Journal of Clinical Densitometry, vol. 6, no. 2, 75–85, 2003 Copyright 2003 by Humana Press Inc. All rights of any nature whatsoever reserved. 1094-6950/03/6:75–85/$20.00 Review Article
Clinical Applications of Body Composition
Measurements Using DXA
Carlina V. Albanese,*,1 Evelyn Diessel,2 and Harry K. Genant2
1Osteoporosis and Bone Pathology Unit of Study, Institute of Radiology, University of Rome “La Sapienza,” Viale Regina Elena, 326, 00161 Rome, Italy; and 2Osteoporosis and Arthritis Research Group, University of California San Francisco, San Francisco CA 94143-0628, USA Abstract
Dual-energy X-ray absorptiometry (DXA) scanning was primarily developed for the diagnosis of osteo- porosis and was initially applied to studies of the clinically important sites of the lumbar spine, femoral neck,and forearm. The rapid adoption of DXA has led to the development of different, competing generations ofequipment. Improvements have been achieved through advances in X-ray generation and detection technol-ogy, modification of data acquisition protocols, and implementation of more sophisticated image analysisalgorithms. As a result, DXA has been extended to allow the study of the total skeleton and its regional parts,as well as soft-tissue composition measurement. The three major components of the body: fat mass, lean mass,and bone mineral mass, can now be easily measured using a single whole body DXA scan with high precisionand low scanning time.
The comprehensive view of body composition provided by DXA makes it an attractive technique for a vari- ety of clinical applications such as the prevention of cardiovascular and metabolic diseases, clinical manage-ment of different chronic diseases, and monitoring of the impact of treatment regimens on body tissues.
In this article we review the contribution DXA has made to the understanding of body composition in clin- Key Words: Adults; body composition; clinical applications; review; whole body DXA.
osteoporosis, the prediction of fracture risk (1–2),and the monitoring of therapies (3). In addition to BMD assessment, DXA devices are capable of mea- devices were primarily developed for the diagnosis suring body composition of the total body or body of osteoporosis. Bone mineral density (BMD) mea- surements in the proximal femur, the lumbar spine, The main measurement technique is based on the or the forearm provide a means for the diagnosis of differential attenuation by bone, fat, and lean tissueof transmitted photons at two energy levels (4). The Received September 26, 2002; Accepted January 29, 2003.
transmission at two energy levels allows the deriva- *Address correspondence to Carlina V. Albanese, Osteo- tion of two different components such as fat and lean porosis and Bone Pathology Unit of Study, Institute of mass in regions without bone. In regions with bone Radiology, University of Rome “La Sapienza,” Viale Regina the two components, bone and soft tissue, are mea- Elena, 326, 00161 Rome, Italy. E-mail: sured, and the composition of the soft tissue needs to DXA Devices for Body Composition and Total Body BMD Measurements a Effective dose in brackets includes ovaries.
b Patient doses according to the manufacturer.
be estimated with respect to the adjacent tissue val- use of BMD measurements in osteoporosis. DXA ues. Therefore, a body-composition scan of the total body-composition measurements show a high corre- body measures three compartments of the body: fat lation with the abovementioned techniques (7–9), and lean body mass, as well as total body bone min- and are rapidly gaining interest and acceptance in eral. Proteins, glycogen, mineral, and water (includ- ing water and organic materials of the bone) are This article provides an overview of the different included in the component of lean tissue (5). areas for which body-composition measurements The DXA output provides information about the with DXA have been instituted in clinical practice.
following masses (in grams): fat, lean tissue, and Our research was based, in part, on a review of the bone mineral content (BMC) of the total body and current literature on body composition in adults.
body regions. The fat content is given in percentage.
Additionally, regional and total body BMD (in DXA Devices
A variety of alternative techniques for body com- DXA technology has improved significantly in position measurements are available and have been the last few years, especially scanning times.
reviewed by Jensen (6). Anthropometry, for exam- Whereas a few years ago a body-composition scan ple, predicts fat content by measuring skinfold thick- required more than 15 min, new DXA devices are ness (ST) and body circumferences. Total body capable of scanning the total body in less than 5 min.
water (TBW) can be measured by isotope dilution Reduced scanning times are more convenient for technique (injection or drinking of tritium or deu- patients and technical staff and have contributed to terium solution). A person’s average body density increased acceptance of DXA measurements in body can be estimated by underwater weighing. Total composition research and clinical practice.
body potassium (TBK) counting predicts lean body Table 1 lists current DXA devices that are mass by measuring the naturally radioactive isotope equipped with a body-composition mode. In addi- potassium 40K. Other available techniques include tion to these devices, older models such as the QDR neutron activation analysis, bioelectrical impedance 1000 and QDR 2000 (Hologic Inc., Bedford, MA, analysis (BIA), computed tomography (CT), mag- USA), XR-26 (Norland Inc., Fort Atkinson, WI, netic resonance imaging (MRI), and ultrasonogra- USA) are still being used in clinical practice.
phy. Many of these techniques are restricted to a For whole body scanning, it is imperative that all small number of laboratories. In contrast, DXA parts of the body (also arms and feet) are included in devices are widely available owing to the widespread the scan field for precise measurements. However, Clinical Applications of Whole Body DXA there are some limitations with respect to the size of higher, and the technical staff should be appropri- the imaging table and the X-ray dosage. For exam- ately protected (15,16). An overview of the patients’ ple, patients taller than 1.82 m (6 ft) may not fit radiation exposure using various DXA device is entirely on the table. The accuracy of the measure- given in Table 1. Considering the annual dose equiv- ment is then slightly reduced. In very obese patients, alent from natural background radiation (2400 µSv e.g., over 135 kg (300 lb), the X-ray dosage may not per annum), and from other imaging procedures be sufficient for imaging the abdomen. Some devices such as dental bitewing (60.0 µSv), chest X-ray offer special modes for obese patients with increased (50.0 µSv), and thoracic and lumbar lateral spine X- ray (820.0 µSv), the radiation exposure from whole To assess lean and fat mass composition, the DXA systems use different calibration techniques.
In comparison to pencil-beam systems, fan-beam The XR-26 and QDR systems rely on external cali- geometry causes projection and magnification arti- bration, using wedges made of aluminum and Lucite facts. The projected area depends on the tissue (polymethylmethacrylate) calibrated against stearic height above the scanning table. The influence on acid as 100% fat, and diluite saline solution as 100% body-composition data is still under investigation; lean tissue (10). The DPX systems use a plastic poly- however, improved correction algorithms are being oymethylen (Delrin) as 40% fat equivalent and water implemented. The Prodigy, listed in Table 1, uses a (~5% fat) as standard measurement (4). Therefore, thin fan beam that requires multiple raster scans sim- when comparing body-composition measurements between various DXA devices, results of fat and lean Quality control in bone densitometry is essential tissue show high correlations but also systematic dif- not only for clinical drug trials or epidemiological ferences owing to different calibration (11). Tothill studies in which multiple densitometers are et al. (12) compared three DXA devices of different involved, but also in routine clinical practice. To manufacturers and found deviations in fat values of ensure consistent performance, a quality-control 6% in the total body and up to 13% in the trunk.
scan with a known standard is carried out daily, and Differences were also found when comparing two the measurement is then compared with previous distinct DXA models of the same manufacturer scans in a quality-control database. The standard used for these daily quality-control scans differs Deviation in measurement results between the with the manufacturer and may consist of anthropo- devices can also be explained by the variations in the morphic phantoms or geometric objects of known technology. Differences exist in hardware (X-ray voltage, higher and lower energy spectra using Different standards for body-composition mea- switching kilovolt or K-edge filters, different detec- surements, such as the Variable Composition tors) and in software (algorithms for edge detection, Phantom (VCP), have been evaluated recently (18). assumptions regarding distribution of soft tissue DXA devices are proven to have long-term stabil- above bone). Additionally, the imaging geometry ity and provide high precision in BMD scans of (pencil- and fan-beam) may cause deviation in mea- 1–2% and in body-composition scans of 2–6% surement results. A pencil-beam (collimated by a pinhole collimator) is coupled to a single detectorand scans the total body in a raster. In contrast, a fan- Clinical Applications
beam (slit collimator) is coupled to a multidetectorlinear array. Fan-beam systems use only three (QDR Precise and accurate measurements of body com- 4500) or four (Expert) parallel sweeps across the position are useful in achieving a greater under- patient for a complete total body scan. The advan- standing of human energy metabolism in physiology tage of these techniques is the improved scanning and in different clinical conditions, and in evaluating time of 3 or 4 min. Fan-beam systems have a higher interventions. Many disease processes affect bone X-ray flux, and thus image quality is also improved.
and soft tissue at the same time. Therefore, the com- As a consequence, radiation doses for patients are prehensive view of body composition provided by Nutritional Disorders
Overview of the Main Field of Clinical Applications of Total body DXA accurately estimates the body composition and the composition of weight loss in 1. Nutritional disorders
obese subjects (19), as well as other clinical condi- tions in both overweight (20–22) and obese (22–23) subjects, and can be used for monitoring such a con- dition during therapeutic interventions.
2. Gastrointestinal disorders
Hendel et al. investigated the relationships between body composition by DXA, fat distribu- tion, sex hormone, and other cardiovascular risk factors in overweight postmenopausal women (19). 3. Hepatobiliary disorders
Androgenicity, cigarette smoking, and alcohol con- sumption correlate independently and positively 4. Renal disorders
with a central fat distribution. Furthermore, athero- genic levels of lipids and lipoproteins were inde- pendently related to central fat distribution, androgenicity, and low levels of estrogens. Carey et 5. Endocrinological disorders
al. investigated the relationship between abdominal fat and insulin sensitivity by DXA in normal and overweight women (21). In this study, abdominal adiposity appeared to be a strong marker and may 6. Bone disorders
be a major determinant of insulin resistance in women. Goodpaster et al. (22) studied obese and overweight women and men, using DXA to evalu- 7. Pulmonary diseases
ate abdominal fat and CT to evaluate subcutaneous abdominal fat. They concluded that subcutaneous fat as a component of central adiposity is also an 8. Drugs and substances
important independent marker of insulin resistance in obesity. A relationship between fat distribution, glucose tolerance, and gallstone pathogenic factors was also demonstrated in obesity with the direct 9. Other disorders
measurements of fat mass by DXA (23). Nutrition plays an important role in skeletal min- eralization. The nutrients known with certainty to be important are calcium, vitamin D, protein, and calo- ries. Therefore, any form of malnutrition may also affect total skeleton mineralization.
It is well known that women with anorexia ner- vosa develop osteoporosis (24). However, afterweight gain an increase in total body fat and leanmass as well as an increase in total BMC was whole body DXA makes it an attractive technique observed in these patients (25). Contrary to the for a variety of clinical research and practice appli- symptoms associated with undernutrition, patients with anorexia tended to remain energetic and Following is a discussion of DXA’s contribution shown high activity levels. There are indications to the understanding of body composition, including that in such patients a high level of physical activ- bone mineral measurements, in different fields of ity may result in an increase of total bone mass Clinical Applications of Whole Body DXA Gastrointestinal Disorders
Two different patterns of tissue loss may be found Malnutrition is a common presenting feature in in cirrhotic patients: in women, lean tissue is main- patients with active Crohn’s disease (27). Analysis tained while fat stores are reduced, as in early star- of body composition is important in states of acute vation; in men, lean tissue is reduced and body fat is and chronic illness to quantify the magnitude of the normal, as seen under conditions of stress (35). The malnutrition. Such knowledge allows the clinician reason for a gender difference in tissue loss in cir- to assess the extent of nutritional depletion, which rhotic patients could be related to the abundance of in turn provides objective guidelines for the type fat stores in females, which are progressively used to and amount of required nutritional support. Patients cope with the metabolic needs until muscle mass with active Crohn’s disease have diminished total remains the exclusive energy store (35). body fat. Fat stores are the most severely affected, Factors influencing muscle mass, such as nutri- being 70% of normal value (27). It has been tional depletion, altered protein turnover, and physi- reported that DXA provides an accurate measure- cal inactivity, may also, in part at least, negatively ment of body fat, compared with other methods of study, in malnourished subjects with Crohn’s dis- Finally, in a study of hepathobiliary disorders by DXA a significant association was reported between Malabsorption in patients with celiac disease increases of abdominal fat mass and gallstone devel- may lead to alteration of nutritional state and cal- cium balance. It is well-known that a gluten-free Renal Disorders
diet may eliminate subjective symptoms and steat- A number of factors may lead to malnutrition in orrhea, but does not restore normal body composi- patients with chronic renal failure. Malnutrition is a tion. In fact, untreated patients show lower body major factor in the greatly increased morbidity and weight, fat mass, lean tissue mass, and BMD at the mortality that occurs in these patients (36). lumbar spine and total skeleton measured by DXA It has been reported (37) that change in body (29). After treatment, only lean mass seems to be weight induced by hemodialysis has no influence on whole body or regional BMC and fat tissue mass Total gastrectomy is another condition known to measurements by DXA. On the contrary, a change in be complicated by both reduction of bone mineral- the measurement of whole body lean-tissue mass is ization (31) and nutritional disorders. However, strongly correlated with change in body weight after Liedman et al., using whole body DXA in a prospec- hemodialysis. These findings agree with prior results tive clinical study, reported a reduction of the body of studies investigating the effect of hemodialysis on fat, but they did not find an increased prevalence of body composition by DXA and support the view that osteoporosis in patients after total gastrectomy, even DXA is a useful tool for estimating short-term changes in body composition, such as those induced Hepatobiliary Disorders
In patients undergoing renal transplantation, rapid Malnutrition frequently occurs in patients with changes in body composition occur, with variations liver disease and may represent a risk factor influ- in fat distribution (40) and bone mineralization (41). encing both their short- and long-term survival (33). In such patients, the widespread use of corticos- The potential role of DXA in the assessment of body teroids for immunosuppression, together with the composition in cirrhotic patients is of particular negative input of surgery and immobilization, could interest, not only because it can provide additional be associated with nutritional deterioration, the and more precise information on their nutritional sta- potential for an increase of body fat, and loss of lean tus, but also because the estimation of metabolically active body compartments by means of body-com-position analysis is essential for physiological Endocrinological Disorders
processes standardization, such as energy expendi- Growth hormone (GH) is one of the main energy metabolism and body-composition regulators (42). GH deficiency in young adults causes a change in Bone Disorders
body composition with increased fat mass and There is a great need for a simple method to iden- reduced lean mass (43). Toogood et al. reported that tify persons at low risk of developing osteoporosis, even in the elderly, in whom GH secretion is nor- because bone densitometry is too expensive and mally very low, the additional imposition of GH time-consuming for general use in an unselected deficiency owing to organic disease may cause population. Such a method would allow low-risk changes in body composition with significant bio- individuals to be excluded from screening with logical impact (44). GH replacement therapy in BMD measurements and/or increase the years hypopituitary adults may alter body composition between follow-up bone mass measurements. Fat through its well-known lipolytic, anabolic, and mass is decreased in osteoporotic patients and may anti-natriuretic actions. A short-term study has have an important protective role on the skeleton shown that GH replacement therapy tends to nor- (50). It was reported that women weighing more malize soft-tissue body composition (43). A long- than 71 kg have a very low risk of being osteopenic term study has demonstrated that the beneficial compared to women weighing less than 64 kg.
effects of GH therapy on body composition, i.e., a Therefore, weight could be used to exclude women reduction in body fat and an increase in lean mass, from a screening program for postmenopausal osteo- are preserved for at least 4 yr in hypopituitary porosis (51). In a large study designed to compare adults (45). An increase of whole body BMC and body composition and BMD in Chinese women with BMD in hypopituitary patients with adult-onset GH vertebral fracture, it was found that not only fat mass deficiency after 2-yr treatment was also reported but also lean mass, height, and BMD at all sites were significantly lower in fractured patients than normal In acromegaly, body composition is characteristi- cally altered by an increase in lean mass and a cor- Paget’s disease is characterized by an increase in responding reduction in fat mass (42). Treatment bone turnover, often at multiple skeletal sites that are with the somatostatin analog, octreotide, reduces more susceptible to deformity or fracture than nor- hormonal effects on target tissue. Short-term mal bone. Whole body DXA measurements allow octreotide therapy reduces GH levels, leading to a regions of interest to be defined, so that the BMD of significant reduction in lean mass as assessed by focal areas within the skeleton can be assessed. It DXA (47). Acromegaly may induce abnormalities in was reported (53) that pagetic bone is more dense bone metabolism. Kayath and colleagues (48) than nonpagetic bone before treatment. With rise- reported that osteopenia occurs in a minority of dronate treatment, whole body BMC increases patients with acromegaly and is predominant in the because there has been an increase at pagetic and spine. The authors did not find any correlation nonpagetic sites. That the greatest increases in BMD between duration of hypersomatotropism, GH/IGF-1 occur at trabecular sites affected with Paget’s disease levels, and BMD, and they concluded that the major- probably reflects, in part, the larger volume of the ity of these patients have preserved BMD despite the pre-treatment remodeling space in trabecular com- Estimating body-composition changes is of inter- The diagnosis of osteopetrosis is based on quali- est in Cushing’s disease, which is characterized by tative description of standard radiographs showing redistribution of fat from peripheral to central parts universal osteosclerosis. However, this technique of the body owing to an excess of adrenocortical does not permit the degree of osteosclerosis to be steroids. Patients with this syndrome show reduced measured. Whole body DXA was used to quantify amounts of fat and lean-tissue masses in the arms the osteosclerosis in the two subtypes of autosomal and a slight reduction of total BMD and BMC com- dominant osteopetrosis (54). In both types, BMC pared with obese subjects and similar to nonobese and BMD were markedly increased at the axial as controls owing to depletion of selective protein well as at the appendicular skeleton compared to depots, as seen in hypercortisolism (49). normals. Moreover, the authors have suggested that Clinical Applications of Whole Body DXA measurements of whole body BMC and BMD may Drugs and Substances
be useful to complete the radiologic examination of Glucocorticoids negatively affect bone mineral- such patients, and in order to establish future thera- ization, lipids, and glucose metabolism and can peutic regimes, DXA might be helpful in monitoring therefore modulate whole body composition. In patients affected by giant cell arteritis, 2-yr treatmentwith high doses of prednisolone during the first 6 mo Pulmonary Diseases
and lower doses thereafter resulted in a significant The measurements of lean mass and fat mass increase in total body fat as well as in trunk fat that reserves in individuals with chronic obstructive pul- remained after switching to a low-dose glucocorti- monary disease (COPD) can aid in designing an coid schedule (60). In female patients with systemic adapted nutritional regimen, e.g., nutritional support lupus erythematosus, the severity of disease and cor- in malnutrition and food restriction in obesity, ticosteroid exposure were independently associated improving the clinical management of this condition with a negative effect both on total body BMD and (55). Body weight and lean mass abnormalities can affect the health-related quality of life (HRQL) in A number of hormones (62–65) have been shown COPD patients. It was demonstrated that although to modulate body composition measured by whole body weight and lean mass abnormalities influence body DXA. The menopause is associated with an HRQL, their effects appear to be mediated through increase in total body fat and decline in lean body increased levels of dyspnoea in patients with sym- mass. Oral estradiol/dydrogesterone and tibolone tomatic obstructive lung disease (56). It was also prevent total body fat changes, whereas transdermal shown that respiratory muscle strength is closely estradiol/oral dydrogesterone and tibolone prevent associated with body weight and lean mass in lean mass changes. Furthermore, oral estradiol/ patients with COPD. The comparison of respiratory dydrogesterone prevents the shift to a central, muscle strength with lean body mass should be use- android fat distribution (62). Tamoxifene, an anti- ful for studying the mechanism of respiratory mus- estrogenic agent used in patients with advanced cle weakness in patients with COPD (57). breast cancer, may lead to an increase in fat content In cystic fibrosis, the combination of pulmonary in women who are undergoing this treatment (63). dysfunction, which can increase energy require- The administration of testosterone enanthate for 6 ments, and malabsorption, caused by pancreatic mo as contraception in healthy men resulted in a insufficiency and reduced bile-salt concentration, modest reduction in fat mass and small increases in make it difficult to provide adequate nutrition.
lean mass, muscle strength, and bone density (64). Knowledge of body composition is important in Exogenous androgens increase lean body mass and states of acute and chronic illness where an individ- modulate abdominal fat distribution in obese post- ual may not be able to consume an adequate diet to meet nutrition needs. Such a knowledge allows clin- GH is a potent anabolic agent that tends to nor- icians to provide nutrients needed for maintenance malize body composition as shown in several studies and repair (58). In addition, in cystic fibrosis, bone on GH-deficient hypopituitary adults (43,45–46). In mineral status may be impaired, although the patho- addition, a low dose of biosynthetic GH can elevate genesis of this bone mineral deficit is still uncertain.
insulin-like growth factor (IGF)-I levels in GH-defi- The reduction of lumbar spine, femoral, and whole cient adults and has a pronounced physical impact body BMD observed in these patients suggests a and a decline in fat mass, without the side effects reduction in both cortical and trabecular BMD.
seen at higher dosage schedules (66). Bachrach and colleagues have proposed that either Total parenteral nutrition (TNP) may be subject to osteopenia or osteoporosis be included as health the inadequate provision of certain nutrients and the risks for adults with cystic fibrosis and that bone resulting nutritional complications may affect bone, mineral status of such patients be assessed on a rou- lean mass, and fat mass. However, it was reported that patients receiving home TNP present a stable body composition with no significant change in lean ered in the design of future intervention studies for mass, fat mass, or total BMC after a mean period of 20 mo. Individual changes in body weight and lean Patients affected by reflex sympathetic dystrophy mass were correlated with change in home par- syndrome exhibited, before treatment, decreased enteral nutrition energy supply (67). lean and bone masses, and increased fat mass ascompared to the unaffected limb after 1-yr treatment.
Other Diseases
In patients whose clinical manifestations had sub- DXA has recently been used to study the body sided, increased bone and lean masses were composition of patients affected by diabetes (68), acquired immunodeficiency syndrome (AIDS) Whole body DXA analysis has been shown to (69,70), and different neurological conditions such reliably detect body-composition changes in amy- as sympathetic dystrophy syndrome (71), amy- otrophic lateral sclerosis (72) and can be used to pro- otrophic lateral sclerosis (72), tetraplegy (73), and vide a basis for appropriate nutritional advice Patients with noninsulin-dependent diabetes An increase in lean mass with a concomitant mellitus (NIDDM) and those with insulin-depen- decrease in fat mass was described in tetraplegic dent diabetes mellitus (IDDM) may present an patients after 8 wk of electrically stimulated leg alteration of fat distribution that can result in pre- mature cardiovascular risks (75). It was shown that The patients, affected by Duchenne muscular dys- abdominal adiposity seems to be a strong marker trophy, exhibit total bone osteopenia and elevated and may be a major determinant of insulin resis- body fat, owing not to obesity, but probably to fatty tance in overweight women (23) and that fat distri- infiltration of skeletal muscles, known to occur in bution becomes more abdominal with age and with this disease. A significant correlation between mus- menopause (76,77). In a controlled study (68), it cle function and the percentage of regional variation was reported that patients with IDDM have signifi- of lean mass was also demonstrated (74). cantly less total body and abdominal fat than thoseaffected by NIDDM, irrespective of age andmenopausal status. In postmenopausal patients Conclusions
with IDDM, total body fat and abdominal fat werelower than those found in normal subjects, whereas these were higher in premenopausal patients with rapid, noninvasive bone measurements and body- NIDDM as compared to normal subjects.
composition estimates with low radiation exposure AIDS is characterized by progressive weight for many clinical applications. Regional and total loss and severe inanition. It was demonstrated that body DXA have been of growing interest in differ- women lose significant lean body mass in the late ent fields of medicine because it offers an interest- stages of wasting. However, in contrast to men, ing alternative to other time-honored reference women exhibit a progressive and disproportionate methods mainly used by nutrition specialists. DXA decrease in fat mass relative to lean mass at all is simple to perform, less dependent on operator stages of wasting, consistent with gender-specific skills and experience, highly reproducible, and effects in body composition in AIDS wasting (69). A longitudinal study on changes in body composi- In the clinical management of patients affected by tion in AIDS showed a reasonable agreement different chronic diseases, whole body DXA may among DXA, TBW, BIA, and ST (70). The authors provide further information about the natural history demonstrate that weight loss is composed of a large of the disease, and more importantly, may offer a proportion of lean mass compatible with undernu- noninvasive method for determining appropriate trition and do not support the hypothesis of exces- nutritional support during disease progression. It can sive lean mass catabolism in such a disease, also be used to evaluate and monitor the response to suggesting that this information should be consid- Clinical Applications of Whole Body DXA Acknowledgments
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ETHNOPHARMACOLOGY AND TOXICOLOGY OF ANTIMALARIAL PLANTS USED TRADITIONALLY IN MSAMBWENI, KENYA. Dr. Joseph Mwanzia Nguta, BVM, MSc (University of Nairobi). Supervisors Department of Public Health, Pharmacology and Toxicology, University of Nairobi Professor Peter K. Gathumbi, BVM, MSc, PhD. Department of Veterinary Pathology, Microbiology and Parasitology, University of Nairobi. De

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