have far reaching consequences on stress responses and susceptibility to disease makes this an important and rel- evant line of inquiry for military medical research. The key question that has never been properly addressed in military or other relevant studies is "can we achieve a sizeable improvement in mental or physical functioning, especially in stressful operational or training conditions, by improving the mineral status of young men and women in the military?" This area of investigation has been hindered by the absence of (1) practical and validated tools to definitely assess outcomes including neuropsychological outcomes and changes in disease sus- ceptibility, (2) adequate indices of mineral status, not confused by stress states including acute phase responses, and (3) clear indications of health and perfor- mance deficiencies.

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APPENDIX B 247 Research conducted under the special performance demands and conditions in which soldiers have to operate will not be addressed elsewhere and needs to be conducted by the Army. In fact, there is no other federal agency with a primary focus on biomedical aspects of performance; more typically the research is focused purely on health outcomes. This work is primarily centered at the U.S. Army Research Institute of Environmental Medicine in the Military Nutrition Division in collaboration with the Pennington Biomedical Research Center and with scientific guidance from the Institute of Medicine's CMNR. The key question(s) can also be framed by a pragmatic question: Should the Department of Defense consider the addition of a mineral supplement pack in every ration with instructions on use for "health and performance optimization," or perhaps other strategies on the use of whole foods? DISCLAIMER The opinions and assertions in this paper are those of the authors and do not necessarily reflect the official views of the Department of the Army. REFERENCES Cline AD, Patton JF, Tharion WJ. 1998. Assessment of the relationship between iron status, dietary intake, performance, and mood state of female Army officers in a basic training population. Technical Report T98-24, September 1998. AD A351 973. Natick, MA: U.S. Army Research Institute of Environmental Medicine. Consolazio CF, Johnson HL, Nelson R. 1979. The relationship of diet to the performance of the combat soldier. Minimal calorie intake during combat patrols in a hot humid environment (Panama). Letterman Army Institute of Research Report No. 76. October 1979. Friedl KE. 2003. Military nutritional immunology. In: Hughes DA, Darlington LG, Bendich A, eds. Diet and Human Immune Function. Totowa, NJ: Humana Press, Inc. Pp. 381396. Friedl KE, Marchitelli LJ, Sherman DE, Tulley R. 1991. Nutritional Assessment of Cadets at the U.S. Military Academy: Part 1. Anthropometric and Biochemical Measures. Technical Report No. T4-91, November 1990. ADA231918. Natick, MA: U.S. Army Research Institute of Envi- ronmental Medicine. Friedl KE, Moore LJ, Marchitelli LJ. 1992. Physiology of nutritional supplements. "Steroid replac- ers": Let the athlete beware! Natl Strength Conditioning Assoc J 14:1419. Friedl KE, Mays MZ, Kramer TR, Shippee RL. 2001. Acute recovery of physiological and cognitive function in U.S. Army Ranger students in a multistressor field environment. In: The Effect of Prolonged Military Activities in Man--Physiological and Biochemical Changes--Possi- ble Means of Rapid Recuperation. Technical Report RTO-MP-042. Neuilly-sur-Seine Cedex, France: North Atlantic Treaty Organization. Ihle R, Loucks AB. 2004. Dose-response relationships between energy availability and bone turn- over in young exercising women. J Bone Miner Res 19:12311240. IOM (Institute of Medicine). 1995. A Review of Issues Related to Iron Status in Women during U.S. Army Basic Combat Training. Letter Report to BG Russ Zajtchuk, December 19, 1995. IOM. 1997. Dietary Reference Intakes for Calcium, Phosphorus, Magnesium, Vitamin D, and Fluo- ride. Washington, DC: National Academy Press.

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248 MINERAL REQUIREMENTS FOR MILITARY PERSONNEL IOM. 1998. Reducing Stress Fracture in Physically Active Military Women. Washington, DC: Na- tional Academy Press. IOM. 1999. Letter Report to the Office of the Surgeon General United States Army on Antioxidants and Oxidative Stress in Military Personnel. Washington, DC: Institute of Medicine. Johnson HL. 1986. Practical military implications of fluid and nutritional imbalances for perfor- mance. In: Predicting Decrements in Military Performance Due to Inadequate Nutrition. Wash- ington DC: National Academy Press. Pp. 5568. Kepczyk T, Cremins JE, Long BD, Bachinski MB, Smith LR, McNally PR. 1999. A prospective, multidisciplinary evaluation of premenopausal women with iron deficiency anemia. Am J Gastroenterol 94:109115. Kramer TR, Moore RJ, Shippee RL, Friedl KE, Martinez-Lopez L, Chan MM, Askew EW (1997). Effects of food restriction in military training on T-lymphocyte responses. Int J Sportsmed 18:S84S90. Kretsch MJ, Conforti PM, Sauberlich HE. 1986. Nutrient intake evaluation of male and female cadets at the United States Military Academy, West Point, New York. Technical Report LAIR-218. April 1986. ADA168120. San Francisco, CA: Letterman Army Institute of Research. Lappe JM. 2003. Efficacy of calcium and Vitamin D supplementation for the prevention of stress fracture in female Naval recruits. Annual Report. Grant # DAMD17-01-1-0807. ADA419678. October 2003. Omaha, NE: Creighton University. Loucks AB, Thuma JR. 2003. Luteinizing hormone pulsatility is disrupted at a threshold of energy availability in regularly menstruating women. J Clin Endocr Metab 88:297311. Moore RJ, KE Friedl, RT Tulley, EW Askew. 1993. Maintenance of iron status in healthy men during an extended period of stress and physical activity. Am J Clin Nutr 58:923927. Sack DM, Holick M, Bondi KR. 1986. Calcium and Vitamin D metabolism in submariners--carbon dioxide, sunlight, and absorption considerations. Technical Report NSMRL-1037. January 1986. ADA166292. Groton, CT: Naval Submarine Medical Research Laboratory. Sandstead HH. 2001. Repletion of zinc and iron deficiencies improve cognition of premenopausal women. Final Report. Grant DAMD17-95-C-5112. December 2001. Galveston, TX: University of Texas Medical Branch. Sauberlich HE. 1984. Implications of nutritional status on human biochemistry, physiology and health. Clin Biochem 17:132142. Shippee RL, Friedl KE, Tulley R, Christensen E, Arsenault J. 1993. Changes in plasma iron, copper, and zinc concentrations of young males during 8 weeks of extreme physiological and psycho- logical stress. J Am Coll Nutr 12:614 (abstract). Singh A, Papanicolaou DA, Lawrence LL, Howel EA, Chrousos GP, Deuster PA. 1999. Neuroendo- crine responses to running in women after zinc and vitamin E supplementation. Med Sci Sports Exerc 31:536542. Westphal KA, Friedl KE, Sharp MA, King N, Kramer TR, Reynolds KL, Marchitelli LJ. 1995. Health, performance, and nutritional status of U.S. Army women during basic combat training. Technical Report No. T96-2. May 1995. ADA302042. Natick, MA: U.S. Army Research Insti- tute of Environmental Medicine.

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APPENDIX B 249 Derivation of the Military Dietary Reference Intakes and the Mineral Content of Military Rations Carol J. Baker-Fulco U.S. Army Research Institute of Environmental Medicine, Natick, Massachusetts This paper presents the nutritional standards for military rations and the mineral composition of military field rations. In addition, it summarizes the findings of a few studies that have estimated mineral intakes of soldiers in the field and in garrison. This paper focuses on operational rations, which are rations intended for military operations, whether combat or field training. A ration is one day's food supply for a group or an individual. The type of ration provided is based upon the unit's mission, tactical scenario, location, and availability of food service equipment and personnel. The operational rations examined in this paper are the Meal, Ready-to-Eat (MRE); Meal, Cold Weather (MCW); one of the Unitized Group Rations (UGR), the Heat-and-Serve (H&S); and the First Strike Ration (FSR). DESCRIPTIONS OF OPERATIONAL RATION The MRE is the standard individual operational ration and consists of heat- processed entrees and other food components that require no preparation. Each meal contains an entre/starch, crackers, a spread (cheese, peanut butter, jam or jelly), a dessert or snack, beverages, and an accessory packet that contains cof- fee, tea or cider and condiments. The MRE is issued at three menu bags per day for a complete ration with an average of 3,900 kcal. For variety, there are twenty- four different meal menus in the inventory. The MCW is a higher calorie ration intended for arctic feeding. This ration contains freeze-dried, cooked entrees and other low-moisture foods that will not freeze. Meal bags for each of the twelve menus contain the entre and a variety of spreads and crackers, cookies, sports bars, nuts, candy, and powdered drink mixes. The MCW is issued at three menu bags per day for a provision of roughly 4,500 kcal. The MCW menus are identical to those of the Food Packet, Long Range Patrol (LRP) which is a restricted ration issued as one menu bag per day during special operations when weight and volume of the ration are critical factors. Another restricted calorie ration considered in this report is the FSR. The FSR is a new, individual combat ration developed for forward deployed ground forces engaged in high-intensity operations. This ration is smaller and lighter than a full day's ration of MREs and is comprised of foods that can be eaten "on the move." The FSR as currently configured provides about 2,800 kcal.

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250 MINERAL REQUIREMENTS FOR MILITARY PERSONNEL The UGR is a group of rations in which all the components for 50 complete meals are packaged as one unit to streamline the ordering and delivery process. There are seven breakfast and fourteen lunch and dinner menus for each type of UGR; however, the lunch meal is often a MRE. The UGR-Heat & Serve (UGR- H&S) is comprised of shelf-stable, ready-to-eat entrees, starches, vegetables, and desserts packaged in short, rectangular plastic trays. It is the more common (hot) group feeding ration for the field and is used when neither cooking nor refrigeration are possible. Each meal, including the mandatory supplement of milk, provides an average of 1,400 kcal. UGR menus may be enhanced with cold breakfast cereal, bread, fresh fruits and salad. There are other UGR options that comprise perishable and frozen ingredients (UGR-A) or are cook-prepared from canned and dehydrated foods (UGR-B), but these will not be discussed in this paper. MILITARY DIETARY AND RATION STANDARDS Nutritional standards for operational and restricted rations (NSOR), i.e., what the rations must contain, are presented in the tri-service regulation, Nutritional Standards and Education, which for the Army is Army Regulation (AR) 40-25 (U.S. Departments of the Army, Navy, and Air Force, 2001). The NSORs are based on the Military Dietary Reference Intakes (MDRI) presented in the same regulation (see Table B-1). The MDRIs are, in turn, based on the Dietary Refer- ence Intakes (DRIs) (IOM, 1997, 1998, 2000a) or earlier Recommended Dietary Allowances (RDA) (National Research Council, 1989). Since the current regula- tion was prepared prior to the 2001 DRI publication (IOM, 2001)--which up- dated the RDAs for iron, iodine and zinc, and established DRIs for chromium, copper, manganese and molybdenum--current MDRIs are based on the 1989 RDAs for iron, iodine, and zinc, and there are no MDRIs for chromium, copper, manganese and molybdenum. A soon to be drafted change to the regulation will update the MDRIs and include additional MDRIs based on the more recent IOM publications. The MDRIs are applicable to healthy, 17 to 50 year old, physically active military men and non-lactating, non-pregnant women. This age range covers the majority of military personnel on active or reserve duty. The 17 to 50 year age range incorporates three of the age classes for which DRIs have been set (14 to 18, 19 to 30, and 31 to 50 years) and three of the age classes used in the 10th edition of the RDA (15 to 18, 19 to 24, and 25 to 50 years). For most nutrients, the MDRI is the highest gender-specific reference value or RDA. However, the MDRIs for calcium, phosphorus, and iron for males and calcium, phosphorus, and magnesium for females, are not based on the highest reference intake or allowance, which is for 14 to 18 year old individuals. Only 23 percent of the military population is 17 to 18 years old; thus, inflating the MDRIs to meet the needs of relatively so few individuals is not warranted. The regulation advises

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APPENDIX B 451 U.S. Departments of Army, Navy, and Air Force. 2001. Nutrition Standards and Education. AR 40- 25/BUMEDINST 10110.6/AFI 44-141. Washington, DC: U.S. Department of Defense Headquarters. Van Beaumont W, Strand JC, Petrofsky JS, Hipskind SG, Greenleaf JE. 1973. Changes in total plasma content of electrolytes and proteins with maximal exercise. J Appl Physiol 34:102106. Van Loan MD, Sutherland B, Lowe NM, Turnlund JR, King JC. 1999. The effects of zinc depletion on peak force and total work of knee and shoulder extensor and flexor muscles. Int J Sport Nutr 9(2):125135. Van Rij AM, Hall MT, Dohm GL, Bray JT, Pories WJ. 1986. Changes in zinc metabolism following exercise in human subjects. Biol Trace Elem Res 10:99105. Weight LM, Myburgh KH, Noakes TD. 1988a. Vitamin and mineral supplementation: Effect on the running performance of trained athletes. Am J Clin Nutr 47:192195. Weight LM, Noakes TD, Labadarios D, Graves J, Jacobs P, Berman PA. 1988b. Vitamin and mineral status of trained athletes including the effects OF SUPPLEMENTation. Am J Clin Nutr 47:186191. The Effects of Iron Deficiency on Physical Performance Jere D. Haas Cornell University, Ithaca, New York INTRODUCTION Iron deficiency is the most prevalent micronutrient deficiency in both the industrialized and non-industrialized world. In the United States iron deficiency affects approximately 34 percent of men and 1214 percent of women between 18 and 45 years, the age of the majority of military personnel in the U.S. (Looker et al., 1997). While the most common consequence of iron deficiency is anemia, or blood hemoglobin concentration below a specified level, the prevalence of anemia underestimates the amount of iron deficiency in the population. WHO (2001) estimates that the prevalence of iron deficiency is more than twice the prevalence of anemia in any given population. Also, while iron deficiency ac- counts for the majority of anemia in the U.S. population, there are numerous additional causes of anemia, including other micronutrient deficiencies. Numerous studies of the effect of iron deficiency on physical performance have been conducted over the past 35 years with conclusive evidence for a causal relationship (Haas and Brownlie, 2001). Most of the evidence from these studies indicates that low hemoglobin concentration and consequent reduced oxygen transport to working muscles is the primary mechanism for reduced performance due to iron deficiency. However, evidence from animal studies and more recently in human studies of non-anemic human subjects suggest that iron deficiency may affect physical performance through other mechanisms. This review addresses the evidence for the effects of iron depletion in non-anemic individuals.

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452 MINERAL REQUIREMENTS FOR MILITARY PERSONNEL ASSESSING MODERATE IRON DEFICIENCY There are a number of indicators of iron nutritional status that when used together can reveal a fairly comprehensive picture of the various body iron pools that are significant for understanding the functional consequences of iron defi- ciency. Figure B-31 shows the progress of iron status from normal to deficient states and the course taken by the major indicators of iron status in common use. The body iron stores reflect the functional iron status of an individual. With increased iron loss or decreased iron intake to compensate for losses, the body iron stores decline to a point indicated as "deficient." The best single indicator of the depletion of iron stores is serum ferritin. Hemoglobin concentration does not start to fall until after iron stores are depleted, and anemia is defined as a hemo- globin level that is achieved during the decline in hemopoiesis. There is a stage of body iron depletion when the iron stores are completely depleted but hemo- globin has not yet reached a level that indicates anemia; this is the iron deficient, non-anemic state (IDNA). Another indicator of iron status that is not represented in Figure B-31 is the blood plasma concentration of the soluble transferrin recep- tor (sTfR). It follows a course similar to that for free erythrocyte protoporphyrin (FEP), and increasing levels indicate a increased demand for iron at the muscle Hemoglobin FEP Ferritin TS Fe stores IDNA anemia IDNA=Iron Deficient Non-Anemic FIGURE B-31 Relationship between various indicators of iron status and the body's level of iron stores. SOURCE: Modified from Guthrie and Picciano (1995).

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APPENDIX B 453 tissue level which is not being met by circulating iron in the iron depleted indi- vidual. This indicator appears to identify non-anemic individuals who will ben- efit from iron supplementation as it affects physical performance (Brownlie et al., 2004). Cook and colleagues (Cook et al., 2003) have developed an algorithm to estimate total body iron from the log of the ratio of soluble transferrin receptor and serum ferritin. EVIDENCE FOR THE EFFECT OF IRON DEFICIENCY ON PHYSICAL PERFORMANCE IN ANEMIC SUBJECTS Most of the research on iron deficiency effects on physical performance has focused on anemic subjects. This literature has been reviewed extensively by Haas and Brownlie (2001) who conclude that there is considerable evidence to support a direct causal relationship. One of the more recent studies that used an experimental design that included randomization of subjects to consume either an iron supplement or a placebo was conducted by Li and colleagues (Li, 1993; Li et al., 1995), who studied the effects of iron deficiency on work capacity in female Chinese factory workers. They assessed changes in physical performance with the VO2max test, an assessment of aerobic power, after 12 weeks of con- suming either an iron supplement or a placebo. The results are summarized in Figure B-32. Li (1993) reported a 5 percent improvement in VO2max in the iron supplemented group which corresponded to a 13g/L increase in hemoglobin con- centration. There was a range of hemoglobin values in this sample and the great- 2 * * different from 1.95 placebo, p < .05 1.9 /min) Before After (L 1.85 max 2 1.8 VO 1.75 1.7 114 127 Hb (g/L) 115 113 Iron Supplemented Placebo Control FIGURE B-32 VO2max in Chinese female cotton mill workers before and after 12 weeks of iron supplementation. SOURCE: Li (1993, unpublished thesis).

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454 MINERAL REQUIREMENTS FOR MILITARY PERSONNEL est effects of iron supplementation on VO2max were seen in the anemic women. The authors also reported an increase in productivity in the workplace after 12 weeks of iron supplementation (Li et al., 1995). There have been a large number of studies of the effects of iron deficiency on physical performance using experimental animals. One of the most interest- ing was conducted by Davies et al. (1982) with post-weaning rats that developed iron deficiency after consuming a low-iron diet and then repleted rapidly by iron therapy. The results are summarized in Figure B-33. This study confirmed previ- ous studies in animals and humans of an improvement in VO2max, which paral- leled an increase in hemoglobin concentration following iron therapy. This study is significant because it also followed changes in another measure of physical performance, endurance capacity, and a measure of tissue oxidative capacity, muscle pyruvate oxidase, throughout the 7-day period following iron repletion. The course of change in endurance lagged behind that of VO2max and paralleled the increase in pyruvate oxidase. These findings indicate that physical perfor- mance may be only partially mediated by the effect of iron deficiency on oxygen transport in the blood, and that tissue iron depletion may also limit performance. FIGURE B-33 The relationship of iron repletion to hemoglobin response, maximal aerobic capacity (VO2max), muscle pyruvate oxidase activity and endurance capacity in rats made iron deficient post-weaning. SOURCE: Davies et al. (1982). Used with permission.

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APPENDIX B 455 They also indicate that different types of physical performance tests need to be considered when studying severe compared to moderate iron deficiency. PHYSICAL PERFORMANCE IN IRON DEPLETED NON-ANEMIC SUBJECTS This section reviews evidence for the effects of iron deficiency on physical performance, focused primarily on non-anemic individuals. Before the evidence is described, a brief review is presented of the rationale for why these affects should be observable and important. Rationale The animal experiments represented by Davies et al. (1982) provide partial rationale for exploring relationships between iron depletion and performance in non-anemic human subjects. Further justification exists when one considers that iron plays an import role in muscle metabolism beyond the transport of oxygen by hemoglobin to the tissue sites for energy conversion to muscular work. Figure B-34 presents a list of iron-containing compounds that are affected by body iron depletion. Approximately 5 percent of the body iron is found in iron-containing enzymes and 10 percent is found in myoglobin. Many of these compounds are involved in transformation of chemical to mechanical energy. A second rationale FIGURE B-34 Iron containing compounds that are affected by iron deficiency.

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456 MINERAL REQUIREMENTS FOR MILITARY PERSONNEL Tissue oxidative Diet capacity Endurance capacity Depletion Functional Maximal of iron iron Anemia Oxygen power output stores deficiency Transport (VO2max) Blood loss Energetic Tissue oxidative efficiency capacity FIGURE B-35 Conceptual model of iron deficiency effects on physical performance. is the relatively large number of individuals in a population that may be affected by iron deficiency. This is a number that exceeds the prevalence of anemia in the population (WHO, 2001). While the effects of iron depletion without anemia may be less severe than the effects of iron deficiency, there is growing evidence that the impact on physical performance is not trivial. The proposed mechanisms for the action of iron deficiency on physical performance are summarized in Figure B-35. Body iron stores become depleted due to an imbalance of iron loss and dietary gain. When levels of body iron become too low there is the beginning of a functional iron deficiency which affects compounds associated with muscle metabolism but probably does not affect hemoglobin synthesis and oxygen transport in the blood. Under conditions of more severe depletion, hemoglobin synthesis is compromised along with skel- etal muscle compounds resulting iron deficiency anemia (IDA). Under IDA a broad range of physical performance measures are affected. The anemia results in reduced oxygen transport that limits aerobic power, endurance, and muscular energetic efficiency. The reduced levels and activity of iron-dependant, muscu- lar tissue compounds seen in non-anemic, iron deficiency (IDNA) contribute to reduced endurance and energetic efficiency, but do not limit aerobic power, since blood oxygen transport is not compromised. Evidence for Effects of Iron Depletion in Non-Anemic Women While the functional effects of iron deficiency have been well documented in those individuals who are anemic, the effects of IDNA have only recently

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APPENDIX B 457 been examined in some detail (Haas and Brownlie, 2001). Three recent iron supplementation trials with iron deficient non-anemic women provided evidence that supports the general conceptual model presented in Figure B-35 (Brutsaert et al., 2003; Hinton et al., 2000; Zhu and Haas, 1998). All of the studies used a similar research design. Female subjects between 18 and 45 years were identi- fied through population screening to be non-anemic (hemoglobin > 120 g/L), but iron depleted (serum ferritin < 20 g/L). Subjects were randomly assigned to consume either supplemental iron (100 to 135 mg FeSO4/day) or a placebo daily for 6 or 8 weeks, following a double blind protocol. A battery of measures of iron status and various measures of physical performance were assessed at base- line and at the end of the supplementation period. The results of these studies are summarized as follows. Metabolic Response to Exercise Zhu and Haas (1998) studied thirty-seven non-anemic, iron-deficient (fer- ritin < 16 g/L) university women who consumed 135 mg/day of FeSO4 (50 mg Fe/day) or a placebo for 8 weeks. Physical performance was assessed by VO2max and time to complete a simulated 15-km time trial with a cycle ergometer, an indicator of endurance. Serum ferritin values increased in the supplemented group but hemoglobin did not change, and there was no group difference in VO2max at the end of the trial. While the iron supplemented group did not complete the time trial in less time than the placebo group, they completed the task at a lower percentage of their VO2max (82 versus 88 percent) and with 5.1 percent less energy expended than the placebo group. While one can conclude that iron defi- cient women are less efficient at doing heavy work, it is not known whether these effects of iron deficiency on performance can be observed under less rigor- ous levels of exertion. The next study addresses this question. Energetic Efficiency in Mexican Women The studies described here (Brutsaert et al., 2003; Haas et al., 2002; Seymour, 2002) investigated the effects of iron supplementation for women on outcomes of physical performance while cycling at different intensities. Forty-three non- anemic, iron deficient (ferritin < 20 mg/L), female Mexican office workers and students consumed 18 mg/day of elemental iron as FeSO4 or a placebo for 6 weeks (Haas et al., 2002). Serum ferritin increased while hemoglobin did not change in the iron supplemented group when compare to the placebo group, and estimated VO2max did not differ between the groups after supplementation. Energy cost of performing 30 and 60 watts of work on a cycle ergometer was assessed at baseline and after 6 weeks. At 60 watts the iron supplemented women showed a 5.2 percent lower energy cost to perform the work after 6 weeks of supplementation (Seymour, 2002). As shown in Figure B-36 this resulted in a

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458 MINERAL REQUIREMENTS FOR MILITARY PERSONNEL 31 Placebo p < .05 (%) 30.5 iron 30 29.5 Efficiency 29 28.5 Work 28 Baseline Final kcal of external work performed at 60W WE = (kcal expended at 60W) - (kcal expended at 0W) FIGURE B-36 Work efficiency (WE) at 60 watts in Mexican women before and after 6 weeks of iron supplementation. SOURCE: Seymour (2002, unpublished thesis). significantly higher net work efficiency which was related to increased iron in- take and decreases in tissue iron status, based on the soluble transferrin receptor concentration (sTfR). In a sub-sample of 20 women from this study, an addi- tional test of a maximal voluntary static contraction (MVC) on a dynamic knee extension exercise was administered to assess local muscle fatigue (Brutsaert et al., 2003). The iron supplemented women performed the task with significantly less muscle fatigue than the placebo group after 6 weeks of supplementation. Adaptation to Physical Training Several papers have reported on a study of the effects of iron status and supplementation on improvements on performance outcomes due to adaptation to physical training (Brownlie et al., 2002, 2004; Hinton et al., 2000). In this study, 42 non-anemic, iron-deficient university women were randomly assigned to consume either 100mg/day of FeSO4 or a placebo for 6 weeks. In addition, an additional exercise intervention for all subjects consisted on 20 days of aerobic training during the final 4 weeks of the supplementation trial. It was reported that both groups benefited from the training by increasing their VO2max and reducing their times on a simulated 15-km time trial with a cycle ergometer. As shown in Figure B-37, the iron supplemented group improved its time in the time trial by 3.4 minutes compared to a 1.6 minute improvement in the placebo group (Hinton et al., 2000). The effect of iron treatment was mediated by changes in serum ferritin but not by changes in hemoglobin. VO2max also improved

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APPENDIX B 459 33 Placebo Iron 32 31 Time trial 30 * Minutes 29 28 27 Baseline Final FIGURE B-37 Improvements in times for women to complete a 15 km bicycle time trial after 4 weeks training while consuming supplemental iron or placebo. Iron group com- pleted final trial 1.6 min faster than placebo group, after adjusting for differences in initial times and work rate, p < 0.05. SOURCE: Hinton et al. (2000). more in the iron supplemented group and the greatest improvement in time-trial time and work efficiency was seen in the iron supplemented women who were most depleted in tissue iron (sTfR) at baseline (Brownlie et al., 2004). From this study one can conclude that iron deficiency reduces the potential benefits of aerobic training in both endurance and VO2max. It remains to be tested whether the effects of iron deficiency on adaptation to aerobic training can be observed in individuals who are already physically fit. CONCLUSIONS We can draw several conclusions from the research literature on physical performance in iron deficiency anemia and from the recent experiments described in this paper on iron depleted non-anemic women: Iron deficiency anemia (IDA) has clear functional consequences across a wide range of tests of physical work capacity and productivity The mechanisms for IDA effects on performance include compromise to both oxygen transport and tissue level oxidative capacity Iron deficiency without anemia (IDNA) is more prevalent than IDA in the general population and carries measurable but less severe consequences to human performance

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460 MINERAL REQUIREMENTS FOR MILITARY PERSONNEL The impact of IDNA is observed for physical endurance rather than aerobic power, and on reducing the ability to adapt to aerobic training. For relevance to physical performance of military personnel, one can conclude: The results on the effects of iron deficiency anemia on physical perfor- mance should apply to all individuals The results on moderate iron deficiency without anemia in females should be extrapolated to males who experience a similar degree of iron deficiency and level of fitness Military personnel should be screened for anemia and body iron status Iron deficiency should be corrected in the long term by dietary adjust- ments and by mineral and vitamin supplementation in the short term, as condi- tions warrant. Future research should consider assessing the effects of moderate iron defi- ciency on energetic efficiency and adaptation to training in more physically fit subjects and under conditions such as basic training. Additional research should consider assessing dietary iron requirements for military personnel which are based on potential iron loss from heavy exertion as well as additional demands to support physical training and maintenance of high levels of endurance. REFERENCES Brownlie T, Utermohlen V, Hinton PS, Giordano C, Haas JD. 2002. Marginal iron depletion without anemia reduces adaptation to physical training in previously untrained women. Am J Clin Nutr 75:734742. Brownlie T, Utermohlen V, Hinton PS, Haas JD. 2004. Tissue-iron deficiency without anemia im- pairs endurance adaptation among previously untrained women. Am J Clin Nutr 79:437443. Brutsaert T, Hernandez-Cordero S, Rivera J, Viola T, Hughes G, Haas JD. 2003. Progressive muscle fatigue during dynamic work in iron deficient Mexican women. Am J Clin Nutr 77:441448. Cook JD, Flowers H, Skikne BS. 2003. The quantitative assessment of body iron. Blood 101:3359 3364. Davies KJA, Maguire JJ, Brooks GA, Dallman PR, Packer L. 1982. Muscle mitochondrial bioener- getics, oxygen supply, and work capacity during dietary iron deficiency and repletion. Am J Physiol 242:E418E427. Guthrie H, Picciano MF. 1995. Human Nutrition. St. Louis, MO: Mosby-Year Book. Haas JD, Brownlie T. 2001. Iron deficiency and reduced work capacity: A critical review of the research to determine a causal relationship. J Nutr (suppl) 131:676S688S. Haas JD, Seymour J, Hernandez-Cordero S, deHaene J, Villalpando S, Rivera J. 2002. Iron depletion increases the energy cost of work in non-anemic Mexican women. Am J Phys Anthropol (Suppl) 34:80. Hinton PS, Giordano C, Brownlie T, Haas JD. 2000. Iron supplementation improves endurance after training in iron-deficient, non-anemic women. J Appl Physiol 88:11031111.

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APPENDIX B 461 Li R. 1993. Functional Consequences of Iron Supplementation in Iron-Deficient, Chinese Female Workers. Unpublished doctoral dissertation. Wageningen, The Netherlands: Wageningen Agri- cultural University. Li R, Chen X, Yan H, Durenberg P, Garby L, Hautvast JGAJ. 1995. Functional consequences of iron supplementation in iron-deficient, female cotton workers in Beijing, China. Am J Clin Nutr 59:908913. Looker AC, Dallman PR, Carroll MD, Gunter EW, Johnson CL. 1997. Prevalence of iron deficiency in the United States. J Am Med Assoc 277:973976. Seymour JM. 2002. Iron deficiency decreases efficiency of intermittent exercise in marginally iron deficient non-anemic Mexican women. Unpublished masters thesis. Ithaca NY: Cornell Uni- versity. WHO (World Health Organization). 2001. Iron deficiency Anemia: Assessment, Prevention, and Control. A Guide for Program Managers. Geneva, Switzerland: World Health Organization. Zhu YI, Haas JD. 1998. Altered metabolic response in iron-depleted non-anemic women during a 15-km time trial. J Appl Physiol 84:17681775.