Barriers to Timely Diagnosis and Management of Breast Cancer: Observations from a Tertiary Referral Center in Resource Poor Setting

Abstract

Breast cancer (BC) is the most common cancer among females worldwide, with over 2 million cases diagnosed every year. In India, it is the most common malignancy overall (15.4%) and accounts for about 27% female cancers. Morbidity and mortality remain high despite improvements in BC therapeutics. Conventionally, a gap of more than 3 months between noticing symptoms and commencing treatment is considered delay in BC management. Delays make BC an important public health problem and lead to poor outcomes. This study aims to identify patient perceived barriers to BC management. A self-designed structured questionnaire consisting of questions pertaining to multiple aspects of BC presentation and management was prepared. The study was conducted from October 2017 to September 2018 and results were analyzed. A delay of 3 months or more was seen in 284 of the 435 patients (65.3%), among which 179 was patient delay, 69 due to provider delay, and 36 due to a combined contribution of both factors. Provider factors were associated with prolonged delay. Misdiagnosis at first consult was the most common factor perceived by patients as a barrier, followed by delay in referral, distance from hospitals, lack of information, financial constraints, and logistic issues. A significant patient and provider delay exists in BC management which prevents effective early therapy. Effective tackling of these barriers may result in the betterment of BC management outcomes. Robust screening, education of patients and providers, and awareness promotion and infrastructure development will be useful in this regard.

Breast cancer (BC) is the most common cancer among females worldwide, with more than 2 million cases diagnosed every year [1]. In India, BC is the most common malignancy overall (15.4% of all cancers) and accounts for 27.7% of all female cancers. It is also the leading cause of mortality among cancer-related deaths (12.11%) [1]. Historically considered a disease of the affluent, its incidence is now increasing in low and medium-income countries (LMIC). Mortality is higher in developing countries compared with developed countries [2]. This is partly attributed to delays in diagnosis, treatment, and advanced stages at presentation.

Conventionally, a gap of 3 months or more between noticing first symptom and start of treatment is considered as delay in BC management. It is further classified into patient delay and provider/system delay [3]. Patient delay is an interval of more than 3 months between noticing symptoms and first consult with a medical doctor. Provider delay is defined as an interval of more than 1 month between first consultation and starting definitive treatment [4]. Various barriers, along with lack of routine screening and primary preventive strategies, make BC an important public health problem. Delay in presentation and initiation of treatment leads to poor outcomes. Early detection and prompt treatment initiation likely improve the results.

Materials & Methods

This study was conducted in the Department of Endocrine & Breast Surgery, King George’s Medical University, a tertiary referral center in Northern India. A self-designed structured questionnaire consisting of questions pertaining to socio-demographic parameters, knowledge and awareness of BC, clinical findings, and patient perceived reasons for delay was prepared. From October 2017 to September 2018, 456 patients with histologically proven BC were approached and 435 among them completed the questionnaire. Previous medical records were verified to reduce recall bias. Categorical data were compared using chi-squared test or Fisher’s exact test. Variables with normal distribution were analyzed with ANOVA. Multivariate linear regression analysis was done to test the association of various factors with delay. Statistical significance was set at p > 0.05. Statistical analysis was done using SPSS software (v. 23).

Results

A delay of 3 months or more was seen in 284 of the 435 patients (65.3%). The time taken for presentation ranged from 2 weeks to 24 months (mean, 4.5; median, 4). Among patients with delay, the mean time of presentation was 6.13 months. Delay due to patient factors was seen in 179 (41.1%), while provider delay was seen in 69 (15.9%) and 36 (8.3%) had both the components (Table 1). Three patients in the study cohort were males and 155 were below the age of 40. About 82% of all patients (357) were rural residents. Only 61 patients belonged to upper or upper middle class (Kuppuswamy classification) (Table 2). About 68% patients presented with advanced stages (stages III and IV).

Table 1.

Delay statistics

Type	Total	3–6 months	6–12 months	More than 12 months
Patient delay	179 (41.1%)	145 (33.4%)	34 (7.9%)	0
Provider delay	69 (15.9%)	29 (6.7%)	39 (9%)	1 (0.23%)
Both	36 (8.3%)	3 (0.7%)	20 (4.6%)	13 (3%)

Table 2.

Demographics

Parameters (n)	Delay n (%)	No delay n (%)	p value
Age
< 40 years (155)	92 (59.4)	63 (40.6)	0.67
> 40 years (280)	192 (68.6)	88 (31.4)
Sex
Male (3)	3 (100)	0
Female (432)	281 (65)	151 (35)
Religion
Hindu (363)	235 (64.7)	128 (35.3)	0.452
Muslim (64)	45 (70.3)	19 (29.7)
Others (8)	4 (50)	4 (50)
Education
Illiterate (273)	192 (70.3)	81 (29.7)	0.0043
Primary (64)	41 (64)	23 (36)
High School (75)	43 (57.3)	32 (42.7)
Graduate (15)	6 (40)	9 (60)
Post graduate (8)	2 (25)	6 (75)
Marital Status
Unmarried (13)	3 (40)	10 (60)	0.004
Married (422)	281 (66.7)	141 (33.3)
SES
Upper (14)	3 (21.4)	11 (78.6)	< 0.0001
Upper-middle (47)	23 (49)	24 (51)
Lower-middle (114)	67 (58.8)	47 (41.2)
Upper-lower (246)	180 (73.2)	66 (26.8)
Lower (14)	11 (78.6)	3 (21.4)
Residence
Rural (357)	243 (68)	114 (32)	0.013
Urban (78)	41 (52.6)	37 (47.4)
Stage at presentation
Stage I (6)	4 (66.7)	2 (33.3)	< 0.0001
Stage II (133)	48 (36.1)	85 (63.9)
Stage III (237)   Stage IV (59)	175 (73.8) 57 (96.6)	62 (26.2) 2 (3.4)

BC awareness was present in 61.6% (n = 268) patients and among them only 64% were aware of breast self-examination (BSE) (Table 3). Only 38 (8.7%) performed BSE. Pain was considered as the sentinel sign of BC by 272 (62.5%). About 65% (n = 284) patients assumed that their symptoms did not indicate anything serious. More than 75% of patients consulted a doctor only after worsening or persistence of symptoms.

Table 3.

Patient factors and delay

Parameters (n)	Delay n (%)	No delay n (%)	p value
Cancer awareness
Present (268)	202 (75.4)	66 (24.6)	< 0.0001
BSE Aware (172/268)	56 (32.6)	116 (67.4)
BSE performed (38)	4 (10.5)	34 (89.5)
Absent (167)	82 (49.1)	85 (50.9)
Initial symptom
Lump (397)	264 (66.5)	133 (33.5)	< 0.0001
Mastalgia (27)	13 (48.1)	14 (51.9)
Axillary lump (4)	3 (75)	1 (25)
Skin changes (3)	2 (66.7)	1 (33.3)
Nipple discharge (4)	2 (50)	2 (50)
Interpretation of the patient
It will go away (284)	243 (85.6)	41 (14.4)	< 0.001
Something serious, merits consultation (83)	26 (31.3)	57 (68.7)
Could be cancer (68)	15 (22)	53 (78)
How does cancer present
Lump (123)	27 (22)	96 (78)	< 0.0001
Pain (272)	228 (83.8)	44 (16.2)
Nipple retraction (9)	7 (77.8)	2 (22.2)
Nipple discharge (31)	22 (71)	9 (29)
Reason for consultation
Symptom appearance (100)	27 (27)	73 (73)	<0.0001
Symptom persistence (102)	65 (63.7)	37 (36.3)
Symptom worsening (231)	190 (82.3)	41 (17.7)
Fear of cancer (2)	2 (100)	0

Overall, 58.8% (n = 256) patients visited a qualified doctor for first consultation, while the remainder either consulted alternative system practitioners or quacks (Table 4). The number of patients going to various governmental set ups were considerably low. Only 51 patients (11.8%) presented directly at a specialty center. Nearly 60% (n = 259) were not offered any investigations on presentation and only about 10% (n = 43) patients were subjected to triple assessment. About 26% patients (n = 116) consulted more than 3 practitioners before proper diagnosis was made.

Table 4.

Provider factors and delay

Parameters (n)	Delay n (%)	No delay n (%)	p value
First consultation
Private practitioner (326)	239 (73.3)	87 (26.7)	< 0.0001
Primary health center (15)	11 (73.3)	4 (26.7)
Community health center (8)	6 (75)	2 (25)
District hospital (35)	21 (60)	14 (40)
Tertiary referral center (51)	7 (13.7)	44 (86.3)
Qualification of provider
Physician/surgeon/GP (246)	105 (42.7)	141 (57.3)	< 0.001
Alternative medicine (105)	96 (91.4)	9 (8.6)
Quack (84)	83 (98.8)	1 (1.2)
Providers consulted before diagnosis
One (138)	27 (19.6)	111 (80.4)	< 0.0001
Two–three (181)	149 (87.2)	32 (18.8)
More than three (116)	108 (93.1)	8 (6.9)
Alternative treatment
Sought (247)	228 (92.3)	19 (7.7)	< 0.0001
Not sought (188)	56 (29.8)	132 (70.2)
Investigations offered
None (259)	240 (92.7)	19 (7.3)	< 0.0001
Mammogram/ USG/FNAC (133)	40 (30)	93 (70)
Triple assessment (43)	4 (9.3)	39 (90.7)
Diagnosis at presentation
Suspected cancer (117)	15(12.8)	102(87.2)	< 0.0001
Presumed benign (318)	269(84.6)	49(15.4)
Presentation at our institution
Referred (384)	277(72.1)	107(27.9)	< 0.0001
First consult (51)	7(13.7)	44(86.3)
Diagnosis before referral
Diagnosed (205)	85(41.5)	120(58.5)	< 0.0001
Not diagnosed (230)	199(86.5)	31(13.5)

Patient-related factors for delay were assessed (Table 5) and 52.5% (149/284) of the patients thought that the symptoms would resolve over time. Social stigma, financial constraints, and attraction towards alternative forms of medicine were other major factors resulting in delay. Misdiagnosis at first consultation was the most frequent patient perceived barrier (41.4%) followed by delays in referral by first contact practitioner, distance traveled to avail expert services, and lack of information about available health facilities. Financial issues, waiting periods at hospitals, and absence of female doctors were also perceived as barriers.

Table 5.

Perceived barriers and reasons for delay

Perceived barriers	n (%)	Reason for delay	n (%)
Misdiagnosis at first consult	180 (41.40)	“Thought symptoms would resolve”	153 (53.9)
Delay in referral	62 (14.2)	Social stigma (embarrassment, fear of	51 (18)
Distance from healthcare services	55 (12.7)	abandonment)
Lack of information regarding facilities	49 (11.3)	Did not know where to consult	14 (5)
Financial issues	31 (7.1)	Financial constraints	44 (15.4)
Absence of female healthcare personnel	23 (5.3)	Preference for alternative forms of	22 (7.7)
Waiting periods at treatment facilities	11 (2.5)	Treatment/fear of conventional therapy
No complaints (mostly urban dwellers)	24 (5.5)

Analysis of variance was done for all the parameters and the overall regression model was found to be significant, F (15, 419) = 156.62, p < 0.0001 and R² = 0.843. Multivariate regression analysis was performed (Table 6) which showed statistical significance for all parameters except education status.

Table 6.

Multivariate analysis

Model	Unstandardized coefficients		Standardized coefficients	t	p value	95.0% Confidence interval for B
	B	Std. Error	Beta			Lower bound	Upper bound
(Constant)	− 45.368	6.002		−7.559	0.000	−57.165	−33.571
Education	− 0.026	0.031	−0.055	−.845	0.399	−0.088	0.035
SES	−0.152	0.033	−0.272	−4.671	0.000	−0.217	−0.088
Residence	−0.260	0.063	−0.209	−4.127	0.000	−0.383	−0.136
Stage	−0.153	0.039	−0.218	−3.958	0.000	−0.229	−0.077
Cancer awareness	−0.097	0.046	−0.100	−2.109	0.036	−0.188	−0.007
BSE awareness	0.150	0.050	0.155	3.016	0.003	0.052	0.249
Breast cancer symptom (According to patient)	−0.185	0.035	−0.295	−5.248	0.000	−0.254	−0.116
Interpretation of symptom	0.270	0.040	0.425	6.740	0.000	0.191	0.349
Reason for consult	0.183	0.052	0.318	3.554	0.000	0.082	0.284
Specialty of doctor	− 0.055	0.021	−0.144	−2.653	0.008	−0.095	−0.014
Diagnosis at first consult	0.106	0.039	0.131	2.720	0.007	0.029	0.183
Doctors consulted (no.)	−0.193	0.076	−0.188	−2.528	0.012	−0.342	−0.043
Alternative treatment	0.412	0.045	0.428	9.247	0.000	0.324	0.499
Marital status	0.503	0.075	0.180	6.675	0.000	0.355	0.651

Discussion

BC is a major cause of morbidity and mortality among women in India [1]. This is ascribed to a large number of patients presenting at advanced stages. Myths and stigma associated with breast cancer, unrealistic fear of treatment, and a general lack of awareness about facilities available result in women presenting at advanced stages [5, 6]. Increasing age is traditionally associated with delay in presentation, although conflicting evidence is present [7, 8]. About 36% patients in the study cohort were below the age of 40 years and this reflects the pattern of rising incidence in younger patients in developing countries. Illiteracy is a social barrier which is shown to affect the time taken to avail health services [9]. This is more relevant in a rural population, where access to information is lesser [10]. Majority of our patients were illiterate but it was statistically insignificant. Marital status was found to be associated with delay. Financial dependence on spouse and domestic stigma may explain this association.

SES has been linked with adverse impact on health-related issues [11, 12]. SES affects affordability and access, with patients in the lower SES often relying on cheaply available alternative medicine/quacks or scarce government hospitals. Overall, SES has an inverse relation with delay in presentation and the same was observed in our study [13]. Majority of our patients were rural dwellers and showed significant delay. Poor awareness and lack of specialty treatment options in rural areas contribute to delay in this context. Distance from health centers influences the presentation time [14]. It is observed that patients who travel more than 50 miles for treatment have a negative impact on their compliance to treatment, disease outcomes, and quality of life. Multiple visits required for the treatment add to the burden [15]. Awareness of BC and knowledge of screening helps in timely diagnosis and treatment [16]. In our study, least delay was seen in patients who performed BSE. Studies from other LMICs have noted similar findings [17, 18]. Educated women and those from higher SES are more aware and compliant with BSE than others; the same was noticed in our study [19, 20]. Even though a palpable lump was the most common presenting symptom in more than 90% of our patients, most of them delayed consulting a provider. A common assumption was that the lump is harmless and will resolve by itself, as there was no associated pain. The notion that cancer is painful results in patients self-assuring themselves that nothing is wrong in delaying medical care [21–24].

More than three-fourths of patients sought help only when symptoms worsened or persisted for long time. Avoiding medical interventions until one is visibly ill is observed in many LMICs and this can be attributed to the socioeconomic factors [25, 26]. Social stigma was another major reason for delaying medical consultation. Misconceptions regarding the disease and a patriarchal nature of the society, especially in a rural setting where women are more dependent on men for their health needs, may lead to such stigma [27, 28]. About 75% of patients visited local practitioners for treatment, who ranged from qualified physicians to quacks. Most of these patients were treated symptomatically for prolonged periods, and no investigations pertaining to BC (imaging/biopsies) were advised. Few patients were subjected to inappropriate and unplanned surgeries. Practitioners in rural areas mostly have a minimalistic infrastructure or may lack expertise to correctly manage malignancies. Even trained providers lack access to update their knowledge regarding changes in the management of cancers [25]. Provider barrier in the form of failure to recognize a lesion or order an apt investigation is well-established [29]. Although evidence lacks regarding efficacy of alternative therapies in cancer treatment, they attract patients mostly because of the claims of “no side effects” and easy/cheap availability [30]. Studies have shown that alternate forms of treatment result in delayed presentation, increased morbidity, and adverse survival outcomes [31–33]. Quackery is notorious to bring about delay in any form of health service and becomes more important in the context of malignancy [34]. A large majority of patients who consulted alternate practitioners or quacks had a significant delay.

Approximately, 12% of all patients presented directly at our institution. Forty-four among them had no delay in diagnosis or initiation of treatment, while the rest presented with patient delay. The mean time from first consult to initiation of treatment at our institution was 8.3 days (range 3–22 days). In total, 284 patients had incurred delay in diagnosis and management, among which 179 was patient delay, 69 due to provider delay, and 36 due to both. The combination of both resulted in maximum delay, with many patients presenting with delay of 12 months more. Provider delays are associated with longer durations and worse outcomes in comparison with patient delays and this may be due to wrong diagnosis at presentation, bad communication between practitioner and patients, poor insurance status, high patient loads, etc. [35, 36]. Misdiagnosis at first consult was the most common factor perceived by patients as a barrier for early diagnosis, followed by delay in referral, distance from hospitals, lack of information, financial constraints, and logistic issues. The patients were asked to pick a single factor which they considered was most significant, but in reality delay was probably multifactorial and is a combination of more than one of the above factors. Although necessary precautions were taken to avoid bias, the results may be limited by recall bias, as the study relied on inputs from patients themselves. The unicentricity of the study is another limitation.

Conclusions

The importance of early diagnosis and management in breast cancer cannot be overstated. The results of the study suggest that a sizeable number of patients face delay which stem from lack of awareness and resources, fallacies in patient perception, and physician approach. Provider delay is as significant as patient delay and is associated with increased unfavorable outcomes. Robust screening strategy, education of patients and primary health providers, and making resources available to rural dwellers will be useful in this regard. The onus also lies on providers to adopt a low threshold for referral to an expert center, rather than treating without proper planning and purpose.