Sage Journals: Discover world-class research

Abstract

Introduction:

Anemia is a significant public health concern, primarily affecting young children, pregnant and postpartum women, and menstruating adolescent girls and women. This study aimed to evaluate the prevalence of anemia and associated factors in women of reproductive age visiting a tertiary care hospital in Karachi, Pakistan.

Objective:

The primary objective was to determine the prevalence of anemia in women of reproductive age, while the secondary objective was to investigate potential causes of anemia within this demographic group.

Design:

A prospective cross-sectional approach was employed, adhering to Strengthening the Reporting of Observational Studies in Epidemiology guidelines. A questionnaire-based method was used to assess anemia, and data were collected from women aged 14 to 40 years.

Method:

The study was conducted at the Jinnah Postgraduate Medical Center from January to May 2023. The study was approved by the Institutional Review Board of Jinnah Sindh Medical University (Institutional Review Board reference number JSMU/IRB/2023/699). A sample of 397 women was included, and various demographic and lifestyle factors were assessed.

Results:

In this study of 397 participants, 71.5% were found to have anemia, primarily microcytic anemia (48.2%). Anemia prevalence was highest among the 14–18 years age group (80.7%) and those from lower socioeconomic backgrounds (73.6%). Factors such as frequent tea consumption, irregular mealtimes, and pica consumption were associated with higher anemia rates. Pregnant women and those with more children were at a heightened risk of anemia.

Conclusion:

The study reveals a notable prevalence of anemia among women of reproductive age with a surprising emphasis on younger individuals and lower socioeconomic groups. Dietary habits, lifestyle choices, and pregnancy status play significant roles in anemia development. Targeted interventions are essential, particularly for younger women, those from disadvantaged backgrounds, and pregnant individuals, to combat anemia effectively in this region.

Plain Language Summary

Anemia is a widespread health concern, especially in young children, pregnant women, and menstruating adolescent girls. This condition, characterized by low hemoglobin levels, leads to insufficient oxygen delivery to organs. Globally, nearly 30% of women of reproductive age suffer from anemia, with a higher prevalence in certain regions such as Pakistan. This study aimed to assess anemia prevalence and associated factors among women of reproductive age in Karachi, Pakistan. Of the 397 participants, 71.5% were anemic. Microcytic anemia was more prevalent than macrocytic anemia. Various factors contributed to anemia, including age (highest prevalence in 14 to 18 years), lower socioeconomic status, irregular meal times, and frequent tea consumption. Surprisingly, individuals who consumed iron supplements exhibited a higher prevalence of anemia. Factors contributing to higher rates of anemia included frequent tea consumption, irregular mealtimes, and the consumption of non-nutritive substances (pica). Pregnant women and those with more children were identified as having an increased risk of anemia. In addition, women with hectic schedules were more prone to anemia. These results highlight the importance of lifestyle choices, dietary habits, and pregnancy status in the development of anemia. The study underscores the need for targeted interventions to address anemia effectively, with a particular focus on younger women, individuals from disadvantaged backgrounds, and pregnant women. By understanding the specific factors contributing to anemia in this population, public health strategies can be tailored to address the unique needs of these groups, ultimately improving the overall health outcomes for women of reproductive age in the region.

Keywords

anemia microcytic anemia prevalence women of reproductive age

Introduction

Anemia, which mostly affects young children, pregnant and postpartum women, and menstruating adolescent girls and women, is a serious public health concern. However, it is both treatable and preventable. It is characterized as a condition in which the quantity or concentration of hemoglobin (Hb) within red blood cells is lower than usual, resulting in insufficient oxygen delivery to organs and tissues. Anemia is defined by the World Health Organization (WHO) as an Hb concentration of 11 g/dL for pregnant women,12 g/dL for non-pregnant women, and < 13 g/dL in men.¹ According to a 2019 report, the global anemia prevalence was 29.9% in women of reproductive age, equivalent to over half a billion women aged 15–49 years. Prevalence was 29.6 in non-pregnant women of reproductive age and 36.5% in pregnant women. Approximately 41.7% of Pakistani women of reproductive age are anemic, according to the National Nutritional Survey-2018, with a slightly higher percentage in rural (44.3%) than in urban (40.2%) settings.²

Fatigue, decreased ability to physically exert oneself, and shortness of breath are all signs of anemia. Anemia has been linked to adverse maternal and perinatal outcomes during pregnancy, such as early birth, low birth weight, and maternal mortality. The most common nutritional shortfall thought to cause anemia is iron insufficiency, primarily caused by insufficient dietary iron consumption. Owing to their specialized functions in the synthesis of Hb and/or the formation of erythrocytes, deficiencies in vitamin A, folate, vitamin B12, and riboflavin can also cause anemia.^3
–6 In addition to these additional factors, anemia is frequently caused by significant menstrual bleeding on a regular basis, pregnancy-related blood volume expansion in mothers, and blood loss during and after childbirth, particularly in cases of postpartum hemorrhage. The likelihood of anemia is increased by several potential factors, including rural residency,^7,8 younger age,⁹ lower levels of female education,¹⁰ lack of women’s empowerment,¹¹ poorer economic conditions,^12,13 and higher rates of childbearing¹⁴ after reviewing the literature.

Owing to the lack of data regarding the prevalence of anemia in our city, this study attempted to evaluate the prevalence of anemia and related variables in women of reproductive age visiting the Jinnah Postgraduate Medical Center (JPMC), a tertiary care hospital in Karachi. Although one of the main risk factors for anemia in our system is poverty, this study was conducted to identify additional causes and determinants to help inform evidence-based therapies for anemia among women of reproductive age.

Methods

The research design employed in this investigation adhered to the STROBE (Strengthening the Reporting of Observational Studies in Epidemiology) guidelines during the article preparation process. This study utilized a prospective cross-sectional approach and employed a questionnaire-based method to assess anemia at a specific point in time. This study was approved by the Institutional Review Board (IRB) of Jinnah Sindh Medical University (JSMU/IRB/2023/-699). The study was conducted in different wards and in the outpatient department (OPD) of the JPMC from January 2023 to May 2023. The sample size was calculated using the WHO sample size calculator using a prevalence of anemia of 25%, with an error limit of 5% and a confidence interval of 5%.¹⁵ Therefore, 397 women were included in this study.

The inclusion criteria were established to define the target population to ensure the relevance of the study findings. Participants included, were both married and unmarried women aged 14 to 40 years. The study included women with gravida (number of pregnancies) or parity (number of live births). Women who had been transfused were excluded from the analysis because transfusions can affect iron levels and potentially confound findings. Male children were excluded.

Data collection procedure

The research group members were responsible for collecting data. Prior to commencing data collection, all participants under the age of 18 were approached for assent, in addition to obtaining informed consent from adult participants. During the data collection process, the research group members conducted face-to-face interviews with participants. Participants were asked questions from a structured questionnaire designed specifically for this study. The research group members manually completed a questionnaire based on the responses provided by the participants. To facilitate efficient data recording and storage, research group members utilized mobile devices or laptops to secure the collected information securely. In addition, to obtain accurate laboratory values, pictures of complete blood count (CBC) reports were taken and recorded in the questionnaire. In addition to the questionnaire-based approach, participant’s socioeconomic status was assessed by asking a series of relevant questions. Rather than solely inquiring about location, the research group members used a comprehensive approach. They verbally asked the participants about various aspects, such as the number of individuals contributing to family income, the number of rooms in their house, the level of ventilation, homeownership status, and the source of drinking water (filtered water, tap water, or boiled water). The research group members checked the appropriate box in the questionnaire after evaluating the participants’ responses.

Statistical analysis

In a descriptive analysis using SPSS software version 26, the study examined key variables such as Hb, mean corpuscular volume (MCV), mean corpuscular Hb (MCH), and mean corpuscular Hb concentration (MCHC) and calculated their mean and standard deviation (SD). Anemia, the primary dependable variable, was also computed based on Hb with a cutoff range below 12 mg/dL. The confidence level (CL) for this analysis was set at 95%, and the data were normally distributed using the Kolmogorov–Smirnov test. Beyond these main variables, the study conducted a comprehensive descriptive analysis, including the assessment of marital status and frequency of anemia occurrence. The analysis was extended to encompass demographic characteristics, risk factors, iron supplement usage, and blood test results, employing chi-square tests to explore the relationships between anemia prevalence and variables, such as risk factors and iron supplement use. The primary goal of this study was to ascertain the prevalence of anemia among women of reproductive age, while the secondary objective was to investigate the potential causes of anemia within this demographic group.

Results

The study’s baseline characteristics, as shown in Table 1, revealed that out of 397 participants, 71.5% of women (n = 284) were identified as anemic, following the removal of one missing value (n = 1). This finding underscored the significant prevalence of anemia within the study group, with the remaining 28.5% (n = 113) of non-anemic women.

Table 1.

Baseline characteristics of included participants.

Baseline characteristics	Total participants (N = 397)
Baseline characteristics	N (%)
Age (years)
14 to18	26 (6.55)
19 to 24	111 (27.96)
25 to 30	146 (36.78)
30 to 40	114 (28.72)
Socioeconomic status
Low	133 (33.50)
Middle	254 (63.97)
High	10 (2.52)
Hemoglobin (Mean SD)	10.36 ± 1.951
MCH (Mean SD)	25.95 ± 4.726
MCHC (Mean SD)	32.35 ± 2.457
MCV (Mean SD)	79.40 ± 9.458
Marital status
Married	354 (89.17)
Unmarried	43 (10.83)
Age at menarche (years)
10 to 11	49 (12.3)
12 to 13	272 (68.5)
14 to 15	75 (18.89)

SD: standard deviation; MCH: mean corpuscular hemoglobin; MCHC: mean corpuscular hemoglobin concentration; MCV: mean corpuscular volume.

Further analysis, as presented in Table 2, revealed that microcytic anemia (48.2%) was more common than macrocytic anemia (23.3%) among participants with anemia, shedding light on the specific types of anemia prevalent in the study population.

Table 2.

Analysis of anemia prevalence in relation to sociodemographic and lifestyle factors among study participants (n = 397).

Sociodemographic factors	Total participants	Anemia present	Percentage, %	p-value
Age (in years)
14 to18	26	21	80.76	0.000
19 to 24	111	84	75.64
25 to 30	146	105	71.9
30 to 40	114	74	65.9
Overall	397	284	71.5
Marital status
Married	354	251	70.9	0.423
Unmarried	43	33	76.74	0.423
Education status
No formal education	91	67	73.62	0.713
Primary	94	69	73.4
Secondary	83	57	68.67
Matric	76	56	73.68
Intermediate	33	20	60
University student	20	15	75
Socioeconomic status
Low	133	98	86.7	0.797
Middle	254	179	70.47
High	10	7	70
Tea intake
One time	110	79	71.8	0.484
Two times	212	157	74
Three times	56	36	78.2
Four times	11	7	63.6
Erratic meal time
Yes	162	125	77	0.037
No	234	158	67.5	0.037
Source of iron
Vegetables	232	169	72.8	0.912
Meat	91	63	69
Pulses	68	48	70.5
Fruits	6	4	66.6
Iron supplements
Yes	188	138	82.1	0.416
No	208	145	69.7	0.416
Pica consumption
Yes	30	25	83.3	0.136
No	367	259	70.5	0.136
Hectic schedule
Yes	100	43	43	0.847
No	297	131	44.11	0.847
Parity
Yes	315	225	71.4	0.02
No	82	59	71.9
Gravida
Yes	335	241	71.9	0.384
No	63	43	68.2
Type of anemia	Total anemia patients	Present
Microcytic	284	192	48.2	0.02
Macrocytic	284	92	23.3	0.74

Regarding marital status, the results showcased that 70.9% of married women and 76.74% of unmarried women were diagnosed with anemia, providing insight into the distribution of anemia across different marital statuses. Age-based analysis revealed that the highest prevalence of anemia was observed in the 14–18 years age group (80.76%) and the 25–30 years age group (71.9%), suggesting age-related factors impacting anemia prevalence. Socioeconomic status emerged as another noteworthy factor, with a study demonstrating that lower-class women had the highest prevalence of anemia (86.7%), underlining socioeconomic disparities in anemia prevalence.

In terms of dietary habits, participants who consumed tea twice daily displayed the highest number of anemia cases (74%), highlighting the potential impact of tea consumption frequency on anemia. In addition, erratic mealtimes were associated with a higher prevalence of anemia (77%), emphasizing the significance of mealtime regularity in managing anemia (p = 0.037). Among the dietary choices, women who predominantly ate vegetables had the highest number of participants with anemia (72.8%), indicating a possible relationship between dietary preferences and anemia prevalence. Iron supplement usage exhibited an interesting pattern, with iron supplement users having an 82.1% prevalence of anemia, while non-users had a 69.7% anemia prevalence, suggesting a complex relationship between iron supplementation and anemia.

Pica consumption emerged as a strong indicator, with an 83.33% prevalence of anemia among women who consumed pica, emphasizing the link between this behavior and anemia. Hectic schedules were associated with a higher prevalence of anemia (44.11%), highlighting the potential impact of lifestyle factors on the occurrence of anemia.

In terms of parity and gravidity, 71.4% (225 out of 315) of patients with parities had anemia, 71.9% (59 out of 82 individuals) had anemia and had no parities, and 71.9% (241 out of 335) gravida patients had anemia, compared to 68.2% (43 out of 63) of patients with anemia, showing that parity was significantly associated with anemia (p = 0.02).

Discussion

The research analyzed the frequency of anemia and its causative factors in women aged 14 to 40 years who were treated at a tertiary hospital in Karachi, Pakistan. The decrease in Hb concentration or red blood cell size below a pre-determined cut-off value leads to anemia, which impairs the blood’s ability to deliver oxygen to the entire body.¹⁶

Reducing anemia is crucial for women and children’s health, yet challenges persist in the world’s poorest regions.¹⁷ The prevalence of anemia in South Asian nations varies; Bangladesh has reported a prevalence of 41.8%, Maldives 58.5%, Nepal 40.6%, and India over 55%.^18,19 According to a National Nutritional Survey-2018 in Pakistan, approximately 41.7% of women of reproductive age are anemic.² We were surprised to discover that 71.4% of women of reproductive age who visited a tertiary care hospital with any illness, aside from all relevant blood diseases, or with a history of blood loss were anemic. One study identified iron deficiency as the most prevalent type of anemia in Pakistani women.² As a result of this survey, we discovered that 48.3% of the individuals in our study (n = 192 out of 397) had microcytic anemia.

In addition to examining the prevalence of anemia, we also wanted to determine what made our subjects more likely to develop anemia. Age group, socioeconomic status, level of education, tea intake, sources of micronutrients, use of iron supplements, hectic routines, irregular mealtimes, current pregnancy, and total number of pregnancies were among these factors. We also looked into the probable connection between anemia and pica, the ingestion of substances other than food, which was previously noted in a study by Baig-Ansari N.¹⁵

Anemia is often thought to be age-dependent, with research in Bangladesh indicating that older age is a key contributor,²⁰ although a study conducted in India indicated a higher likelihood of severe anemia among individuals aged 15 to 29 years.²¹ Surprisingly, the younger age group (14–18 years) had the highest prevalence of anemia (80.7 %) according to our comprehensive study. In addition, this group had a higher prevalence of microcytic anemia (69.2%). This odd trend may be ascribed to factors such as poverty, poor nutrition, lack of knowledge regarding iron loss during menstruation, and limited control over one’s own health and finances among young women.

Another component in our analysis was socioeconomic status, which was significantly correlated with outcomes in India.²² We discovered that the majority of participants with anemia (73.6%) belonged to lower socioeconomic groups and were predominantly from rural Sindh and the outlying districts of Karachi. These areas are prone to poor diet, micronutrient deficiencies, lack of access to public services, and low income. High frequency of infectious diseases, poor housing, polluted drinking water, and inadequate sanitation are other factors that lead to anemia in these places.

Anemia is influenced by a number of nutritional factors, including lack of iron and folic acid, lack of fruits and eggs, and high intake of tea.²³ However, our research revealed mixed results, demonstrating that not all causes of anemia had a substantial effect. Participants who drank more tea, for instance, had lower anemia rates than those who did not consume iron supplements (except during pregnancy).

Strong correlations between pica and vitamin deficits were found in a meta-analysis, indicating that pica status could be utilized as a preliminary clinical indicator of micronutrient deficiency in women.²⁴ Intriguingly, we discovered a strong relationship between pica and anemia, particularly microcytic anemia. We discovered that the majority of individuals intentionally consumed non-food items including laundry starch, clay, mud, and ice.

Finally, in line with research,^25
–28 our data confirmed that the risk of anemia was higher in pregnant women and those who had more children. This risk is related to hemodilution during pregnancy, which is worsened by blood loss during labor. The highest prevalence of anemia in our study (80.9%) was found in primigravida women. Delays in prenatal care and insufficient vitamin supplementation have been identified as potential causes. Microcytic anemia was present in 40.7% of people who were presently pregnant and in 37.4% of those who were parous.

Our study had several strengths. First, we conducted a comprehensive examination of the factors influencing anemia. Moreover, our research uncovered uncommon patterns that contradicted conventional wisdom, notably the highest occurrence of anemia among the younger age groups.^14
–18 This finding adds an intriguing dimension to our study.

However, it is important to acknowledge the limitations of this study. The questionnaire utilized in our research was not pilot tested, which may have implications for its reliability and effectiveness in capturing the nuances of anemia-related factors. The majority of participants in our study came from lower socioeconomic backgrounds, which restricts the generalizability of our findings to larger socioeconomic groups. To address this issue, future studies should consider incorporating more diverse data sources from a broader perspective. Furthermore, not all probable causes of anemia were explored in our study, such as consanguineous unions leading to thalassemia or B12/folate deficiency causing macrocytic anemia. A more comprehensive questionnaire could effectively address these aspects. In addition, our study’s diagnostic approach was limited because we relied solely on CBC tests to determine anemia prevalence, without specific B12, folate, or iron profile studies. This limitation affected our ability to differentiate between nutritional and non-nutritional causes of anemia among the participants.

Conclusion

In conclusion, our study provides valuable insights into the prevalence of anemia and its associated factors among women of reproductive age in Karachi, Pakistan. These findings emphasize the need for targeted interventions to address anemia in this population, particularly among younger women, those from lower socioeconomic backgrounds, and pregnant women. Understanding the multifaceted factors contributing to anemia is crucial for developing effective public health strategies to combat this prevalent condition in the region.

Supplemental Material

sj-pdf-1-whe-10.1177_17455057241227364 – Supplemental material for Prevalence and factors influencing anemia in women of reproductive age visiting a tertiary care hospital (Jinnah Postgraduate Medical Center) in Karachi: A cross-sectional study

Supplemental material, sj-pdf-1-whe-10.1177_17455057241227364 for Prevalence and factors influencing anemia in women of reproductive age visiting a tertiary care hospital (Jinnah Postgraduate Medical Center) in Karachi: A cross-sectional study by Farheen Ashraf, Muhammad Musab Nafees Uddin, Muhammad Saqlain Mustafa, Zaib Un Nisa Mughal and Sajid Atif Aleem in Women’s Health

Footnotes

I would like to extend my heartfelt appreciation to my dedicated colleagues,Samra and Iqra Parveen,for their invaluable assistance in the meticulous data collection process,which significantly contributed to the success of this research.

Declarations

ORCID iD

Muhammad Saqlain Mustafa

Supplemental material

Supplemental material for this article is available online.

References

Haemoglobin concentrations for the diagnosis of anaemia and assessment of severity. Vitamin and Mineral Nutrition Information System. Geneva: World Health Organization, 2011, https://www.who.int/publications/i/item/WHO-NMH-NHD-MNM-11.1

The Ministry of National Health Services Regulation and Coordination. National nutrition survey: key findings report, 2018,. https://www.unicef.org/pakistan/reports/national-nutrition-survey-2018-key-findings-report

The global prevalence of anaemia in 2011. Geneva: World Health Organization, https://www.who.int/ (2015, accessed 18 June 2019).

Janus

Moerschel

SK.

Evaluation of anemia in children. Am Fam Physician 2010; 81(12): 1462–1471.

Bates

McKew

Sarkinfada

Anaemia: a useful indicator of neglected disease burden and control. PLoS Med 2007; 4(8): e231.

Jin

Yeung

Cogswell

, et al. Prevalence of anaemia among pregnant women in South-East China, 1993-2005. Public Health Nutr 2010; 13(10): 1511–1518.

Siddiqui

Goli

Reja

, et al. Prevalence of anemia and its determinants among pregnant, lactating, and nonpregnant nonlactating women in India. SAGE Open 2017; 7(3): 2158244017725555.

Goli

Doshi

Perianayagam

Pathways of economic inequalities in maternal and child health in urban India: a decomposition analysis. PLoS ONE 2013; 8(3): e58573.

Adamu

Crampin

Kayuni

, et al. Prevalence and risk factors for anemia severity and type in Malawian men and women: urban and rural differences. Popul Health Metr 2017; 15(1): 12.

10.

Schouten

Wang

, et al. Anemia prevalence among pregnant women and birth weight in five areas in China. Med Princ Pract 2009; 18(5): 368–372.

11.

Gupta

Pingali

Pinstrup-Andersen

Women’s empowerment and nutrition status: the case of iron deficiency in India. Food Policy 2019; 88: 101763.

12.

Lebso

Anato

Loha

Prevalence of anemia and associated factors among pregnant women in Southern Ethiopia: a community based cross-sectional study. PLoS ONE 2017; 12(12): e0188783.

13.

Ivoke

, ed. Anaemia prevalence and associated factors among women attending antenatal clinics in South-Western Ebonyi State, Nigeria, 2013, https://www.semanticscholar.org/paper/Anaemia-Prevalence-and-Associated-Factors-among-in-Ivoke/7881111aacfc2ada39891d51466d721c795d4892.

14.

Balarajan

Fawzi

Subramanian

SV.

Changing patterns of social inequalities in anaemia among women in India: cross-sectional study using nationally representative data. BMJ Open 2013; 3(3): e002233.

15.

Baig-Ansari

Badruddin

Karmaliani

, et al. Anemia prevalence and risk factors in pregnant women in an urban area of Pakistan. Food Nutr Bull 2008; 29(2): 132–139.

16.

Beutler

Waalen

The definition of anemia: what is the lower limit of normal of the blood hemoglobin concentration?

Blood 2006; 107(5): 1747–1750.

17.

Stevens

Finucane

De-Regil

, et al. Global, regional, and national trends in haemoglobin concentration and prevalence of total and severe anaemia in children and pregnant and non-pregnant women for 1995-2011: a systematic analysis of population-representative data. Lancet Glob Health 2013; 1(1): e16–e25.

18.

Rahman

Aziz Rahman

, et al. Prevalence of and factors associated with anaemia in women of reproductive age in Bangladesh, Maldives and Nepal: evidence from nationally-representative survey data. PLoS ONE 2021; 16(1): e0245335.

19.

Sharif

Das

Alam

Prevalence of anemia among reproductive women in different social group in India: cross-sectional study using nationally representative data. PLoS ONE 2023; 18(2): e0281015.

20.

Kamruzzaman

Rabbani

Saw

, et al. Differentials in the prevalence of anemia among non-pregnant, ever-married women in Bangladesh: multilevel logistic regression analysis of data from the 2011 Bangladesh Demographic and Health Survey. BMC Womens Health 2015; 15: 54.

21.

Lahiri

Conditional selection of multifactor evidence for the levels of anaemia among women of reproductive age group. Eval Program Plann 2023; 100: 102344.

22.

Bentley

Griffiths

PL.

The burden of anemia among women in India. Eur J Clin Nutr 2003; 57(1): 52–60.

23.

Ali

Khan

Feroz

Prevalence and determinants of anemia among women of reproductive age in developing countries. J Coll Physicians Surg Pak 2020; 30(2): 177–186.

24.

Miao

Young

Golden

CD.

A meta-analysis of pica and micronutrient status. Am J Hum Biol 2015; 27(1): 84–93.

25.

Ullah

Zahid

Ismail

, et al. Prevalence of anemia in pregnant women in district Karak, Khyber Pakhtunkhwa, Pakistan. IJB 2013; 03: 01–07.

26.

Page

Patel

Hibberd

PL.

Does smoke from biomass fuel contribute to anemia in pregnant women in Nagpur, India? A cross-sectional study. PLoS ONE 2015; 10(5): e0127890.

27.

Addis Alene

Mohamed Dohe

. Prevalence of anemia and associated factors among pregnant women in an Urban Area of Eastern Ethiopia. Anemia 2014; 2014: 561567.

28.

Kedir

Berhane

Worku

Khat chewing and restrictive dietary behaviors are associated with anemia among pregnant women in high prevalence rural communities in eastern Ethiopia. PLoS ONE 2013; 8(11): e78601.

Supplementary Material

Please find the following supplemental material available below.

For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.

For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.

0.17 MB

0.00 MB