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. 2022 Apr 22;8(5):368–375. doi: 10.1159/000524257

Nail Changes in People Living with Human Immunodeficiency Virus: Observational and Cross-Sectional Study in a Third-Level Hospital

Luis R Flores-Bozo a, Silvia Méndez-Flores a, Valeria Olvera-Rodríguez a, Josune Echevarría-Keel a, Lilly Esquivel-Pedraza a, Andrea Rangel-Cordero b, Pablo F Belaunzarán-Zamudio b, Judith G Domínguez-Cherit a,*
PMCID: PMC9485993  PMID: 36161090

Abstract

Introduction

Nail changes in people living with human immunodeficiency virus (HIV) have been scarcely reported. The aim of this study was to establish the frequency and characteristics of nail alterations observed in adults with HIV infection in a third-level hospital in Mexico.

Method

Observational and cross-sectional study carried out in 205 patients receiving care at the HIV/AIDS Clinic of the Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán (INCMNSZ) in Mexico City. We performed a nail and iconographic assessment of both hands and toenails. We collected information of demographic and clinical variables, as well as drugs use, and antiretroviral treatment used by the participants through a questionnaire and from medical records. We performed direct cytological examinations and nail mycological cultures in participants with symptoms of onychomycosis.

Results

The participants were predominantly male patients (91.2%), with a mean age of 41 (range 21–78) years, under antiretroviral therapy (91.2%), with a suppressed viral load (78.5%) and mean CD4+ lymphocyte count of 379.5 (range 20–1,162) cells/μL. Fitzpatrick's IV phototype was prevailing in the studied population (70%). Nail changes were documented in 72.2% of the patients; being pigmentary changes (37.1%) and trauma (30.7%) the most frequent. Onychomycosis was observed in 26.3%; with total dystrophic onychomycosis as the most frequent clinical variant (68.5%). We obtained fungal isolates in 59.3% of participants and Candida parapsilosis was the most frequent of these (37.5%).

Conclusions

We observed a high prevalence of nail changes with very diverse etiology, as well as a variety of nondermatophytic yeasts and molds isolates associated with cases with onychomycosis. These findings reinforce and confirm the need for routine nail examination and stress the importance of medical personnel working with people living with HIV to have broad knowledge of nail pathology.

Keywords: Nail, Nail disorder, Human immunodeficiency virus, Onychomycosis, Nail fungus

Introduction

There are several mucocutaneous changes or specific skin diseases associated with human immunodeficiency virus (HIV) infection [1]. The study of the nail in people living with HIV has aroused a keen interest in recent years. Nail changes have been described in up to 67% of people with HIV [1]. Paradoxically, combined antiretroviral therapy (cART) has significantly increased the incidence of some infectious and noninfectious nail conditions. Longitudinal melanonychia, leukonychia, transverse lines, onychoschizia, and clubbing are the most common reported alterations [2, 3].

Onychomycosis is an invasive fungal infection of the nails, regardless of the specific etiologic agent. This clinical entity represents one of the early manifestations of HIV infection with an estimated prevalence of 10–44% [4, 5]. Nondermatophyte molds (NDMs) account for 2–12% of onychomycosis, with variations depending on the population and geographic area studied [4]. Frequencies four times higher have been reported for people with HIV [6, 7]. The NDM group most frequently isolated in onychomycosis samples corresponds to yeasts, and within these, Candida parapsilosis has been described as the main etiologic agent in people with HIV [8].

Nonetheless, onychomycosis in people with HIV can be caused by a wide range of species, including Aspergillus spp., Scopulariopsis spp., Scytalidium spp., Rhodotorula spp., Rhizomucor spp., and Fusarium spp. [9, 10, 11, 12, 13, 14, 15, 16]. This has been related with more aggressive clinical presentations, including greater involvement of the nail plate surface, the number of compromised nails (including fingernails), and treatment refractoriness [17]. On the other hand, it has been noted that the clinical stage and the CD4+ lymphocyte cell count partly determine the development of onychomycosis, as is generally seen with a CD4+ count of 450 cells/mm3 [18]. Therefore, the presence of onychomycosis may be a visible marker of the immunodeficiency level [18]. Total dystrophic onychomycosis (TDO) and distal and lateral subungual onychomycosis (DLSO) are the major patterns observed in people with HIV, although proximal white superficial onychomycosis and superficial white onychomycosis represent the most characteristic variants [19, 20, 21].

Although the incidence of onychomycosis has decreased in patients living with HIV/AIDS after the introduction of cART and the prophylactic use of antifungal agents when indicated, this disease constitutes a significant source of morbidity [17, 18, 19, 20, 21]. The study of nail changes in people living with HIV/AIDS, its association with their immune status, phototype, and other environmental factors, such as occupation and traumatic injuries, represent an unexplored field. Hence, the objective of this study was to describe the frequency and characteristics of such alterations among people living with HIV receiving medical care in a tertiary level hospital in Mexico City.

Materials and Methods

We conducted an observational and cross-sectional study to evaluate the prevalence of onychomycosis and their etiopathological and clinical variants among people living with HIV at the Immune-Infectious Diseases Ambulatory Clinic at the Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán (INCMNSZ) in Mexico City, over the period July 1, 2015, to July 13, 2017. Patients were selected by consecutive and convenience sampling. We included adult patients (>18 years), who had a CD4+ lymphocyte cell determination and an HIV viral load measurements in the previous 3 months. Informed consent was obtained in order to participate in the current study. This study was approved by the INCMNSZ Ethics Committee (DER-1475-15/15-1).

Patients with any other known cause of immunosuppression, either primary or secondary were excluded, as well as those who had received topical or systemic antifungal therapy during the last 6 months. We reviewed the medical records, while clinical, pharmacological, and laboratory variables were documented through a questionnaire. The phototype was determined according to the Fitzpatrick classification [22]. A standardized nail and iconographic assessment of the fingers and toenails was performed. Changes in surface, color, thickness, and curvature of nail plates were recorded and properly cataloged according to descriptive terms and etiology as proposed and established by other authors [2, 3, 23].

After standardized examination, those cases with clinical findings suggestive of onychomycosis (including subungual hyperkeratosis, dystrophy, chromonychia, and onycholysis) were tested for cytologic examination and culture identification. The sample was obtained by scraping of subungual hyperkeratotic debris. The scrapings of infected nails were collected by sterile curette; discarding the scale obtained in the first curettage to reduce the risk of sample contamination. The sample was processed for direct examination with 15% potassium hydroxide and inoculated on Sabouraud dextrose agar (SDA) at 35°C in test tubes for 4 weeks. Cultures with filamentous molds or yeast growth were isolated for correct identification. For yeasts, the germ tube and sensitivity test were performed using the VITEK identification system [24]. Filamentous fungi were identified by macroscopic and microscopic morphology with lactophenol cotton blue staining. Given the condition of immunosuppression, all isolates were considered significant, with the possible role of contaminating fungi as pathogens and considering that the sample came from nails with morphological alterations.

Additionally, patients with onychomycosis were classified into the following groups based upon clinical appearance of fungal invasion on the nail plate, regardless of the etiological agent: TDO, DLSO, proximal white subungual onychomycosis, and superficial white onychomycosis.

We estimated sample size based on the precision of an estimate and calculated that 205 participants were necessary to obtain an accepted error (or precision) of 10% with a confidence interval level of 95%, assuming a normal distribution and frequency of nail abnormalities of 50%. The statistical program SPSS version 20.0 was used to collect and analyze the data. Descriptive statistics were performed, according to the sample size and distribution of the variables. Data variables are expressed as medians and frequency intervals and the frequency of the undetectable HIV viral load, in proportions.

Results

The main characteristics of the studied population are detailed in Table 1. Of the 205 patients, 148 (72.2%) had abnormal appearing nails. In this population of 148 patients, toenails were involved in 66 (32.2%) subjects, and fingernails in 22 (10.7%), while 60 (29.3%) had both fingernails and toenails affected. Seventy-six (37.1%) patients exhibited pigmentary changes, 63 (30.7%) traumatic onychopathy, 56 (27.3%) infectious processes, 2 (1%) inflammatory nail conditions, 2 (1%) tumor-associated changes, while 12 patients (5.9%) could not be classified in the previous categories. It should be noted that all abnormal findings on the same nail were recorded. For example, nails with onychomycosis and pigmentary changes.

Table 1.

General characteristics of 205 patients receiving care for HIV compared to the subgroup with onychomycosis (n = 54) in a third-level hospital in Mexico City (2015–2017)

Characteristics Onychomycosis patients (n = 54)
 All patients (n = 205)
n (%/range) n (%/range)
Sex
 Male 45 (83.3) 187 (91.2)
 Female 9 (16.7) 18 (8.8)
Age, years* 44.5 (27–74) 41 (21–78)
Fitzpatrick phototypes 0 (0)
 II 3 (5.5) 2 (1.0)
 III 39 (72.2) 34 (16.6)
 IV 12 (22.2) 144 (70.2)
 V 0 (0) 25 (12.2)
Antiretroviral therapy 51 (94.4) 187 (91.2)
CD4+ lymphocytes, cells/µL* 379.5 (20–1,162) 448 (1–1,481)
 Patients under cART (n = 187)* 393 (20–1,162) 470 (1–1,481)
 Patients without cART (n = 18)* 65 (45–1,10) 100 (14–602)
Viral load, copies/mL** 40 (40–363,926) 40 (40–2,437,113)
 <40 copies/mL** 45 (83.3) 161 (78.5)
 >40 copies/mL** 9 (16.7) 44 (21.5)
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cART, combined antiretroviral therapy.

*

Median (minimum-maximum interval).

**

Values expressed in proportions <40 copies/mL. The <40 copies/mL threshold is the cut-off used in our clinical practice to define adequate HIV suppression, since we use the Abbott m2000sp, RealTime HIV-1 instrument to measure HIV-RNA with a lower limit of detection of 40 HIV RNA copies/mL.

One of the major findings was the high frequency of longitudinal melanonychia, present in 52 (25.3%) patients. Among this group, 50 (24.4%) cases corresponded to racial melanonychia (shown in Fig. 1a), 1 case (0.5%) was associated with zidovudine therapy, while another case (0.5%) was consistent with pigmented squamous-cell carcinoma. We also observed leukonychia in 21 patients (10.2%), 13 of them corresponded to diffuse apparent leukonychia, 5 (2.4%) to leukonychia punctata, and 3 (1.5%) were consistent with Terry's nails. Erythronychia was noted in 10 (4.9%) patients, with 7 (3.4%) cases compatible to the diffuse form, 2 (1%) to longitudinal erythronychia, and finally, 1 (0.5%) to red lunulae.

Fig. 1.

Fig. 1

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Main nail changes observed in the study: racial melanonychia (a), TDO (secondary to C. parapsilosis) and onychocryptosis (b), traumatic onycholysis (c), median canaliform dystrophy (habit-tic deformity) (d), subungual pigmented SCC (e), and subungual KS (f). TDO, total dystrophic onychomycosis; SCC, squamous-cell carcinoma; KS, Kaposi sarcoma.

Traumatic etiology was identified in 63 (30.7%) patients. Onychocryptosis was present is 31 (15.1%) patients (shown in Fig. 1b), traumatic onycholysis in 23 (11.2%) (shown in Fig. 1c), subungual hematomas in 9 (4.4%), paronychia in 7 (3.4%), while 4 (2%) patients individually (0.5% each) showed consistent findings with splinter hemorrhages, anonychia, canaliform dystrophy (habit tic) (shown in Fig. 1d), and dorsal pterygium, respectively. History of previous trauma or inappropriate nail cutting was documented in 47 (23%) patients.

Additionally, both patients classified within the inflammatory nail conditions group had the diagnosis of psoriasis. Nail pitting was observed in 1 case, and oil spots in the other one. On the other hand, one of the 2 cases with tumor-associated inflammation corresponded to pigmented squamous-cell carcinoma (shown in Fig. 1e), while the other to Kaposi sarcoma (KS) (shown in Fig. 1f), both were corroborated by histopathological examination.

The cases that could not be classified in the previously described categories included onychorrhexis in 8 (4%) patients, brachyonychia in 2 (1%), and Beaus' lines in the last 2 (1%). Nail alterations related to infectious processes included periungual warts (as multiple periungual keratotic neoformations) and herpetic whitlow (with acute paronychia), each entity in 1 (0.5%) case.

A clinical diagnosis of onychomycosis was made in 54 (26.3%) patients (shown in Fig. 2). All of them (26.3%) presented chromonychia and pachyonychia; subungual keratosis was observed in 51 (24.9%) cases and onycholysis in 9 of them (4.4%). Fungi cultures were performed in all 54 patients. Onychomycosis of the toenails was observed in 34 (63%) patients, while involvement of both fingernails and toenails was documented in 20 (37%) patients. The morphological variants of onychomycosis and the fungal agents isolated are displayed in Table 2.

Fig. 2.

Fig. 2

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Clinical picture of onychomycosis and respective cultures: SWO secondary to C. parapsilosis (a), TDO due to Rhodotorula mucilaginosa (b) and Fusarium oxysporum (c), and DLSO secondary to Aspergillus niger (d). SWO, superficial white onychomycosis.

Table 2.

Morphological variants of onychomycosis and fungal agents isolated

Onychomycosis variant n % Positive cultures Etiological agent
Total dystrophic onychomycosis 37 68.5 23/37 Candida parapsilosis (8)
Candida sp. (3)
Penicillium sp. (3)
Trichosporon mucoide (2)
Candida guillermondii (2)
Rhodotorula mucilagi (2)
Fusarium oxysporum (2)
Candida albicans (1)
Aspergillus sp. (1)
Mucor sp. (1)
Scytalidium sp (1)
Geotrichum capitatum (1)
Hormonema dematioides (1)
Cryptococcus unigut (1)
Monilia sitophila (1)
Fusarium sp (1)
Distal and lateral subungual onychomycosis 15 27.8 8/15 Candida parapsilosis (3)
Mucor sp (2)
Candida sp (1)
Aspergillus niger (1)
Candida guillermondii (1)
Proximal white subungual onychomycosis 1 1.9 1/1 Candida parapsilosis (1)
Rhodotorula mucilagi (1)
Superficial white onychomycosis 1 1.9 0/1 No pathogen isolated
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The group of patients with onychomycosis was characterized by lower CD4+ cell count compared with the rest of the participants (379.5 cells/μL vs. 448 cells/μL). Positive direct examination with potassium hydroxide was noted in 41 (76%) patients. Fungi cultures were positive in 32 (59.2%) patients. Among this group, one pathogen was isolated in 25 (78.1%) cases, two pathogens in 5 (15.7%), and three pathogens in 2 (6.2%). Candida species was isolated in 20 (62.5%) subjects, and C. parapsilosis was the most frequently isolated microorganism (12 patients, 37.5%). No isolation of dermatophytes was obtained.

Discussion/Conclusion

The aim of this study was to analyze the frequency and characteristics of nail changes in a population of people living with HIV. Antiretroviral agents were administered in 91.2% of them, with adequate immunological response overall. The frequency of nail changes in our group was similar to the 67.7% reported by Cribier et al. [1]. Our work also shows that onychomycosis affects a considerable proportion of this population. Patients with onychomycoses exhibited lower CD4+ cell counts.

Pigmentary changes and traumatic processes were the most frequent nail findings. The notable occurrence of racial melanonychia was associated to skin phototypes of the examined population; with a clear prevalence of phototype IV according to the Fitzpatrick Skin Phototype Classification. Onychocryptosis and traumatic onycholysis were present in more than 10% of our patients, mainly because of inadequate nail cutting techniques. No other mechanical factor could be demonstrated. Both patients with inflammatory processes corresponded to psoriasis, a systemic immune-mediated disease with a higher incidence among people with HIV. We found the presence of two malignant tumors, which highlights the importance of nail exploration. Subungual KS is a very interesting finding. In this case, the patient presented with extensive cutaneous, mucosal, and visceral involvement, confirmed by histopathology. The prevalence of subungual lesions in patients with KS is unknown and is probably a consequence of the scant nail examination during the general physical examination.

As stated above, onychomycosis is a common disorder in people living with HIV. In this study we found a 26.3% prevalence of clinically diagnosed onychomycosis, which is lower than the 41% reported by Jimenez-Gonzalez et al. [25] in a similar setting in Mexico City. However, the prevalence of microbiologically diagnosed onychomycosis was very similar in both studies (15.6% vs. 17% found by Jimenez-Gonzalez et al. [25]). Consistent with previous studies, the predominant clinical presentation in our patients was TDO (68%) and DLSO (28%) [25, 26, 27, 28, 29]. The causative organism mainly isolated corresponded to Candida sp., specifically C. parapsilosis (62.5% and 37.5%, respectively), which correlates with recent reports of yeasts as common agents in nail infections in immunocompromised hosts, including people living with HIV.

NDM account for 2–22% of onychomycosis with variations depending on the population and geographic area studied [4, 17, 27]. We identified NDM as prevalent etiological agents, particularly Fusarium, Rhodotorula, Penicillium, and Aspergillus. However, dermatophytes remain the most frequent etiological agents of onychomycosis in most series [18, 22]. Jimenez-Gonzalez et al. [25] reported dermatophytes, including Trichophyton rubrum and Trichophyton tonsurans, as the second most prevalent causative microorganisms in people living with HIV receiving care at their third-level care center in Mexico City. In contrast, no dermatophytes were isolated in our study. This discrepancy could be attributed to differences in fungal culture procedures; in our institution, we routinely use SDA with 5% sheep blood medium for isolation of any yeast and phytopathogenic fungi, considering the degree of immunosuppression in most patients receiving care in our hospital. Most studies, including the aforementioned, used SDA supplemented with cycloheximide 0.04 g/L and chloramphenicol 0.05 g/L to inhibit NDM growth [30].

In conclusion, this study reinforces the need for systematic nail examination as part of routine care of people living with HIV as the prevalence of nail abnormalities other than onychomycosis is high in this population, and some of them could be related to the degree of immunosuppression. In order to recognize and offer prompt management, medical personnel involved in the care of people living with HIV should be aware of nail pathology and the tools and techniques (dermoscopy, imaging studies, nail clipping, cultures) available during workup.

Statement of Ethics

This study protocol was reviewed and approved by the INCMNSZ Ethics Committee (DER-1475-15/15-1). Written informed consent was obtained from patients to participate in the study.

Conflict of Interest Statement

The authors have no conflicts of interest to declare.

Funding Sources

The authors received no financial support for the research, authorship, and/or publication of this article.

Author Contributions

L.R.F.-B., S.M.-F., J.E.-K., and J.G.D.-C. contributed to review and analysis of the available literature; patient selection according to the inclusion criteria; physical examination; compilation of clinical pictures; clinical and statistical analysis; and manuscript writing. V.O.-R. contributed to review and analysis of the available literature; clinical and statistical analysis; and manuscript writing. L.E.-P. contributed to statistical analysis and manuscript writing. P.F.B.-Z. contributed to patient selection; evaluation of antiretroviral treatment schemes and immunological status for classification; statistical analysis; and manuscript writing. A.R.-C. contributed to processing of nail scales for direct examination and mycological culture, reading, and classification of the same. All the authors read and approved the final version for submission.

Data Availability Statement

All data generated or analyzed during this study are included in this article. Further enquiries can be directed to the corresponding author.

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Associated Data

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Data Availability Statement

All data generated or analyzed during this study are included in this article. Further enquiries can be directed to the corresponding author.

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