Congenital Anemia, Dyskeratosis, and Progressive Alopecia in Polled Hereford Calves
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Vet Path ol 28:234-240 ( 199 1)
Congenital Anemia, Dyskeratosis, and Progressive Alopecia
in Polled Hereford Calves
D. J. STEFFEN, H. W. LEIPOLD, J. GIBB, AND J. E. SMITH
Department of Path ology, College of Veterinary Med icine, Kans as State Unive rsity,
Manh att an , KS; and Am erican Polled Hereford Association Kan sas City, MO
Abstract. A new syndrome of anemia , alopecia, and dyskeratosis was identified in Polled Hereford calves
in thi s study. Cutaneo us changes includ ed hyperkeratosis and hair loss around the mu zzle and ear margin s,
which progressed to a generalized alop ecia and hyperkerat otic dermatitis. Histolo gically, orth okeratotic hyper-
keratosis with dyskeratosis of epidermal and follicular kerat inocytes was present. Alopecia was correlated with
dyskeratosis of Huxley's layer and an increasing prop ortion of follicles in the telogen phase of the hair cycle.
Dermatitis was characterized by a mild dermal mon onucl ear cell infiltrat e and mild lymphocytic perivascular
derm atiti s. The an emi a present at birth was non progressive and was classified as norm ochromic and normocytic
to macrocytic. Reticulocytosis was ab sent , but bone marrow was markedl y hyperp lastic. Nuclear cytoplasmic
asynchrony of the rub ricyte and metarubricyte stages occurred in the bone ma rrow. Abno rmal rubri cyte nuclei
and maturat ion arrest at the late rubricyte stage were commo n. Cytologic features of the erythro id series are
similar to those of type I congenita l dyserythropoietic anemia of hum an beings. Genealogic features suggest
that thi s is a prim ary hereditary defect. The mode of inheritance, however, rem ains to be determ ined.
Key words: Alopecia; anemia; cattle; dyserythro poiesis; dyskeratosis; ineffective erythro poiesis .
Many different congenital defects affect bovin e were sampled and fixed in 10% neut ral buffered formalin.
skin.s'-'! Man y more undoubtedly exist and await de- Tiss ue samples were processed routinely, embedded in par-
scription. Th ese defects can occur as isolated defects affi n, sectioned at 6 j.lm, and stai ned routinely with hema-
afflicting only the skin , or they can be associated with toxylin and eosin. Bone mar row sections were fixed in Zen-
defects of oth er body system s.':' Most have been due ker-form alin, washed to remove mercury chloride precipitate,
processed as abo ve, and then stai ned with Giemsa and he-
to homozygosity at a single autosomal locus; som e
matoxylin and eosin, as previously described." When live
have suspected etiologies, and a few remain unknown. ' calves were submitted, bone marrow was aspirated from the
Recentl y, we found a new syndrome in Polled Hereford dorsal tenth rib, smears were mad e, and myeloid : erythroid
calves that was characterized by congenital anemia, ratio s were calculated. Hem ogram s includ ed erythrocyte and
dysk eratosis, and progressive alop ecia. This study de- leuko cyte blood 'counts, reticulocyte counts, and differenti al
scrib es the historical, clinical , hematologic, and his- blood counts (Coulter S Plus IV, Coulter Electronics, Hialeh ,
topathologic findings of the affected calves . FL). Serum concentrations of sodium, pota ssium , chloride ,
glucose, urea nit rogen, creatinine, alkaline phosphatase, gam-
ma glutamyl tran sferase, aspartate am ino-transferase, total
Materials and Methods bilirubin , direct bilibu rin, total protein, albumin, globulin,
Reports of th is disease were received from various part s calcium, phosphorus (Dacos , Cou lter Corpo rate Commu-
of the Unite d States and Canada as part ofa long-term study nications, Hialeh , FL), and sorbitol dehydrogenase (Abbott
ofbov ine congenital defects. T he methods for th is study have VP Bichrom atic Analyzer, Abbot Laborator ies, Dallas, TX)
been outli ned previously.' Initially, calves were reported with were determ ined.
an alopecia distinct from hypotrichosis.v-!? Calves and their When calves could not be tran sported to us, the following
pare nts were blood typed to verify parentage, and five gen- were obtai ned: case histories, gross descript ions, skin biop-
eration pedigrees were obtained to constr uct a genealogy." sies, and blood samples (collected with di potassium ethylene
Reports were suppleme nted by skin biopsies (fixed in 10% diam inotetracetate as anticoagulant). Biopsies were collected
neut ral buffered formalin), additional biopsies, and blood from either the lateral margin of the ear or the lateral neck,
sa mples. Finally, affected calves were tran sport ed to the an- fixed in 10% neutral bu ffered form alin, and processed as
ima l resources facilities at Kan sas State University for sam- above . Th ey were stained with hem atoxylin and eosin and
ple collectio n and necrop sy. Calves were euthanatized with Altma nn's acid fuchsin meth yl green technique. Hem ogram s,
intraveno us T -61 (American Hoechst Corporation, Somer- including reticulocyte counts, were performed on blood re-
ville, NJ) and necrop sied using standard procedures. Skin ceived by our laboratory.
and interna l organs, includ ing endocri ne glands and brain, T he comparable histop ath ologic findings of twent y-five
234
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Fig. 1. Genealogy of congenital anemia , dyskeratosis, and progressive alopecia in Polled Hereford cattle. 0 denotes
normal appearing male and 0, norm al fema le. • repr esent affected males, whereas . denote affected fema les. Rom an
notat ion denotes generatio ns. Notice that sire 1-6 is the ancestor patern ally as well as mat ernall y to all cases of anemia,
dyskeratosis, and progresive anemia represented here.
calves are report ed here. Necro psies were perform ed on 15 an cestor (Fig. 1). Although this syndrome was recog-
calves, bone marrow aspirates on II , hem ograms on 15, and nized during the spring of 1988, several unconfirmed
serum chemistry profiles on 12. Data on an add ition al six cases had occurred previously.
calves were limited to skin biopsies and gross descriptions. Calves afflicted with this syndrome were often small
Thirty unconfirm ed gross descript ion s were received but not at birth. Calves had a characteristic prominent fore-
included in th is report. Affl icted calves were from 15 states
head and a hyperkeratotic mu zzle that attracted dirt
and one Canadian province. Thi rteen were bulls, II were
heifers, and the sex of one was unreported. Calves ranged in
and saliva. This gave th em a " dirty-faced" appearan ce
age from 3 da ys to 9 mo nths. (Fig. 2). Periocular irritati on and conj unctivi tis were
Calves had been weaned when they were submitted and also ev ident.
were from several management systems and geographic Ha ir ofafflicted calves was wiry and kink ed or tightl y
localit ies. In th ree cases where complete managem ent in- curled and epilated easily. Alopecia and hyperke rat osis
formation was available, cows (but not calves) had been were first evide nt over th e bridge of th e nose, lat eral
deworm ed and vaccinated for leptospirosis and campylobac- auricular margins, and th e base of th e ears . Alopecia
teriosis. Manu facturers and types of vaccines varied from and hyperkeratosis were pr ogressive, and a generali zed
farm to farm. Several calves were observ ed for vary ing pe- sebo rr hea developed by 3 months. Th e head , lat eral
riods prior to necropsy. neck, sho ulde rs, and dorsal lumbar areas were most
seve rely affected. Cutaneous surfaces were co vered by
Results a loose dander of keratin debris, sebum, and dirt. Sec-
Th is syndrome appeared to have a famili al ba sis. ondary dermatophilosis occurred in two calves . A
Affected calves had a single com mon ancestor on both marked wrinkling of skin develop ed over th e face and
th e sire's and dam's side of the pedigree, often more neck and became more pronounced as th e calves aged
than onc e (Fig. 1). Sire 1-6 appeared as the common (Fig. 3).
Downloaded from vet.sagepub.com by guest on July 23, 2015236 Steffen et al.
ger calves . Twenty to 30 rubricytes or metarubricytes
per 100 white blood cells were typical. Numbers varied
considerably between samples of individual calves
without any particular pattern. Leukocyte number and
distribution appeared normal.
Examination of bone marrow samples indicated in-
creased erythroid precursors with myeloid to erythroid
ratios that ranged from 0.021 : 1 to 0.15: 1, (normal
0.3-3 .33: 1).6 Erythroid cells showed a marked pre-
dominance of late rubricytes with lesser numbers of
metarubricytes. Nuclear cytoplasmic asychrony was
evident. The cytoplasm of rubricytes was homoge-
neous and eosinophilic, typical offully hemoglobinized
cells. Polychromatophilic metarubricytes were absent.
Dysplastic features were seen in moderate numbers of
rubricytes. Features including binucleate rubricytes,
abnormal chromatin patterns, irregular nuclear shapes,
and irregular nuclear margins were found. Granulo-
cytic series appeared normal.
Many calves were hypoproteinemic; both albumin
and globulin fractions were decreased. No consistent
biochemical abnormalities were noted for any other
serum analytes.
At necropsy, in addition to the skin lesions, there
was a marked subcapsular hepatic fibrosis, giving the
capsular surface a distinctive mosaic appearance (Fig.
4). Active erythropoietic marrow had proliferated from
Fig. 2. Three-day-old calf affected with congenital alo- the endosteal regions to fill the entire metaphysis and
pecia and anemia. Note the appearance of the hair and skin diaphysis of each humerus and each femur (Figs. 5, 6).
and the d irty face and protruding tongue. An extensive erythropoietic marrow was also present
Fig. 3. Six-month-old calf, neck and shoulder. There is
in each tibia and each ulna . Mucous membranes, sub-
marked wrinkling and alopecia of the skin.
cutaneous tissues , and kidneys were pale. Small to
moderate amounts of clear yellow fluid were present
Mucous membranes of afflicted calves were pale in in the pericardial, thoracic, and peritoneal cavities.
color, and calves were intolerant of exercise. Calves Older calves had deep fissures in the skin of the caudal
were stressed easily by transport and by heat, and tra- aspects of the distal limbs. Four often calves had uni-
chypnea and tachycardia occurred on warm days. Sev- lateral corneal scarring, and three calves had dilated
eral calves demonstrated subtle neurologic signs, such flabby hearts; two had superficial fibrosis of the left
as difficulty in rising and nursing at birth, abnormal ventricle. Spleens from affected calves were very small,
mentation, protruding tongues, and regurgitated fluid firm, and had relatively thick capsules.
ruminal contents during rumination. Geophagia was Histopathologic changes were present in the skin,
noted in three calves. Calves often had recurrent di- rumen, liver, kidney, bone marrow, spleen , cardiac
arrhea. Calves had a normal appetite, but failed to muscle , and thyroid. Skin lesions were generalized and
thrive on adequate diets and often were euthanatized characterized by orthokeratotic hyperkeratosis and hy-
or died in a cachexic state before reaching 6 months pergranulosis. These changes extended down the fol-
of age. licular infundibuli. Occasionally, keratin debris plugged
A persistent nonregenerative anemia (packed cell the follicles (Fig. 7). Dyskeratosis of individual epi-
volume < 25) was observed (Table 1). Erythrocytes dermal and follicular keratinocytes was prominent.
were normocytic to macrocytic (mean corpuscular vol- Individual keratinocytes had become detached from
ume 44.4 fl to 64.7 fl) and normochromic. Significant surrounding cells and had pyknotic nuclei and
polychromasia and reticulocytosis was absent. There hyperchromatic eosinophilic cytoplasm (Fig. 8). The
was a moderate anisocytosis and varying numbers of epidermal surface appeared plicated, and follicular
circulating nucleated erythrocytes, rubricytes, and density was normal to slightly increased. Many follicles
metarubricytes. Nucleated erythrocytes ranged from 0 were in the telogen phase and contained club hairs or
to 130 per 100 leukocytes, with highest counts in youn- no hair shafts. The internal root sheaths had kerati-
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Table 1. Hematologic values o f 15 Poll ed Herefo rd calves affected with co ngenital a nem ia, d yskeratosis, and pr ogressive
alopecia .
Recitu -
Mean locytes
Herno-
Ery thro - Packed Corpus- Ret icu- Nu cle- Myeloid!
Leuk o-
Age cytes Cell cytes
Calf No. Sex globin cular locytes ated Erythroid
(gldl) (millionsl Volume Volume % IOOWBCs Ratio ( x 1,0001
Ill) %
(11) Leuko- Ill)
cytes
1 7 months F 4. 8 2.24 13.4 60.0 1.5 14 0.035 8. 1
2 6 months M 5.0 2.73 14.9 54.4 4.1 0.05 0.0 3 1 7.9
3 3 days M 6.6 3.97 19.7 49.7 NO* 0 NO 5.2
4 2 m onths F 5.4 3.26 16.0 49.0 NO 2 NO 5.5
5 2 m onths F 5.3 3.07 15.6 50.8 NO 0 NO 8.4
6 9 m onths M 5.1 3.17 15.6 49.1 NO 0.5 0.0 5 1 8.6
7 3 months F 4.7 2.26 13.0 57.6 0.2 0 0.15 7.6
8 I month M 5.3 3.0 9 15.4 49.7 0.5 5 0.0 7 8.8
9 2 months F 6.7 4.23 20.1 47.4 0.5 I 0.05 9.9
10 6 m onths F 5.7 3. 18 16.9 53.0 1.0 4 NO 4.5
11 I month F 4 .3 2.86 12.7 44 .4 0. 5 14 0.0 46 4. 3
12 8 days F 6.3 3.6 17.3 48.1 < 0. 1 2 NO 9.5
13 I mon th M 6.4 3.08 18.4 59.8 0.4 56 0.0 2 1 7.2
14 I month M 6.9 3.23 20. 1 62 .2 0.7 17 0.0 56 7.5
15 4 months F 4.5 2.52 16.3 64.7 NO 32 < 0. 1 7.8
ND = not done.
nized prematurely and degenerated. Dyskeratotic cells by a marked erythroid hyperplasia with a predomi-
were present in Hu xley's layer of many hai r follicles nan ce ofla te rubricytes and metarubricytes. Dysplasti c
(Fig. 9). Sebaceous glands were atrophied, and sweat features, as described cytologically, were found to be
glands were dilated, with th e glandular epithelium at- present in colonies of erythroid cells associated with
tenuated. A superficial dermal inflammatory reaction individual reticular (nurse) cells. Numerous morpho-
was characterized by a mild, perivascular, lymphocytic logically normal colonies of erythroid cells were also
infiltrate and a diffuse increase in mononuclear cells present. Hyperplasia of the megakaryocyte series was
throughout the superficial dermis. Altmann's sta ining evi de nt. Diaphyseal fatt y marrow was repla ced by co-
highlighted the hyperkeratosis and dyskeratotic cells. alescing sheets of erythro poietic cells (Figs. 10, II).
Dermal elastin and collagen were similar to those of Phago cytosis of nucl eated erythrocyte precursors was
controls. Hyperkeratotic changes were most severe in also present in bone marrow sections. Prussian blue
older calv es and from areas with th e most severe gross sta ining of bone marrow smears showed increased
lesions . The labia and th e rumen had similar histo- stored iron. Splenic hemosidero sis was present in two
pathologic features, with moderate hyperkeratosis and calves.
num erous, indi vidually dyskeratotic cells in th e su- Cardiac mu scle was characterized by sub epicardial
perficial mucosa. and sub endocardial fibrosis in three cases. No degen-
Histopathologic lesions in th e liver were character- erative or necrotic changes in cardiac muscle were found
ized by marked capsular and subcapsular fibrosis . Yel- in hematoxylin and eosin-stained sections or frozen
low-gold granular pigment occurred in Kupffer cells sections stai ned with oil red O.
and in periportal hepatocytes of several calves. Mid- The follicular size ofthyroid glands markedly varied.
zonal and centrilobular hepatocytes had a mild to mod- Colloid was homogeneous eosinophilic and occasion-
erate vacuolar degeneration and were swollen. Bile duct ally vacuolated. Occasionally, ma cro phages appeared
proliferation was not evident. Renal lesions were char- in the vacuolated colloid. Th yroid follicular epithelium
acterized by mild swelling of proximal tubular epith e- was low cuboidal with few mi cro villi and littl e scal-
lial cells, and yellow pigment was present focally in loping of colloidal margins.
proximal, convoluted , tubular epithelial cells. Hepatic
pigm ent stained positi vely for iron (Pru ssian blue re- Discussion
action), but yellow pigm ent in kidn eys failed to stain The syndrome of an emia and alope cia app ear s to be
for iron . an eme rging probl em in the Polled Hereford breed of
In affected calves, bone marrow was characterized catt le. Pedigree analysis suggests that thi s is an inh er-
Downloaded from vet.sagepub.com by guest on July 23, 2015238 Steffen et al.
Fig. 4. Diaphragmatic surface of liver; Polled Hereford Fig. 7. Skin; 2-month-old Polled Hereford calf. Note or-
calf. Note the mottled appearance of liver surface caused by thok eratotic hyperkeratosis and mononuclear cell infiltrate
capsular thickening (arrow). in dermis. HE.
ited defect. Confirmation regarding mode of inheri- had a mild orthokeratotic hyperkeratosis with indi -
tance through controlled breeding trials is needed. vidual keratinocyte necrosis and low numbers of an-
The gross dermatologic changes at birth, a coarse agen follicles. A mild to moderate superficial mono-
curly hair coat and mild hyperkeratosis of the nasal nuclear cell perivascular dermatitis appeared to follow
region , became generalized and increased in severity the alopecic and hyperkeratotic changes as the calves
as the calves aged. Alopecia started in nasal and au- aged and is presumed to occur as a secondary event.
ricular regions , and also slowly became generalized. Hair follicles continued to cycle through anagen, ca-
Epidermal maturation and keratinization defects could tagen, and telogen . A higher proportion oftelogen fol-
be consistently demonstrated by biops y of the lateral licles was found in alopecic calves. Follicular density
auricular margins. Histologically, the youngest calves appeared normal. A premature keratinization and de-
generation of the internal root sheath was evident in
Fig. 5. Sagittal section of hum eru s; Polled Hereford calf
affected with anemia and dyskeratosis. Note that active
erythropoietic bon e marrow fills the entire diaphysis and
both metaphyses. Fig. 8. Dyskeratosis and necro sis of ind ividual keratin -
Fig. 6. Sagittal section of hum erus; normal , 2-month-old ocytes are seen in many skin section s (arrow); 2-month-old
calf. For comparison with Fig. 5. Polled Hereford calf. HE.
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Fig. 9. Base of a hair follicle; Polled Hereford calf with
alopecia . Note abnormal keratiniz ati on of internal root sheath
(arrow). HE.
many follicles and also contributed to the development
of alopecia. Similar but not identical dermatologic le-
sions have occurred due to nutritional and chronic
endocrine diseases." Zinc levels were reported for two
affected calves: 18.4 and 16.7 iLMol/liter, respectively
(normal 11-20 IlMol/liter). The histologic similarity
between cutaneous epidermal lesions and ruminal ep-
ith elial lesions suggests a common pathogenesis.
The anemia appeared to be nonregenerative (no re-
Fig. 10. Bone marrow diaphysis; norm al, 2-m onth-old
ticulocytosis), but marked erythropoiesis was present calf. HE.
in the bone marrow. A maturation defect of the ery- Fig. 11. Bone marrow from diaph ysis; 2-month-old Polled
throid cells was evident. Erythropoiesis was ineffective, Hereford calf affected with alopecia. Note solid sheets of
and maturation was arrested at the late rubricyte stage. hem atopoietic cells. HE.
Anemia was apparent in calves at birth and did not
progress in severity with age. Ineffective erythropoiesis
can result from many genetic and environmental caus- abnormal clumping and distribution ofchromatin, and
es.1.3,6 Nutritional deficiencies such as lack of iron, B nuclear fragmentation . Bon e marrow features resem-
vitamins, and copper have resulted in erythrocyte mat- bled those oftype I dyserythropoiesis in human beings.
uration defects. ' > Microcytosis as seen with iron de- Congenital dys erythropoietic an emias in human beings
ficiency was not present in any affected calves, neither are thought to be inherited, types I and II as simple
were the megaloblastic changes characteristic of co- autosomal recessive traits, and type III as an autosomal
balamin and folate deficiencies. B vitamins are syn- dominant trait. 8
thesized by ruminal flora, and a nutritional deficiency An idiopathic dyserythropoietic anemia has recently
was considered unlikely. been described in a dog ." Com m on features included
In human beings several genetically determined anemia, ineffective erythropoiesis, hypercellular mar-
erythropoietic disorders have been studied. t-v Con- row , nuclear fragmentation , and binucleate rubricytes.
genital dyskeratosis has been described in human be- Common secondary causes were ruled out, and the
ings with an accompanying anemia, but the anemia author concluded that the defect was primary and pos-
was aplastic.' More than three distinct types of con- sibly genetic.
genital idiopathic dyserythropoietic syndromes in hu - The relationship between the dyserythropoiesis, cu-
man beings have been described. ' ,3,8 Results from pre- taneous lesion and hepatic fibrosis remains unclear.
lim inary morphologic studies in calves have suggested Abnormal cellular maturation is pres ent in both the
a similarity to congenital dyserythropoiesis in human epidermis and the erythroid cells. This maturation de-
beings. Similar features include anemia, hypercellular fect is likely due to a simple genetic defect or defects
bone marrow, and ineffective erythropoiesis. Com m on in two closely linked loci , as all calves did have both
dysplastic features include th e following: binuclearity, changes. Increased hemosiderin deposits in bone mar-
irregularly shaped nuclei, irregular nuclear outlines, row, liver, and spleen suggest intramedullary eryth-
Downloaded from vet.sagepub.com by guest on July 23, 2015240 Steffen et aI.
rocyte destruction, and decreased life span of circulat- erythropoie tic an emia type II: association oflo w level of
ing erythrocytes. Minimal diagnostic requirements membran e-bound form of galactosyltran sferase. Blood
should include skin biopsies and hemograms and, 73:13 31-133 9,1 989
when ever practical, bone marrow cytologic evaluation. 6 Jain NC: Hemolytic anemias of noninfectiou s origin.
In: Schalm 's Vete rinary Hem atology, 4th ed., pp. 627-
Acknowledgements 654. Lea & Febiger, Philadelphia, PA, 1986
7 Leip old HW , Hu ston K, Dennis SM: Bovine congenital
T his research was supported by the Am erican Polled Here-
defects. Adv Vet Sci Com p Med 27:197-2 71,1 983
ford Associati on , Kansas City, MO. This research was part
8 Lewis SM, Path FR C, Verwilgh en RL: Dyserythro-
of the Regional Project NC-2.
poiesis and dyserythropoietic anemias. Prog Hematol 8:
99- 129, 1983
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Request reprints from Dr. S. Steffen, College of Veterin ary Medicine, Kan sas State University, Manh att an , KS 66 506 (USA).
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