Fungal infect ions o f the nails in Western Australia

Rose McAleer Medical Mycology Laboratory, 267 St. George's Terrace, Perth, Western Australia

Abstract

Between 1963 and 1972, 986 fungi were isolated from the nails of patients in Western Australia. Three clinical types of infections in both finger and toe nails were studied. All 3 types occurred more commonly in adults over the age of 20. Multiple infections were relatively frequent. Two hundred and fourteen of the nail infections were caused by dermatophyte fungi. Trichophyton rubrum was the predominant aetiologic agent isolated from both finger and toe nails, T. mentagrophytes and other dermatophytes were involved to a lesser degree. Paronychia of the finger nails was common and mainly caused by C. albicans. Aspergillus species were the most frequent fungi grown from superficial white onychomycosis.

Introduction

As part of a 10 year study of superficial and cutaneous mycoses, a total of 986 fungal infections of nails were investigated. Nail infections have been studied in detail in some countries (2, 7, 8, 9, 10) but no previous work had been done on these diseases in Western Australia.

This report deals with both finger and toe nail infections of fungal aetiology. Aspects studied include the different clinical types which occurred, the relative frequency of the causal fungi, their epidemiology and their occurrence in relation to age and sex.

Materials and methods

specimens were collected. Standard techniques for collection and culture of

specimens were followed (1). Extra care was exer- cised in collection procedures to ensure accurate results. The specimens varied depending on the type and stage of the infection, and included were clippings, parings from the sides, base and centre of the nail, epidermal detritus and pus.

Microscopy was performed using Parker Quink stain with 30% KOH, and specimens were cultured on 2 Sabouraud's dextrose agar slopes (I), one with added cycloheximide 0.5 mg/ml and chloram- phenicol 0.05 mg/ml and the other with chloram- phenicol only added. Cultures were held at 26 ~ for 28 days before they were discarded.

Persons aged up to 14 years were classified as children and from 15 years upwards as adults.

Over 80 per cent of the patients studied were sent for investigation by dermatologists and medical practitioners in the Metropolitan ai'ea of Perth, and the rest were examined indirectly from specimens sent by medical practitioners in country areas throughout the State. All patients had nail prob- lems suspected to be of fungal aetiology, no survey

Results and discussion

Clinical features

Three main clinical types of nail infections were seen in Western Australia. Onychomycosis of both

Mycopathologia 73, 115-120 (1981). 0301-486X/81/0732-0115 $1.20. �9 Dr. W. Junk B.V. Publishers, The Hague. Printed in the Netherlands.

116

finger and toe nails due to dermatophyte fungi showed the usual range of symptoms and involved toe nails more frequently than finger nails. Paro- nychia type infections of the finger nails were of frequent occurrence and most commonly affected the index and middle fingers of the most used hand. Superficial white onychomycosis most frequently affected the great toe nails.

This third type of infection usually gave the nail a white matted appearance resembling paper-bark. It commenced with small opaque white spots on the surface of the nail (Fig. l) which gradually spread and joined, often to include the whole nail (Fig. 2). These 2 figures are from the right foot of the same patient. The title 'paper-bark effect' was adopted by me in 1966 to describe this clinical entity, because of its appearance and the way tissue could be pared off with a blade in strips reminiscent of peeling paper bark.

Predominant organisms involved in Western Australia

Fungi responsible for these 3 clinical types were: a) Dermatophytes. There were 214 dermatophyte

infections of nails over the 10 year period, 62 infections of the finger nails and 152 of the toe nails. Trichophyton rubrum was the chief dermatophyte causing nail infections (Table 1), followed by T. mentagrophytes.

T. rubrum caused 75.8% of the finger nail

Fig. 1. White spots in the right great toe nail infected with Cephalosporium species.

Fig. 2. Total nail involvement with superficial white onychomycosis produced by Aspergillus species on the third right toe nail of the same patient.

infections; T. mentagrophytes and T. tonsurans 8.1% each, and M. eanis and E. floccosum caused 4.8% and 3.2% respectively. For toe nails the proportions were somewhat different. T. rubrum was the causative agent in 63.8%, next T. mentagrophytes 29.6%, T. tonsurans 3.9% and then E. floccosum and M. canis each with 1.32%.

b) Candida species. In paronychial infections of the fingernails C. albicans was most frequently isolated, 58.6% of the total, followed by C. parapsilosis 24.6%, C. tropicalis 6.5%, C. guiltier- mondii 5.3% and C. krusei 5.0%. The most common Candida species isolated from toe nails was C. parapsilosis 40% then C. guilliermondii 25.7%, C. albicans 17.1%, C. krusei 12.9% and C. tropicalis 4.3%.

An interesting feature with paronychia infections of the finger nails was the relative frequency of mixed infections involving Candida and Asper- gillus niger which were isolated together from 43 patients. From one patient a heavy growth of Candida and Cladosporium were isolated together from both finger and toe nails. The significance of this was not known.

The green-nail usually attributed to infection of the finger nails with Pseudomonaspyocyanea, was most often caused by a Candida species and when of bacterial origin the pathogen was usually Staphylococcus aureus.

e) Non-dermatophyte filamentous fungi were the

Tab

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spec

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each

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63-1

972.

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rich

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ton

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F

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F.

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na

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nail

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nail

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oe

F.

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F

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1963

3

9 1

6 1

1964

5

7 I

~7

3 19

65

1 6

2 2

1966

2

6 5

I 19

67

3 9

3 19

68

5 12

6

1969

10

7

5 1

1970

7

.12

1 3

1 19

71

8 13

1

5 1

1 19

72

3 16

1

3

1 2

1 1

53

6 6

15

59

21

23

4 6

17

29

21

20

11

3 8

23

19

50

11

2 12

52

23

70

8

4 12

74

20

70

4

5 19

75

23

72

5

10

13

82

18

81

6 9

16

90

22

70

8 12

20

82

28

72

7

5 20

77

27

TO

TA

L

47

97

5 45

5

6 2

2 3

2 58

1 70

62

15

2 64

3 22

2

Tab

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par

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Age

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1-10

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1 8

11

1 2

10

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3 2

1 1

11

20

1 2

4 37

4

5 43

2

5 2

4 2i

30

5

5 7

93

I 9

13

107

19

8 3

5 2

31_4

0 10

5

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103

2 6

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114

23

7 10

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-50

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7 6

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116

4 24

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6 26

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Age

Un

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1 3

7 43

7

8 53

6

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3 4

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15

7

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32

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9 59

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118

main cause of superficial white onychomycosis or paper-bark effect, although T. mentagrophytes was associated with this condition on several occasions. All of these fungi formed numerous hyphae in the nail plate, so it is possible that they were actually parasitizing the nail. Five different genera of non- dermatophyte fungi were isolated from these nails, chief of which was Aspergillus 43%, Fusarium 21.6%, Cephalosporium 11.8% and Penicillium 7.8%. Scopulariopsis was not isolated.

Microscopy and culture

The type of fungal elements seen in the direct microscopy varied with the type of fungus involved. Dermatophyte infections were usually indicated by the presence of fine septate, sometimes distorted mycelium and arthrospores. Candida infections showed pseudomycelium and blastospores and non-dermatophyte filamentous fungi were repre- sented on most occasions by broader empty more markedly septate mycelium (Fig. 3), or by mycelium with many chlamydospores (Fig. 4).

Sometimes repeated microscopic examinations were necessary to find fungal elements in nail. Similarly repeated cultures were done when the direct microscopic examination was positive and cultures failed to grow. Positive microscopy with failure to obtain growth occurred in 0.5% of finger nails and 2.3% of toe nail specimens. The mycelium present in each case indicated a dermatophyte infection.

Fig. 3. Mycelium of Aspergillus in the nail seen in Fig. 2.

Fig. 4. Mycelium and chlamydospores of Cephalosporium in the nail seen in Fig. 1.

The problem of negative microscopy with positive culture was more marked. From dermato- phyte infections 4.8% of finger nail and 13.1% of toe nail specimens had negative microscopy. Davies (4) had a comparable figure for nails, i.e. 15%. In non- dermatophyte filamentous infections of the finger nails, 56 of the 70 isolates were involved in mixed infections with Candida. Non-dermatophyte fila- mentous fungal infections of the toe nails had positive direct microscopy in 60.8% of the total and all had growth from more than 5/20 of the inocula. This figure has been recommended by English (6) as being the desirable amount of growth to prove infection.

A high proportion of nails from which Candida was isolated were negative on direct microscopy, 52.5% for finger nails and 47.1% for toe nails, this was partly due to the difficulty of seeing yeast cells in nail when no pseudomycelium was present.

Aetiology of nail infections

The comparative environments of finger and toe nails were so different in .our shoe-wearing population that one would expect different aetiological agents to predominate in each case. Although the same causal organisms occurred in each location they varied in their importance, most likely due to the influence of their local environment. The toe nail environment seemed more favourable for growth of filamentous fungi.

There was frequently damage to nails from constantly wearing shoes and the feet of many patients were moist for at least 12 hours each day.

Dermatophyte infections occurred 21/z times more frequently in toe nails than in finger nails. T. rubrum occurred twice as frequently and T. mentagrophytes 9 times more frequently. This latter would be expected, as T. mentagrophytes is associated more often with feet than with hand infections.

Candida infections were much more common in finger nails that had been frequently immersed in water and detergents than they were in toe nails, despite the humid environment of the latter. Damaged finger nails absorbed moisture and stayed wet for many hours in persons frequently wetting their hands.

It was probable that the damage caused to toe nails by constant pressure of footwear eventually made them susceptible to invasion by non- keratinolytic filamentous fungi as these invasions were more common in adults over the age of 30. These fungi are said to take advantage of partial dematuring of keratin by some previous disease or t rauma (6).

Epidemiology o f nail infections

The majority of patients had only some finger or toe nails affected and other nails normal. Also there was frequently only part of the hand or foot, i.e. nails, toes, toe spaces or soles involved without infection spreading to adjacent tissue. This indicated that some t rauma was necessary before. infection developed.

There was an obvious association between finger nail and hand infections and between feet and toe nail infections for dermatophyte fungi particularly T. rubrum. And infections of feet and toe nails were more common in adult males than were hand and finger nail infections.

In our population more males then females participated in sporting activities and therefore had greater contact with communal bathing facilities. Men wore closed footwear most of the time whereas many women wore open sandals for at least 5 months of the year. These factors influenced the spread of infection and the more frequent occurrence in males of toe nail infections.

Drills have been used in Western Australia for

119

management of all types of thickened nails for approximately 12 years. Suction equipment on drills has only been introduced in the last 3 years. It is possible that dust created by drilling and perhaps inadequately sterilized drills could have con- tributed to spread of infections in the more elderly patients who attended chiropodists.

Nail infections in relation to age and sex

Nail infections occurred in both men and women but were rare in children (Table 2). The age with the greatest number of infections varied depending on which group of fungi were involved but on the whole, infections in finger and toe nails became more common in patients over the age of 20.

Dermatophyte infections occurred with equal frequency in the finger nails of males and females but Candida and non-dermatophyte filamentous fungi were 6 times as frequent in females. Toe nail infections due to dermatophyte fungi occurred twice as often in males but both other fungal groups were of almost equal frequency in each sex.

Seasonal variations

Most of the nail infections seen were long term diseases and patients usually had the infection many months before being tested by th e laboratory. It is unlikely that any climatic influence can be established because infections of the nails were more influenced by local environment of the hands or feet than by climate.

Monthly variations in numbers of infections did occur (Fig. 5) but this could not be seen to be the influence of climate. Numbers of toe nail infections reached a peak at the end of spring but then dropped and stayed low during the summer

100,

80.

60,

40, ,,=,

:~ 20. .=

- - F I N G E R NAIL - - - T O E NAIL

Fig. 5. Combined monthly variations of fungal isolates from finger and toe nails.

120

months. Finger nail infections had 2 peaks, one in winter (August) and the other at the end of spring (November), the curve for finger nails really depicts Candida infections as there were too few dermatophyte infections to make any impact.

Multiple infections

Multiple infections involving the nails were common and occurred on 46 occasions with finger nails and 127 with toe nails. The areas most commonly infected in association were the hands with finger nails in 22 patients, and the feet with toe nails in 83 patients. Ih some cases 3 or more different areas of the body were infected with the same fungus. Finger and toe nails were both infected with the same fungus on 21 occasions.

7". rubrum was the fungus most commonly causing multiple infections and was responsible for 26 of these infections when finger naris were involved and 80 with toe nails.

Mixed and concurrent infections

Mixed dermatophyte infections were rare and occurred on one occasion with finger nails, and one with toe nails. In both cases T. rubrum was one aetiologic agent and occurred with T. mentagro- phytes in the former and M. canis in the latter case. More mixed infections were observed when a Candida species was involved with either a dermatophyte, or in paronychia of the finger nails wi th one of the non-dermatophyte filamentous fungi; in 43 patients with Aspergillus niger.

Concurrent infections were uncommon and occurred 6 times in the finger nail series and 9 in the toe nail.

Conclusions

Dermatophyte fungi although prevalent in our community infected nails relatively infrequently in this series when compared with the infection rate on some parts of the body. They occurred almost 21/2 times as often in toe nails as in finger nails. The only fungal infection of the nails which was common in Western Australia was paronychia of the finger nails mainly caused by Candida albicans.

Tinea unguium does not seem to be increasing in Western Australia. The numbers of infections recorded remained constant (Table 1) over the 10

years despite the fact that the numbers of patients examined increased annually.

Tinea of the nails was mainly caused by anthropophil ic dermatophyte species and was frequently found in association with a cutaneous infection of the nearby skin. T. rubrum was the most common of these fungi infecting nails in Western Australia. This fungus was also the most frequent aetiologic agent of tinea unguium in England (5), the U.S.A. (3), Canada (7), Romania (2), Norway (9), and Mexico (8). In this series it was responsible for 67.3% of the dermatophyte nail infections over the 10 year period 1963-1972.

Acknowledgements

The author would like to thank Professor N. F. Stanley for criticising this paper, the staff of the State Health Laboratory Services Medical Mycol- ogy Laboratory for technical assistance, the Audio- Visual Section for photographic and artistic assistance and the Commissioner of Public Health and Medical Services, Doctor J. C. McNulty, for permission to publish.

References

1. Ajello, L., Georg, L. K., Kaplan, W. & Kaufman, L., 1963. Laboratory Manual for Medical Mycology, Public Health Service Publication No. 994. U.S. Government Printing Office, Washington, D.C.

2. Alteras, I., 1971. A short review on the onychomycoses by dermatophytes in Romania. Mycopathologia 45:113 117.

3. Blank, H., Smith, J. G., R'oth, F. J. & Zaias, N., 1959. Griseofulvin for the systemic treatment of dermatomycoses. J .A.M.A. 171: 2168-2173.

4. Davies, R. R., 1968. Mycological tests and onychomycosis. J. Clin. Path. 21: 729-730.

5. Davies, R .R . , Everall, J . D . & Hamilton, E. 1967. Mycological and clinical evaluation of griseofulvin for chronic onychomycosis. Br. Med. J. 3: 464-468.

6. English, M., 1976. Nails and fungi. Br. J. Dermatol. 94: 697 -701.

7. Fischer, J. B. & Wrong, N. M., 1952. Fungous infections of the skin, hair and nails. Can. Med. Assoc. J. 67:398 403.

8. Gonzfiles-Ochoa, Orozco, A. & V. C., 1974. Frequency of occurrence of principal dermatophytoses and their causative agents observed in Mexico City. Internat. J. Dermatol. 13: 303-309.

9. Reiers61, S., 1962. Mycologic investigation of diseased nails and skin in 131 patients. Acta. Pathol. et Microbiol. Scand. 54: 30-38.

10. Walshe, M. M. & English, M. P., 1966. Fungi in nails. Br. J. Dermatol. 78: 198-207.