Tropical ulcer in Zambia

132 TRANSACT~NS

OF THE ROYAL SOCIETY OF TROPICAL MEDICINE

Tropical Dept.

of Medical

Microbiology,

AND HYGIENE

ulcer

(1986)

80,

132-137

in Zambia

D. C. ROBINSON AND R. J. HAY London School of Hygiene and Tropical London

WClE

Medicine, Keppel

Street,

7HT

Abstract The clinical featuresof 86tropical ulcersin 64subjectsseenin hospitalsand rural clinicsin Zambia are described. Pre-ulcerativelesionswere identified. 85% of the patientscamefrom subsistence farmingfamilies.Few wore shoesbut morethan a quarter woreclothesbelowthe kneeat sometime. No associationwith dental cariesor gingivitis was observed.Ulcers were seenin someclinically well-nourishedindividuals of appropriate weight for height and occurred in areaswhere animal protein was plentiful. Family studies showed that concurrent caseswithin householdswere uncommon. Introduction

Tropical ulceris a painful, distressinganddisabling condition of the lower leg affecting mainly young adultsand older children. It is easyto recognizein its acute stagealthough it lacks a more preciseclinical definition than that suggestedby LOEWENTHAL (1963): “an acute specificlocalisednecrosisof skin andsubcutaneous tissuesendemicin but not confined to the tropical regions.After the acutestagea chronic non-specific ulcer may persist”. It is not known whetherthe condition is identicalin the many partsof the tropics and subtropicsfrom which it has been reported and little is known about predisposing causes,incidence or mode of spread. This paper reports clinical features of tropical ulcer in rural Zambia with someobservationson socialand family background. Methods and Subjects

Patientswith tropicalulcerswerestudiedat St. Francis Hospital,Katete (EasternProvince)and in the Zambia FlyingDoctorServiceruralclinicsin afurthersixprovinces at altitudes between 500 and 1200 metres. Information was obtained by questionnaire aboutthe patients’socialand

economic circumstances, in some cases confirmed by ahome

visit. A full clinical history was taken and the patients were examined, weighed and measured. Results

The 64 patients,33male,31female,had 86tropical ulcersat the time of examination.44 of them (69%) werein their seconddecadeandonly onewasthought to be over the age of 30. There were two children about the ageof five but none younger. Sex and age distribution is shown in Fig. 1. 20 patients (9 male, 11 female)or in the caseof younger children, their accompanyingrelatives rememberedan injury, often trivial or vague,occurring at aboutthe time of the onsetof the ulcer. Of these11 describedan injury while farmingor walking through the bush. Only one recalleda precedinginsectbite at the site of the ulcer. 35 (55%) describeda preulcerative lesion,the patient or his interpreter using the word pimple, boil or blister. Table I illustratesthat more than half thought that the interval betweenthe appearanceof the ulcer and attendanceat a clinic or hospital was less than a month. Eight rememberedhaving a previousulcer, a history that wasconfirmedin eachcaseby a lower leg

scar. Another three patients described recurrent ulceration at the site of an apparently healedulcer. Judged by questionnaireresponsesand visits to villagesand homesmostof the patientslived in rather similar circumstances.51 (85%) camefrom subsistencefarming familiesliving asti rule in villagesof 10 to 100 housesmade of dried mud or locallv made bricks and roofed with thatch. The hous& were typically divided into two to four rooms(average2.4) with a separateoutside kitchen. There were on average6.3 individuals per household. At the timeof examination93%of the patientswere barefoot and 73% had bare lower legs. A small minoritv (12%) saidthev usuallv or sometimeswore shoes6~; many more (27%) usually or sometimes worelongtrousersor a dressbelowthe knee.27 (42%) of the patients were schoolchildren. They nearly alwayswent to schoolbarefoot; as uniform the boys wore shorts and the girls a dressto the knee. At about puberty children often sleepin separate huts sharingwith oneor moreindividualsof the same sex: 17 of the patients had these arrangements. Nearly all helpedto someextent with the farming, the womenmore than the men, the adultsmorethan the children. In many of the villages poultry and domesticanimals(pigs,cats, dogsandgoats)areto be seenin closeproximity to human dwellings.But in tsetsefly areaswhere tropical ulcers are alsoprevalent, no domesticanimals,apart from a few cats, are kept in the villages. 14patientsfrom 57 familiesgavea positive history of a leg ulcer in a relative of whom 13 were siblings (five included in this series).Sevenof the 14 were living in the samehouseholdas the index caseand developedan ulcer concurrently. Thesesevensecondarv caseswere onlv a smallorooortion (2.3%)of the 29gpeopleliving ai the timhwiih the patientsin the 57 households.These findings are summarizedin Table II. Most of the ulcers were small, only 17 of the 86 (20%) had a maximum diameterof more than 3 cm and none more than 6 cm. They were all below the knee, 56 (65%)wereof the lower third of the leg and, of these, 36 (64%) were on the anterior and lateral aspects.Many were nearly circular with a raisededge and a slough adherent to the ulcer floor (Fig. 2). Nearly all were initially painful and tender, the pain often bad enoughto immobilize the patient. Typical

133 DISTRIBUTIOPJ

BY AGE AND SEX

16 14 12 10

8 6

4 2

C

o-4

5-9

Fig. 1. Distribution

Table I-Length of history, ple ulcers in 64 patients

recurrence

lo-14

15-19

and multi-

Remembered interval between onset of ulcer and first presentation at clinic or hospital

Lessthan a month A month 1 or more Uncertain

Recurrence

Pasthistory of tropical ulcerwith confirmatoryscar 8 3 History of recurrent ulcerationat samesite 11 Multiple

ulcers present at time of examination: 16

patients (25%) No. of ulcers 1 48 (75%)

Unilateral

2 13 (20%) 3 2 (3%) 4 1 (2%)

7

20-24

Age lyeat-s: by age and sex of 64 patmm

Bilateral

6

7

i

: 9

25-2930-34 with rrop~al

ulcer.

ulcersalsoshowedsurroundingoedemaand bleeding from the base although these appearanceswere modified by treatment and in chronic lesions.Sometimes there was marked hyperpigmentationof the skin just beyondthe edgeof the ulcer. Healedulcers left a scar which was typically discoid and often depressed(Fig. 3). Small superficialpapulesor pustulesa few millimetersin diameteroften with surroundinghyperpigmentation were frequently seenon the lower legs, somecloseto the presentingulcer but often remote from it or on the other leg. Two patients, one of whom had had severalulcersin the past, pointed out such lesions on themselvesas ulcer precursors. They were characterizedby raisedlooseepithelium which waseasilyandpainlesslyremovedwith aneedle revealing a superficial ulcer without a slough, less than a centimetre in diameter but larger than the original overlying papule (Fig. 4). 16 patientshad more than oneulcer at the time of examination occurring as often bilaterally as unilaterally (Table I). The history wasusually that the secondhad started a few days after the first. When two or moreulcersoccurredon the samelegthey were often widely separatedthough smalldaughtergravitational ulcers closeto and below the main ulcer as describedby MCADAM (1966) were also seen. Overt malnutrition was not a feature of these patientsthough many lookedimpoverishedand thin. Oedemawhen present was always confined to the

134

Fig.

TROPICAL

2. Acute

tropid

ulcer

on the anterior

aspect

of the ankle.

ULCER

The ulcer

IN

ZAMBIA

is nearly

circular,

the edge raised

Fig. 3. Two discoid scars on the anterior aspect of the right lower leg are the sites of previous tropical centre. The ulcer over the medial malleolus of the left foot shows a rim of hyperpigmentation.

ulcer.

and a slough

TYe lower

cove, s the floor.

scar is depressed

in the

Hyperpigmentatlc'

Exuding pus from !he cenW

Approximate extsnl of znde:lyirq u ce~

Fig. 4. A pre-ulcerative pustuleof the lower kg. Some purulenr material exudes from the centre. The loose, slightly raised eplthelium was easily and painlessly removed with a needle exposing a superficial ulcer less than 1 cm in diameter but larger than the presentiog lesion.

Table Male -

Female n = 22

I1 = 24

* l

f . .

:

A-

Lower of *desirable range

-Lower limit of desirable range

*

0

11rn1t

fi

r f

:

,"

. 00

-

t -20:;

5 . a

Key A Fenial i‘ A Gl:is l 0

RCl?S 3,J,,‘-

Fig. 5. The body mass (Quetelet) index (W/H’) of 46 patients with tropical ulcer. Children under the age of 10 are charted separately. The upper arrows indicate the suggested lower limit of the ‘desirable’ range in American adults. The lower arrows are 20% below this hmir.

II--Households

of tropical

ulcer patients

57 Householdstudied 361 No. of individuals 6.3 Averageno. per household No. of tropical ulcer patients 361 - 62 = 2;; Individualsat risk Individuals developingulcers 7 (2.3%) _^-..____II affected leg and maximal closeto the ulcer. Haemoglobulin estimationsin 26 patientsincluding all those suspected of anaemiaclinically wereall above10G%. The body mass(Quetelet)index (W/H*), wascalculatedin 56patients.As shownin Fig. 5 thereis a wide scatter. The indicesfor nine patients fell within the et ‘desirable’rangesetfor Americanadults(THOMAS al., 1976)while 20(43%)were20%or morebelowthe lower limit of that range. Information from the dietary history did not suggesta critical shortageof first classprotein in most cases. Of 53 out-patients questioned, 45 (85%) recalled eating fish or meat at least once in the previous week and 21 (40%) three times or more. There waslessfishingduring the rainy seasonbut the availability of meat did not appear to vary much according to season. There was no clinical evidenceof an association betweentropical ulcer and other skin or systemic disease and mostof the patientshadhealthy teeth and gums:53of 62 patientsexaminedhad no obvioussign of dentaldecayor gumdisease andno missingor filled teeth. Discussion

The sex incidence of tropical ulcer varies in different countriesand under different conditions:in publishedreportsthere is a higher incidencein males

136

TROPICAL

in Madras City (RAO et a1.,1949), in females in Uganda (LOEWENTHAL, 1963), in men in the towns and sugar nlantations of Paoua New Guinea but in women- of- the rural areas’ of the same country (KARIKS, 1957). In rural Zambia where both men and women work as subsistence farmers both sexes are about equally prone. This study confirms many previous reports that there is a predominance of patients in their second decade with sparing of children under the age of five and that the ulcers occur most commonly on the anterior and lateral aspects of the lower leg. These features are all compatible with the concept of trauma as a predisposing cause in a rural population who habitually go barefoot with unprotected lower legs. But the evidence that a breach of skin continuity is necessary for the development of a tropical ulcer is far from conclusive. Children under the age of five are very active about the villages and certainly prone to leg trauma yet they rarely develop ulcers. MCADAM (1966) was able to induce ulcers experimentally in‘ healthy volunteers by bathing untraumatized skin in ulcer pus. Of the patients reported here less than a third recalled a history of injury, a few wore shoes and more than a quarter at least sometimes wore long trousers or a dress below the knee. That multiple and recurrent ulcers are common suggests as, PANJA (1945) pointed out 40 years ago, that the condition confers little or no immunity, a view that is supported by the experimental evidence: nroduction of an ulcer bv .DUS inoculation is as likelv to be successful in a patient with an active lesion as in a healthy volunteer (SMITH & ELMES, 1931; McADAM, 1966). The papules, pustules or vesicles described by patients as preceding ulceration and observed here in association with established ulcers closely resemble the experimental lesions described by McAdam. It may be that only a few of the lesions develop into ulcers, a question needing further investigation if the pathogenesis is to be understood and ulceration prevented by early treatment. Many of the patients were seen in remote, thinly populated areas where travel was difficult and the clinics often many miles away. Yet the length of history before first presentation was relatively short and most of the ulcers were small and uncomplicated. The occasional outbreak of tropical ulcers sometimes amounting to an epidemic (Fox, 1920; PANJA, 1945; KUBERSKI & KOTEKA, 1980) is not understood. Nor is the often reported increased incidence related to the rainy seasons in areas where the condition is endemic. The role of flies as potential vectors has been postulated (FOX, 1920) as has been shown to occur in yaws (SATCHELL & HARRISON, 1953). Flies, mainly Musca sorbens, were much in evidence in the villages visted and very prone to settle on the ulcers even when they had been dressed. But the apparent low infectivity of the ulcers in the patients studied suggests that flies are probably not important as vectors under these rural conditions. Many authors have reported the presence of fusiform bacteria and spirochaetes in smears. The discovery that some diseases of domestic animals such as swine dysentry are caused by anaerobic spirochaetes (HARRIS & KINYON, 1974) raises the interesting possibility that tropical ulcers might arise from animal

ULCER

IN

ZAMBIA

infection. But the absence of domestic animals from the villages in tse-tse fly areas where tropical ulcers are prevalent makes this unlikely. Because of similarities with bacterial flora seen in Vincent’s angina, the human mouth has been suggested as a source of infection. CLEMENT (1936) observed a relationship between tropical ulcer and suppurative gingivitis but no such association was observed in these Zambian patients, almost all of whom had very healthy gums and teeth and they all denied applying saliva to their sores. Nutritional deficiency has been postulated as an important predisposing factor because malnutrition and tropical ulcers are commonly associated (BURNIE, 1931) and because outbreaks have occurred in famine conditions (PANJA & GHOSH, 1944) and prisoner-ofwar camps (SMYTH, 1946). Tropical ulcers have been claimed to be rare where fish is nlentiful (LOEWENTHAL, 1963). Not unexpectedly in a Zambian rural population of subsistence farmers many of the patients described were thin, some very thin, as shown in Fig. 5. But a significant minority were clinically well nourished and not underweight, including some patients who suffered from recurrent ulcers for years. Many of the patients had ready access to fish. For example, of 13 patients seen at four clinics in the River Luapula basin where tropical ulcers are common only one had not eaten fish in the previous week and seven had had fish three or more times in the same period. These findings and the rarity of tropical ulcers in children under the age of five suggests that nutritional deficiency may not be a prerequisite or a major aetiological factor. Acknowledgements

We are grateful to Dr. V. R. Chelemu, Director of the Zarnbian Flying Doctor Service for much help in making arrangementsfor one of us to seepatients in rural clinics and to Dr. P. C. Lapsiwala for practical assistance. We thank Mr. James Cairns, Medical Superintendent of St. Francis Hospital, Katete,. for permission and facilities to study patients. This work was supported by a generous grant from the Royal Colleges of Physicians and Surgeons, the Liverpool School of Tropical Medicine and the London School of Hygiene and Tropical Medicine. References

Burnie, R. M. (1931). Observations on tropical ulcer. Afican

Medical

Joumal,

Wesr

4, 77-86.

Clements, F. W. (1936). Tropical ulcer with special reference to its aetiology.MedicalJoumal of Australia, ii, 615-644. Fox, E. C. R. (1920). Naga Sore. IndianJownal of Medical Research,

8, 694-698.

Harris, D. L. & Kinyon, J. M. (1974). Significanceof anaerobic spirochaetes in the intestines of animals. A&an 3ownal of Clinical Nutrkion, 27, 1297-1304. Kariks, J. (1957). Tropical ulcer amongstthe nativesof New Guinea.

Medical

Journal

of Australia,

ii, 346-350.

Kuberski, T. & Koteka, G. (1980). An epidemiccof tropical ulcer in the Cook Islands. American Journal of Tropical Medicine

and Hygiene,

29, 291-297.

Loewenthal, L. J. A. (1963). Tropical phagedeniculcer: A review. International Review of Tropical Medicine, 2, 267-285. McAdarn, I. (1966). Tropical phagedeniculcers in Uganda. ‘foumal

of the Roval

Colle.ee ofSu=eons

of Edinbuwh,

11,

-196-205.- - Panja,G. & Gosh, L. M. (1944). Report on the occurrence of Naga sore in Calcutta. Indian Medical Gazette, 79, 17-19.

Panja, G. (1945). Aetiology and treatment of ulcus tropicurn. Indian Joumal of Medical Research, 33, 11-16. Rao, V. R., Kini, M. G. & Subrahmanyan (1949). Tropical ulcers in Madras City. Indian Medical Gazette, 84,88-92. Satchel& G. H. & Harrison, R. A. (1953). Experimental observations on the possibility of transmission of Yaws by wound feeding Diptera in Western Samoa. Transactiuns of the Royal Society of Tropical Medicine and Hygiene, 47, 148-153. Smith, E. C. & Elmes, G. T. (1931). Experimental tropical

ulcer. West Affican Medical 3ouwd, 4, 87-91. Smyth, E. A. (1946). The treatment of tropical ulcer. 3oumal of the Royal Army Medical Corps., 87, 141-142. Thomas, A. E., McKay, D. A. & Cutlip, M. B. (1976). A nomograph method for assessing body weight. American Journal

Accepted

of Clinical

for

Nutrition,

publication

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