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51]
Original article 27
Keywords:
chronic renal failure, cutaneous manifestations, hemodialysis
duration of 5 months or more and age ranging from purpura in 2% of patients. Rare skin manifestations of
15 to 65 years. Exclusion criteria included patients who CRF such as bullous dermatosis (1%) (Fig. 3) were also
had undergone HD following renal transplant, patients observed. Xerostomia (46%) was the most common
who had undergone peritoneal dialysis, and patients with
other systemic or cutaneous diseases. All patients were Figure 1
subjected to a complete assessment of history, with a
special focus on the onset of cutaneous manifestations and
their relation to HD and the etiology of CRF. Thorough
general and dermatological examinations were performed
including skin, hair, nail, and oral mucosa. Photos of
lesions were taken using a Sony Cybershot 14.1 mega
pixels camera (Sony Corp. Japan). Blood samples were
obtained to investigate the complete blood count, fasting
and postprandial blood glucose levels, liver function tests
[serum glutamic pyruvic transaminase (SGPT) serum
glutamic oxaloacetic transaminase (SGOT)], and for
kidney function tests (serum urea and creatinine). Serum
urea and creatinine levels were compared with their before
dialysis levels (obtained from the patient’s files).
Xerosis.
Statistical analysis
The data collected were analyzed using the statistical
package for social sciences (version 16; SPSS Inc., Chicago, Figure 2
Illinois, USA). Quantitative data were analyzed using
mean and SD, whereas frequency and percentage were
used to describe qualitative data. The Z-test and c2-test
were used to compare frequencies. A P value of less than
0.05 was considered statistically significant and values less
than 0.001 were considered highly statistically significant.
Results
Among the patients, there were 66 male and 34 female.
Their age ranged from 15 to 65 years (mean ± SD
50.27 ± 11.23 years). The total duration of HD ranged
from 0.5 to 16 years (mean ± SD 5.64 ± 3.45 years). The
Kyrle’s disease.
blood urea level before HD ranged from 120 to 250 mg/dl
(mean ± SD 165.59 ± 30.22 mg/dl), which decreased to
40–120 mg/dl (mean ± SD 70.79 ± 21.97 mg/dl) during Figure 3
HD. The blood creatinine level before HD ranged from
6 to 16 mg/dl (mean ± SD 9.91 ± 2.11 mg/dl), which
decreased to 4–9 mg/dl (mean ± SD 5.45 ± 1.33 mg/dl).
oral mucosal manifestation, followed by macroglossia half and half nail (41%) (Fig. 5), koilonychia (29%),
with teeth markings (43%) (Fig. 4), fissured tongue splinter hemorrhages (15%), subungual hyperkeratosis
(17%), uremic breath (17%), ulcerative stomatitis (12%), onycholysis (10%), onychomycosis (7%),
(11%), and angular cheilitis (6%). The relation between Muehrcke’s lines (7%) (Fig. 6), Mees’ lines (6%), and
the onset of skin and oral mucosal manifestations with Beau’s lines (1%) (Fig. 7). Hair manifestations included
HD showed that xerosis (65.3%), pruritus (69.2), and sparse scalp hair (48%), sparse body hair (41%), and
pallor (91.2%) statistically significantly manifested brittle and lusterless hair (39%). The relation between
before HD (P = 0.006, 0.002, and <0.001, respectively), the onset of nail and hair manifestations with HD
showed that AL (96.7%) was the only manifestation
whereas hyperpigmentation (86.4%), wrinkles (93.9%),
that statistically significantly manifested before HD (P
ecchymosis (90.6%), macroglossia (83.4%), fissured
< 0.001), whereas half and half nail (95.1%), onycholysis
tongue (94.1%), and ulcerative stomatitis (81.8%) (90%), and Muehrcke’s lines (85.7%) statistically
statistically significantly manifested after HD (P < significantly manifested after HD (P < 0.001, <0.001,
0.001 for all except ulcerative stomatitis, P = 0.006) and 0.007, respectively) (Table 2).
(Table 1). Nail changes were absent lunula (AL) (61%),
Figure 5
Figure 4
Table 1 Skin and oral mucosal manifestations and the relation between their onset and hemodialysis
Onset [n (%)]
Variables N Before HD After HD Z P
Skin
Xerosis 72 47 (65.3) 25 (34.7) 2.7 0.006*
Pruritus 52 36 (69.2) 16 (30.8) 3.0 0.002*
Hyperpigmentation 44 6 (13.6) 38 (86.4) 7.0 <0.001*
Pallor 34 31 (91.2) 3 (8.8) 10.1 <0.001*
Skin wrinkles 33 2 (6.1) 31 (93.9) 6.2 <0.001*
Ecchymosis 32 3 (9.4) 29 (90.6) 7.4 <0.001*
Fungal infection 18 9 (50.0) 9 (50.0) 0.0 1.0
Bacterial infection 6 3 (50.0) 3 (50.0) 0.0 1.0
Viral infection 4 2 (50.0) 2 (50.0) 0.0 1.0
Kyrle’s disease 7 2 (28.6) 5 (71.4) 1.3 0.21
Gynecomastia 7 4 (57.1) 3 (42.9) 0.38 0.7
Purpura 2 0 (0.0) 2 (100.0) – –
Bullous dermatosis 1 0 (0.0) 1 (100.0) – –
Oral mucosa
Xerostomia 46 29 (63.0) 17 (37.0) 1.83 0.07
Macroglossia with teeth marking 43 7 (16.3) 36 (83.7) 5.99 <0.001*
Fissured tongue 17 1 (5.9) 16 (94.1) 7.7 <0.001*
Ulcerative stomatitis 11 2 (18.2) 9 (81.8) 2.74 0.006*
Angular cheilitis 6 2 (33.3) 4 (66.7) 0.87 0.39
HD, hemodialysis; *P < 0.05 was considered statistically significant and P < 0.001 was considered statistically highly significant.
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Figure 6 Figure 7
Table 3 Skin and oral mucosal manifestations and their relations to the etiology of chronic renal failure
Cause of CRF [n (%)]
Manifestations DM (18) HTN (53) PK (2) Analgesic (6) RUTI (3) SLE (4) Urinary tract Unknown (5) Total
obstruction (9) number (N)
Skin
Xerosis 13 (18) 34 (47.2) 2 (2.7) 6 (8.3) 2 (2.7) 4 (5.5) 9 (12.5) 2 (2.7) 72
Pruritus 14 (26.9) 22 (42.3) – 6 (11.5) 3 (5.7) 2 (3.8) 4 (7.6) 1 (1.9) 52
Hyperpigmentation 7 (15.9) 25 (56.8) 1 (2.2) 4 (9) 2 (4.5) 1 (2.3) 2 (4.5) 2 (4.5) 44
Pallor 3 (8.8) 18 (52.9) 2 (5.8) 1 (2.9) – 3 (8.8) 5 (14.7) 2 (5.8) 34
Skin wrinkle 5 (15.1) 16 (48.4) 1 (3) 2 (6) 2 (6) 2 (6) 3 (9) 2 (6) 33
Ecchymosis 5 (15.6) 13 (40.6) – 2 (6.2) 1 (3.1) 1 (3.1) 7 (21.8) 3 (9.3) 32
Fungal infections 8 (44.4) 5 (27.7) 1 (5.5) – – 2 (11.1) 1 (5.5) 1 (5.5) 18
Kyrel’s disease 5 (71.4) – – – – – 2 (28.5) – 7
Bacterial infections 2 (33.3) 1 (16.6) – 2 (33.3) 1 (16.6) – – – 6
Viral infections 2 (50) 2 (50) – – – – – – 4
Purpura 1 (50) 1 (50) – – – – – – 2
Bullous dermatosis – 1 (100) – – – – – – 1
Oral mucosa
Xerostomia 8 (17.3) 17 (36.9) 1 (2.1) 3 (6.5) 2 (4.3) 4 (8.6) 9 (19.5) 2 (4.3) 46
Macroglossia 7 (16.2) 25 (58.1) 1 (2.3) 4 (9.3) 3 (6.9) – 2 (4.6) 4 (9.3) 43
Fissured tongue 2 (11.7) 8 (47) 1 (5.8) 1 (5.8) – – 3 (17.6) 2 (11.7) 17
Ulcerative 1 (9) 6 (54.5) 1 (9) – – – 1 (9) 2 (18.1) 11
stomatitis
Angular cheilitis 2 (33.3) 2 (33.3) – 2 (33.3) – – – – 6
CRF, chronic renal failure; DM, diabetes mellitus; HTN, hypertension; PK, polycystic kidney; RUTI, recurrent urinary tract infections; SLE,
systemic lupus erythematosis.
Table 4 Nail and hair manifestations and their relations to the etiology of chronic renal failure
Cause of CRF
Manifestations DM (18) HTN (53) PK (2) Analgesic (6) RUTI (3) SLE (4) Obstruction (9) Unknown (5) Total number
Nail
Absent lunula 13 (21.3) 29 (47.5) 2 (3.2) 6 (9.8) 1 (1.6) 4 (6.5) 5 (8.1) 1 (1.6) 61
Half and half 8 (19.5) 20 (48.7) – 2 (4.8) 2 (4.8) 2 (4.8) 4 (9.7) 3 (7.3) 41
Koilonychia 6 (20.6) 8 (27.5) 2 (6.8) 2 (6.8) 2 (6.8) 3 (10.3) 6 (20.6) – 29
Splinter 2 (13.3) 9 (60) – 1 (6.6) 1 (6.6) – 2 (13.3) – 15
hemorrhage
Subungual 1 (8.3) 5 (41.6) 1 (8.3) – – – 3 (25) 2 (16.6) 12
hyperkeratosis
Onycholysis 1 (10) 5 (50) – 2 (20) – – 2 (20) – 10
Muehrcke’s line 4 (57.1) 1 (14.2) 1 (14.2) – – – 1 (14.2) – 7
Onychomycosis 2 (28.5) 3 (42.8) – – – – 1 (14.2) 1 (14.2) 7
Beau’s line – 1 (100) – – – – – – 1
Hair
Sparse scalp hair 8 (16.6) 25 (52) – 4 (8.3) 3 (6.2) 3 (6.2) 1 (6.2) 4 (8.3) 48
Sparse body hair 12 (29.2) 27 (65.8) – – – – 2 (4.8) – 41
Brittle, 5 (12.8) 17 (43.5) 1 (2.5) 6 (15.3) 2 (5.1) 2 (5.1) 4 (10.2) 2 (5.1) 39
lusterless hair
CRF, chronic renal failure; DM, diabetes mellitus; HTN, hypertension; PK, polycystic kidney; RUTI, recurrent urinary tract infections; SLE,
systemic lupus erythematosis.
neurophysiological hypothesis is considered to play an hyperpigmentations in 7.5% of the Nigerian CRF patients
important role in CRF-associated pruritus [10]. studied. This could be attributed their dark skin color as
hyperpigmentation in black skin may be masked unless it
The prevalence of hyperpigmentation in this study was
is extensive. The onset of hyperpigmentation in our study
44% and presented as localized or diffuse brownish-black
statistically significantly manifested after HD in 86.4%.
pigmentations on sun-exposed areas. Abdelbaqi-Salhab
et al. [11] reported that pigmentary alteration occurs in Hyperpigmentation can be attributed to the retention of
25–70% of the dialysis population and increases over chromogens and deposition of melanin in the basal layer
the duration of renal disease. Our results were different and superficial dermis because of failure of the kidneys to
from those obtained by Falodun et al. [4], who detected excrete b-melanocyte-stimulating hormone [12].
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Pallor was observed in 34% of patients in this study. This associated with CRF patients (18%), whereas it was
is in agreement with Attia et al. [13], who observed pallor 38% in the Indian patients; also, onychomycosis (19%)
in 42.2%, but not in agreement with Udayakumar et al. was also observed in addition to the skin infection,
[2], who observed pallor in 60% of Indian patients, which whereas onychomycosis was a nail manifestation in
may be attributed to nutritional factors. The onset of pallor the present study. Excessive use of antibiotics in our
in our study statistically significantly manifested before community may be the reason for this lower incidence.
HD (91.2%). Patients with CKD are at risk of blood loss
because of platelet dysfunction. Erythropoietin deficiency In terms of fungal infections, we believe that the lower
is considered the most important cause of anemia in percentage of PV infection in comparison with tinea
CKD [14]. Other contributory factors included absolute pedis resulted from the reduction in the function of
iron deficiency as HD patients may lose 3–5 g of iron the pilo sebaceous and eccrine sweat glands in patients
per year [15]; the survival of red blood cells is reduced by with CRF as the sebum is one of the important factors
approximately one-third in HD patients and vitamin B12 in the development of PV. There was no statistically
deficiency [16]. significant difference between the onset of skin
infection and HD.
The prevalence of early wrinkling and exaggerated
skin markings was observed in 33% of the patients in Kyrle’s disease was detected in 7% of the patients
this study. These results are in agreement with those of in the present study. This was in agreement with
Sultan et al. [7], who observed early wrinkles in 40% of Sultan et al. [7], who reported Kyrle’s disease in 3%
patients. The onset was because of the early occurrence of the CRF patients on HD. However, Deshmukh
of actinic elastosis in patients undergoing long-term et al. [18] and Udayakumar et al. [2] reported Kyrle’s
HD [12]. The onset of appearance of wrinkles in our disease in 17.14 and 21%, respectively, in their
study statistically significantly manifested after HD patients. This difference could be explained by the
(93.9%). higher frequency of diabetic patients (51 and 38%,
respectively) compared with 18% in our patients. The
Ecchymosis was detected in 32% of the studied onset of Kyrle’s disease manifestations in our study
patients. It was observed around the arteriovenous was not statistically significantly related to HD. The
fistula, which is in agreement with Hajheydari et al. [3] pathogenesis of the disease is not known, but it may
and Sultan et al. [7], who observed ecchymosis in 30 occur as a result of dermal connective tissue dysplasia
and 27% of their patients, respectively. In contrast, and decay. Suspected causes include an inflammatory
Attia et al. [13] observed ecchymosis in 1.8% of their skin reaction secondary to the presence of uremic
dialysis patients. Defects in primary hemostasis such as toxins, uric acid deposits, or scratching-induced
increased vascular fragility, abnormal platelet function, trauma [19]. Microvascular deposition of calcium may
and the use of heparin during dialysis are the main interrupt blood flow to connective tissue in the dermal
causes of ecchymosis in CKD patients on HD [17]. In layer, causing death and necrosis [20].
this study, ecchymosis appeared in 90.6% of patients
after HD, and this was statistically significant. This Gynecomastia was observed in the present study in 7%
may be because of the repeated venopuncture necessary of patients, whereas Udayakumar et al. [2] reported it
for HD in addition to the lack of connective tissue- in 1% of patients. This difference may be because of
supporting blood vessels that occur with aging and associated schistosomiasis in our patients.
debilitating conditions.
In this study, bullous lesions in the form of
Skin infections was observed in 28% of the patients pseudoporphyria (PP) were noted in 1% of patients,
studied: fungal infections in 18% (PV in 11.1% and which matched with the reported percentage of
tinea pedis in 88.8%), bacterial infections in 6% (in bullous disease range of 1–18% in patients with CRF
the form of folliculitis), and viral infections in 4% on HD [11]. Usually, this PP is equivalent to porphyria
(disseminated plane warts in 50% of patients and cutanea tarda, showing blistering and mechanical
common warts in 50%). Sultan et al. [7] reported skin fragility of skin subjected to sunlight and incidental
infections in 40% of patients in their study (fungal trauma. It typically begins only after several months or
infections, bacterial infections, and viral infections years of dialysis therapy. Hypertrichosis is less common
in 33, 5, and 2%, respectively). Udayakumar et al. [2] and plasma porphyrin levels are usually normal [21].
reported skin infections in 67% of their HD Indian The etiology of PP remains unclear; however, CRF
patients (fungal infections, bacterial infections, and patients with PP show abnormal porphyrin profiles
viral infections in 30, 13, and 12%, respectively). The because of impaired excretion, rather than a deficiency
lower percentage of skin infections in the present in the enzyme uroporphyrinogen decarboxylase, in
study may be because of the lower percentage of DM contrast to true porphyria cutanea tarda [22].
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AL was the most common nail change observed in the onycholysis in 3% only of their patients. Certain
present study (61% of patients). This is in agreement medications that cause photosensitivity can induce
with Martinez et al. [23], who reported AL in 62.9% photo onycholysis as reported in HD patients who
of CRF patients on HD. However, Saray et al. [24] receive large doses of cephalordine or cloxacillin [25].
and Salem et al. [25] observed AL in 31.9 and 17%
of patients, respectively. Visible lunula is a good sign Onychomycosis was observed in 7% of the patients
in healthy cases of CRF on HD [25] and the lower in this study, is in agreement matched with Bencini
percentage in their reports may be because of the et al. [8], who reported onychomycosis in 6.2% of
better general health of their patients. The onset of their patients. However, Saray et al. [24] reported
AL was the only nail manifestation that statistically it in 19.2% of their patients. This may be because of
significantly appeared before HD. the difference in the number of study patients; they
included 182 patients in their study.
In total, 41% of the patients in this study had nail
manifestation in the form of half and half nail (HHN), In this study, sparse scalp hair was the most common
which is in agreement with Lubach et al. [26] and hair disorder. Its prevalence was 48%, followed by sparse
Pico et al. [6], who reported HHN in 50.6 and 40% body hair in 41% and brittle and lusterless hair in 39%
of their patients, respectively. In contrast, Deshmukh of the patients studied. These results were in agreement
et al. [18] and Salem et al. [25] reported HHN in 19.04 with those of Sultan et al. [7], who found sparse scalp
and 20% of their patients, respectively. Malnutrition is hair in 46%, sparse body hair in 27%, and lusterless
an important cause for HHN [27] and its presence hair in 47% of their patients. Our results were different
in some patients may be the reason for the higher from those observed by Udayakumar et al. [2], who
percentage in this study. The pathophysiology of this reported sparse scalp hair in 11%, sparse body hair in
phenomenon is related to the proximal half of the nail 30%, and lusterless hair in 16% of their Indian patients.
appearing white because of edema associated with a Also, Hajheydari et al. [3] reported sparse scalp hair in
dilated capillary network and the other half of the nail 10%, sparse body hair in 9%, and lusterless hair in 2%
bed appearing normal [28]. of their Iranian patients. The higher percentage of hair
changes in the Egyptian patients detected in this study
Koilonychia was observed in 29% of CRF patients in in comparison with Indian and Iranian patients may be
this study. Our results were in agreement with those of because of the racial variation in hair density [7].
Sultan et al. [7], who reported koilonychia in 39% of
their patients. However, Onelmis et al. [29] reported This study detected no statistically significant relation
koilonychia in 19% of their CRF patients on HD. between the onset of hair manifestations in patients
This difference may be because of the fact that the with CRF on regular HD.
prevalence of koilonychia increased with increasing
HD duration [3]. The most common oral mucosal manifestation in
this study was xerostomia, found in 46% of patients.
Splinter hemorrhage was present in 15% of the patients This is in agreement with Malekmakan et al. [32] and
in this study, which is in agreement with Sultan Onelmis et al. [29], who reported it in 48.6 and 40%
et al. [7], who observed it in 16% of their patients. In of their patients, respectively. However, Udayakumar
contrast, Martinez et al. [23] and Udayakumar et al. [2] et al. [2] found xerostomia in 31% of their patients and
reported splinter hemorrhage in 7 and 5% of their the lower percentage may be because of the inclusion of
patients, respectively. Splinter hemorrhage was widely fewer hypertensive patients (18%) and administration
considered to result from microtrauma [30]. of antihypertensive drugs. Dry mouth in HD patients
is a multifactorial phenomenon that may be because of
Subungual hyperkeratosis was found in 12% of water restriction, excessive water intake may increase
patients in this study, which is in agreement with the risk of elevated blood pressure and heart failure,
Udayakumar et al. [2] and Tercedor et al. [31], who and low saliva flow, minor salivary glands parenchymal
reported subungual hyperkeratosis in 12% of their fibrosis and atrophy, medication use (fundamentally
studied patients. In contrast, Salem et al. [25] observed antihypertensive agents), and oral breathing secondary
subungual hyperkeratosis in 3% of their patients. to lung perfusion problems [33].
Onycholysis was observed in 10% of the included Macroglossia and teeth markings were detected in 43%
patients, which is in agreement with Salem et al. [25] of the patients in this study. This result is in agreement
and Onelmis et al. [29], who reported onycholysis in with that of Sultan et al. [7], who found it in 42% of the
10 and 9% of their patients, respectively, whereas both patients studied, but it was different from the results
Sultan et al. [7] and Hajheydari et al. [3] reported detected by Udayakumar et al. [2], who reported it in
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